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Knee malalignment and variations in foot posture and function affect the forces transmitted through the knee joint and are associated with knee pain and medial tibiofemoral cartilage damage [ 1]. However, it is unclear whether altered foot posture and function are a compensatory mechanism to accommodate knee malalignment. Therefore, this study investigated changes in foot posture and function after realignment of the knee following total knee replacement (TKR) in people with medial compartment knee OA.

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Changes in foot posture and function following total knee replacement surgery - Journal of Foot and Ankle Research

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Knee malalignment and variations in foot posture and function affect the forces transmitted through the knee joint and are associated with knee pain and medial tibiofemoral cartilage damage [ 1]. However, it is unclear whether altered foot posture and function are a compensatory mechanism to accommodate knee malalignment.

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Affiliations

1. Department of Podiatry, La Trobe University, Melbourne, Australia

Tamara J Lane, Karl B Landorf, Daniel R Bonanno & Anita Raspovic

2. Lower Extremity and Gait Studies Program, La Trobe University, Melbourne, Australia

Karl B Landorf, Daniel R Bonanno, Anita Raspovic & Hylton B Menz

Corresponding author

Correspondence to Tamara J Lane.

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The effect of shoe-sole hardness on plantar pressure and comfort in older people with forefoot pain - Journal of Foot and Ankle Research

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Department of Podiatry, La Trobe University, Melbourne, Australia Tamara J Lane, Karl B Landorf, Daniel R Bonanno & Anita Raspovic Lower Extremity and Gait Studies Program, La Trobe University, Melbourne, Australia Karl B Landorf, Daniel R Bonanno, Anita Raspovic & Hylton B Menz Correspondence to Tamara J Lane.

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-5-S1-P33

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Several risk factors for the development of running injuries have been identified, however, the etiology is still not completely clear [ 1]. A number of prospective studies have identified gait-related risk factors for lower leg overuse injuries [ 2- 6]. On the other hand, running injuries only develop by overloading the lower extremity. Fatigue can therefore be hypothesized to be a primary contributing factor. However, in determining injury etiology the relationship between the injury, the gait-related risk factors and overloading by fatigue is a complex model and the amount of contribution of each factor is difficult to assess. It might therefore be interesting to check 1) the interaction between fatigue and the roll-off pattern during running and 2)if fatigue generates specific gait-related risk factors for running injuries.

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The effect of fatigue on plantar pressure distribution during running in view of running injuries - Journal of Foot and Ankle Research

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Several risk factors for the development of running injuries have been identified, however, the etiology is still not completely clear [ 1]. A number of prospective studies have identified gait-related risk factors for lower leg overuse injuries [ 2- 6]. On the other hand, running injuries only develop by overloading the lower extremity.

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/s13047-021-00476-6.pdf

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Foot symmetry and change in foot structure as a function of weight bearing status have not been investigated in a large cohort study. The foot structure of 1,054 incoming cadets at the US Military Academy (172 female, 18.5±1.1 years, 24.5±3.0 kg/m ²) was examined. Arch Height Index (AHI) was assessed in sitting and standing condition, and its value was used to classify each foot into 3 foot types as previously described [ 1].

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Foot type symmetry and change of foot structures from sitting to standing conditions

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Foot symmetry and change in foot structure as a function of weight bearing status have not been investigated in a large cohort study. The foot structure of 1,054 incoming cadets at the US Military Academy (172 female, 18.5±1.1 years, 24.5±3.0 kg/m 2) was examined.

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Effect of plano-valgus foot posture on midfoot kinematics during barefoot walking in an adolescent population                                      Emma De Vidts

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Open Peer Review reports

Background

Plano-valgus is a common alteration of the paediatric foot, characterized by valgus hindfoot, foot pronation and drop of the medial longitudinal arch. Despite their importance in the diagnosis and classification of plano-valgus foot condition, little information is available on functional alterations of the major joints spanning the medial longitudinal arch - i.e. midtarsal and tarso-metatarsal. Aim of the study was to provide objective description of the alterations in plano-valgus midfoot joints with respect to those in an age-matched normally-developed feet population.

Methods

Twenty adolescents (13.3 ± 0.8 years) with bilateral plano-valgus feet underwent clinical examination and were gait-analysed via a validated 4-segment foot model. This allowed to measure static foot posture, kinematics of the main foot joints, and medial longitudinal arch deformation during walking at comfortable speed. Range of motion and temporal profiles of joint rotations were compared to those from a control population of age-matched adolescents with normally-developed feet.

Results

The plano-valgus midtarsal joint was more dorsiflexed, everted and abducted than that in the control group, and showed reduced sagittal-plane RoM (plano-valgus = 15.9 degrees; control = 22.2 degrees; P  <  0.01). The tarso-metarsal joint was more plantarflexed and adducted, and showed larger frontal-plane RoM. The MLA showed larger RoM and was lower throughout the stance phase of the gait cycle.

Conclusion

Significant postural and kinematic alterations are present at the midtarsal and tarso-metarsal joints of adolescents with plano-valgus feet. Objective identification and quantification of plano-valgus foot alterations, via non-invasive gait-analysis, is relevant to improving the diagnosis of this condition and to evaluating the effect of conservative treatments and of surgical corrections by different techniques.

Plano-valgus foot (PV) is a complex 3D-deformity of the foot, often asymptomatic, characterized by plantarflexion and eversion of the calcaneus relative to the tibia, plantarflexion of the talus, dorsiflexion of the navicular and supination of the forefoot [, ]. The most obvious features characterizing PV are valgus hindfoot and flattening of the medial longitudinal arch (MLA) during weightbearing. The MLA starts developing at the age of 2 and becomes structurally mature at around 10-13 years old []. Accordingly, the incidence of PV changes with age: it is present in about 37-60% of 2-6 year old children, and in about 16-19% of adolescents - around 8-13 years old - after growth plates closure [-]. While morphological signs of flexible PV disappear in the unloaded condition, deformity is always present in rigid PV due to structural alterations, collagen and neuromuscular disorders [, ]. A Cochrane review has shown that the reported incidence of PV is limited by variable sampling, age groups and assessment measures, thus resulting in different findings []. It is generally recognized that PV signs decrease with age, and that joint hypermobility and body weight increase the incidence of PV at all ages.

Clinically, the paediatric PV midfoot is significantly collapsed in weightbearing. Therefore, it has been postulated that the PV midfoot is everted and dorsiflexed for longer during late stance, thus making push-off less efficient [-]. Later in life, extended hindfoot pronation and arch collapse may lead to anterior pelvic tilt, internal hip rotation, knee valgus and internal rotation of the tibia [-]. Since alterations of foot posture in static conditions are not always correlated to those occurring in dynamic conditions, gait analysis in combination with a number of multi-segment foot models has been increasingly used for objective quantification of the complex multi-planar kinematics characterizing PV. A review of the most relevant literature on this topic is reported in Table . Twomey et al. [], using the Heidelberg foot measurement method, reported increased forefoot supination and greater MLA deformation during gait in children with low arched feet. Hosl et al. [] reported increased hindfoot eversion with limited dorsiflexion and frontal range of motion (RoM), compensated by increased supination, abduction and sagittal RoM of the forefoot both in symptomatic and asymptomatic flat feet. Saraswat et al. [] reported increased hindfoot eversion and plantar flexion along with increased midfoot dorsiflexion and pronation in PV. Kerr et al. [] reported increased hindfoot eversion in static conditions, with compensating forefoot abduction and supination, in children with flat feet. Finally, Kothari et al. [] reported increased hindfoot eversion compensated by forefoot supination.

Despite the clinical relevance of midfoot posture, our current understanding of paediatric PV function during gait is related to hindfoot, forefoot and hallux motion. Since most of the clinical signs and postural alterations of PV concern a number of joints spanning the medial longitudinal arch, a thorough functional analysis of PV can not disregard the information on 3D static alignment and motion of the joints in the midfoot - i.e. midtarsal and tarso-metatarsal joints. Improving our understanding of midfoot joints alterations is critical to shed more light on the clinical signs and extent of PV deformity requiring intervention, and to assess the effectiveness of non-invasive approaches and of surgical treatments.

Therefore, in order to better characterize PV kinematics, a validated multisegment foot model comprising the midfoot segment was used in this study to assess differences in posture and gait between asymptomatic PV and healthy feet joints. It was hypothesized that static posture and gait kinematics of the PV midtarsal and tarso-metatarsal joints are significantly different from those in normal-arched healthy feet.

Participants

Twenty adolescents (13 M and 7 F; age: 13 ± 1 years; height: 164 ± 7 cm; weight: 53 ± 11 kg; shoe size: 38-44 EU) were recruited for the study following their diagnosis of bilateral asymptomatic PV by two paediatric orthopaedic surgeons (NP and AP). Ten age-matched adolescents (4 M and 6 F; age: 13 ± 1 years; height: 156 ± 10 cm; weight: 48 ± 12 kg; shoe size: 37-44 EU) with normally-developed feet (ND) were used as control group.

According to the clinical protocol of the hosting Institution, participants who had calcaneal valgosity > 16° were included in the study. This was measured as the relative angle between neutral calcaneal stance position (NCSP) to resting calcaneal stance position (RCSP). Radiological indicators of PV condition, such as the calcaneal pitch, lateral talo-first metatarsal angle, and talo-navicular coverage, were measured using weightbearing X-rays. Valgosity of the calcaneus was measured with a goniometer. Exclusion criteria were the following: lower limb musculoskeletal disorders; concomitant systemic diseases; clinical signs of joint laxity, and major lower limb trauma. Children practicing sports at a competitive level were also excluded. The study was performed according to the ethical standards of the Declaration of Helsinki (1964) and its later amendments. Acknowledgement of the Hospital's IRB was granted (protocol n° 7/17) and parents' informed consent was obtained for all children recruited in the study.

In order to limit inter-observer variability [], a single experienced operator performed clinical, radiographic and instrumental evaluation of all participants.

Kinematic analysis

Statistics

Average left and right foot kinematic data were calculated across three walking trials for each participant in the PV and ND group, for a total of 60 samples. Mann-Whitney U test was used to assess differences in anthropometric (demographic) and kinematic parameters between PV and ND. A Bonferroni correction was applied to the significance level to account for the multiple comparisons in static posture and RoM between the two groups (α = 0.01). A post-hoc power analysis confirmed that the samples used for statistical analysis of midtarsal and tarso-metatarsal joints RoM in the three anatomical planes were sufficient to identify statistical differences between the two groups with a power of 0.8. One-dimensional statistical parametric mapping [] was used to determine differences in time-histories of joint rotations between PV and ND.

No significant differences in age, height, and body mass were observed between groups. All PV radiological and clinical measurements were consistent with a diagnosis of flexible plano-valgus foot [-] and confirmed that feet in the PV group were clinically different from those in the ND group (Table ). Normalized walking speed and stride length were lower in the PV group (Table ).

Static posture

Temporal profiles of joint rotations

In the PV group, metatarsus and midfoot were more dorsiflexed with respect to the hindfoot than those in the ND group throughout the whole gait cycle. In addition, the midfoot was more everted and abducted with respect to the calcaneus. The calcaneus was more plantarflexed and everted with respect to the shank, and the forefoot was more plantarflexed and more adducted with respect to the midfoot. The forefoot was also more inverted to the calcaneus at push-off (52-62% of gait cycle) and prior-to and in early stance (90-100% and 0-7% of gait cycle).

The first metatarsophalangeal joint was more dorsiflexed throughout most of the stance duration, and showed a larger maximum dorsiflexion at push-off in the PV group (Fig. ).

The MLA was lower (i.e. larger MLA angles) in the PV group during the whole gait cycle (Fig. ).

RoM analysis

The paediatric foot has been extensively studied clinically and radiographically. However, clinical evaluation allows only quantification of the hindfoot frontal-plane alignment in upright standing position. While x-ray imaging can provide accurate information on the two-dimensional alignment of the foot bones, the exposure to ionizing radiation and the complexity of coronal plane measurements strongly limit its use for PV diagnosis. Therefore, skin-markers based gait analysis and multisegment foot protocols have been increasingly used to provide objective evaluation of foot posture and kinematics in the paediatric PV population. Compared to the normal-arched control feet, paediatric PV feet have been shown to present increased hindfoot eversion, and greater forefoot abduction and supination (Table ). In the lower limb joints, larger external hip rotation in early stance and larger anterior pelvic tilt were observed in 5 years old children with bilateral valgus hindfoot [].

To the best of the authors' knowledge, this is the first time a detailed multi-segment postural and kinematic analysis of the paediatric asymptomatic PV has been performed. The present functional evaluation has confirmed that significant alterations are present in PV with respect to age-matched normally developed feet. The differences observed between PV and ND in static posture were consistent with the diagnosis of plano-valgus foot condition, and were strongly related to those observed in gait kinematics. Similar to what was reported in previous studies, the PV hindfoot was significantly everted [, -], and plantarflexed [] relative to the tibia. In the PV group, in accordance with [], MLA deformation was significantly larger and the hallux was more dorsiflexed throughout most of stance duration. This may be related to reduced efficiency of those anatomical structures spanning the midfoot, such as plantar intrinsic foot muscles and aponeurosis, altering the arch rising effect of the windlass mechanism [] (Fig. ). This mechanism was shown to occur also in early stance [], thus alteration of its efficacy may affect foot biomechanics in the loading response phase, when the hindfoot everts and the foot arch lowers to absorb the ground reaction forces. Evidence of kinematic alteration across the medial longitudinal arch in the PV group appears consistent with a recent morphometric analysis of pes-planus in which a reduced cross-sectional area of the 1st ray intrinsic muscles, and reduced plantar fascia thickness were observed [].

In addition to the current understanding of PV function, it was possible to better identify in which joints most of the static and kinematic alterations that characterize pediatric flexible pes-planus are present. The midtarsal joint was significantly dorsiflexed, everted and abducted throughout gait, and the tarso-metatarsal joint was plantarflexed and slightly adducted. As a result, no significant abduction was observed in the forefoot with respect to the hindfoot. RoM analysis revealed some novel information on the mechanics of the pediatric flexible plano-valgus foot during gait. In the PV group, increased frontal plane RoM was observed at the tarso-metarsal joint and between forefoot and hindfoot, whereas sagittal-plane RoM was reduced at the midtarsal joint. In accordance with the joint posture measured in static conditions, the PV midtarsal joint was more dorsiflexed throughout the whole gait cycle with respect to the ND; however sagittal-plane RoM of the midtarsal joint was reduced. In the frontal plane, the PV group showed increased ankle and midtarsal joint eversion both in terms of offset to the corresponding ND profiles and, albeit not statistically significant, in RoM. From a biomechanical perspective this may be due to the midtarsal joint having reached the largest possible dorsiflexion allowed by skeletal and ligaments constraints (Fig. ). Conversely, extra mobility is allowed in the frontal plane as the flexible plano-valgus foot can reach a more everted posture compared to normally developed feet.

In accordance with what observed by Lin et al. [] on a slightly younger PV population, but in contrast with other reports [, ], the PV group walked with reduced stride length and walking speed. This is normally associated with some functional deficit, and may be due to the significant foot postural alterations displayed by those children included in the PV subgroup. However, kinetic and pressure analyses could not be performed due to limitations of the present setup, thus functional impairments and compensations in the lower limb joints associated with PV kinematic alterations shall be addressed in future investigations. Although PV kinematics could not be compared to a speed-matched gait data set, this appeared to have only marginally affected the differences in joint kinematics between PV and ND, as most of the kinematic alterations were strongly consistent with those measured in static posture. Moreover, the effect of cadence on foot joints range of motion was found to be significant mainly between slow- and fast-walking cadence, in the frontal and transverse planes only []. It should also be highlighted that only 20 PV adolescents were analysed, and that the age was limited to 13 years - the age at which children's feet reach full skeletal maturity [, , ] and clinical assessment of pes-planus condition is recommended at the authors' Institution. These limitations somehow restrict the generalizability of these results to a larger plano-valgus paediatric population. Nevertheless this study provides objective information on foot kinematics for a critical paediatric population presenting significant alterations of foot skeletal morphology, and for which the choice of the most appropriate treatment is still highly debated. In terms of limitations of the methodology, while the Rizzoli Foot Model is a widely used and extensively validated kinematic protocol [, , ] presenting a balance of moderate repeatability and reasonable test-retest error [], it should be reminded that kinematic analysis of foot joints via skin-markers is intrinsically affected by skin-motion artifacts. The magnitude of this error on the calculated foot joints RoM is difficult to determine with precision, thus making the interpretation of the absolute joint rotations rather difficult. However, this has likely biased both groups to a similar extent, with negligible effects on the differences detected between the groups.

Multisegment kinematic analysis based on skin-markers has proved to be an effective non-invasive technique to detect functional alterations of foot segments in the three anatomical planes, which can not be identified clinically or radiographically. According to the results of this study, significant postural and kinematic alterations are present at the midtarsal and tarso-metarsal joints of adolescents with asymptomatic PV with respect to normal-arched healthy feet. While larger dorsiflexion of midfoot joints and greater MLA collapse provide evidence for a hindered windlass mechanism, further studies should nonetheless be sought to fully comprehend the effect of these alterations to PV function, as well as modifications following surgical correction by different techniques.

Acknowledgements

The authors would like to acknowledge Maurizio Ortolani for helping with the gait data acquisition and pre-processing.

Funding

The study is partially funded by the Italian 5 × 1000 funding scheme.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

PC assisted with designing the study, performed the data analysis, helped with the interpretation of the results and the preparation of the manuscript. CS assisted with designing the study, helped with the interpretation of the results and the preparation of the manuscript. AL assisted with designing the study, helped with the interpretation of the results and the preparation of the manuscript. AP assisted with designing the study, recruited the participants, acquired the kinematic data, and helped with the interpretation of the results and the preparation of the manuscript.

Ethics approval and consent to participate

Acknowledgement of the Hospital's IRB was granted (protocol n° 7/17) and parents' informed consent was obtained for all children recruited in the study.

Consent for publication

Parents' consent to publish was granted.

Competing interests

The authors declare that they have no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/ ), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/ ) applies to the data made available in this article, unless otherwise stated.

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Effect of plano-valgus foot posture on midfoot kinematics during barefoot walking in an adolescent population

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Plano-valgus is a common alteration of the paediatric foot, characterized by valgus hindfoot, foot pronation and drop of the medial longitudinal arch. Despite their importance in the diagnosis and classification of plano-valgus foot condition, little information is available on functional alterations of the major joints spanning the medial longitudinal arch - i.e.

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/1757-1146-5-S1-O51.pdf

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/1757-1146-7-S1-A11.pdf

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/s13047-019-0365-7.pdf

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00410-2

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Journal of Foot and Ankle Research 13, Article number: 40 (2020) Cite this article

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Abstract

Background

Sex-related differences of plantar pressure distribution during activities should be thoroughly inspected as it can help establish treatment and prevention strategies for foot and ankle problems. In-shoe measurement systems are preferable without space and activity restrictions; however, previously reported systems are still heavy and bulky and induce unnatural movement. Therefore, a slim and light plantar pressure sensor was newly developed to detect the effect of sex difference on plantar pressure during standing and walking.

Methods

One-hundred healthy adult volunteers (50 women and 50 men) were recruited. Ten plantar pressure sensors were implanted in a 1-mm thick insole, with a total weight of 29 g. Plantar pressure was recorded with 200 Hz during 3 s of standing and while walking 10 steps. The maximum loads during standing and walking were analyzed in each sensor, and the results were compared between different areas of the foot in the antero-posterior direction and the medio-lateral direction and between different time points. The movement of the center of pressure (COP) during walking was also evaluated. Analyses were adjusted for body mass index and gait speed.

Results

The movement of COP was constant for both sexes. In all cases, the maximum load was observed on the medial of the foot. Women had a significantly higher peak pressure on the hallux, toes, forefoot, and medial aspect of the foot compared to men while standing and walking ( p  < .05).

Conclusions

A newly introduced in-shoe plantar pressure sensor demonstrated a typical loading transition pattern of the foot. Furthermore, higher plantar pressure in the forefoot was detected in healthy women as compared to men during standing and walking activities.

Peer Review reports

Introduction

Analysis of the loading condition of the sole during walking and running is vital to improve footwear design [ 1], sports performance analysis and injury prevention [ 2], balance control [ 3], and for diagnosing diseases [ 4]. Various foot pressure evaluation devices have been developed, and the currently available systems are categorized into the plantar platform system and the in-shoe system.

At present, over 50 different devices are used for foot loading analysis [ 5]. Some systems require specialized laboratories, whereas others require relatively expensive and delicate insoles with pressure sensors [ 6]. The in-shoe system is preferable over the plantar platform system because of its portability, simplicity, and applicability on various shoe types [ 7], and participants can perform natural movement during the experiment without the restriction of space and activity [ 8]. However, existing in-shoe systems are heavy and bulky, and induce unnatural movement, urging the need of a light and slim in-shoe type sensor.

Skeletal structure and muscular strength differ between women and men. However, the effect of sex on plantar pressure during activities remains undetermined. Putti et al. did not find any sex-based differences in plantar pressure while walking eight steps on the same walkway [ 9]. Darlene et al. reported that no significant differences were found in normalized plantar pressure values between men and women [ 10]. On the other hand, in some investigations, there was a significant difference in the peak pressure between men and women. Demirbuken et al. reported that higher toe peak pressure was identified more often in women than in men during early adolescence [ 11]. Chung et al. indicated that men had higher peak pressure in the medial toe and all forefoot areas than women [ 12]. McKay et al. reported that there was no significant difference between boys and girls aged 3-9 years, at ages 10-19, men had significantly higher midfoot peak pressure than women and at age 20 and older men had significantly higher rearfoot peak pressures than women [ 13].

To examine the effect of sex difference on plantar pressure, testing activities should be performed in positions as natural as possible, without any obstruction from the measurement.

Therefore, a slim plantar pressure sensor was newly developed to measure plantar pressure of healthy adults during unrestricted activities. The purpose of this study was to evaluate pressure distribution on the sole during gait and stance using the newly developed in-shoe measurement system and compare the results between sexes.

Materials and methods

Participants

One hundred healthy adult volunteers (50 women and 50 men) were included in the study. Demographic data are shown in Table 1. We analyzed both left and right feet in all 100 cases. There was no difference between left and right feet, and, therefore, the results of the left foot were presented. Participants were excluded if they had experienced foot pain within the previous 6 months, had previously undergone foot surgery, or had presented with congenital or acquired foot deformities on clinical examination. Demographics including age, sex, height, weight, and foot size were recorded. The study protocol was approved by the Institutional Review Board of our institution and written informed consent was obtained from all participants before their enrollment.

Table 1 Demographic data.

Measurement devices

The newly developed plantar pressure sensor (University of Fukui Graduate School of Engineering, Japan) has 10 sensors of 1 mm thickness and 12 g weight. They are connected to a measuring unit that has 200 Hz of sampling rate and is 17 g in weight (Fig. 1). Three sensors were placed on the toes, four on the forefoot, two on the midfoot, and one on the hindfoot. Four sizes (23 to 28 cm) of sports shoes and corresponding sizes of plantar pressure sensors were prepared to provide the best fit shoes for each participant.

Plantar pressure measurements. a Ten of the sensors are attached underneath the insole and connected to the measuring unit. The sensors are only 1 mm in thickness and total 12 g in weight. b The measuring unit is only 17 g in weight and collects data at 200 Hz. c The sensor is placed underneath the insole and connected to the measuring unit on the top of the foot

Measurement and analysis

The participants were allowed to acclimatise to the shoes by walking a minimum of 10 steps before data collection, which did not begin until the participant verified that they were comfortable. Each participant rested for 3 s after wearing the device, after which plantar pressure was measured while standing. Next, participants were instructed to walk at least 10 steps at a comfortable speed while the plantar pressure was recorded (Fig. 2). The maximum loading while walking was measured in the hallux (the sensor a), and the movement of the maximum loading point while walking was analyzed by evaluating in different areas of antero-posterior (AP) direction and medio-lateral (ML) direction (Fig. 3). The hallux was measured individually, considering that there might be a difference in the hallux between women and men because hallux valgus was more common in women. The prevalence of hallux valgus was 22.8% in Japan. The prevalence in women was 2.54 times higher than in men [ 14]. Results were compared between sexes by converting body mass index (BMI) to 22 and gait speed to 118 steps / min (Excel 2016, Microsoft and COP graph creator, University of Fukui Graduate School of Engineering, Japan). The gait speed was 120 ± 9 steps / min for women and 116 ± 11 steps / min for men and there was no significant difference between men and women. Since the overall average was 118 steps / min, we used that value for adjustment. The movement of COP during walking was analyzed in the AP and ML directions. When compared based on sex, the sensor was converted to 25.5 cm equivalent and calculated.

Plantar pressure during walking. Plantar pressure in each the toes, forefoot, midfoot and hindfoot area during walking. The maximum loading in each part reached its peak starting from the hindfoot, the midfoot and the forefoot, consistently

The evaluation of plantar pressure. a The value of the sensor a in the figure was defined as Hallux. b Areas for analyzing weight-bearing point in anteroposterior direction. The evaluation was divided into four parts: toes, forefoot, midfoot, and hindfoot, and the average value was calculated. c Areas for analyzing weight-bearing point in medio-lateral direction. The average value was calculated separately for the medial and lateral

Statistical analysis

A two-sample t-test was used for a sex-based comparison of the data (Excel 2016, Microsoft). For all analyses, statistical significance was set at P  < .05. All analyses except of demographic data was used Bonferroni's correction for multiple comparisons. All data were reported as the mean ± SD.

Results

Women had a significantly higher peak pressure on the hallux, toes, forefoot, and medial aspect of the foot compared to that of men during standing (Table 2. All; p < .05). Similar to the results during standing, a significantly higher peak pressure was observed on the hallux, toes, forefoot, and medial aspect of the foot in women than men during walking (Table 2, All; p < .05). In all cases, greater loading was applied to medial aspect of the foot in the middle of the stance phase than lateral. COP movements were similar across participants such that they translated from the hindfoot through the middle of the midfoot, and finally toward the base of the first toe (Fig. 4). There were no significant differences between sexes (Table 3, All; p  > .05).

Table 2 The state of standing and walking peak pressure.

The COP movement. A typical case of COP movement during walking. The COP movements were similar across participants such that it translated from the hindfoot through the middle of midfoot, finally toward the base of first toe

Table 3 The COP movement.

Discussion

The most important finding of this study was that women applied a significantly higher peak pressure on the hallux, toes, forefoot, and medial aspect of the foot while both standing and walking than men. Women have a higher pelvic tilt and a center of gravity anterior to men [ 15], which can result in higher plantar pressure at the toes and forefoot. The movement of knee-in while walking was likely to occur in women because of weaker gluteus medius strength compared to men [ 16]. Thus, the peak pressure at the medial aspect of the foot may be higher. In previous reports, the results regarding the difference in peak pressure between men and women were varied. Some reports indicated that there was no significant difference between men and women [ 9, 10], and some reports indicated that men have higher peak pressure in the medial toe and all forefoot areas than women [ 12]. On the other hand, higher toe peak pressure was identified more often in women than in men during early adolescence [ 11]. It is also reported that the peak pressure shifts from the hind foot to the forefoot depending on the age [ 13].

Technical improvement of the measurement system was demonstrated for evaluation of the plantar pressure during natural activities. The Pedar system (Novel gmbh, Munich, Germany) and F-scan system (Tekscan, Inc., Boston, MA) are the main models of the in-shoe plantar pressure measurement system in the previous studies [ 17, 18]. However, they are relatively heavy (The Pedar system; 400 g, F-scan system; 400 g) and bulky (The Pedar system; 600 cm ³, F-scan system; 300 cm ³). To evaluate natural walking, the size and weight of a measurement device should be as light and small as possible. The newly developed in-shoe device in the current study weighs 17 g and has a volume of 15 cm ³, making it possible to perform standing and walking with less interference than previous products. Additionally, conventional products have 50 Hz of sampling rate, whereas this device has 200 Hz of sampling rate. Therefore, the new system could have less chance to miss some instant and important changes of the plantar pressure during activities. The newly introduced device can be applied to faster movements, such as running and sports activities.

The COP is defined as the centroid of the total number of active sensors, which suggests the spatial distribution of pressure over time [ 19]. It has been suggested that the COP provides greater insight into dynamic foot function compared to pressure at discrete regions [ 20]. Buldt et al. reported a difference between the planus and a normal foot in relation to the medial shift of the lateral-medial force index during terminal stance [ 21]. In this study, COP movements were similar across healthy adult participants such that they translated from the hindfoot through the middle of the midfoot, and finally toward the base of the first toe. Future studies comparing healthy feet with pathological conditions, such as flat foot and hallux valgus, are warranted.

Although this study did not include cases of hallux valgus (HV), women had a higher plantar pressure at the hallux than men. Nix reported a meta-analysis that estimated that female HV prevalence (30%) was 2.3 times greater than in men (13%) [ 22]. Studies have reported plantar pressure in HV in the past; however, their results have been inconsistent. Some have reported a high plantar pressure on the hallux [ 23, 24], while others have reported an inverse correlation between severity and plantar pressure at the hallux [ 25]. There are various causes of HV; however, this sex-based difference in pressure can be suggested as one of the causes.

The findings of this study should be considered after taking into consideration five limitations. We have not recorded the foot posture of the participant in this study, however, according to a systematic review of foot posture by Buldt et al., there was a significant difference in peak pressure between the pes cavus, the pes planus, and the normal foot [ 6]. Since we selected healthy foot participants, it was considered that foot posture had little effect on peak pressure. We have not recorded the foot morphology of the participant in this study. Mahshid et al. reported that Japanese women had narrower feet in the heel and forefoot, and their instep, first and fifth toes and navicular height were also lower than men's [ 26]. Zhao et al. demonstrated that Japanese men generally had longer, larger and higher arched feet than women [ 27]. Since we adjusted the shoe size to 25.5 cm and compared, it was considered that foot morphology had little effect on peak pressure. Plantar pressure measurement systems are limited in that they only measure force perpendicular to the sensor surface. Therefore, other relevant forces including shear force cannot be measured. However, the current study examined the force during standing and walking when a vast majority of force is applied perpendicular to the foot. The influence of other related forces might be considered when more active sporting activities are involved, i.e. turning, stop-and-go motions. Footwear characteristics such as sole bending stiffness are likely to influence the parameters. To avoid this impact, the same shoes of different sizes were used in the current study; however, care should be taken when using different shoes in future studies. Lastly, although statistical significance was achieved in the comparisons, the sample size might be insufficient to apply this study result to the general population of wider age and/or other cultural backgrounds. It should be noted that the current study results stem from participants who were relatively younger than most foot and ankle patients, but older than most active sport athletes.

The current study result could be used to develop sex specific design of insole or shoes. Wearing appropriate shoes may help prevent foot and ankle pathological conditions. In addition, checking the COP movement may help improve gait balance and gait posture. In order to invent therapeutic ones, further detailed evaluations of plantar pressure in pathological feet are needed, and the new measurement tool might be applicable.

Conclusions

Women tend to put more pressure on the front and medial side of the foot during natural standing and walking than men.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding authors on reasonable request. Please contact authors for data requests (MD, PhD. Yuichi Hoshino - email address: yuichi-h@mta.biglobe.ne.jp).

Abbreviations

COP:

Center of pressure

AP:

Antero-posterior

ML:

Medio-lateral

HV:

Hallux valgus

Acknowledgements

The authors would like to thank Editage ( www.editage.jp) for the English language review. We wish to thank Mr. Kiryu Miyahira for his great assistance with collecting this study data.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Author information

Affiliations

1. Department of Orthopaedic Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-cho, Chuo-ku, Kobe, 650-0017, Japan

Tetsuya Yamamoto, Yuichi Hoshino, Noriyuki Kanzaki, Koji Nukuto, Takahiro Yamashita, Kazuyuki Ibaraki, Kanto Nagai, Daisuke Araki, Takehiko Matsushita & Ryosuke Kuroda

2. Human and Artificial Intelligent Systems, University of Fukui Graduate School of Engineering, Fukui, Japan

Kouki Nagamune

Contributions

TY, YH and NK were involved in study conception and design, data collection, data analysis and interpretation, and drafting the manuscript. KN, KI and KN were involved in data interpretation and contributed to drafting the manuscript. DA, TM and RK was involved in study design, data interpretation, and contributed to drafting the manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Yuichi Hoshino.

Ethics declarations

Ethics approval and consent to participate

The study protocol was approved by the institutional review board of Kobe University Graduate School of Medicine (No. B190150). Written informed consent was obtained from each participant.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Yamamoto, T., Hoshino, Y., Kanzaki, N. et al. Plantar pressure sensors indicate women to have a significantly higher peak pressure on the hallux, toes, forefoot, and medial of the foot compared to men. J Foot Ankle Res 13, 40 (2020). https://doi.org/10.1186/s13047-020-00410-2
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Keywords

Plantar pressure

In-shoe pressure sensor system

Sex difference

Center of pressure

# data[].attributes.attachment_link.title
Plantar pressure sensors indicate women to have a significantly higher peak pressure on the hallux, toes, forefoot, and medial of the foot compared to men - Journal of Foot and Ankle Research

# data[].attributes.attachment_link.description
Background Sex-related differences of plantar pressure distribution during activities should be thoroughly inspected as it can help establish treatment and prevention strategies for foot and ankle problems. In-shoe measurement systems are preferable without space and activity restrictions; however, previously reported systems are still heavy and bulky and induce unnatural movement.

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https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183883/

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Abstract

Background:

Unilateral offloading footwear prescribed to patients with diabetic foot ulcers elevates one limb relative to the other, which may lead to limp and abnormal gait. This study investigated whether the unilateral foot ulcer and offloading combination negatively impacts gait function beyond diabetic peripheral neuropathy.

Methods:

Eighty-six participants were recruited in 3 groups: 12 with diabetic peripheral neuropathy and unilateral foot ulcers wearing offloading footwear (offloading group, age=55.6±9.5years, BMI= 30.9±4.5kg/m ²), 27 with diabetic peripheral neuropathy (neuropathy group, age=64.3±7.7years, BMI= 30.9±5.4kg/m ²), and 47 non-diabetic controls (non-diabetic group, age=62.9±16.1years, BMI= 29.0±6.0kg/m ²). Gait function was quantified during a habitual speed walking test using a validated wearable platform.

Findings:

The offloading group exhibited deteriorated gait function compared to the non-diabetic group ( p<0.005, Cohen's effect size d=0.90-2.61). They also had decreased gait speed ( p<0.001, d=1.79) and stride length ( p<0.001, d=1.76), as well as increased gait cycle time ( p<0.001, d=1.67) and limp (p<0.050, d=0.72-1.49) compared to the neuropathy group. The offloading group showed increased gait unsteadiness compared to the neuropathy group, but the difference did not reach statistical significance in our samples.

Interpretation:

This study demonstrated that while diabetic peripheral neuropathy deteriorates gait function, including increasing gait unsteadiness and limp, the diabetic foot ulcer and offloading combination magnifies the deterioration beyond diabetic peripheral neuropathy. These findings promote caution of the current standards of care for treating diabetic foot ulcers with offloading footwear. However, it is possible that a contralateral shoe lift may remedy deteriorated gait function and improve quality of life for unilateral offloading users.

Keywords: diabetic foot ulcers, offloading, diabetic peripheral neuropathy, gait function, limp, gait unsteadiness

1. Introduction

Diabetic foot ulcers (DFUs) are a burden to people with diabetes and the health care system. Affecting up to one-third of people with diabetes, DFUs are the most common complication associated with diabetes mellitus [ 1- 3]. These wounds often lead to infections [ 4] and lower extremity amputations, costing US health care systems greater than $10 billion annually [ 5]. DFUs cause deterioration in gait function, which is the major determinant of an independent and productive life and is essential for predicting poor quality of life, morbidity, and mortality [ 6]. Literature reports that people with DFUs ambulate with slower gait speed and shorter step lengths compared to healthy individuals [ 7]. DFUs are also reported to hinder gait initiation, resulting in a greater distance and number of steps to reach steady state ambulation [ 8, 9]. Without timely intervention, gait function deterioration among people with DFUs may lead to serious adverse outcomes, including worsening DFUs, amputation, early frailty, risk of falling, and loss of independency, all of which may further complicate their conditions [ 10- 12].

Offloading devices are commonly prescribed to people with DFUs [ 13]. These devices redistribute plantar pressure and manage excessive plantar tissue stress in order to heal and prevent DFU formation [ 14- 17]. While several studies have demonstrated the effectiveness of offloading devices in improving foot health, other studies have shed light on the detrimental effects that offloading devices impose on gait and mobility [ 15, 18- 21]. Offloading devices reduce gait speed [ 22] and ankle motion if the device crosses the ankle joint, which limits propulsion during gait [ 16, 23]. More importantly, if used unilaterally, offloading footwear may elevate one limb relative to the other [ 22, 23]. This induced limb elevation is sometimes as high as 5 cm [ 24] and has been shown to decrease gait speed in both people with diabetes [ 25] and healthy individuals [ 22, 23]. Uneven limb elevation due to offloading footwear may also create asymmetry in step length between the right and left limbs, resulting in a limp while walking.

Diabetic peripheral neuropathy (DPN) is a common comorbidity seen among people with diabetes and DFUs [ 3, 26]. DPN is a dysfunction of the peripheral nerves, resulting in the loss of sensation of the extremities. This loss of sensation increases difficulty to maintain normal gait patterns [ 8, 9, 27- 29] and increases the risk of developing DFUs [ 1, 4, 17, 30]. Currently, most studies only focus on how DPN deteriorates gait function, but few studies evaluate the impact of DFUs and offloading devices on gait function. Considering the frequent use of offloading devices for patients with DFUs and DPN, it is important for clinicians to be aware of any effects that DFUs and offloading devices impose on gait.

In this study, we used a validated wearable platform to objectively quantify gait function in patients with DPN and DFUs wearing offloading devices. We proposed to determine the magnitude of gait deterioration potentially caused by DFUs and offloading devices beyond diabetes and DPN. To examine the degree of degradation in gait function caused by DFUs and offloading devices, we compared gait performances among people with DPN and DFUs wearing offloading devices to those with DPN but without DFUs, as well as to age-matched non-diabetic controls. The hypotheses of this study were: (1) compared to age-matched, non-diabetic controls, people with DPN and DFUs using an offloading device have poorer gait function; (2) DFUs and offloading devices magnify the decline in gait function beyond DPN, including limp caused by offloading-induced limb elevation imbalance.

2. Methods

Eighty-six eligible participants were recruited in this study: 12 participants with DPN and unilateral DFUs wearing offloading footwear (Offloading), 27 participants with DPN but no foot ulcer (DPN), and 47 age-matched non-diabetic controls (ND). Status of an active foot ulcer was confirmed by the clinical investigator for the Offloading group. Participants in the Offloading group wore unilateral forefoot-offloading wedge shoes prescribed by their Podiatrist and their habitual closed-toe and closed-heel athletic shoe on the contralateral limb. Although contralateral footwear was not standardized, all contralateral footwear had a standard heel height and did not exhibit any characteristics that would alter gait. Participants were excluded from the study if they were non-ambulatory, had severe gait or balance problems (e.g., unable to walk a distance of 15 m independently with or without assistive devices or unable to stand still without moving feet), or were unwilling to participate. All participants signed a consent form prior to participation. This study was approved by the local institutional review board.

Participants' demographics, including age, sex, height, weight, and body-mass-index (BMI), were collected. For all participants, five wearable sensors (LEGSys™, BioSensics, Watertown, MA, USA) were attached to the following locations: (1) dorsum of back; (2) anterior right thigh; (3) anterior left thigh; (4) anterior right shin; (5) anterior left shin, to quantify gait parameters of interest () [ 31]. Participants were asked to walk at their habitual gait speed for 10 meters without any distraction using the protocol described in our previous studies [ 29, 32]. The gait test was performed with an investigator walking alongside the participant to aid in stability, if needed, during the trial. Gait parameters were calculated during steady state phase of walking using validated algorithms [ 33- 35]. Steady state phase of gait was estimated using the algorithm suggested by Lindeman et al. [ 36].The evaluated gait parameters included gait speed and gait speed unsteadiness, stride length and stride length unsteadiness, gait cycle time, double support and double support limp, as well as step length limp. Gait speed unsteadiness was defined as coefficient of variation of stride-to-stride velocity during steady-state of walking [ 35, 37]. To determine gait symmetry, we estimated double support limp and step length limp. Double support limp was estimated by calculating the absolute difference between initial and terminal double support [ 34]. Step length limp was estimated by the percentage of difference between right and left step lengths [ 38].

All continuous data were presented as mean (standard error). All categorical data were expressed as percentage of the sample size. Analysis of variance (ANOVA) was used for between-group comparison of continuous demographics. Analysis of Chi-square was used for comparison of categorical demographics. In order to control for the effects of demographics on gait performance, analysis of covariance (ANCOVA) was employed to compare between-group gait performance, with adjustment for BMI and gender. Fisher's least significant difference-based post-hoc test was performed for pairwise comparison to explore significant main effects and interactions. Cohen's d effect size was calculated to assess the magnitude of difference between each group. Values ranging from 0.20 to 0.49 indicated small, and values between 0.50 and 0.79 indicated medium effects. Values ranging from 0.80 to 1.29 indicated large, and values above 1.30 indicated very large effects. Values less than 0.20 were considered as having no noticeable effect [ 39]. For all comparisons, significance was accepted at p<0.050. All statistical analyses were performed using IBM SPSS Statistics 25 (IBM, Chicago, IL).

3. Results

summarizes the analysis of demographic and clinical data. The three groups were matched with age and BMI. However, the DPN group and Offloading group had significantly less females than the ND group ( p=0.015).

Table 1.

The Offloading group demonstrated deteriorated gait performance compared to both the ND and DPN groups (). Compared to the ND group, the Offloading group had reduced gait speed ( p<0.001, d=2.61, ) and stride length ( p<0.001, d=2.51), as well as increased gait cycle time ( p<0.001, d=2.13) and double support ( p=0.001, d=1.19). Compared to the DPN group, the Offloading group also had poorer gait performance in gait speed ( p<0.001, d=1.79, ), stride length ( p<0.001, d=1.76), and gait cycle time ( p<0.001, d=1.67).

Table 2.

For gait variability, the Offloading group had increased gait speed unsteadiness ( p=0.004, d=0.96) and stride length unsteadiness ( p=0.004, d=0.97, ) compared to the ND group. At the same time, the Offloading group showed larger gait unsteadiness than the DPN group, however the between-group difference was not statistically significant ( p>0.050).

For gait symmetry, the DPN group and the ND group had similar performances ( p>0.050). However, compared to both the ND and DPN groups, the Offloading group showed significantly increased double support limp ( p=0.007, d=0.90 and p=0.041, d=0.72, respectively) and step length limp ( p<0.001, d=1.46 and p<0.001, d=1.49, respectively, ).

4. Discussion

In this study, we examined how unilateral DFUs and offloading footwear may alter gait function beyond sensory feedback alteration caused by diabetes and peripheral neuropathy. We were able to confirm our hypothesis that people with DPN and DFUs wearing offloading devices have poorer gait function compared to healthy controls. We were also able to confirm our hypothesis that DFUs and offloading devices further deteriorate gait beyond DPN, specifically for performance in gait speed, stride length, gait cycle time, and gait symmetry. However, the effects of the DFU and offloading footwear combination on other gait parameters of interest, including double support, gait speed unsteadiness, and stride length unsteadiness, were small to medium ( d=0.32-0.50), which didn't achieve statistical significance in our sample. A few previous studies have reported deteriorated gait in people with DFUs [ 7, 8], and those wearing offloading devices [ 15, 22, 23], which is consistent with findings in this current study. However, none of the previous studies compared gait function of the DFU and offloading population with cohorts of well-established gait impairment models, such as people with DPN, as this current study did.

Compared to the ND group, the Offloading group had significantly worsened gait performance, including gait unsteadiness and limp. However, when comparing between the Offloading group and the DPN group, gait unsteadiness was not found to significantly differ in our sample. A previous study demonstrated similar findings in regards to the coefficient of variability for stride velocity [ 8]. This shows that the DFU and offloading footwear combination may alter gait speed and gait symmetry, but may not have much influence beyond DPN to cause inter-stride difference. We speculate that gait unsteadiness is mainly related to cognitive performance and autonomic nervous system [ 40], but is less affected by limb discrepancy. However, the altered gait symmetry could lead to potential adverse outcomes, such as increased risk of falls, reduced gait efficiency, joint pain, and formation of DFUs on the contralateral side [ 10- 12].

Previous studies have posed potential remedies for improving gait function in people who wear offloading footwear. Crews et al. demonstrated that using a contralateral shoe lift with unilateral offloading footwear reduces variability in walking velocity [ 25]. Another study reported that normal gait patterns were achieved in unilateral offloading users when a walking boot heel-sole profile matched the height of the contralateral walking shoe [ 23]. It is possible that using a shoe lift could potentially reduce gait unsteadiness and asymmetry for those with unilateral DFUs who wear offloading footwear. Future studies are needed to verify this hypothesis.

The small sample size was the major limitation in this study. Other limitations include a relatively shorter walking distance for the testing protocol compared to protocols used in other studies that studied gait variability in general older adults [ 35, 36]. However, for patients with diabetic neuropathy and (risk of) diabetic foot ulcers, the relatively shorter walking distance of 10-meter has been suggested [ 41- 43]. Additionally, the type of footwear worn by participants was not standardized. In this study, all people with diabetes wore prescribed diabetic shoes and participants in the control group were asked to wear regular footwear without excessive heels (higher than 2.5cm). No participants wore sandals or other types of footwear that may alter gait. We used this test protocol, as we believe testing participants with their daily footwear can more accurately represent gait presentation in daily life compared to a standardized shoe. Furthermore, duration of experience wearing an offloading device was not considered when analyzing results. However, this allows our results to reflect how offloading footwear may affect gait performance regardless of wear experience.

5. Conclusions

This study demonstrated that while DPN deteriorates gait function, including increasing gait unsteadiness and gait asymmetry (limp), the DFU and offloading combination magnifies the deterioration beyond DPN. These findings promote caution of the current standards of care for treating DFUs with offloading footwear. However, it is possible that a contralateral shoe lift may remedy deteriorated gait function and improve quality of life for unilateral offloading users. Future studies are needed to verify the findings of this study in a larger sample size.

​

Unilateral foot ulcers and offloading footwear deteriorate gait beyond neuropathy

Unilateral foot ulcers and offloading footwear deteriorate gait speed and symmetry

A contralateral shoe lift may improve gait in unilateral offloading users

7. Acknowledgments

We thank Hanger, Inc. for permitting participant recruitment and data collection at their facilities.

6. Funding

Partial support was provided by the National Institutes of Health/National Institute on Aging (Award No. R42-AG032748) and the Qatar National Research Foundation (Award No. NPRP 7-1595-3-405). The content is solely the responsibility of the authors and does not necessarily represent the official views of sponsors.

Footnotes

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8. Declarations of Interest:

None

9. References

7. Fernando ME, et al., Gait parameters of people with diabetes-related neuropathic plantar foot ulcers. Clinical Biomechanics, 2016. 37: p. 98-107. [[ PubMed] Google Scholar]

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17. Lazzarini PA, et al., Measuring Plantar Tissue Stress in People With Diabetic Peripheral Neuropathy: A Critical Concept in Diabetic Foot Management. J Diabetes Sci Technol, 2019: p. 1932296819849092. [ PubMed] PMC free article] [

22. Gulgin H, et al., 3D gait analysis with and without an orthopedic walking boot. Gait & posture, 2018. 59: p. 76-82. [[ PubMed] Google Scholar]

25. Crews RT and Candela J, Decreasing an Offloading Device's Size and Offsetting Its Imposed Limb Length Discrepancy Lead to Improved Comfort and Gait. Diabetes care, 2018: p. dc172584. [ PubMed] PMC free article] [

32. Zhou H, et al., Instrumented Trail-Making Task: Application of Wearable Sensor to Determine Physical Frailty Phenotypes. Gerontology, 2018: p. 1-12. [ PubMed] PMC free article] [

33. Najafi B, Khan T, and Wrobel J, Laboratory in a box: wearable sensors and its advantages for gait analysis. Conf Proc IEEE Eng Med Biol Soc, 2011. 2011: p. 6507-10. [[ PubMed] Google Scholar]

39. Cohen J, Statistical power analysis for the behavioural sciences. 1988, Hillsdale, NJ: erlbaum. [ Google Scholar]

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The impact of diabetic foot ulcers and unilateral offloading footwear on gait in people with diabetes.

# data[].attributes.attachment_link.description
Unilateral offloading footwear prescribed to patients with diabetic foot ulcers elevates one limb relative to the other, which may lead to limp and abnormal gait. This study investigated whether the unilateral foot ulcer and offloading combination negatively impacts gait function beyond diabetic peripheral neuropathy.

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Foot posture in people with medial compartment OA

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Artikel - journal of foot and ankle research 

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Journal of Foot and Ankle Research 9, Article number: 14 (2016) Cite this article

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Abstract

Background

The complex relationship between foot posture, flexibility, body mass and age in children is not well understood. The objectives of this post hoc analysis were to explore the relationships between foot posture, flexibility, body mass in children aged seven to 15 years.

Methods

Thirty healthy, asymptomatic children (20 girls, 10 boys) aged 7 to 15 years with a mean age (SD) of 10.7 (2.3) years, were recruited through the Auckland University of Technology (AUT) Podiatry Clinic, Auckland, New Zealand. Clinical data were collected by a podiatrist with 20 years' experience and included: height and weight (for Body Mass Index), Foot Posture Index-6 (FPI), Beighton score, Lower Limb Assessment Scale score (LLAS); and ankle lunge angle. For this post hoc analysis, Pearson's test and Spearman's rho were used to explore relationships between variables. Statistical significance level was p  < 0.05.

Results

Data for each of the 30 participants for each variable were included in analyses, which returned the following statistically significant results: higher FPI was associated moderately with higher Beighton score ( r = 0.44, p = 0.01); greater lunge angle was associated moderately with higher Beighton ( r = 0.40, p = 0.02) and LLAS ( r = 0.42, p = 0.02) scores; older age was associated strongly with higher BMI ( r = 0.52, p = <0.01) and moderately with lower Beighton ( r = −0.41, p = 0.024) and LLAS ( r = −0.40, p = 0.03) scores; and higher Beighton score was associated strongly with higher LLAS ( r = 0.85, p = <0.01). There was no difference in foot posture between girls and boys ( p  = 0.21).

Conclusions

In this sample of healthy, asymptomatic children age 7 to 15 years, children with a more pronated foot type exhibited greater lower limb and whole-body flexibility, but not greater ankle joint flexibility. There was strong agreement between lower-limb and whole-body flexibility. This study highlights the importance of assessing the paediatric flat foot in the context of a developing body.

Peer Review reports

Background

The complex relationship between foot posture, flexibility, body mass and age in children is not well understood. As discrete factors, age, body mass, and joint flexibility have each been associated with variance in paediatric foot posture [ 1- 3]. In a study of 835 Austrian children age three to six years, Pfeiffer [ 1] reported that age, body weight, and gender correlated with flat foot posture; with younger, heavier boys having flatter feet. Similarly, a study of 1598 children of the same age in Taiwan found correlation between age, body weight, gender, joint flexibility, habitual W-sitting and flat foot posture [ 2]. This study illustrated that bilateral flat foot posture reduces with the child's age, but may be retained or increased in boys who are overweight for their age, have increased joint flexibility, and/or sit in the W-position [ 2].

Some critique of these studies is in order given the young ages of the children examined (when flatfoot is morphologically expected) and given the rudimentary methods of identifying flatfeet, which were not reportedly tested for repeatability. Both the Pfeiffer [ 1] and Chen [ 2] studies identified flatfoot by the visualised appearance of the medial arch, supplemented by heel position in the Pfeiffer study [ 1]. Of the young children examined, Pfeiffer [ 1] identified flatfoot in 44 %, and Chen identified bilateral flatfoot decreasing with age from 55 % at age 3 years to 21 % at age 6 years. Chen [ 2] visually identified children as having flat or normal feet, and then subdivided children with flat foot posture into bilateral and unilateral presentations, and, in the latter, age and obesity were not associated with the child's unilateral flat foot posture. The difference in bilateral and unilateral flatfoot presentations deserves attention, as the findings were discrepant. While Chen [ 2] found reducing prevalence of bilateral flatfoot from 3 to 6 years of age, unilateral flatfoot was detected in 14 % of three year old children, and 18 % of children aged six years [ 2]. Given the criteria by which foot posture was assessed and the age of the children when they are seldom still, these findings may be imprecise. Interestingly, the same authors did not address laterality in two subsequent studies of the same cohort, having then adopted less subjective footprint analysis of foot posture instead of visual assessment [ 3, 4].

A larger Taiwanese investigation of 2083 older children aged 7 to 12 years, also found correlation between flatfoot and age, gender and body weight [ 5]. This study used static footprints to assess foot posture, and then categorised the visual appearance of the footprints: normal and grades 1 to 3 indicating increasing medial arch loading, surmised to indicate a flatter foot. Acquiescent with previous studies [ 1, 2] flatter feet were most prevalent in younger, overweight/obese boys, but clearly the method of foot posture assessment differed as did the age group of the children examined. Chang [ 5] also found reducing flatfoot with age (69.8 % at age 7 years to 39.0 % at age 12 years), but in a non-linear manner. Given the subjective classification system of the footprints, and the combining of moderate and severe categories, the prevalence of flatfoot as presented by Chang et al. [ 5] is perhaps less useful than assessing the associations between the individual gradings of foot posture and factors such as age, BMI and gender. Many of the different grading and scoring systems for flatfeet are largely subjective. In contrast, the FPI is a superior method with gradings identified in a more rigorous way.

The relationship between paediatric foot posture and the correlates of body mass, joint flexibility, age and gender have been investigated [ 2, 5- 8], but using variably defined methods in children whose ages have differed. The objectives of this post hoc analysis were to: (1) explore, using validated and reliable methods, the relationships between foot posture, flexibility, body mass in children aged seven to 15 years in Auckland, New Zealand; and (2) explore difference in foot posture between girls and boys in the same sample.

Methods

Between February 2011 and March 2012, a convenience sample of thirty healthy, asymptomatic children with no history of foot injury or surgery, and not reporting current foot pain, aged between 7 and 15 years were recruited through the Auckland University of Technology (AUT) Podiatry Clinic, Auckland, New Zealand. The AUT Ethics Committee approved the study (approval number 10/291) and parents/guardians provided written informed consent.

Age, gender and ethnicity were recorded to characterise the sample. Clinical data collected were: Body Mass Index, left Foot Posture Index-6 (FPI) [ 9], Beighton Scale score [ 10], Lower Limb Assessment Scale score (LLAS) [ 11]; and left ankle lunge angle [ 12]. The order of physical measures was consistent among participants. One podiatrist with 20 years' experience (AE) performed all tests. We demonstrated excellent test-retest reliability (intra-class correlation coefficient >0.85 [mean 95 % CI 0.86-0.97]) for all clinical measures [ 7, 13].

Procedure

FPI-6 for the left foot only [ 14] was measured following a published protocol [ 9]. FPI was measured after the patient took five or more steps on the spot and came to rest in a comfortable standing position with arms by their sides and looking straight ahead. Each foot was scored using six criteria: (1) talar head palpation; (2) curves above and below the lateral malleolus; (3) inversion/eversion of the calcaneus; (4) bulge in the region of the talonavicular joint; (5) congruence of the medial longitudinal arch; and (6) abduction/adduction of the forefoot on the rearfoot. Each criterion was given a score between-2 and 2, where scores less than zero indicate a supinated alignment and scores greater than zero indicate a pronated alignment. Scores of all criteria were added together to create an overall score for each foot from-12 (most supinated) to +12 (most pronated).

The Beighton scale [ 10] was rated to ascertain the presence of joint hypermobility at the wrist, fifth metacarpal phalangeal joint, elbow, knee (all bilateral and non-weight-bearing) and the lumbo-sacral spine (forward flexion, in stance). The Beighton scale yields a score out of 9-points, whereby the arbitrary cut-off of 5/9 or greater conventionally indicates joint hypermobility [ 10].

The LLAS [ 11] was assessed to gauge joint hypermobility of the lower limb. One point is awarded per limb for each of the following: (1) hip flexion where the anterior thigh contacts the chest; (2) hip abduction where the lateral femoral condyles touch the plinth; (3) knee hyperextension where the heels lifts >3 cm from the plinth when the foot is lifted when in a long sitting position; (4) positive knee anterior draw test; (5) > 1 cm medial or lateral, or > 2 cm overall rotation of the tibia at the knee; (6) >15° ankle dorsiflexion when the knee is flexed; (7) positive ankle anterior draw test; (8) >45° subtalar joint inversion with lateral prominence of the talar head assessed non-weight-bearing; (9) >45° midtarsal joint inversion; (10) >1 cm midtarsal abduction/dorsiflexion and adduction/plantarflexion; (11) >90° 1st metatarsophalangeal joint dorsiflexion; (12) subtalar joint at end range of pronation when weightbearing. Each limb yields a final score out of 12-points, whereby the cut-off of 7/12 or greater conventionally indicates joint hypermobility [ 11]. In this study only the left leg was assessed, and given a score out of 12-points.

Weight-bearing ankle dorsiflexion range of the left limb only [ 14] was assessed using the Lunge test [ 12, 15], a weight-bearing measure of ankle (talocrural joint) dorsiflexion range when the knee is flexed. The participant stood on a solid, horizontal surface facing a solid, vertical wall with both hands resting on the wall for support. The testing foot was placed perpendicular to the wall (to limit dorsiflexion through subtalar and midfoot joints), and the contralateral foot was placed in a comfortable, stable position. The test involved the participant lunging the knee as far forward as possible over the foot whilst maintaining the heel on the floor. At the maximum lunge point, the investigator recorded the angle of the tibia to the vertical as a measure of ankle dorsiflexion using a digital inclinometer (Smart Tool™) applied to the anterior surface of the tibia.

Data analysis

Data were transcribed to SPSS version 20 (SPSS, Inc., Chicago, IL, USA). As this is a post hoc analysis of existing data, no power calculation was conducted. Descriptive statistics were used to characterise the sample.

Age, BMI, ankle lunge, Beighton score and LLAS were analysed as continuous data. Normality and symmetry was assessed using histograms and the Kolmogorov-Smirnov test. Relationships between continuous variables were explored with Pearson's point-biserial correlation coefficient for normally distributed continuous data and Spearman's rho for non-normally distributed continuous data. As FPI raw scores were normally distributed (Kolmogorov-Smirnov test p = 0.08; mean and median within 10 %; skewness and kurtosis values between-1 and 1) FPI was also analysed as continuous data rather than as categorical data [ 9]. An independent sample t-test with statistical significance level of p < 0.05 was conducted to explore difference in foot posture between girls and boys. The magnitude of effect sizes was estimated using the following parameters suggested by Cohen [ 16]: small (weak) = 0.1, medium (moderate) = 0.3 and large (strong) = 0.5. Due to limitations imposed by the sample size, regression analysis to determine dependence and independence of relationships was not performed [ 17].

Results

Thirty children (20 girls, 10 boys) age 7 to 15 years with a mean (SD) of 10.7 (2.3) years participated. Ethnicity was reported by parent/guardian as Caucasian for 27 (90 %) children, Asian for 2 (7 %) children and Maori for 1 (3 %) child. Descriptive statistics are presented in Table 1 and the strength and direction of relationships between variables are presented in Table 2.

Table 1 Demographic Characteristics

Table 2 Relationship Between Variables (R-value and p-value)

Higher FPI was associated with higher Beighton score ( r = 0.44, p = 0.01). Greater lunge angle was associated with higher Beighton ( r = 0.40, p = 0.02) and LLAS ( r = 0.42, p = 0.02) scores. Older age was associated with higher BMI ( r = 0.52, p = <0.01) and lower Beighton ( r = −0.41, p = 0.02), and LLAS ( r = −0.40, p = 0.03) scores. Higher Beighton score was associated with higher LLAS ( r = 0.85, p = <0.01). There was no statistically significant association between FPI with BMI ( r = 0.14, p = 0.48), ankle lunge ( r = 0.17, p = 0.36), LLAS ( r = 0.27, p = 0.16) or age ( r = −0.01, p  = 0.98). The difference between Foot Posture Index total scores for girls with a mean (SD) of 2.5 (2.5) and boys with a mean (SD) of 3.6 (1.8) was not significant (p = 0.21).

Discussion

The findings were commensurate with previously reported investigations [ 1, 2], in that a relationship was found between flatter foot posture and joint flexibility. In contrast, there was no relationship detected between foot posture and age, body mass index or gender.

This study agreed with several previous investigations in finding that children with a flatter foot posture exhibited greater lower limb and whole-body flexibility [ 4, 5]. The findings of this study also indicate that increased flexibility is correlated between three reliable clinical measures: LLAS, Beighton scale, and the ankle lunge [ 6]. However, whilst flatfoot correlated with whole body and lower limb flexibility as detected by the Beighton scale and the LLAS respectively, there was no significant relationship between flatfoot and increased flexibility of ankle lunge. In essence, it appears that whole body hypermobility may be associated with increased ankle dorsiflexion and flatfoot. The relationship between foot pronation and joint flexibility may need to be considered in children who are presenting with symptomatic flatfoot.

This study found strong agreement between lower-limb and whole-body flexibility, and medium strength agreement between ankle flexibility with lower-limb and whole-body flexibility. The lesser strength of association between ankle flexibility and the other measures of flexibility may be due to the functional demands placed on the calf musculature in gait, which differs between children depending on their gait style (for example, increased demand and possible subsequent calf tightness in toe walking). Importantly, there was no notable association between foot posture and ankle flexibility.

Within this convenience sample of normal children, the older children exhibited less lower limb and whole-body flexibility, but not less ankle joint flexibility. Given the small sample size and defined age range within childhood, this may indicate that ankle joint range remains static at these ages, or that this finding was specific to this cross-sectional set of observations, rather than generalizable. Given the morbidity associated with hypermobility which may persist across the lifespan [ 18], it is important that clinicians recognise and appreciate the impact of this presentation, which is too often disregarded as being benign or even advantageous [ 19]. Whilst there was no significant difference detected between foot posture and gender in this study, the small sample size may have underpowered analysis. However, there is the supported expectation that the foot posture of children across the bounds of the age group of this study (7 to 15 years) will vary; less so in those aged 10-15 years, and more so in those aged 7-10 years [ 5, 20]. Clinically children in their first decade are more likely to have flatter feet when younger, overweight and male [ 21, 22]. The adult foot posture and less variation is expected after age 10 years, where flatfeet are less common, or may be associated with specific physiology viz. connective tissue hypermobility [ 23].

This is a cross-sectional study so no inferences should be made about cause-effect relationships. The convenience sample included predominately Caucasian children who were all asymptomatic and between the ages of 7 and 15 years. Gender distribution was uneven. Results should not be generalised outside of this population, for example to adults, younger children or symptomatic people. FPI, Beighton score and LLAS data were statistically analysed using non-parametric tests. Children with unilateral flatfoot were not excluded. This should be considered when planning eligibility criteria for future studies.

There is a growing evidence base for factors associated with flat foot in children. There is a need for prospective observational studies to investigate potential predictors of flatfeet in children. Additional studies spanning from childhood, through adolescence to adulthood will provide important information about the evolution of flatfoot and strengthen the evidence base for decisions about treatment of children with asymptomatic flat feet.

Conclusion

In this sample of healthy, asymptomatic children age 7 to 15 years, children with a more pronated foot type exhibited greater lower limb and whole-body flexibility, but not greater ankle joint flexibility. Older children exhibited less lower-limb and whole-body flexibility, but not ankle joint flexibility. Higher body mass index was not associated with a more pronated foot type and there was no important relationship between age and foot posture. There was strong agreement between lower-limb and whole-body flexibility. A large longitudinal study is required to explore potential predictors of foot posture throughout development and to investigate the independence of relationships between variables. Such an investigation needs to incorporate measures of foot posture which are demonstrably robust.

Abbreviations

BMI:

body mass index

FPI:

foot posture index-6

LLAS:

lower limb assessment scale score

SD:

standard deviation

References

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Acknowledgement

The original project was funded by AUT summer studentship. This post- hoc analysis was unfunded.

Author information

Affiliations

1. School of Health Sciences, University of Newcastle, Ourimbah, NSW, Australia

Fiona Hawke

2. Health & Research Rehabilitation Institute, School of Podiatry, AUT University, Auckland, New Zealand

Keith Rome

3. Discipline of Podiatry, College of Science, Health, and Engineering, La Trobe University, Victoria, 3086, Australia

Angela Margaret Evans

Corresponding author

Correspondence to Fiona Hawke.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

AE and KR conceived the design of the original study. AE collected the data. FH suggested the post hoc analysis reported in this paper. FH analysed and interpreted the data. All authors were involved in drafting the manuscript and have given final approval of the version to be published. All authors read and approved the final manuscript.

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Hawke, F., Rome, K. & Evans, A.M. The relationship between foot posture, body mass, age and ankle, lower-limb and whole-body flexibility in healthy children aged 7 to 15 years. J Foot Ankle Res 9, 14 (2016). https://doi.org/10.1186/s13047-016-0144-7
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Foot posture

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The relationship between foot posture, body mass, age and ankle, lower-limb and whole-body flexibility in healthy children aged 7 to 15 years - Journal of Foot and Ankle Research

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Background The complex relationship between foot posture, flexibility, body mass and age in children is not well understood. The objectives of this post hoc analysis were to explore the relationships between foot posture, flexibility, body mass in children aged seven to 15 years.

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Abstract

Background

High plantar pressures are associated with increased foot ulcer risk in people with diabetes. Identification of high plantar pressures in people with diabetes is clinically challenging due to time and cost constraints of plantar pressure testing. Factors affecting foot biomechanics, including reduced joint range of motion and foot deformity, are implicated in the development of high plantar pressures and may provide a method to clinically identify those at risk of pressure related complications. The aim of this study was to investigate the contribution of joint range of motion and foot deformity measures on plantar pressures in a community dwelling group with diabetes.

Methods

Barefoot (Tekscan HR Mat™) and in-shoe (Novel Pedar-X®) plantar pressure variables, weight bearing ankle dorsiflexion, hallux range of motion, lesser toe deformities and hallux abductus (HAV) scale were assessed in 136 adults with diabetes (52.2% male; mean age 68.4 years). Multivariate multiple linear regression was used to assess the effect of the four biomechanical factors plus neuropathy and body mass index on plantar pressure variables. Non-parametric bootstrapping was employed to determine the difference in plantar pressure variables for participants with two or more foot biomechanical pathologies compared to those with less than two pathologies.

Results

Almost one third (32%) of the cohort had two or more foot biomechanical pathologies. Participants with two or more foot biomechanical pathologies displayed significant increases in all barefoot plantar pressure regions (except forefoot), compared to those with less than two pathologies. No significant changes were found for the in-shoe plantar pressure variables. The regression model explains between 9.9% (95%CI: 8.4 to 11.4%) and 29.6% (95% CI: 28.2 to 31%), and between 2.5% (1.0 to 4.0%) and 43.8% (95% CI: 42.5-44.9%), of the variance in the barefoot and in-shoe plantar pressure variables respectively.

Conclusions

Participants presenting with two or more factors affecting foot biomechanics displayed higher peak pressures and pressure time integrals in all foot regions compared to those with less than two factors. The tests used in this study could help clinicians detect elevated plantar pressures in people with diabetes and present an opportunity for early preventative interventions.

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Background

Identification and subsequent early treatment of clinical factors that contribute to increased risk of foot ulcer and amputation in people with diabetes should be a high priority for primary care clinicians. In 2017 it was estimated that 8.8% of adults worldwide had diabetes, and this is expected to increase to greater than 10% by 2045 [ 1]. Diabetes-related foot ulcer (DFU) is one of the most common diabetes-related complications, with a lifetime risk of a DFU between 15 and 34% [ 2, 3], and a global prevalence of DFU of 6.3% [ 4]. Prevention of initial DFU, and the recurrence of DFU, is crucial as the evidence shows that up to 85% of lower extremity amputations are preceded by DFU [ 5]. In addition to the high personal costs of DFU and amputation, there are also high associated medical costs, with 20 to 30% of all diabetes-related health care costs spent on foot complications [ 6, 7].

Peripheral neuropathy is widely recognised as a critical factor in the development of DFU [ 5], and considerable effort has been dedicated to developing tests that allow clinicians to detect neuropathy with minimal time and cost. These include a 10-g Semmes-Weinsten monofilament, 128-Hz tuning fork, pinprick sensation, ankle reflexes and vibration perception threshold testing using a neurothesiometer [ 8]. As a result, neuropathy is regularly tested in clinical practice [ 9]. The International Working Group on the Diabetic Foot (IWGDF) guidelines state that high plantar pressures are also a significant independent risk factor for DFU and should therefore be avoided [ 10]. Elevated plantar pressures have been associated both prospectively and retrospectively with increased DFU risk in people with diabetes [ 11, 12, 13], with DFU recurrence [ 14], and may also be predictive in determining specific plantar sites prone to ulceration [ 12, 15]. However, the cost of plantar pressure testing equipment and the time required for testing and evaluation of data means it is not widely used in general clinical practice [ 10]. Identification of risk of elevated plantar pressures, by clinic based measures where plantar pressure testing is unavailable, will assist clinicians in determining treatment plans.

Therefore, the aims of this study were to investigate the prevalence of easily measured foot deformities and joint limitations that have been shown to increase plantar pressures [ 16], in a largely low risk community dwelling group with diabetes. Then, to examine the effect of these factors, plus other factors also associated with elevated plantar pressures (peripheral neuropathy and body mass index [ 17, 18]) on barefoot and in-shoe plantar pressures. Screening for these factors, individually and in combination, where plantar pressure testing is not available, may provide an early indication of increased ulcer risk in people with diabetes. Early referral of suspected higher risk patients for plantar pressure testing, or initiation of conservative therapies designed to reduce plantar pressures may help preserve functional limbs in this population.

Methods

Participants

Participants were recruited from the University of Newcastle Podiatry Clinic at Wyong Hospital, NSW Australia and from newspaper advertisements in local newspapers, between June 2016 and October 2017. Inclusion criteria were adults, 18 years of age and over, ability to speak and read basic English, and a diagnosis of either type 1 or type 2 diabetes only. Exclusion criteria were existing DFU affecting plantar pressure measurement, any previous lower limb amputation, any surgery to the foot or lower limb involving fixation of a joint, any neurological condition that may affect the lower limb other than loss of sensation due to diabetes, inability to walk 8 m unaided, or current pregnancy. Ethics approval was granted by the University of Newcastle Human Research Ethics Committee and written informed consent was obtained from all participants.

Procedures

All data were collected at one testing session at the University of Newcastle Podiatry Clinic, Wyong Hospital, NSW, Australia. Testing was conducted on the participants' dominant leg only, to maintain the independence of data [ 19]. Dominance was determined by asking the participant which foot they would kick a football with. Details of chronic medical conditions and medications, glycated haemoglobin, and duration of diabetes were obtained by self-report and from medical history supplied by the participant's general practitioner. Neuropathy status was assessed using a monofilament which is a regularly used and reliable test for measuring loss of protective foot sensation (LOPS) [ 8]. Four points on the plantar surface of the dominant foot (1st, 3rd and 5th metatarsal heads and the distal hallux) were tested with a 10-g Semmes-Weinsten monofilament. An abnormal test was noted and the participant recorded as having neuropathy if they failed to identify the monofilament at one or more test sites [ 8].

Foot pressure testing was conducted barefoot and in-shoe. The Novel Pedar-X® system, (Novel GmbH, Munich, Germany) was used to measure in-shoe plantar pressures, and has been shown to be a reliable and valid measurement system [ 24]. Participants walked along a flat 12 metre walkway at their normal walking speed wearing an appropriately sized standardised shoe (New Balance® 624), with the insole placed between the sock and the shoe. A minimum of two walking trials was required to capture 12 midgait dominant foot footsteps [ 24]. Barefoot plantar pressures were collected using the Tekscan HR Mat™ Pressure Measurement System (Tekscan Inc., South Boston, USA) using a 2-step protocol which has been shown to collect reliable pressure data, and an average of four successful trials was used for data analysis [ 25]. The foot was divided into 5 masks for assessment of both in-shoe and barefoot pressures: rearfoot, midfoot, forefoot, hallux and lateral toes (Additional file 1). Percentage masks were applied for in-shoe footprints where the rearfoot occupied 28% of the total foot length, the midfoot 22%, and the forefoot 30%. Of the remaining 20% of the foot length, the hallux occupied the medial 35% and the lateral toes the lateral 65% [ 26]. To evaluate the barefoot pressures, a method similar to that used in previous studies to examine plantar loading in older people was applied [ 27], with the only change being a consolidation of three metatarsophalangeal joint regions into one forefoot region. Pressure time integral (PTI) and peak pressure (PP) values are reported.

Statistical analysis

Statistical analyses were conducted using Stata 16.0 (StataCorp, College Station, Texas, USA). Descriptive data were summarised as counts (percentages) for categorical variables and means and standard deviations for continuous variables. Due to the association between the 10 pressure outcome variables, multivariate multiple linear regression was used to assess the effect of the four biomechanical factors, plus neuropathy and BMI on plantar pressure variables for both barefoot pressure and in-shoe pressure scenarios. As all models included the same factors, the R-squared statistic was used to assess relative goodness of fit. In addition, appropriate visual model diagnostics (Additional file 2) were checked such as normality of residuals and heteroscedasticity. A measure of the total number of foot biomechanical pathologies was calculated by summing the dichotomous variables of presence weight bearing ankle dorsiflexion restriction, presence of hallux limitus, presence of HAV deformity and presence of any lesser toe deformity. Non-parametric bootstrapping with 1000 iterations was employed to calculate point and interval estimates to determine the percentage change in plantar pressure variables for participants with equal or greater than 2 foot biomechanical pathologies compared to those with less than two pathologies. A two-sided p  < 0.05 was considered statistically significant.

Results

One hundred and thirty-six people with diabetes were recruited for the trial (Table 1). The majority of participants had a diagnosis of Type 2 diabetes (90.4%) and were predominantly a low risk cohort based on the low reported levels of diabetes-related complications including a history of DFU (3.7%), retinopathy (2.9%), nephropathy (2.2%) or LOPS with foot deformity (11.8%) [ 28]. The prevalence of foot biomechanical pathologies was high, with 62% ( n = 84) of the group having at least one of the assessed foot biomechanical pathologies. A weight bearing ankle dorsiflexion limitation (31%) was the most commonly recorded problem, followed by hallux limitus (28%) and toe deformities (21%) (Table 1). While almost one third (32%) of the cohort had two or more pathologies, none of the participants had all four of the investigated biomechanical foot pathologies.

Table 1 Characteristics of the study population

The results of the multivariate multiple linear regression, used to identify which of the four biomechanical factors plus neuropathy and BMI contributed to the plantar pressure changes in different foot regions are shown in Figs. 1 and 2. Model diagnostics indicated the results of this modelling to be valid. The model explains between 9.9% (95%CI: 8.4 to 11.4%) and 29.6% (95% CI: 28.2 to 31%) of the variance in the barefoot pressure variables (Fig. 1), and between 2.5% (1.0 to 4.0%) and 43.8% (95% CI: 42.5-44.9%) of the variance in the in-shoe plantar pressure variables (Fig. 2). Individual predictors that were significantly associated with increased or decreased barefoot and in-shoe plantar pressures are illustrated in Figs. 1 and 2 respectively.

Determinants of barefoot peak plantar pressure regions (left) and pressure time integral regions (right). Values in plantar pressure regions (rearfoot, midfoot, forefoot, lateral toes and hallux) are R-square values and individual predictors significantly associated with each region are listed. Factors in red signify a decrease in plantar pressure. DF, dorsiflexion; *, p < 0.05; **, p  < 0.001; #, no significant factors; BMI, body mass index; HAV, hallux abducto valgus; ROM, range of motion

Determinants of in-shoe peak plantar pressure regions (left) and pressure time integral regions (right). Values in plantar pressure regions (rearfoot, midfoot, forefoot, lateral toes and hallux) are R-square values and individual predictors significantly associated with each region are listed. Factors in red signify a decrease in plantar pressure. DF, dorsiflexion; *, p < 0.05; **, p  < 0.001; #, no significant factors; BMI, body mass index; HAV, hallux abducto valgus; ROM, range of motion

When participants were grouped into those with two or more foot biomechanical pathologies and those with less than two pathologies, all but two of the barefoot point estimates (forefoot PP and forefoot PTI), which illustrate the percentage change in plantar pressure variables, were statistically significant (Table 2). The largest increase was seen for toe PTI which was estimated to be 57% (95%CI: 13.4 to 119.3%). No significant changes were found for the in-shoe plantar pressure variables (Table 2).

Table 2 Mean (SD) and difference in plantar pressure variables for participants with greater than two foot biomechanical pathologies compared to less than two

Discussion

After grouping participants into those with two or more foot biomechanical pathologies and those with less, the group with two or more pathologies displayed higher barefoot peak pressures and pressure time integrals in all foot regions, although the forefoot increases did not reach statistical significance. Without costly and time-consuming plantar pressure testing equipment, the elevated plantar pressures present in this cohort would not be able to be detected during a standard podiatry consultation. No significant differences were seen between the two groups for in-shoe plantar pressure variables. This may be explained by the effects of the sports shoe used for in-shoe pressure measurement. Lower plantar pressure variables can be expected in-shoe compared to barefoot as the sports shoes used in this trial are designed to provide impact attenuation for the body by altering the ground reaction force and rate of loading [ 31]. This is consistent with previous studies in people with diabetes which revealed that the use of running shoes resulted in reductions in plantar pressures of 31 to 47% at the forefoot and 32% at the hallux compared to Oxford shoes [ 32, 33].

Of the two non-biomechanical factors examined, BMI was seen to exert more wide-ranging effects than neuropathy. BMI had a significant effect on both barefoot and in-shoe midfoot PPs and PTIs, in-shoe forefoot PP and PTI, barefoot toe, forefoot and rearfoot PTIs and in-shoe toe PTIs. This agrees with prior studies that show a high body mass and high BMI adversely affect plantar pressures [ 17, 43, 44]. In this study the only significant effect that neuropathy had was on in-shoe forefoot PTIs. Neuropathy has previously been associated with increased plantar pressure variables [ 18] and also with the development of the majority of foot ulcers [ 45], so it may be the case that the neuropathy seen in this community dwelling group may not yet be severe enough to adversely impact PP variables.

There are calls for greater efforts to delay or prevent the first DFU in people with diabetes [ 48]. While high plantar pressures have been associated both retrospectively and prospectively with increased DFU risk [ 11, 12, 13] they can be easily overlooked by primary care clinicians as they present without obvious clinical signs and symptoms. Our results show that fast, low cost clinical tests may be used to assist with early detection of elevated plantar pressures in people with diabetes. The tests may be appropriate in situations where plantar pressure testing equipment is not available, or when screening low risk diabetes participants where costly testing or further referral is not warranted. A number of first line options are available to primary care clinicians who suspect high plantar pressures in their clients with diabetes. As shown in this and other trials, walking barefoot is associated with higher plantar pressures in older people both with and without diabetes, and a recommendation to wear relatively inexpensive off the shelf running shoes can help to alleviate high plantar pressures [ 33, 49]. Other footwear such as rocker bottom shoes have also shown peak pressure reductions of approximately 50% in the central forefoot compared to Oxford and semi-orthopaedic shoes in people with diabetes [ 50]. Patient education, regularly scheduled foot examinations and timely treatment of pre ulcerative signs (callus, blisters, fungal infections and thickened or ingrown toenails) may also be considered by the clinician who suspects the presence of high plantar pressures [ 48].

The results of this study should be considered in light of several limitations. Only a selected number of easily measured clinical variables were used in the multivariate multiple linear regression analysis. Previous studies in non-diabetes populations have identified other factors, such as measurement of foot and ankle structure derived from radiographs and muscle activity [ 51, 52] that impact plantar pressures, and the variance not accounted for in this model may be due to the omission of further predictor variables. Similarly we did not sub-classify toe deformities into reducible and non-reducible deformities with the different deformity type potentially having differing impacts on plantar pressures. Additionally, the non-probability sampling method and lack of vascular assessment means it is difficult to determine how generalisable our results are to the general population with diabetes. However, the relatively low incidence of LOPs and the small number of participants affected by previous DFU suggest this may be a largely low risk cohort and we are likely to see more significant changes in plantar pressures in higher risk cohorts. Further research could confirm these results in higher risk diabetes cohorts and also investigate which combination of clinical tests are superior in detecting elevated plantar pressures.

Conclusions

Easily measured foot deformities and joint limitations significantly contributed to elevated plantar pressure variables in a largely low risk group of community dwelling adults with diabetes. Participants presenting with two or more of these foot pathologies displayed higher peak pressures and pressure time integrals in all foot regions than those with less than two pathologies. Elevated plantar pressures have been associated in the literature with increased DFU risk, DFU recurrence and delayed DFU healing in people with diabetes. These tests may be used to allow early detection of this mostly asymptomatic DFU risk factor, especially where plantar pressure testing equipment is unavailable.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

BMI:

Body mass index

CI:

Confidence interval

DFU:

Diabetes related foot ulcer

HAV:

Hallux abductus valgus

LOPS:

Loss of protective foot sensation

PP:

Peak pressure

PTI:

Pressure time integral

ROM:

Range of motion

Acknowledgements

None.

Author information

Affiliations

1. School of Health Sciences, Faculty of Health and Medicine, University of Newcastle, PO Box 127, Ourimbah, NSW, 2258, Australia

Vivienne H. Chuter, Martin J. Spink, Sean Lanting & Angela Searle

2. Priority Research Centre for Physical Activity and Nutrition, University of Newcastle, Callaghan, Australia

Vivienne H. Chuter

3. School of Medicine, Griffith University, Brisbane, Queensland, Australia

Michael David

Contributions

VHC conceived the project and AS, VHC, SL & MS conducted data analysis and interpretation. AS & MS collected the data. MD conducted all the statistical analysis. VHS, AS, SL & MS drafted the final manuscript. All authors read, corrected and approved the final manuscript.

Corresponding author

Correspondence to Vivienne H. Chuter.

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Ethics approval and consent to participate

Ethics approval was granted by the University of Newcastle Human Research Ethics Committee (H-2015-0354) and written informed consent was obtained from all participants prior to their participation.

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Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Chuter, V.H., Spink, M.J., David, M. et al. Clinical foot measurements as a proxy for plantar pressure testing in people with diabetes. J Foot Ankle Res 14, 56 (2021). https://doi.org/10.1186/s13047-021-00494-4
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Keywords

Diabetes

Plantar pressure

Biomechanical

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Clinical foot measurements as a proxy for plantar pressure testing in people with diabetes - Journal of Foot and Ankle Research

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Background High plantar pressures are associated with increased foot ulcer risk in people with diabetes. Identification of high plantar pressures in people with diabetes is clinically challenging due to time and cost constraints of plantar pressure testing.

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Journal of Foot and Ankle Research 14, Article number: 35 (2021) Cite this article

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Abstract

Background

Diabetes mellitus is associated with changes in soft tissue structure and function. However, the directionality of this change and the extent to which either tissue thickness or stiffness contributes to the pathogenesis of diabetes-related foot ulcerations is unclear. Hence, this systematic review aims to summarise the existing evidence for soft tissue structural differences in the feet of people with and without diabetes.

Methods

In compliance with MOOSE and PRISMA guidelines, AMED, CINAHL, MEDLINE, ProQuest Health & Medical Collection, ProQuest Nursing & Allied Health Database, and Web of Science electronic databases were systematically searched for studies published from database inception until 1st October 2020 [Prospero CRD42020166614]. Reference lists of included studies were further screened. Methodological quality was appraised using a modified critical appraisal tool for quantitative studies developed by McMaster University.

Results

A total of 35 non-randomised observational studies were suitable for inclusion. Within these, 20 studies evaluated plantar tissue thickness, 19 studies evaluated plantar tissue stiffness, 9 studies evaluated Achilles tendon thickness and 5 studies evaluated Achilles tendon stiffness outcomes. No significant differences in plantar tissue thickness were found between people with and without diabetes in 55% of studies (11/20), while significantly increased plantar tissue stiffness was found in people with diabetes in 47% of studies (9/19). Significantly increased Achilles tendon thickness was found in people with diabetes in 44% of studies (4/9), while no significant differences in Achilles tendon stiffness were found between people with and without diabetes in 60% of studies (3/5).

Conclusions

This systematic review found some evidence of soft tissue structural differences between people with and without diabetes. However, uncertainty remains whether these differences independently contribute to diabetes-related foot ulcerations. The heterogeneity of methodological approaches made it difficult to compare across studies and methodological quality was generally inadequate. High-quality studies using standardised and validated assessment techniques in well-defined populations are required to determine more fully the role of structural tissue properties in the pathogenesis of diabetes-related foot ulcerations.

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Introduction

Histological changes have been observed in the plantar soft tissues [ 7, 8] and Achilles tendon (AT) [ 9, 10] in diabetes. Non-enzymatic glycosylation following persistent hyperglycaemia, a key characteristic of diabetes, results in an excessive accumulation of advanced glycosylation end-products (AGEs) in most human organs and tissues [ 11]. This includes, but is not limited to, muscles, nerves, skin and tendons [ 12, 13]. Concomitant remodelling in the structural composition of the affected tissue [ 14] could alter mechanical behaviour, and in the presence of other established risk factors such as diabetes-related peripheral neuropathy (DPN) and foot deformity [ 4], may increase the risk of DFU development.

Increased tissue stiffness [ 15], particularly in the AT [ 16], and decreased tissue thickness are perceived to be independent risk factors for DFU. Increased plantar tissue stiffness (PTS) is thought to alter the distribution of tensile stresses in the plantar soft tissues during gait [ 15]. Consequently, repetitive biomechanical stresses normally sustained by the foot through activities of daily living may no longer be as effectively dissipated. Combined with a reduction in plantar tissue thickness (PTT), these changes could collectively decrease the mechanical loads required to initiate soft tissue breakdown and thus lead to DFU formation.

As a separate entity, increased Achilles tendon stiffness (ATS) reduces ankle joint motion and is associated with increased forefoot plantar pressures [ 16]. The AT is a compliant tendon, and its ability to stretch and recoil as it produces propulsion and absorbs ground reaction forces is integral to locomotion [ 17]. Increased ATS could negatively affect its dynamic potential and ankle joint range of motion [ 18]. Such changes may not only increase the AT's susceptibility to mechanical fatigue [ 19], and thus predisposition to Achilles tendinopathy [ 20], but it could also lead to the abnormal distributions of forces across the plantar surface of the foot during weightbearing activities. Should these forces be concentrated over a focal area, plantar pressures could potentially increase beyond the withstanding capacity of affected plantar tissues.

Altogether, these changes bear the potential to reduce shock-absorbing capacity of the plantar tissues thus lowering the threshold for which integrity of the skin is breached, while at the same time magnify biomechanical stresses at localised sites, thereby considerably increasing the individual's propensity to ulceration. However, the extent to which tissue thickness and stiffness contributes to DFU pathogenesis is unclear. Ulcerations and their recurrence are frequent sequelae [ 6, 21], yet prospective studies investigating changes to plantar tissue structure and function appear scarce. Therefore, the aim of this systematic review was to evaluate the evidence for changes to soft tissue thickness and stiffness at the plantar tissues and AT in people with diabetes.

Methods

This systematic review was conducted in compliance with the Meta-analyses Of Observational Studies in Epidemiology (MOOSE) [ 22] and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [ 23] guidelines. The protocol was prospectively registered on Prospero [CRD42020166614].

Search strategy

Six electronic databases were systematically searched by the first reviewer (B.K.) for studies published from database inception until 1st October 2020. The databases were: EBSCOhost (AMED, CINAHL, MEDLINE), ProQuest (Health & Medical Collection, Nursing & Allied Health Database), and Web of Science. No date restrictions were imposed, however, studies were restricted to those published in English and in peer-reviewed journals only. Boolean operators and relevant MeSH terms were used and keywords were adapted for each database (Additional file 1).

Inclusion and exclusion criteria

Studies which met criteria in the following five categories were eligible for inclusion. (1) Population: cohorts comprised of adults 18 years old and above were included; experiments conducted on animals, artificial tissues, cadavers or minors below 18 years old were excluded. (2) Interventions: no restrictions set. (3) Comparison: studies which had made a comparison between cohorts with and without diabetes were included; non-comparative studies, specifically studies which had not included a control group of otherwise healthy adults, were excluded. (4) Outcomes: in-vivo assessments of either thickness and/or stiffness of plantar soft tissues and/or the AT were included; in-vitro studies, studies which assessed other body parts or internal body organs, or technical studies solely evaluating the physics or engineering of the measurement technique were excluded. (5) Type of study: quantitative primary research studies published in peer-reviewed journals were included; qualitative studies, case reports, commentaries, conference proceedings, narrative reviews, and studies published in non-peer reviewed journals were excluded.

Study selection

All articles retrieved in the search were first exported to RefWorks for removal of duplicates and subsequently exported to Covidence. Two reviewers (B.K. and R.B.) independently screened all titles and abstracts against pre-established inclusion and exclusion criteria. Articles which appeared to be eligible were retrieved in full and assessed by both reviewers. Upon mutual agreement for inclusion, the reference lists of included articles were additionally screened. This iterative process was performed until no further articles could be included. Where full-text articles could not be accessed, university library services were employed and authors contacted directly; this was successful on six occasions. Throughout this process, discrepancies were first resolved by consensus between the two reviewers (B.K. and R.B.) with adjudications sought from a third reviewer (J.W.) where required.

Methodological quality assessment

All included studies were appraised for their methodological quality using a modified critical appraisal tool for quantitative studies developed by McMaster University [ 24]. This modified tool comprehensively evaluates 14 different aspects of methodological quality, categorised under the domains: study purpose, literature, design, sample, outcome, assessment technique, results, conclusions and implications. Quality assessment was performed by the first reviewer (B.K.) and checked in full by the second reviewer (R.B.). As the thresholds for distinguishing between study quality grades have not been established, study quality was scored upon mutual agreement by two reviewers (B.K. and R.B.). Assessment rubrics [ 25] provided by McMaster University to guide the completion and interpretation of each criterion were adhered to, and where additional criteria were applied by the reviewers, these are detailed as follows.

Criteria for assessing sample

The sample description was deemed as limited if participant inclusion or exclusion criteria, and/or baseline characteristics of body mass index (BMI), duration of diabetes or HbA1c levels of the cohort were not reported. This lack of detail limits the reviewers' attempts to establish comparability of diabetes, DPN and DFU cohorts within studies. Potential confounders were identified a priori as age, sex and BMI due to their known effects on soft tissue thickness [ 26, 27, 28] and stiffness [ 29, 30, 31, 32]. Where groups were matched for all three baseline demographics, studies were deemed to have adopted strategies to reduce confounding. Where studies matched for only one or two of the aforementioned baseline demographics or any other potential confounders, the confounding strategy was deemed as limited.

Criteria for assessing reliability or validity of outcome measures

Studies which had either tested for or cited previous works demonstrating the reliability or validity of their chosen assessment tool for the relevant outcome measures were recognised to have addressed these domains. Where reliability or validity was addressed for other assessment techniques within the study, but not those relating to PTT, PTS, Achilles tendon thickness (ATT) or ATS outcomes, or was not mentioned at all, the study was deemed to not have addressed this domain.

Data extraction

Data extraction was performed independently by the first reviewer (B.K.) and checked for accuracy by the second reviewer (R.B.). A pre-specified data extraction sheet was used to extract data from all studies, which includes: (1) Article information: title, authors and year of publication; (2) Methods: study design, setting, participant demographics, participant inclusion and exclusion criteria, type of assessment tool utilised, outcome metric, and method of measurement for thickness or stiffness; and (3) Main findings. Within studies, statistical significance was defined as p  < 0.05.

Data synthesis

A descriptive synthesis was conducted using summary data from individual studies to identify the directionality of PTT, PTS, ATT and ATS changes in people with diabetes when compared to their controls. Absolute values for PTT and ATT were further extracted. Where sufficient data permits, subgroup analysis was undertaken to identify the presence of any anatomical variations across the plantar aspect of the foot and the length of the AT, and to explore how findings may compare across cohorts with different diabetes-related complications. This includes people with DPN or people with either an active or history of DFUs.

Results

Studies were published across three decades (1985 to 2020), with sample sizes ranging from 8 to 190 participants. The mean age of participants with diabetes was 58.5 years and their mean BMI was 27.3. The mean age of controls was 51.6 years and their mean BMI was 26.0. Participant comparison groups included healthy controls, people with diabetes but without DPN, people with DPN, and people with either an active or history of DFUs.

Methodological quality assessment

All 35 papers included were non-randomised observational studies assessed to be of low quality. Overall, the degree of reporting was deemed to be inadequate for the following components of methodological quality: study design, sample size justifications, strategies to reduce confounding, reliability and validity of outcome measures utilised, and assessment techniques (Table 2).

Study purpose, literature and design

The purpose of the study and supporting background literature was generally well reported. Even though study designs were explicitly stated in only 43% of studies (15/35), the designs were considered appropriate.

Sample

Reliability and validity of outcome measures

Validity of outcome measures was reported in 11% of studies (4/35). All four studies had cited previous works in demonstrating the validity of their chosen assessment tools for their specified outcome measure(s). Two studies [ 45, 55] have indicated that the validity of the TUPS had been demonstrated for both PTT and PTS. One study [ 44] had indicated that the validity of the durometer had been demonstrated for PTS. In relation to the AT, only one study [ 68] had indicated that the validity of US had been demonstrated for ATS. None of the studies that assessed ATT had reported on the validity of their assessment technique. No mention of validity was reported in the remaining 89% of studies (31/35).

Outcome metrics

Assessment techniques

Assessment tools

Plantar tissue thickness

Plantar tissue stiffness

Achilles tendon thickness and stiffness

Method of measurement

Plantar tissue thickness

Achilles tendon thickness

Anatomic sites examined

Plantar tissue thickness

Across 20 studies examining PTT, 30% examined the hallux, 60% examined the first metatarsal head (MTH), 45% examined the second MTH, 45% examined the third MTH, 30% examined the fourth MTH, 40% examined the fifth MTH and 60% examined the heel. Robertson et al. (2002) [ 57] did not report their findings for each MTH individually, instead providing it as a mean and standard deviation across all five MTHs for each cohort. Thomas et al. (2003) [ 52] had similarly merged their findings for the third to fifth MTHs. None of the studies had examined PTT at the lesser toes.

Plantar tissue stiffness

Across 19 studies examining PTS, 37% examined the hallux, 58% examined the first MTH, 26% examined the second MTH, 32% examined the third MTH, 5% examined the fourth MTH, 26% examined the fifth MTH, 11% examined the medial and lateral midfoot, and 84% examined the heel. 16% of studies had merged their findings for the third to fifth MTHs [ 44, 51, 52]. One study had compared the microchambers and macrochambers in the heel [ 46]. One study had compared the plantar skin and fat layer at the heel [ 34]. None of the studies had examined PTS at the lesser toes.

Achilles tendon thickness and stiffness

Key findings

The main findings for PTT, PTS, ATT and ATS outcomes are tabulated in Table 4.

Plantar tissue thickness and stiffness

Achilles tendon thickness and stiffness

Across nine studies that analysed ATT, 44% (4/9) found a significant increase across all examined portion(s) in people with diabetes when compared to healthy controls [ 33, 35, 41, 66] (Additional file 6). No significant differences in ATT between groups were observed in 33% of studies (3/9) [ 38, 47, 67]. One (11%) study found reduced ATT in people with diabetes, however it is not known if this difference was significant as inferential statistics was not conducted for ATT measurements [ 65]. Sex variations in findings were noted in 22% of studies (2/9) [ 47, 48]. Both studies reported significantly greater ATT in women with Type 2 diabetes when compared to women without diabetes, but no significant differences were found between men with Type 2 diabetes and men without diabetes.

Sub-group analysis

Participants with diabetes-related peripheral neuropathy

Participants with an active or a history of diabetes-related foot ulcerations

Brink (1995) [ 59] and Thomas et al. (2003) [ 52] were the only two studies to directly compare their findings for either active or healed DFU sites with non-ulcerated sites. Both studies found PTS at DFU sites to be increased when compared to non-ulcerated sites. Hsu et al. (2000) [ 53] limited their cohort to participants with active forefoot DFUs (Wagner grade 2 or 3) whilst investigating PTS at the heel.

Comparing findings across diabetes-related foot complications

Anatomical variations

Plantar soft tissues

Regional variations in PTS were observed in only one out of all other examined sites in 26% of studies (5/19) [ 36, 41, 44, 51, 52]. More extensive regional variations in PTS were noted in only one study [ 59] (5%) with contradictory findings (Additional file 5). Kwak et al. (2020) [ 34] reported differences between plantar fat pad and skin stiffness, while Hsu et al. (2009) [ 46] reported differences in micro- and macrochamber stiffness in the heel pads.

Achilles tendon

Only two studies distinguished their findings between the three segments of the AT (myotendinous junction, mid-portion and insertion) [ 33, 38], both studies utilised US. While they shared the observation that ATT findings for each individual segment had not differed from each other [ 33, 38], Evranos et al. (2015) [ 38] noted that ATS differed in the proximal segment (myotendinous junction) when compared with the mid- and distal (insertional) segments (Additional file 6). Additionally, only two studies analysed the US-derived echotexture of the AT [ 33, 65]. Altered patterns were found in people with diabetes in the form of hypoechogenicity, loss of fibrillar pattern, calcification at the tendon insertion at the calcaneus and/or retrocalcaneal bursitis.

Discussion

Principal findings

This systematic review investigated the evidence for differences in plantar soft tissue and AT thickness and stiffness in people with and without diabetes. The general consensus among studies was that diabetes is associated with a significant increase in PTS, however the differences in PTT is not significant. Studies also found that diabetes is associated with a significant increase in ATT, however the differences in ATS is not significant.

Methodological considerations

Extensive methodological heterogeneities and deficiencies was a key finding of this systematic review. Sample sizes were seldom justified (3%, 1/35). Additionally, reporting was generally inadequate across the domains of study designs and the reliability and validity of outcome measures. Case definition for participants with diabetes and subgroups formed on the presence and history of DFU or DPN were often absent or inadequately defined. Furthermore, the risk of selection bias cannot be eliminated in the majority of studies as only 6% of studies adopted a consecutive sampling method for recruiting people with diabetes; the remaining 94% of studies (33/35) made no mention of their sampling strategy for their cohorts with diabetes.

No gold standard assessment techniques have been established for tissue thickness and stiffness assessments and this was reflected in the diverse approaches reported in this review. Studies that employed novel biomedical technologies and tissue engineering outcomes are additionally not easily reproduced and are not well understood in clinical settings. Ultrasound-based techniques were favoured - utilised by 80% of studies (16/20) investigating PTT, 47% of studies (9/19) investigating PTS, 89% of studies (8/9) investigating ATT, and 100% of studies (5/5) investigating ATS - but standardisation in its usage is lacking. Ultrasound-based techniques are also known to be highly dependent on the knowledge, experience and skill of the operator [ 69]. Therefore, the extent to which outcomes have been reliably measured is important. However, no mention of reliability was made in 60% of studies (21/35).

Studies further differed in their measurement techniques. Using PTT for example, while the majority of studies (70%, 14/20) measured PTT as the distance between skin and bone, overall six different methods of measurements were observed. Combined with the use of different assessment techniques and examination of different anatomical sites, these wide-ranging methodological heterogeneities made it difficult to compare and synthesise results across studies. The lack of standardisation also renders derivation of normal and diagnostic cut-off values extremely challenging and hampers routine clinical utility for at-risk screening, detection and longitudinal monitoring.

Role of plantar soft tissues thickness and stiffness in DFU

On the plantar aspect of the foot, areas at high risk of ulceration are the apices of the toes, metatarsal heads, medial aspect of the midfoot and the heel [ 4]. This systematic review observed that evidence for the differences in PTS is more consistent across included studies than PTT (Additional file 5). However, regional variations in either PTT or PTS appear modest. This implies that other risk factors such as tissue load, in the presence of structural tissue changes, may be more important for the development of DFU rather than either factor alone. These findings reinforce the multi-factorial nature of plantar DFU pathogenesis [ 5, 6] and the need for further mechanistic and outcome focused research.

The lifetime incidence of DFUs is estimated to be up to 35% [ 6]. DFU recurrence rates are also high, with the pooled global recurrence rates estimated in a meta-analysis to be 22.1% per person-year (95% CI, 19.0-25.2%) [ 21]. However, the extent to which plantar soft tissue changes contribute to either the development of primary ulcerations or its recurrence is little understood. No firm conclusions can be drawn from this review, as only 6% of studies (2/35) directly compared either active or healed DFU sites with never-ulcerated sites. Additionally, none of the included studies measured differences in PTT or PTS at the apices of the toes. Combining the paucity of studies primarily investigating these associations with the methodological shortfalls identified in existing studies, the clinical significance of tissue thickness or stiffness changes in its role in contributing towards plantar DFUs remains unclear.

Role of Achilles tendon thickness and stiffness in DFU

Achilles tendon changes in diabetes are recognised to potentially alter ankle biomechanics [ 16], increase forefoot plantar pressures and contribute to tissue breakdown [ 70]. This systematic review identified that people with diabetes, particularly those with DPN and DFU, may have a thicker AT but reduced AT stiffness. The International Working Group on the Diabetic Foot (IWGDF) guidelines [ 71] recommend AT lengthening procedures to be considered as a potential management option for the prevention of DFU recurrence. It is not clear what the implications of these findings are for such procedures. The authors of this systematic review are unaware of studies that have specifically investigated the association of either ATT or ATS with AT lengthening procedures and this merits further investigation.

Thickening in tendons are often regarded as pathological clinically [ 17, 72]. While the site of localised thickening could be important, this review and the evidence synthesised does not elucidate. It is further uncertain if a thicker or thinner AT, stiffer or less stiff AT, presenting simply by virtue of its different thickness or stiffness when compared to an otherwise healthy cohort, can therefore be viewed as pathological in diabetes. To the best of the authors' knowledge, the normative values of ATT or ATS have not been established in a cohort of people with diabetes, such that even in the absence of symptomology, said AT changes should therefore be regarded as tendinopathic.

Potential confounders

It is further unclear to what extent baseline factors such as age, sex, BMI, duration of diabetes and glycaemic control are associated with soft tissue changes in diabetes. In this systematic review, the differences between groups with diabetes and control groups in age, sex and BMI were statistically not significant in 40% of studies which appears to reduce the potential for confounding. However, studies reviewed have documented poor correlations between age with PTT [ 37, 40], PTS [ 40] and ATT [ 33] differences; BMI with PTT and PTS differences [ 40]; duration of diabetes with PTT [ 40], PTS [ 40] and ATT [ 33] differences; as well as HbA1c levels with PTT [ 39, 40], PTS [ 40] and ATT [ 33] differences between people with and without diabetes. Strong correlations have however been found between triglyceride levels and PTS differences in the heel for people with diabetes [ 40]. Nonetheless, it was difficult to tease out whether soft tissue alterations were due to the adequacy of glycaemic control, chronicity of hyperglycaemia, hypertriglyceridemia, severity of DPN or other potential confounders in demographics. This requires careful attention in future studies.

Strengths and limitations

This systematic review has several strengths. The review included all studies published to date on the topic, including a body of knowledge from the biomedical technology field where assessment techniques were utilised in cohorts of people with diabetes and associated risk factors for DFU. Extensive search strategies were employed with detailed, careful and critical assessment to identify risk of bias. The review is, however, limited by the methodological deficiencies of included studies. The critical appraisal tool by McMaster University [ 24] has also not been validated and the threshold for distinguishing between grades of methodological quality have not been established. Substantial methodological heterogeneities prevented the conduct of meta-analysis which further limits the review. Additionally, two papers with similar cohorts may have contributed to the observed heterogeneity. However, since no pooled analysis was undertaken, the effect on the precision of the estimated outcome is unclear.

Conclusions

This systematic review found some preliminary evidence supporting differences in soft tissue properties in the feet of people with and without diabetes. However, uncertainties remain largely due to methodological heterogeneities and deficiencies. Tissue thickness and stiffness are putative risk factors for DFU and may be a viable treatment target. High-quality studies using standardised and validated assessment techniques in well-defined populations are required to advance our understanding and to determine more fully the role of soft tissue thickness or stiffness changes in the pathogenesis of DFU. Should soft tissue compromise be indicative of imminent tissue breakdown in the diabetic foot, this has the potential to aid clinical triage and inform the timely adoption of targeted preventive measures.

Availability of data and materials

All data generated or analysed during this study are included in this published article (and its supplementary information files).

Abbreviations

AGEs:

Advanced glycosylation end-products

AT:

Achilles tendon

ATS:

Achilles tendon stiffness

ATT:

Achilles tendon thickness

BMI:

Body mass index

CT:

Computed tomography

DFU:

Diabetes-related foot ulceration

DPN:

Diabetes-related peripheral neuropathy

ICC:

Intra-class correlation coefficient

MOOSE:

Meta-analyses Of Observational Studies in Epidemiology

MRI:

Magnetic resonance imaging

MTH:

Metatarsal head

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

PTS:

Plantar tissue stiffness

PTT:

Plantar tissue thickness

TUPS:

Tissue ultrasound palpation system

US:

Ultrasonography

References

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Acknowledgements

B.K. would like to thank The Carnegie Trust for the Universities of Scotland for funding this work.

Additional declarations

Poster presentation at the Diabetic Foot Study Group (DFSG) of the European Association for the Study of Diabetes (EASD) 2020 virtual conference, 18-19 September 2020; awarded 1st prize.

Funding

B.K. is a PhD student in podiatry in the School of Health and Life Sciences at Glasgow Caledonian University. She is a recipient of a PhD scholarship funded by The Carnegie Trust for the Universities of Scotland. The funding body played no role in the design or conduct of the study, preparation of the manuscript or the decision to submit this work for publication.

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Affiliations

1. Department of Podiatry and Radiography, School of Health and Life Sciences, Glasgow Caledonian University, Glasgow, G4 0BA, Scotland, UK

Benedictine Yen Chen Khor, James Woodburn, Lisa Newcombe & Ruth Barn

2. School of Health Sciences and Social Work, Griffith University, Queensland, Australia

James Woodburn

Contributions

All authors made substantial contributions to the conception and design of this work, analysis and interpretation of data. B.K. drafted the manuscript, all authors revised it critically for important intellectual content. All authors approved the submitted version. All authors agree to both be personally accountable for the author's own contributions and to ensure that questions related to the accuracy or integrity of any part of the work, even ones in which the author was not personally involved, are appropriately investigated, resolved, and the resolution documented in the literature.

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Correspondence to Benedictine Yen Chen Khor.

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Khor, B.Y.C., Woodburn, J., Newcombe, L. et al. Plantar soft tissues and Achilles tendon thickness and stiffness in people with diabetes: a systematic review. J Foot Ankle Res 14, 35 (2021). https://doi.org/10.1186/s13047-021-00475-7
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Keywords

Achilles tendon

Diabetic foot

Diabetic foot ulcer

Diabetes related foot ulcer

Plantar soft tissues

Soft tissue properties

Tissue stiffness

Tissue thickness

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Plantar soft tissues and Achilles tendon thickness and stiffness in people with diabetes: a systematic review - Journal of Foot and Ankle Research

# data[].attributes.attachment_link.description
Background Diabetes mellitus is associated with changes in soft tissue structure and function. However, the directionality of this change and the extent to which either tissue thickness or stiffness contributes to the pathogenesis of diabetes-related foot ulcerations is unclear.

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Journal of Foot and Ankle Research 10, Article number: 14 (2017) Cite this article

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7 Citations

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Abstract

Background

Despite significant advancements in new treatment modalities for rheumatoid arthritis with biological therapies, foot complications remain a disabling and common feature of the disease. In this study the aim was to explore and describe the personal experiences of people with rheumatoid arthritis in receipt of biologic treatments in a bid to understand the impact of this form of medication on their mobility.

Methods

An interpretative phenomenological analysis (IPA) was undertaken to explore in depth the individual experience of rheumatoid disease through personal accounts of the patient journey spanning both 'before' and 'after' the instigation of biologic therapy. A purposive sampling strategy was adopted and in-depth semi structured interviews used to facilitate rich, detailed interview data exploring the lived experiences of individuals undertaking biological therapy and the changes to mobility experienced as a result. Thematic analysis was employed with an IPA framework to identify key meanings, and report patterns within the data.

Results

Five people with rheumatoid arthritis participated in the study. The mean disease duration was 20.2 years (range: 6 -32) and all were being treated with biologic therapies. Four key themes emerged from the data: 1) Life before biologic treatment, depicted in accounts as a negative experience characterised by painful and disabling symptoms and feelings of hopelessness. 2) Life with biologic treatment, often experienced as a life changing transition, restoring function and mobility and offering renewed hope. 3) Sense of self, in which the impact of rheumatoid disease and the subsequent changes arising from biologic therapy reveal a profound impact on feelings of personal identity both pre and post biologic therapy; an effect of footwear on self-image emerges as a dominant sub theme; 4) Unmet footcare needs were evident in the patient narrative, where the unrelenting if diminished impact of foot pain on mobility was viewed in the context of problematic access to foot health services.

Conclusion

Whilst the findings from this study mirror those within the existing literature, which report improvements in physical function related to biological therapy, foot problems clearly remained an unremitting feature of life for patients with rheumatoid disease, even when in receipt of biologics.

Peer Review reports

Background

Rheumatoid arthritis (RA) is the most common form of chronic inflammatory polyarthritis [ 1] with a relatively constant prevalence across many developed populations worldwide, including the UK at 0.5-1.0% [ 2]. Improved understanding of the molecular pathways responsible for driving the disease are demonstrated in the variety of biologic treatments now available, each with varying immunological targets and modes of action [ 3]. There is a growing body of evidence demonstrating improvements in patient outcome measures in those taking biologics [ 4- 7], although much of this evidence is derived from quantitative research studies, with relatively little attention focused on the individual patient experience.

The prevalence of foot involvement and foot pain in RA is well documented in the literature with an estimated range of 35-70% [ 8, 9]. Despite the significant advances in new treatment modalities for RA, such as the availability of disease modifying anti-rheumatic drugs (DMARDs) and biologic treatments, foot complications remain a disabling and common feature of life for many patients [ 9]. Indeed, the presence of forefoot pain (63.9%) and ankle pain (42.7%) was highlighted by Otter et al. [ 9] from a cross sectional survey of patients with RA ( N = 585). However, these estimates may actually be higher, as the prevalence of foot involvement and the extent of foot symptoms in the RA patient group can be under-estimated [ 9, 10].

Foot complaints and impaired foot function occurring in both the early and chronic stages of RA have been shown to severely limit an individual's daily activities, in particular reducing ambulation and functional mobility [ 11- 14]. Pain from rheumatoid forefoot disease has also been linked to disability in a number of weight bearing activities [ 14]. Indeed, in a survey by Grondal et al. [ 12] forefoot symptoms were reported as a primary cause in walking impairment in the rheumatoid population, significantly more so than symptoms from either the knee or hip joints ( N = 1000). Consequently, investigators have begun to highlight the negative impact of RA related foot disease on quality of life (QOL) [ 15, 16] although few studies have demonstrated this unequivocally [ 17].

A new paradigm for the management of foot manifestations of RA has been proposed, which includes tighter disease control through the use of biologic treatments [ 18]. Other investigators have shown that patient reported foot pain and disability may decrease in people who have RA (PwRA) following 12 weeks of anti-TNFα treatments compared to those on conventional DMARDs [ 19]. Conversely, in a study comparing self-reported foot pain in PwRA treated with and without anti-TNFα, Otter et al. [ 9] found that foot pain was significantly increased within the anti-TNFα treated group ( P = 0.012). The authors suggest that the success of the TNF inhibitors may encourage a greater degree of mobility in the patients receiving it, which in turn may increase foot symptoms [ 7, 9, 20]. This may be evidenced by observed improvements in gait amongst PwRA successfully treated with anti-TNFα [ 21].

From an extensive review of the literature it is clear that very little evidence is available to confirm these theories. Three key qualitative publications have been identified within the area of biologics and experiences of PwRA. Marshall et al. [ 22] reported improvements in physical function, pain and well-being using interview data ( N = 19). They indicated a greater range of benefits from biologic treatments than those routinely measured in quantitative research [ 22]. Arkell et al. [ 23] found that participants were very positive about anti-TNFα medication, which they felt led to dramatic changes in their physical symptoms. Equally, Linden and Bjorklund [ 20] concluded that successful treatment with anti-TNFα medication led most participants to experience dramatic improvements in the quality of their lives, resulting in a return to leisure interests, enhanced social activity and improved or continued productivity in education and/or occupation. However Linden and Bjorklund also cautioned that such dramatic changes may risk overuse and consequent strain [ 20].

A constant challenge for service providers remains the appropriate targeting of resources, which ideally would be guided by patient reported experiences, particularly where pharmacological management is especially effective at reducing pain and disability. This is very notable in relation to patient experiences of mobility in those who have commenced anti -TNFα drug therapy. As a result, the aim of this study was to gain a deeper understanding of the experiences of PwRA who are receiving biological therapy treatment in relation to their lower limb mobility.

Methods

A qualitative research study design was employed to enable a deep exploration of the lived experiences of individuals with RA in receipt of pharmacological treatment with biologic therapies, which would examine the impact of these treatments on their world. Interpretative phenomenological analysis (IPA) provided the most appropriate approach. IPA is a qualitative approach that involve an idiographic focus which is concerned with providing insights into how a individual in a specific context make sense of a particular issue (phenomenon) [ 24]. In this study, this involved trying to understand the unique personal meanings and actual experiences of PwRA patients attempting to regain and maintain mobility whilst receiving biological therapy treatment. This exploratory idiographic approach was adopted using semi structured interviews, and it deployed a chronological narrative mapping of experiences before the onset of RA, after its onset, and the journey through the transition to biologic therapies and their impact, thus spanning a significant timeframe in the participants' lives.

Ethical approval

Full ethical approval for the study was granted by the Faculty of Health Sciences, University of Southampton Ethics Committee via the online approval system ERGO (Ethics and Research Governance Online). Our original proposal had a tighter inclusion criteria for specific anti-TNF therapies, however this substantially reduced our potential recruitment sample and therefore we widened our criteria to include PwRA who were receiving any biologic therapy. The amendment to extend the sample to include patients receiving all current biologics rather than just one specific branch, anti-TNFα was approved.

Participants

Participants were recruited through branch membership of the National Rheumatoid Arthritis Society (NRAS) using the Salisbury and North Hampshire branches. All members of NRAS have rheumatoid arthritis. Potential participants were approached with a short presentation that explained the study by the primary investigator (LS) at the meeting of each branch. Those interested in joining the study were provided with an information sheet along with the contact details of the primary investigator (LS). Individuals volunteering to join the study then contacted the primary investigator (LS) for additional information, to have any further questions answered, and to be pre-screened against the inclusion criteria.

A purposive sampling strategy was undertaken, consistent with the qualitative paradigm and study design adopted. This enabled the study to capture insightful and meaningful data exploring individual patient experiences, and to note any common experiences across the sample. Participants were included if they had a confirmed diagnosis of rheumatoid arthritis; were currently receiving biologic treatment, where the duration of biologic treatment was over 6 months; where they were aged 18 or over and were able to give consent to participate in the study. Participants were excluded if they had a diagnosis of inflammatory arthritis other than rheumatoid arthritis, or were unable to speak or understand English.

Procedure

Individual, face-to- face, semi-structured interviews were undertaken, generating data which was transcribed verbatim prior to analysis. Each interview was conducted by one researcher (LS) to enable consistency in approach, whilst also capturing individual accounts and narratives. An interview topic guide (Additional file 1) was used to enable a degree of continuity across the interviews, whilst acknowledging the need to capture the individual experiences of each participant. To begin the interview a broad open question about the participant's experiences of everyday life with rheumatoid arthritis prior to biologic therapy was used. The answers were then followed up with exploratory questions, probes and prompts. As there has been little published work on patient experiences of RA when undergoing biologic therapy, the topic guide was informed by, and constructed from, the clinical experience of the research team. Participants were able to choose the venue of the interviews, either in their own homes or in a room at the University of Southampton. The interviews lasted between 40-60 min each and all were audio-recorded. Interview audio recordings were transcribed verbatim. One researcher (LS) read and re-read transcripts several times to enable familiarity and immersion of the data. To verify the accuracy of the researcher's transcription, the first participant was offered a copy of their transcribed interview to check for veracity, accuracy and to ensure rigour which was confirmed by the individual participant (respondent validation).

Thematic analysis was used to analyse the data within an IPA framework focussing on the individual lived experience. One researcher (LS) undertook a line by line analysis of the experiences and understanding of each participant. These initial notes were used to develop codes which informed the further development of themes and sub-themes. Codes were generated from transcripts by noting recurring words or comments of interest. Following this process all codes were then laid out and collated into groups of similar features which served as potential themes. The emerging themes were discussed and viewed by the wider research team (LS, MDH, CB) to verify the themes, identity any additional areas of interest and agree the themes. This involved discussion and looking at patterns across the data, but did not involve each member analysing the data individual and then comparing the finding. To further develop the themes and make clear links to the transcripts, extracts from the transcripts were collated into a table for ongoing analysis (Additional file 2). Potential themes were then discussed again with the research team (LS, MDH, CB) to identify any alternative interpretations. The process of verifying themes as a team provided a more rigorous approach, different perspective and agree on the final themes.

Results

The study recruited seven participants, two male and five female from the two NRAS branches. However one female participant was unable to attend interview and therefore withdrew. One further interview was initially postponed and the participant opted to withdraw. Five interviews were finally conducted that included one male and four female participants (mean age 64, range 35 to 78 years). The average duration of disease was 20.2 years (range 6-32 years). The average duration of receiving biologic therapy was 5.4 years (range 2005-2013), although several participants had been on other biologics before and these were brought up in the interviews. At the time of the interviews, the participants were experiencing varying degrees of effectiveness of their biologic treatments. Two participants were having infusions of Rituximab, one of which was waiting to change to Abatacept due to poor efficacy. Two participants were having Humira injections and one patient was having Enbrel injections. Three participants had no prior history of biologic drug therapy, whilst one participant was awaiting the start of a third different biologic and another was starting on a fourth.

The analysis identified four key themes: 1) Life before biologic treatment, 2) life with biologic treatment, 3) sense of self, and 4) podiatric implications. Each theme is discussed and supported with direct extracts drawn from the transcripts. Participants are assigned numerical identifiers to ensure confidentiality.

Life before biologic therapy: "If you did too much you went to bed"

This theme related to individuals experiences and key events in the years prior to the receipt of biologic therapy, including the physical, social and emotional impact. Some of these accounts convey the experience of a dark period in participants' lives, associated with "survival" and a time "not to visit again".

Each account captured the contrast between life prior to biologic therapy and that after it, providing a context within which to comprehend the extent of the impact of the drugs. Symptoms of pain were common to all the participants, albeit to a varying degree. However, the intensity of the impact of living with pain is captured in the concise but descriptive and powerful phrases employed by some of the female participants, all of whom were diagnosed more than 10 years previously.

"Every single joint is on fire" (P01)

"Absolute agony; if you just touched me I would scream with the pain" (P02)

"A normal day was agony" (P03)

"The damage comes with really severe pain" (P05)

All participants clearly experienced the undesirable and troublesome impact of physical symptoms arising from rheumatoid arthritis, with each identifying a range of distressing and disabling restrictions, including 'tiredness' and 'exhaustion'. One short data extract particularly captures the extent of the disabling impact of their symptoms.

Joint and limb stiffness as much as pain were viewed as disabling, preventing the accomplishment of the simplest of everyday tasks.

Participants also described the experience of becoming less active, or diminishing physical capabilities, leaving a sense of loss and requiring a re-evaluation of self-image and identity. For example, those participants who had previously participated in sport had been forced to abandon it altogether.

Strong emotional feelings were expressed when discussing life prior to being treated with biologic therapy. One participant in particular (P05) found it very 'emotional and difficult' talking about the time around her diagnosis, becoming quite tearful on several occasions and expressing suicidal thoughts.

Loss of sense of self and self- identity were very evident, where comparisons were drawn between the person they had been (active, sporty) to that which they had become (disabled).

Life with biologic therapy: "I'm doing more than I thought possible"

This theme relates to participant narratives reporting experiences since commencing biologic therapy. All participants reported the remarkably liberating effects of what was described as a 'miracle' treatment, even referring to life as 'glorious' in some cases.

Each narrative was marked by the use of highly evocative and descriptive language suggestive of a dramatic life-changing event, evident when the biologic treatment was effective.

The startling effectiveness of the biologic therapy also enabled participants to re-engage with physical activities that were presumed lost for ever, prompting them to take every opportunity to do so.

"I can go and do things, so any chance now I get, I go!" (P01)

"I can even push a lawn mower now!" (P02)

"I ran the great south run this year" (P04)

"I walk up the hill, it's in a valley, and it's a really steep hill and I've been on health walks with the local health group walk. And I walk on my own, and I walk for an hour (P05)

Unsurprisingly, the ability to resume physical activities that had seemed unlikely prior to biologic therapy brought a sea change in mood and an uplift in psychological well-being.

Not all the respondents experienced such dramatic improvements, particularly those who had tried several biologics previously, but had experienced a reduced tolerance of the drug or a failure in efficacy, or, in some cases, a regression and resumption in symptoms, with an understandable loss of optimism.

Equally, in some instances respondents had experienced a remission in symptoms of pain and stiffness, and had avoided irreversible joint damage and deformities, but nevertheless had been left with some residual effects and limitations to everyday activity, often met with resignation.

""I think every joint has gone back to roughly being ok... I think the biggest thing for me is the fatigue...There are times when I can't keep playing with them (children) and I do have to come and sit down, which gets me a bit frustrated. So, so [pause] yeh it has become the 'norm' so I don't think about it as much and I have just accepted that I have to come and do it" (P04)

Sense of self: "You're a woman & want to feel nice"

Bury's classic work (1982) on biographical disruption powerfully captured the impact of the onset and deterioration of rheumatoid disease on personal identity and self-image, and Williams's subsequent work on biographical reconstruction (1984) took account of the normalisation process following successful medication, although neither works were able to address the changes heralded by the modern use of biologic therapy [ 25, 26]. Unsurprisingly, notions of self-identity and self-image were, as evidenced in the data presented here, transformed with the advent of biologic therapy, although established signs of disease continued to result in feelings of being labelled.

With deformity established as a residual effect of earlier active disease, participants reported a self-consciousness generated by the knowledge that visible signs of their disease, such as found in the hands, were highly noticeable to others around them.

Individual sense of self-image may be drawn from, and constructed around, a sense of how individuals are seen by others, which was evident in the data and seemed to reflect a desire to be viewed as 'normal' in one's public self ('normalisation' as a form of coping, bracketing off the impact of the disease - see Williams [ 27]), which also maps with William's reflections [ 27] on 'corporeal dysappearance (dysfunctional appearance)'.

Self-image, personal identity and the participants' 'public self' was most evidently affected in accounts concerning the individuals' social life. For example, one participant spoke about friends who had met partners via online dating sites, contrasting this with her own situation in which she felt unable to consider any such activity as realistic or feasible, given her physical appearance.

Another element of concern expressed about the effects of changed physical appearance was the focus on the accompanying special footwear often prescribed for patients with particular foot problems, such as deformity. In such cases, it was no longer possible to walk comfortably, or fit into, 'ordinary' footwear (that which might be purchased in a high street shoe shop). However, prescription orthopaedic footwear is notable for its bulky, functional appearance, with very little aesthetic consideration in its design, a matter of particular concern to female patients. Wearing such footwear therefore marks out the individual, highlighting the disability.

"How can you wear things like that, even no matter how much pain I was in there was no way I'm gonna be seen dead in them, I'm not even gonna be put in my coffin in one of those on me" [sic] (P02)

"I have to wear these (pause) ghastly things (laughs) to get any degree of comfort" (P03)

"Have you ever seen those great big shoes? I said I can't wear that, that is insulting really. I still wanna be, I'm still a woman!" (P02)

Theme 4. Podiatric Implications: "They never tell you anything about your feet"

In some instances the reported beneficial effects of biologic therapy did not extend to foot pain. Whilst global pain had diminished, foot pain remained. This may have been due to established deformity acquired prior to biologic therapy, or a consequence of foot surgery.

Access to allied healthcare professionals was an area of importance to all participants; all the participants reported finding it difficult to access services, due to a lack of referral, with the common consensus being that "you've got to go and ask for it" (P01). In addition, it is clear that a lack of inter-professional co-ordination hampers effective and timely referral, and the criteria adopted for referral may appear iniquitous.

Access to podiatry services specifically appears particularly problematic, possibly due to a lack of awareness by other professionals of the roles within podiatry.

"...I have never seen a podiatrist ... I've never been recommended to see one..." (P01)

"They [nurses and physicians] feel your knees and sorts of things and see how you can move your ankles but they never seem to bother much about the feet" (P02)

"I'm sure I mentioned it to my GP and rheumatologist umm but I think that was just part of the overall symptoms and my feet individually weren't really looked at" (P04)

Discussion

Exploring the lived experience of individuals with rheumatoid arthritis in receipt of biologic therapy marks a step forward from the work of Bury [ 25] and Williams [ 26], in that it allows a glimpse into the world of patients whose lives have been transformed by these new drugs. Whereas Bury and Williams established and developed the concepts of biographical disruption and biographical reconstruction, the advent of biologics treatment has opened the door to a new dimension in the subsequent normalisation process. In this paper the focus has been on those elements of individual life experience which impact on mobility and self-image, capturing both the life before and the life after biologic therapy. In doing so it allows the links between transformative drug therapy use and personal self-identity to be explored, and to examine ways in which this modifies or reflects the processes outlined by Bury and Williams in their seminal works [ 25, 26]. The participant narratives in this study resonate strongly with those identified by Bury, Williams and others in examining the impact of chronic illness and the disabling effect on mobility and physical changes that effect self-image. Following biologic therapy, the narratives assume a quite different course - an accelerated form of normalisation which brings its own unique problems; notably overuse of joints, ligaments and soft tissues in previously damaged, deformed and vulnerable feet.

Broadly, the experiences of biologic therapy reported by the participants suggested a dramatic and significant improvement in symptoms, enabling a return to near normal activity in some instances. These findings are largely consistent with Marshall et al. and Arkell et al. [ 22, 23], although they explored the effects of anti- TNFα only, rather than the wider group of biologic drugs. Unsurprisingly, the changes noted in those starting biologics were linked to perceived improvements in quality of life (QOL). Similar results were also found in a range of recent quantitative studies, with anti- TNFα treatment shown to significantly improve health related QOL [ 4, 28].

Another important finding from our study was the dramatic improvement in the degree of physical activity and participation possible as a result of biologic therapy. This is consistent with the conclusions reached by other investigators [ 4, 9, 20, 28].

It is clear that the value of the physical improvements resulting from biologic therapy was transformative, bringing with them a feeling of well-being through re-engaging in physical activity. Linden and Bjorklund [ 20] also reported improved physical and mental well-being in patients treated with anti- TNFα, as did Loeppenthin et al. [ 29], where patients were treated with biologics.

In the accounts presented here, it is clear that those participants who experienced a return to near normal physical activity following biologic therapy appeared to normalise rapidly, to the extent that their expectations of life were raised to that of life as it was before the advent of disease. To feel restored to normal function and ability naturally encouraged the participants to attempt to engage in activities in the way they may have done prior to the onset of RA. For those patients with advanced or chronic long standing disease, this may not be a realistic expectation, given the extent of muscle atrophy and fatigue or deformity that may have accumulated over a number of years prior to commencing biologics.

PwRA overstraining themselves due to receding symptoms and a resultant normalisation is highlighted by Linden and Bjorklund [ 20]. Although patients may need to learn to balance their 're-born' lifestyle with enough rest, our findings agree with those of Linden and Bjorklund [ 20] and suggest that further input from allied health professionals may be beneficial in assuming a more measured approach to regaining activity. For PwRA who are positive responders to biologics, those with early access and recent diagnosis may require different interventions to those with long-standing chronic disease, as the latter may have a greater level of tissue damage, deformity or history of surgery. Those PwRA with chronic disease who 'over-do-it' may experience such complications as tissue viability loss due to increased activity involving vulnerable structures, as described by some participants.

In such circumstances podiatrists are able to monitor areas at risk of ulceration occurring from increased demand. Avoiding ulceration is critically important, given the enhanced risk of infection associated with taking biologic drugs, and the potential for flares if treatment is temporarily stopped. Prescription foot orthoses may also provide additional protection and help to minimise the dangers of overuse of the feet.

A lack of choice surrounding footwear could impact upon the negativity expressed regarding the aesthetics of the orthopaedic footwear issued to some patients. This is already acknowledged in the current literature by Williams et al. who suggest that footwear may reinforce a negative self-image [ 30]. Similar themes around identity and footwear were also found by Farndon et al, however they also highlighted conflict in what podiatrists and the people that they support and treat look for in a shoe [ 31]. Biologics might make a person feel better physically, but established deformity is irreversible and a damaged self-image may therefore persist. Footwear aesthetics may need to be acknowledged and addressed by clinicians if patients are to effectively use prescription shoes.

Importantly, if we are to acknowledge that effective response to biologics can lead to improved physical function and increased physical activity, combined with improved foot function, and that 'over use' may be an unintended consequence, then a role in closely monitoring foot health in these patients is clear.

It is also clear that podiatrists may provide that service, as is acknowledged in both the literature and in clinical guidelines, which recommend access to a specialist in foot health such as a podiatrist for assessment and review of foot health needs [ 16, 32, 33]. Despite this, there appears to be a lack of access to podiatry services for PwRA and this has been consistently reported within the recent literature relative to the UK [ 34, 35] and other countries [ 13, 36]. Whilst new models of foot care for PwRA have been proposed [ 37, 38] further exploration of these is recommended for implementation of such strategies within routine practice.

Study limitations

A reflection on the study methodology is relevant, given the sample size was less than expected. By incorporating the experiences of a wider group of people more themes may have been generated, or the current themes identified may have been seen as more or less significant. It is likely that age at diagnosis, disease duration and experiences of illness before accessing biologics are key variables. Although this varied in participants for this study, a larger sample would have enabled comparisons between variables such as differing lengths of disease duration. Finally, recruitment from a support group for PwRA could mean that the participants were well motivated and may have influenced the data obtained. If we had sought participants outside of this group we may have resulted in a different narrative.

Conclusion

The findings from this study advance the work of Bury and Williams, and highlight the personal and social impact of biologic therapy on patient mobility. Most participants experienced dramatic changes in their daily lives due to a reduction in symptoms from effective biologic treatment. However, it is clear that there are consequences to this improvement in function, in that over exertion may lead to further foot problems, highlighting a need for specialist foot health care monitoring and improvements in patient education which could be provided by podiatrists.

Abbreviations

NICE:

National Institute for Health and Care Excellence

NRAS:

National Rheumatoid Arthritis Society

PwRA:

People living with rheumatoid Arthritis

RA:

Rheumatoid arthritis

References

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Acknowledgements

The authors would like to thank all the participants of the study and the health professionals and leaders of NRAS groups who helped with study recruitment.

Funding

This report is independent research arising from LE being supported to undertake a Masters in Clinical Research (MRes) Fellowship from The National Institute for Health Research. The views and opinions expressed herein are those of the authors and do not necessarily reflect those of National Institute for Health Research, NHS or the Department of Health.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Authors' contributions

CB, and LS conceived of the study. LS conducted the interviews and extracted and produced the first draft. LS, MDH, AB, CB, analysed the data. LS, MDH, AB, CB critically reviewed the academic content and participated in producing the final draft. All authors read and approved the final manuscript.

Competing interests

Dr Alan Borthwick is Editor UK and Prof Catherine Bowen is the Deputy Editor UK of the Journal of Foot and Ankle Research. It is journal policy that editors are removed from the peer review and editorial decision-making processes for papers they have co-authored. The remaining authors declare no conflicts of interest in relation to this work.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Full ethical approval for the study was granted by the Faculty of Health Sciences, University of Southampton Ethics Committee via the online approval system ERGO (Ethics and Research Governance Online: Ref 4998, 23.05.13). This was later amended to extend the sample to include patients receiving all current biologics rather than just one specific branch, anti-TNFα (approved 19.07.13).

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Affiliations

1. Faculty of Health Sciences, University of Southampton, Highfield Campus Building 45, University Road, Southampton, Hampshire, SO17 1BJ, UK

Lucy Sanders, Margaret Donovan-Hall, Alan Borthwick & Catherine J. Bowen

2. NIHR Musculoskeletal Biomedical Research Unit, University of Oxford, Oxford, UK

Catherine J. Bowen

Corresponding author

Correspondence to Catherine J. Bowen.

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Sanders, L., Donovan-Hall, M., Borthwick, A. et al. Experiences of mobility for people living with rheumatoid arthritis who are receiving biologic drug therapy: implications for podiatry services. J Foot Ankle Res 10, 14 (2017). https://doi.org/10.1186/s13047-017-0195-4
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Keywords

Rheumatoid arthritis

Biologic therapy

Mobility

Footcare

# data[].attributes.attachment_link.title
Experiences of mobility for people living with rheumatoid arthritis who are receiving biologic drug therapy: implications for podiatry services - Journal of Foot and Ankle Research

# data[].attributes.attachment_link.description
Background Despite significant advancements in new treatment modalities for rheumatoid arthritis with biological therapies, foot complications remain a disabling and common feature of the disease. In this study the aim was to explore and describe the personal experiences of people with rheumatoid arthritis in receipt of biologic treatments in a bid to understand the impact of this form of medication on their mobility.

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-021-00494-4#Sec2

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Clinical foot measurements as a proxy for plantar pressure testing in people with diabetes - Journal of Foot and Ankle Research

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Background High plantar pressures are associated with increased foot ulcer risk in people with diabetes. Identification of high plantar pressures in people with diabetes is clinically challenging due to time and cost constraints of plantar pressure testing. Factors affecting foot biomechanics, inclu…

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-7-22

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Background/aims

Charcot foot is a rare but devastating complication of diabetes. Little research is available on the mental health impact of Charcot foot. Aim of the study is to assess mental health in diabetes patients with Charcot foot and to investigate the moderating effects of socio-demographic factors. The severity of the problem will be statistically evaluated with the help of a reference data set.

Methods

Cross-sectional questionnaire data using the Hospital Anxiety and Depression Scale (HADS) and demographic background were collected from 50 patients with diabetes and Charcot complications (males 62%; mean age 62.2 ± 8.5 years). Statistical comparisons with a large data set of general diabetes patients acting as a point of reference were carried out.

Results

Anxiety and depression levels were high, (anxiety and depression scores 6.4 ± 4 and 6.3 ± 3.6 respectively). Females reported more severe anxiety and depression. Ethnic minorities and patients out of work reported more severe anxiety. Comparisons with published HADS data indicate that diabetes patients with Charcot foot experience more serious levels of anxiety and depression.

Conclusions

The high levels of mental health problems which were found in this study in diabetes patients with Charcot foot require recognition by researchers and clinicians. The findings imply the need to screen for mental health problems in diabetes patients with Charcot foot.

Charcot foot is a rare but potentially devastating complication of diabetes mellitus []. Despite an extensive literature linking diabetes and psychological morbidity, the clinical management of diabetic foot problems does not focus on psychological issues.

Charcot foot, also known as 'neuroarthropathy/neuropathic osteoarthropathy', 'Charcot joint' [] or 'neurogenic osteoarthropathy' [], is a disease of bone that is chronic and progressive, and results in destruction of joints or bones which have lost sensation []. Loss of protective sensory innervation causes neuropathic changes which can render the condition either painful or painless []. No universally accepted criteria for the diagnosis of Charcot foot are available []. Patients may present with inflammation of the foot or ankle [] which may have been triggered by traumatic injury despite no obvious structural damage. The joint area is usually warm and the temperature elevated by between 3 to 6° Celsius []. In the first three weeks of acute Charcot foot there are normally no changes seen on X-ray []. During later stages of Charcot foot radiographic investigation may reveal some evidence of dislocation or fracture of the foot [].

Diabetes mellitus and depression are recognised as two of the most important public health issues in the UK and elsewhere. Major reviews of cross-sectional data argue that as a rule of thumb diabetes increases the risk of depression 2-fold compared to those without diabetes [, ]. However, absolute figures vary as function of type of assessment with questionnaire studies reporting twice the prevalence compared to studies based on psychiatric interviews. This difference has also been observed in non-diabetic populations; the prevalence of depressive disorders in non-diabetic comparison groups, as assessed by full diagnostic interview, has been reported as 5% in a meta-analytic review (9). Both diabetes and depression have profound consequences for individuals and society []. Anxiety can manifest itself in a variety of overlapping neurotic disorders including generalised anxiety disorder, phobias, obsessive-compulsive disorder, post-traumatic stress disorder and panic disorder []. Anxiety symptoms are more common in patients with diabetes compared to those without [].

Psychological comorbidity confers additional risks on patients with diabetes resulting in poorer self-care and poorer outcomes []. Depression in type 2 diabetes has been shown to be associated with twice the rate of a first diabetic foot ulcer over a 4 year follow-up period [] and higher rates of amputation []. In addition depression in first diabetic foot ulcer is associated with a two-fold increase of mortality over 5 years [].

In patients with diabetes, both depression and anxiety levels have been demonstrated to be higher in those with chronic foot ulceration than in controls []. For anxiety, it has been argued that its links with self-care and clinical diabetes outcomes are less clear compared to those of depression; dependent on the nature of the anxiety problem, poorer or even enhanced self-care may be envisaged [].

Existing research has not focused on psychological morbidity in patients specifically with diabetic Charcot foot. Ulcerations and Charcot foot have either been grouped together [] or Charcot foot is not mentioned as a distinct diagnosis []. Existing studies are based on small groups of Charcot patients, but findings specific to this group are not presented in publications []. Foot ulceration is much more common than Charcot foot in diabetes; thus it is not unusual to recruit samples which exclude patients with Charcot foot [, ]. The severity of foot problems in diabetes has been addressed in qualitative research, but only in persons with a diabetic foot ulcer rather than with Charcot foot again suggesting that the latter condition has not been studied specifically in qualitative research either: 'When you stop to think about it [the ulcer] you could just get up and go and now you can't; you're restricted; you have to take care not to knock your leg; you have to be careful that you don't tread on anything that you know is on the ground.' In the same paper a male having lost his job consequent to ulceration is quoted: 'I would lose my life as well. In fact I think I did.'[]. Whether ulceration or Charcot foot is worse, is an open question. However, it is clear that very limited data is available on mental health in patients with diabetes and Charcot foot.

Thus, the aim of the present paper is twofold: (i) to report on mental health on the basis of HADS scores (anxiety and depression symptoms) in patients with diabetes and Charcot foot and (ii) to compare our findings with HADS comparison data in patients with diabetes with and without complications. We shall report full details on our patient group with diabetes and Charcot foot, as the authors are not aware of any recent study specifically recruiting patients with diabetes and Charcot foot.

A cross-sectional questionnaire survey was carried out. A group of patients with a confirmed diagnosis of diabetes with Charcot foot were recruited from a tertiary care facility in South London (King's College Hospital) between March 2010 and July 2010. King's College Hospital diabetic foot clinic is a referral centre for diagnosis and treatment of Charcot foot as well as a variety of other serious foot complications. The main treatment offered for Charcot foot is a total contact cast to stabilise and off load pressure from joints and foot. All patients were recruited from the same clinic waiting area; assistance was provided as and when necessary (e.g. questions were read out to individuals with impaired vision).

Data on anxiety and depression were collected by means of the validated and widely used Hospital Anxiety and Depression Scale (HADS) []. A major advantage of this scale is that it carries a lower risk of confounding diabetes-related and psychological morbidity symptoms compared to some other widely used scales. The internal consistency reliabilities of the HAD sub-scales were calculated using Cronbach's alpha coefficient. Alpha coefficients for anxiety and depression were 0.86 and 0.78 respectively, indicating good reliability. HADS data were initially analysed using standard classifications: the HADS scores for anxiety and depression were categorised into three groups: scores 0-7 "no risk", 8-10 "borderline risk of anxiety or depression" and scores of ≥11 as intermediate or severe risk of anxiety or depressive ("intermediate risk" for short). In addition, anxiety and depression scores were dichotomised using the following cut points: a score between 0 and 7 was classed as normal and a score between 8 - 21 points as increased risk. Diabetes related information and demographics were provided by patients on a self-designed recording sheet: patient age at time of recruitment, gender, self-reported ethnicity, marital status (married/cohabiting, separated/divorced, single, other), occupational status and the foot site affected by Charcot.

The case definition for Charcot foot was: (1) diagnosis by an expert clinician with a confirmed date of diagnosis; (2) Charcot was located in the anatomical foot. Exclusion criteria were any active foot ulceration or amputation, learning disability, inability to read and write in English, pregnancy or lactation, and other significant acute or chronic illnesses. Patients currently receiving psychoactive drugs or psychiatric treatment were excluded because these treatments would be expected to considerable improve anxiety and depression levels and therefore lead to an underestimation of mental health problems in patients with Charcot foot.

Ethical approval was obtained from University of Roehampton, King's College Hospital NHS Foundation Trust and Outer North London Research Ethics Committee (REC Ref No 10/HO724/8). Participants provided informed consent.

Statistical analysis

Data were checked and analysed using Microsoft Excel and SPSS V20. Frequencies and percentages were calculated. Normality assumptions for the HADS scales were not violated (Kolmogorov-Smirnov test p-values >0.10). Means and standard deviations (mean ± SD) are reported for scaled data, but where the focus is on differences or the comparison with reference data (see below) we used 95% confidence intervals. We chose this form of presentation to provide the most relevant information to the reader (standard deviations and confidence intervals can be mutually transformed if relevant sample sizes are provided as we did). Anxiety and depression scores were analysed using dimensional scale scores and also as grouped data, after converting scale scores into 2 or 3 risk categories (full details in results section). Bi-variate comparisons used t-tests. Comparisons with published data from Collins et al. [] will be used as a key point of reference as far as possible; we refer to these data as the reference data. Their relatively large population sample of 1456 patients (general practice and out-patients from the Republic of Ireland) includes 296 patients with type 1 diabetes; both bi- and multi-variate results do not suggest an effect of type of diabetes on anxiety or depression scores. It is therefore justified to carry out the comparisons with these reference data (this approach is supported by Perry as the senior author of the paper, personal communication, 2013) []. All analyses using SPSS applied bootstrap methods to minimise potential problems associated with non-normality and the relatively small Charcot patient group of n = 50. Significance was set at p ≤ 0.05; whenever statistical associations or differences are discussed, they are significant (unless stated otherwise). Full details on statistical findings are provided in tables and figures.

Patient characteristics

Mental health: anxiety and depression

Mental health and demographics

Female patients experience significantly higher levels of anxiety and depression. Full details can be found in Table . Age is not correlated with anxiety or depression scores (p-values >0.50). Following dichotomisation of age into those up to 60 years old and those older than 60, both anxiety and depression scores are lower for the older group, but the differences did not reach significance.

Duration of diabetes and Charcot foot

The mean duration of diabetes was 20.6 (SD = 10.3 years). The mean duration of Charcot foot was 5.0 years (SD = 3.4). Correlations between duration of Charcot foot and anxiety (r50 = 0.23, p = 0.11) and depression scores (r50 = 0.08, p = 0.59) were weak and did not reach significance. We also dichotomised these time-defined variables using the median split. Differences in anxiety and depression scores in relation to diabetes duration (up to 17 years vs longer) and Charcot foot duration (up to 4 years vs longer) were very small and did not reach significance (see Table ).

Comparisons with published HADS data

High levels of anxiety and depression scores and a high prevalence of being at risk of mental health problems were observed in our sample of 50 diabetes patients with Charcot foot. Incidentally the figures are exactly the same for anxiety and depression risks. The literature on mental health in diabetes focuses on depression and only limited data is available on anxiety levels and risks. Comparisons with findings on depression from meta--analyses of general diabetes samples [, ] suggest that in our sample the prevalence for depression risk is double that of around 20% which is typically found for general diabetes samples.

Statistical comparisons with findings from a study which used the HADS in a large sample of diabetes patients (with and without complications) again support the view that diabetes patients with Charcot foot are at a considerably increased risk of anxiety and depression. Further comparisons with this data set on the basis of the number of complications shows that diabetes patients with Charcot foot have significantly higher depression scores than diabetes patients which have 2 or more complications. The figures for anxiety show similar patterns (P <0.10). While we did not collect data on the number of complications in our sample, the trends clearly show that patients with Charcot foot experience high levels of anxiety and depression symptoms. We accept that it is possible or likely that patients in this study are likely to suffer from other complications; this is typical for most studies focusing on advanced complications of diabetes. These additional complications may affect mental health and wellbeing and are of conceptual interest, but for the practitioner it is important to note that patients with Charcot foot, irrespective of the presence or absence of other complications, do suffer from very high levels of depression and to a lesser extent from increased anxiety compared to those patients from our reference sample who have 2 or more complications (26).

Demographic characteristics are linked to mental health in this sample of Charcot patients. Women suffer higher anxiety and depression levels, and members of BME groups and people out of work suffer higher depression levels, but differences for anxiety do not reach significance. Higher levels of anxiety and depression in females are in line with general trends in population samples []. Interestingly differences between the genders are more pronounced in the Charcot sample compared to the general diabetes sample.

Higher depression levels in BME patients and patients out of work are not unexpected and are likely to reflect greater vulnerability to mental health issues []. Marital status is unrelated to mental health, but it is perhaps surprising that single or divorced patients report lower, but statistically non-significant, scores. No associations were found between mental health and disease duration.

HADS data were also reported in a study by Boulton and his colleagues in Manchester (UK) [] on patients with chronic foot ulceration and matched diabetes controls (n =13 and 26 respectively). These authors reported median scores and ranges only for the combined HAD scale (sum of anxiety and depression score): for ulceration the median = 9 (range O-16) and controls the median = 4 (O-26). We calculated the same statistic for the two groups in our study: medians for the entire HAD scale were 14 (0 - 28) for the patients with Charcot foot and 14 (0 - 34) in the comparison group. Our values are considerably higher than those observed by Boulton and colleagues (statistical significance could not be determined for this comparison, due to insufficient data provided in the paper).

This paper presents possibly the first study addressing mental health problems specifically in a sample of diabetes patients with Charcot foot. Another strong point is the use of the HADS scale which carries a lower risk of confounding symptoms of anxiety and depression with symptoms due to diabetes. The PHQ-9 questionnaire which is widely used for the assessment of depression risk, in contrast, contains items which assess symptoms common to depression and diabetes [].

The Charcot patients were carefully identified and confounding with other acute foot problems was kept to a minimum. It needs to be remembered that Charcot foot is a rare condition with an incidence rate of 0.3% per year for a large diabetes clinic in Denmark []. Also all patients were recruited from the same specialist tertiary care centre, facilitating the recruitment of a sizable sample. The instrument for assessing psychological morbidity, i.e. the HADS, is one of the most widely used questionnaires for screening and risk assessment for anxiety and depression. It is accepted that a psychiatric diagnostic interview [] would have been preferable but was not practicable for this study. Future research may also want to consider collecting more details on the history of foot problems and a detailed assessment of the severity of the current state of the Charcot foot, either by clinician judgement or using a system comparable to the Wagner or Texas classification systems [].

There are currently no other studies available examining the mental health status in patients with Charcot foot which would allow direct comparisons with our findings. However there are two studies which have looked at health status using the SF-36 questionnaire in patients with Charcot foot [, ]. They both found that the so-called 'physical health component summary scores' (PCS), which is a measure of physical healthstatus, were lower in patients with Charcot foot when compared to general population data, indicating not surprisingly poorer health status in the Charcot group. Interestingly both papers reported that the so-called 'mental component summary scores' (MCS) which cover aspects of mental health were not different in patients with Charcot foot compared to the general population [, ]. In addition the mean mental and physical component summaries were not affected by gender, ethnicity and Charcot stage []. However, neither of the studies assessed anxiety and depression levels; we interpret these negative findings as reflecting the lack of suitability of the SF-36 as an instrument for adequately assessing mental health in this group of individuals.

Anxiety and depression problems are more severe and more common in diabetes patients with Charcot foot. Female gender, being a member of a BME group and out of work carry additional risks. While problems around depressive symptoms are widely discussed in the general diabetes literature, anxiety is possibly insufficiently recognised. In our sample anxiety scores were particularly high for females. Given the poor outcomes in patients with diabetes and co-morbid depression [] and the availability of effective psychological interventions for patients with diabetic foot complications [], it is important to prevent and treat depression, and to review guidelines accordingly. Whether the same applies to anxiety, cannot be asserted without further studies, but similarly to depression, effective treatments exist for anxiety problems and are provided in the UK through the Improving Access to Psychological Therapies services []. Clinician awareness of the high risk of anxiety and depression in these mostly older and vulnerable adults [, ] should guide appropriate screening and care planning including access to psychological support, hopefully resulting in better outcomes.

Acknowledgements

The data reported in this paper were collected as part of the MSc Dissertation by the first author (MSc Diabetes, University of Roehampton, London). The authors would like to thank and acknowledge the help and support of Professor Michael Edmonds, Professor William Jeffcoate, Pradeep Solanki, Reginald Grant and also the colleagues at King's College Hospital Diabetic Foot Clinic who facilitated data collection. We are also grateful to the reviewers for their helpful comments.

Authors' original submitted files for images

Competing interests

Authors' contribution

ZC developed the idea for the study, collected all the data and road an initial report as part of her MSc dissertation which was supervised by JH. CH and ZC jointly produced the initial manuscript. CH updated literature searches as part of producing the manuscript. JH produced the figures, carried out comparison analysis with other HADS data and revised the manuscript. All authors read and approved the final manuscript.

The authors declare that they have no competing interests.

Below are the links to the authors' original submitted files for images.

# data[].attributes.attachment_link.title
High levels of anxiety and depression in diabetic patients with Charcot foot

# data[].attributes.attachment_link.description
Charcot foot is a rare but devastating complication of diabetes. Little research is available on the mental health impact of Charcot foot. Aim of the study is to assess mental health in diabetes patients with Charcot foot and to investigate the moderating effects of socio-demographic factors.

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/s13047-020-00389-w.pdf

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/s13047-019-0327-0.pdf

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-6-28

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Journal of Foot and Ankle Research 6, Article number: 28 (2013) Cite this article

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Abstract

Background

Ill-fitting footwear can be detrimental to foot health with the forefoot being an area for most discomfort. Studies on footwear have primarily examined sports or orthopaedic prescription shoes and little is known about the effects that everyday flat shoes have on the forefoot. The aim of this study was to investigate the effect of toe box shape in a popular slip-on pump on dorsal and plantar pressures with particular interest around the forefoot in a healthy female population.

Method

A convenience sample of 27 female participants with no known foot pathologies was recruited. After assessment of foot size, plantar foot pressure and interdigital pressures were recorded for each of the 3 different toe box styles; round, square and pointed. Participants walked at a self-selected speed over a 10 m walkway whilst wearing each of the 3 styles of shoe and also whilst barefoot. Processed and analysed data extracted included peak pressure, time to peak pressure, contact time and pressure time integral. ANOVA and Freidman analysis was used to test for statistical significance.

Results

Shoes with a round toe showed least pressure around the medial aspect of the toes whilst the pointed shoe had least pressure on the lateral toes. Contact times for the plantar regions were not altered in any shoe condition yet contact around the medial aspect of the toes was highest in the pointed shoe.

Conclusion

This study highlights that the shape of the toe box in footwear can significantly influence the amount of pressure applied to the forefoot. Furthermore, the contours of the shoe also have an impact on the contact time and pressure time integral around the forefoot and also the peak plantar pressure in the toe region. The changes observed could be significant in the development of pathology in certain footwear toe box shapes. Consideration should be given to footwear design around the toe box to improve fit and reduce pressure. Further work is required to investigate the effect of toe box shape and volume on a pathological population with pressure related lesions.

Peer Review reports

Background

Analysis of the effects footwear has on foot function have previously focused on how changes in material composition, design of heel counter, sole stiffness and thickness and motion control alter whilst wearing the shoe [ 1- 4]. This body of research has focused on running and athletic shoes and results have highlighted that a stiffer heel counter reduces rearfoot motion and improves comfort [ 5, 6]. Sole stiffness and thickness alter stability and balance [ 7- 9] and motion control has a varied impact on rearfoot kinematics [ 6, 10]. However, running and athletic shoes are infrequently chosen by females for everyday use [ 11]. Current research suggests that footwear related pain in the general population is dominated by females who associate up to 60% of foot pain to the shoes that have been worn with the elderly female population reporting a high association between ill fitting footwear and foot pain [ 12].

The concept of ill fitting footwear for females within published literature often leads to the assumption that joint pathologies and deformities are caused by wearing high heels. It is widely reported that the use of a heeled shoe for a prolonged time can have detrimental effects on foot health [ 13- 15]. Studies investigating the effects of heel height have primarily focused on the influence of heel elevation on plantar pressure and triceps surae function rather than any other characteristics this shoe type imposes. Furthermore, these reported changes in increased forefoot pressure and altered triceps surae function do not directly identify the impact high heeled shoes have on toe deformities. Shoe toe box shape and volume may have a similar impact on foot health than the height of the heel. Reduced volume in the toe box causing cramping of the toes has been associated with foot deformities including the development of joint pathologies and forefoot lesions [ 12]. Hammer toe deformity where the interphalangeal joint is often prominent, may cause pain and callus due to irritation from shoe wear [ 16]. Increases in forefoot plantar pressure have been associated with the development of metatarsalgia, callus formation and increased risk of ulceration under the metatarsal heads [ 17- 20]. Treatment of these lesions should provide symptomatic relief and alleviate the underlying mechanical cause yet continuation of ill fitting footwear will ensure these painful conditions persist [ 21].

Most soft tissue lesions can be managed conservatively by the use of shoes with a good fit and appropriate padding to redistribute pressure. Off loading pressure does in fact represent an indispensable precondition both for encouraging the tissue-repair mechanism, where active lesions are present, and for stopping the potential progression of pre-ulcerative conditions toward lesions. Previous studies indicate that for the site to be off loaded effectively, peak pressures needs to be below 99 N/cm ²[ 22, 23]. However, Pressure-time Integral is thought to have a greater role in lesion pathogenesis as the length of time that pressure is applied can be significant in the formation of pathology [ 20, 24].

The forefoot has been highlighted as the most frequent area of pain in subjects who have foot pain related to footwear. Furthermore, subjects who had pain in the forefoot associated that pain with the footwear worn and had a significantly larger circumference of the foot than the subjects without any pain [ 12]. Other studies report similar findings around forefoot shape and fit, in particular the width fitting of shoes worn by two thirds of elderly females has been shown to be too narrow at the toe box [ 25, 26]. This altered fit and disparity between forefoot shape and shoe volume are thought to significantly contribute to the development of toe deformities and the persistence of symptoms that require clinical intervention [ 27]. Changes in footwear from narrow fitting shoes to a broader walker style have shown to reduce the incidence of foot pain [ 28]. Education on the ill-effects of tight fitting footwear is poor and research indicates that footwear in the younger population is influenced by fashion and colour [ 29, 30]. Footwear choice in young females is determined by the activity that is planned with high heels being chosen for socialising, boots for warmth and flat ballet pumps for school [ 11].

This study aimed to investigate differences in toe box volume and shape with a particular focus on peak pressure, time to peak pressure, total contact time and pressure time integral around the dorsal aspect of the forefoot and defined plantar foot regions in a healthy young female population with no known foot pathology.

Methods

Participants

27 asymptomatic healthy females were recruited from a convenience sample with an average age of 22.5 (+/− 4.5) years, body mass of 63.3 (+/− 8.9) kg, height of 1.64 (+/− 0. 6.5) m, shoe size UK 5.5 (+/− 0.8). All recruited subjects gave full consent to participate in the study. Ethical approval was sought and granted from Staffordshire University ethics committee. All subjects included in the study were asymptomatic at the time of testing and were excluded if any musculoskeletal foot pathologies were present, particularly in the forefoot for example: hallux valgus, lesser toe deformities and fifth metatarsophalangeal joint deformities.

Foot sizing measurements for foot length were taken using a Brannock device® to match the foot tested with the appropriate footwear size. A subjective assessment for footwear fitting and comfort was conducted for each subject prior to testing in that shoe. Three types of footwear were used within this study. The key difference in the 3 footwear styles tested was the shape and dimensions of the toe box: square, round and pointed toe (Figure 1). Colour and design were controlled by including black ballet pumps with an accessory feature on the toe box. Subjects were blinded to the brand of the footwear by removing all labelling. Sole thickness and material were assessed and closely matched, however differences in sole material were present. The volume of each shoe's toe box was measured by calculating the average quantity of fine sand that filled the shoe to a level where the toe box upper finished (Figure 1).

Three toe box shapes, (A) round, (B) square and (C) pointed. All shoes were a slip on flat pump. The volume of each shoe was measured using the indicated shoe width and upper for definition of toe box, highlighted by white arrows. The table indicates the volume (cm ³), width and depth (cm) of the toe box for each shoe size tested.

Data collection

Plantar foot pressure was measured for each shoe condition as well as a barefoot condition using a 1 m pressure plate (Footscan®, RsScan Olen, Belgium). The plate was built into the walkway and placed 4 m along a total length of 10 m. This enabled the subjects to attain a normalised walking speed prior to data capture and prevent stepping onto the plate [ 31]. The plate was calibrated to each individual participant's body weight prior to data collection. Each condition was tested in a randomised order determined prior to data collection with subjects choosing a folded card identifying the order of the test condition. There were two successful walking trials collected for barefoot, square shoe, round shoe and pointed shoes.

Interdigital and dorsal pressure was collected separately using Walkinsense® (Tomorrow Options Microelectronics, Portugal). See Figures 2 and 3. This new system allows for individual sensors to be located anywhere on the foot and has been previously validated [ 32]. Eight piezoresistive force 100Hz sensors were individually secured with adhesive tape (Micropore™) to the following landmarks (Figure 3):

Walkinsense equipment. Sensors are 1 cm ² and <1 mm thick.

Sensor placement 1-8 starting at the medial aspect of the 1st metatarsophalangeal joint and finishing on the lateral aspect of the foot at the 5th metatarsophalangeal joint.

1. (i)
medial border of the 1st metatarsophalangeal joint,

2. (ii)
medial border of the 1st interphalangeal joint,

3. (iii)
interdigital (1/2, 2/3, 3/4, 4/5)

4. (iv)
proximal interphalangeal joint,

5. (v)
5th proximal interphalangeal joint

6. (vi)
lateral border of the 5th metatarsal head

Footwear was tested in the same randomised order as the plantar pressure and data were collected from self selected walking speed over a 10 m walkway. Barefoot data was not captured for interdigital and dorsal pressures as recorded data is only captured whilst pressure is exerted on the sensor. Data was captured for a whole gait cycle and the overall pressure was analysed from footstep 3 and 6, these were identified to represent normal walking [ 33].

Data processing and analysis

Plantar pressure data from the pressure platform and dorsal and interdigital pressure data from sensor placement pressure measurement system were averaged and processed to obtain the following measures: peak pressure, time to peak pressure, contact time and pressure time integral. These measures were assessed for each of the 8 individual sensors and for the 10 anatomical areas of the plantar pressure recording (heel lateral, heel medial, midfoot, metatarsal 1,2,3,4 and 5, 1st digit and toes 2-5) [ 34].

Processed data was then statistically analysed using SPSS ver.19 (IBM, USA). Each data set was assessed for normalcy and those test conditions meeting all parametric assumptions were statistically analysed using a one way repeated measures analysis of variance (ANOVA). Test conditions that failed to meet all assumptions for parametric testing were analysed using the non parametric alternative Freidman Test with significant results being further analysed with a post hoc Wilcoxon Signed Rank Test with a Bonferroni adjusted alpha value.

Results

The volume for each shoe tested varied between style and size (Figure 1). The round shoe shape had the least volume in the toe box across all sizes and the square toed shoe had the highest volume except in size 5.

Peak pressure

Statistical tests showed a significant difference between shoe conditions for peak pressure at sensor 1, 2, 3, 4, 7 and 8 with the round shoe condition producing the least amount of pressure for sensor 1, 2, 3, 4 and 8. The pointed shoe applied the least pressure over sensor 6 and 7 which were applied on the fifth digit, with the square shoe producing the most pressure over this digit. Mean plantar peak pressure was significantly different across all masked areas of the foot with the exception of the second metatarsal where no difference was observed. Pointed shoes demonstrated the highest peak plantar pressure at the medial heel yet this shoe condition was the lowest pressure value for the toe regions (Tables 1 and 2).

Table 1 Interdigital and dorsal pressure results - mean (SD)

Table 2 Plantar pressure results - mean (SD)

Time to peak pressure

Results from sensors 2, 4, 5 and 8 demonstrated significant differences, with the round shoe condition demonstrating an earlier time to peak pressure in all 8 sensors. Plantar foot regions demonstrated exhibited similar time to peak pressure in all of the masked regions however there was a significant difference between the barefoot condition and all shoe conditions (Tables 1 and 2).

Contact time

Sensors 2, 3, 4 and 5 and the toe regions showed significant differences in contact time, whilst all other sensors and plantar foot regions showed no differences between shoe shape and barefoot conditions. The square shaped shoe and pointed shoe was where the significance fell with a pointed shoe being in contact with the foot for longer periods of time on the dorsal aspect of the foot and the square shoe being in contact with the toes two - five in the plantar aspect of the foot.

Pressure time integral

Sensors 2, 3, 4 and 8 showed variable significant differences between the pointed shoe having a higher pressure time integral at 2, 3 and 4 and the round shoe being significantly lower at sensor 8. The midfoot region, first toe and toes −2-5 were areas that also showed a significant difference between conditions, with variance lying between the pointed shoe at the midfoot (having a significant lower pressure time integral than the other conditions) and the square shoe conditions. The barefoot condition had a higher pressure time integral around the plantar region of the toes 2-5.

Discussion

The results of this study clearly indicate that the shape of a shoe's toe box has a significant impact on dorsal and plantar pressures of the foot. Round toe shoes were shown to produce less peak pressure around the medial aspect of the foot, and the pressure time integral is also lower in this region. Conversely, the pointed style of shoe distributed the least amount of pressure in the lateral toe area. These observations can be related directly to the dimension and shaping of each the round and pointed shoe styles which correlate to the natural anatomical contours of the foot. However, the volume of the shoe was not correlated to forefoot pressure, with the round shoe having the least volume in the toe box across all shoe sizes tested and this condition demonstrated the lowest pressure values. This lack of correlation might be due to the stylised point of the shoe. This pointed shoe has an extended length to the normal foot contour, which increases the measured volume but does not alter the toe pressure due to lack of direct contact. The shape of the toe box therefore should be considered as a cause of increased forefoot pressure and not just the width of the shoe as previously mentioned as a problematic design of ill-fitting footwear [ 12, 25, 26].

The dorsal digital area showed higher peak pressure on the medial side of the foot whilst wearing a square and pointed shoe shape, with the design of the shoes encroaching on the natural shape of the first digit. Similarly this correlation of shoe shape and foot shape was also seen in the square toed shoe which exerted the highest amount of peak pressure over the fifth digit. The gradient of the lateral border of the toe box was similar both in the square shaped and the pointed shoe. There was greater variability regarding regional significance of peak plantar pressure in the masked areas of the plantar pressure with each shoe condition showing significance at different regions of the foot. The sole material of each shoe was not controlled within the study design and will have altered plantar pressure distribution and results. Although care was taken to choose three designs that only differed by toe box shape it was difficult to replicate the same sole characteristics. However, the round shoe shape did consistently result in higher peak plantar pressure within the forefoot region accompanied by lower dorsal peak pressures around the medial forefoot. This could be due to a lower recorded volume of the toe box and possible cramping of the normal toe profile altering toe function and plantar pressure during toe off.

It is also worth highlighting that the pointed shoe condition produced a significantly higher peak plantar pressure at the medial heel region than then other shoes. The pointed shoe that was tested had a more flexible heel counter compared to the other two shoe conditions, this feature had not be controlled for, which could possibly explain the increased medial heel pressure due to lack of structure.

The time to reach peak plantar pressure differed only at the masked toe region with all shoe conditions reducing the time to peak pressure compared to the barefoot condition. The contact time for this region was also lower for all shoe conditions excluding the shoes with a square toe which resembled the barefoot condition. This could be due to the stiffness of the sole of the shoe rather than the shape of the toe box which resulted in the toe area having reduced contact. The dorsal aspect of the foot around the fifth metatarsal and the first digit were most different when wearing the pointed shoe with increased time to peak pressure and contact in these regions. This shoe shape intensifies pressure over the border of the forefoot due to its angular shape.

There were significant differences between footwear conditions when analysing the pressure time integral data, which has been identified as significant when considering chronic tissue strain in the formation of callus and other hyperkeratotic skin lesions [ 20, 24]. The lateral border of the foot around the fifth metatarsal and digit exhibited the greatest differences when wearing the pointed shoe with a lower pressure time integral. The square shoe condition had the highest pressure time integral around this area. The fit of the foot in this style of shoe due to its dimension and the lack of control for heel to ball of foot measure could have induced this higher result with the alignment of the toes differing between participants.

Clinical presentation of hyperkeratotic skin lesions around the 5th digit could therefore be due to the shape of the shoe toe box rather than the perception of whether the shoe is a good fit or not. For example, a well supported lace up shoe with a pointed or square toe box may cause lateral irritation to the foot even though it is deemed a good fit elsewhere.

The results of this study did not exceed the reported peak pressure values of over 99Ncm ², which have been acknowledged to be the threshold for tissue damage [ 22, 23]. The recorded forefoot pressures studied were purposefully from a sample with no known pathological foot problems to gather pre-pathology data. The inclusion of toe deformities and forefoot pain may present with differing results. There is, however, a lack of information to define what quantity of pressure is required to develop chronic responses to mechanical strain with the common formation of hyperkeratotic callus, and further studies into this area are recommended.

The fifth toe and interdigital fourth and fifth area are common locations to develop focal chronic callus lesions. The results from this study suggest that the shape of the toe box may play a part in the development of such lesions with the lateral border of the forefoot resulting in higher peak pressure and pressure time integrals in the square shoe. An increase in pressure may be attributed to the graduation of the toe box shape if does not follow the anatomy of the foot. Changes to footwear style may help to reduce the incidence of these common problems and improve comfort for many females. Cases have been reported where the fifth digit has been amputated to accommodate the foot in a desired shoe [ 35]. Further research into the impact of footwear styling at the toe box on pathological feet is recommended.

Considering the results from this study, development of shoe design needs to advance to encompass an accepted toe box for fashion as well as foot health. This may involve the medial border of the shoe around the 1st metarsalphalangeal joint and the first toe being designed in a round shape and the lateral border around the 5th interphalangeal joint having a pointed graduated shape. These style features could minimise peak pressure, contact times and consequently pressure time integral in the forefoot. This style and shape of shoe is infrequently seen in the market place with the majority of footwear styles adopting a narrowed toe box with equal shaping to the medial and lateral side of the shoe. By limiting consumer choices on footwear shape people are forced to choose footwear that has been shown to alter pressure to the forefoot. Providing footwear choices that do not impact on forefoot pressure could prevent pathologies that are associated with ill fitting shoes.

There are limited studies to investigate the impact that footwear shape and style have on foot pathologies however, there are strong links between foot pain and ill fitting footwear especially in the elderly population [ 36]. Footwear choices are led by fashion and image rather than health [ 11, 29, 30]. Changes in footwear design for younger adults, to accommodate natural foot position and shape, may be a useful way to help prevent painful foot pathologies and deformities occurring prior to old age.

The style of footwear investigated in this study was determined by fashion and the most popular choice amongst young females [ 11]. Although, the fit of the foot in the shoe around the toe box may alter with increased heel height, fastening of the shoe, shoe upper material and also last shape, the conclusions outlined in this manuscript do not address these factors. Further structured investigation into quantifying the pressure under the upper is required. Furthermore, there should be a detailed examination of all shoe styles with varied toe box shapes. The pointed shoe employed within this investigation was longer in the toe box region than the square and round shoe and therefore had an increased volume. The styled extension of this toe box may have masked the actual fit of the foot inside the shoe. This might require further scientific study of the relationship between design and function. In addition to this, studying a population with foot pathology will help in understanding the contribution footwear style makes to development of foot disorders.

Conclusion

The shape of the toe box can alter the pressure applied to the forefoot around the digits and plantar aspect of the foot in healthy young women with no known foot pathology. Hence, footwear advice with reference to the shape of the toe box is essential in the management of pressure related lesions and when preventative measures are being considered.

Author information

Author notes

Affiliations

1. Centre for Sport, Health and Exercise Research, Faculty of Health Sciences, Staffordshire University, Leek Road, Stoke on Trent, ST4 2DF, UK

Helen Branthwaite, Nachiappan Chockalingam & Andrew Greenhalgh

2. London Sport Institute, School of Health and Social Science, Middlesex University, Hendon, NW4 4BT, London, UK

Andrew Greenhalgh

Corresponding author

Correspondence to Helen Branthwaite.

Additional information

Competing interests

All authors involved in this manuscript can declare that they had no competing interests.

Authors' contributions

HB led this study and was involved in the study design, data collection and extraction including statistical analysis and prepared this manuscript. AG wrote the code to extract and process all the raw data. NC was involved in the design of the study and the preparation of the manuscript. All authors reviewed and agreed on the final manuscript before submission.

Helen Branthwaite, Nachiappan Chockalingam and Andrew Greenhalgh contributed equally to this work.

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Branthwaite, H., Chockalingam, N. & Greenhalgh, A. The effect of shoe toe box shape and volume on forefoot interdigital and plantar pressures in healthy females. J Foot Ankle Res 6, 28 (2013). https://doi.org/10.1186/1757-1146-6-28
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Keywords

Foot pressure

Shoe shape

Digital pressure

Footwear

Toe box

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The effect of shoe toe box shape and volume on forefoot interdigital and plantar pressures in healthy females - Journal of Foot and Ankle Research

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Background Ill-fitting footwear can be detrimental to foot health with the forefoot being an area for most discomfort. Studies on footwear have primarily examined sports or orthopaedic prescription shoes and little is known about the effects that everyday flat shoes have on the forefoot.

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-018-0296-8

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Charcot neuroarthropathy patient education among podiatrists in Scotland: a modified Delphi approach - Journal of Foot and Ankle Research

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Background This evaluation sought to determine current Charcot neuroarthropathy (CN) diabetes patient education practices among Scottish National Health Service (NHS) and academic podiatrists and evaluate novel visual tools and develop expert consensus for future practice. Methods Questionnaires col…

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00422-y

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1. Introduction

Diabetes mellitus (DM) is the most common endocrine metabolic disease, and its prevalence has been increasing steadily all over the world with recently diagnosed cases (1,2). The most significant and devastating complications of diabetes are foot ulcers and other foot problems causing major morbidity and mortality in patients with DM. Diabetes mellitus generally affects the lower extremities more than the upper extremities, leading to death in some cases. The treatment period of the ulcers lasts for a long time, and active ulcers can lead to limb amputation due to poor treatment (3-7). Diabetic foot complications are the most common causes of nontraumatic lower extremity amputations and are associated with a five-year mortality rate of 43% to 55%, which is even higher than some common types of cancer such as Hodgkin's disease, breast and prostate cancers (8-10).

Several pathogenic abnormalities, such as intrinsic flaws in the blood supply, angiogenesis, and other extrinsic factors, such as infections and continued trauma, contribute to failure of recovery from diabetic foot ulcers (11,12). Organisms causing diabetic foot infection (DFI) are not often identified completely by clinical laboratories. Although recent articles state that DFIs are usually polymicrobial, few papers from the literature report a low incidence of fungal isolation from the diabetic foot wound. Despite current treatment modalities for nonhealing diabetic foot ulcers, following systemic antifungal therapy will lead to improvement (13-21).

In spite of the evidence for fungal infection in diabetic foot lesions, clinicians and surgeons treat diabetic foot wounds as if they could only be bacterial infections and treat them with antibacterial agents. They often neglect fungal infections and do not routinely investigate deep tissue from the wound bed for fungal culture and sensitivity due to insufficient information in the literature. In this study, we aimed to evaluate fungal etiology of invasive fungal DFI which is rarely reported in the literature.

3. Results

Bone or deep tissue cultures were positive in 13 patients who were diagnosed with diabetic foot infection (ten females, three males, mean age 59.8 ± 9 years). Age, sex, diabetes type, HbA1c level, CRP, osteomyelitis, vasculopathy, neuropathy, response to antibacterial therapy, wound characteristics, treatment types and results, and bacteriology and mycology of the ulcers were summarized in Table. Six patients had a history of prior diabetic foot infection and decreased lower extremity arterial perfusion.

One of the patients refused amputation; therefore, only antifungal therapy was given. Five of the patients received antifungal therapy in addition to surgical treatment. Since two patients had died of cerebrovascular pathology before the culture results were available, antifungal therapy could not be started. Despite amputation, five patients had fungal growth in the culture. In spite of fungal growth in the culture, antifungal therapy was not given to these five patients thanks to adequate and clean surgical wound area at amputation level. Mixed infections were observed in 11 of 13 patients and pure fungal infections in two. The most common cause of fungal infections of diabetic foot ulcers was the Candida species (Table).

4. Discussion

Diabetes mellitus is the most common endocrine metabolic disease and its incidence is increasing rapidly. Foot ulcers and their complications are major causes of morbidity and mortality as are other complications in people with DM (12,22). Little is known about invasive fungal infections in the literature because there are only a few studies on osteomyelitis caused by fungal pathogens. The reasons are that clinicians do not routinely request fungal culture and sensitivity test for deep tissue from the wound bed due to lack of literature support and that fungi are neglected as causative agents after cultivating bacteria in the cultures. Patients with poorly-controlled diabetes are more prone to fungal infections (23). According to a brief overview of the literature, the rate of fungal isolation from diabetic foot ulcers varies from 5% to 27% (13-21,23). Chellan et al. (13) reported the incidence of fungal infections in patients with diabetic foot ulcer as 27.2%. The present study is retrospective and aims to reveal the fungal infections of diabetic foot ulcers analyzed from tissue biopsies in patients who did not recover despite proper antibacterial therapy. This is one of the large series that have been reported in the literature about invasive fungal infections as causative pathogens in diabetic foot infections.

Eckhard et al. (18) stated that fungal foot infection in patients with diabetes was correlated with age, sex, and duration of diabetes. Males were more frequently affected than females. Only HbA1c level was found to be significant in the incidence of fungal foot infection in the type-2 DM group. Although another study noted no difference in fungal foot infection rates among patients' age, sex, depth of wound, duration of diabetes, it was mentioned that poor and inadequate glycemic control among diabetes patients is a risk factor for fungal infection (13). Raiesi et al. (23) compared skin and nail fungal infections with diabetic foot ulcers. Only the type of diabetes was significantly different in diabetic foot ulcers, and no significance was revealed in the average age of patients and the duration of diabetes. Skin and nail lesions were more common in type-2 DM patients whereas diabetic foot ulcers were more common in type-1 DM patients. Although the ratio of fungal infection was 19.1% in diabetic foot ulcers, it was 28% in patients with skin and nail lesions. In this study, all cases suffered from type-2 DM (duration of 1-23 years, mean duration: 12-15 years). Most of the patients were male, only three were female. The mean age was 60.1 (50-79).

Diabetic foot infections are multifactorial processes involving neuropathy, peripheral vascular disease, and susceptibility to infection, all contributing to tissue damage. Vasculopathy and neuropathy often lead to nonhealing ulcers coupled with recurrent soft-tissue infections and subsequent osteomyelitis of foot bones (24). In this study, 11 of the 13 patients had vasculopathy, 10 of the 13 patients had neuropathy, and eight patients had both vasculopathy and neuropathy. Osteomyelitis was present in all cases except for two. Although vasculopathy and neuropathy play a central role, osteomyelitis was not observed in those two patients who had vasculopathy and neuropathy. It is suggested that some factors disrupting skin integrity should also be included in the development of diabetic foot infections.

Diabetic foot infections are often polymicrobial (25). Acute infections are usually caused by gram-positive cocci ( Staphylococcus aureus, B-hemolytic streptococci). However, gram-positive cocci and Enterobacteriaceae, diphtheroid species, Pseudomonas aeruginosa, other nonfermentative gram-negative bacilli and fungi are mostly observed in long-term nonhealing wounds, which are treated with long-term broad-spectrum antibiotic therapy. In the wounds, these are necrotic or ischemic and the most common causative agents are anaerobes (26-29). In line with the literature, concurrent bacterial infections were also detected in 11 of 13 patients with fungal diabetic foot infections. Seven patients responded to antibacterial therapy partially, whereas five patients did not benefit from it. In spite of the partial response to antibacterial therapy, six of them underwent surgical treatment. Despite the antifungal therapy, gram-negative bacteria accompanied fungi in the two patients who underwent amputation. Infection caused by the Candida species was observed only in two patients. Before the culture results were out, one of the patients had amputation and the other died. Four of six patients who had gram-negative bacterial infection also underwent amputation without culture results. Three of 13 patients, who were given antifungal therapy, recovered without surgery. Early initiation of therapy may reduce morbidity in cases when antibiotic treatment is not successful due to possible fungal infection.

In patients with diabetes, fungal foot infections like tinea pedis and onychomycosis are even more common inflammatory skin diseases compared to general population (23,26-31). The predisposing factors, which are high blood glucose, vasculopathy, neuropathy and various immunological disturbances, facilitate conditions for colonization of pathogen fungi, including Candida spp., Dermatophytes, Malassezia, Mucorales, Aspergillus, and Fusarium spp. (29). These fungi can also be caused by skin and soft tissue infections or onychomycosis in patients whose feet remain in moisture for a long time, or in cases of poor hygiene and trauma. Many studies show that fungal infections of the skin and nails including tinea infections are risk factors for cellulitis (31). The presence of superficial fungal foot infections could not be assessed and this was a limitation of our study. Many studies consistently identified fungal foot infection as a factor in the development of cellulitis, especially inter-digital rather than plantar and nail infections (31). Similar to our study, the most common pathogen in the literature is Candida spp. (13-21,23). Candida and other superficial fungal infections lead to a combination of higher humidity and thinner skin, which makes it more susceptible to infection (31). In DM, some pathogens other than bacteria like myiasis can cause delayed healing of the wound or even death of a patient because of distribution of integrity of the skin and immune system as well as poor self-care (32). Opportunistic fungi may invade deep into the wounds and contribute to delayed wound healing in some of the patients with diabetes who are otherwise immunocompromised when compared to the group without diabetes (11). If these infections are not noticed in time, these fungi colonize and damage the integrity of the skin, cause secondary infection through fissures, and increase the risk of soft tissue infections on the affected extremities. Although there is no evidence of fungal infection in the skin and nails of the patients, the infection is thought to develop after colonization.

Mold infections are less common but more progressive than Candida spp. However, factors such as uncontrolled diabetes, presence of other underlying diseases, trauma, poor foot care, and recurrent infections may predispose the development of mold infections. There are only a few case reports that present causative fungal pathogens: calcaneal osteomyelitis is caused by Aspergillus ochraceus and infections of flexor digitorum-peroneal tendon sheaths by Blastomyces (33,34). Osteomyelitis is caused by the Fusarium species, filamentous fungi present as saprophytes in soil and animals, was first reported in a patient with diabetes by Bader et al. (30). Fusarium spp. is also the cause of onychomycosis (30,35). It is stated that osteomyelitis caused by the progression of skin and soft tissue infections may be originated from patient's onychomycosis. Skin and nails are the main portals of entry, and cutaneous infections often develop after skin breakdown at the infection site and are present as necrotic lesions, cellulitis, chronic ulcers, and abscesses (30). In this study, only three patients had mold infections and the Fusarium species were causative; although one of the patients was amputated, the other two recovered after the antifungal treatment. Since the cases in this study were evaluated retrospectively, the presence of any fungal skin lesion or onychomycosis was not known before the diagnosis of diabetic foot infection.

The proper management of DFI needs appropriate antibiotic selection (22). Despite a proper surgical and antibacterial therapy, the outcome of patients could be poor and wound healing may be delayed up to 18 weeks (24,36,37). Several pathogenic abnormalities from intrinsic flaws in blood supply, angiogenesis, and matrix turnover to extrinsic factors such as infections and continued failure of recovery lead to diabetic foot ulcers trauma (11).

Chellan et al. (13) mentioned the importance of studying the pathogenicity of fungi in deep tissues of DFI and their possible contribution to delayed wound healing. They also revealed that the use of antifungal therapy besides antimicrobial therapy for invasive fungal infections in diabetic foot not only reduces the wound size rapidly but also leads the way to complete healing. It was shown that fluconazole and standard treatments were more effective than the standard treatment alone in diabetic foot patients with invasive fungal infections in terms of wound size reduction and complete wound healing. Hence, it is important to investigate all specimens from DFI for the presence of fungi in addition to bacteria. These patients should be treated with culture-specific antifungal agents along with antibacterial agents (13,21). Heald et al. (14) mentioned that the Candida species is associated with long term nonhealing wounds in diabetic foot which heals after systemic antifungal therapy.

In conclusion, it is important to suspect invasive fungal infections in patients with uncontrolled glucose levels and in patients unresponsive to antibacterial treatment. Although rare, invasive fungal infections can cause diabetic foot infections long before the detection of neuropathy and vasculopathy, which are first tested in order to prevent foot infections. Early detection of fungal infections in high‑risk individuals is critical for the prevention of severe consequences such as foot amputation. Diabetic foot infections require the utmost attention and a multidisciplinary foot care team including an infectious disease specialist and a medical microbiologist.

# data[].attributes.attachment_link.title
A neglected causative agent in diabetic foot infection: a retrospective evaluation of 13 patients with fungal etiology

# data[].attributes.attachment_link.description
Diabetes mellitus (DM) is the most common endocrine metabolic disease, and its prevalence has been increasing steadily all over the world with recently diagnosed cases (1,2). The most significant and devastating complications of diabetes are foot ulcers and other foot problems causing major morbidity and mortality in patients with DM.

# data[].attributes.attachment_link.readable_text
1. Introduction

Diabetes mellitus (DM) is the most common endocrine metabolic disease, and its prevalence has been increasing steadily all over the world with recently diagnosed cases (1,2). The most significant and devastating complications of diabetes are foot ulcers and other foot problems causing major morbidity and mortality in patients with DM. Diabetes mellitus generally affects the lower extremities more than the upper extremities, leading to death in some cases. The treatment period of the ulcers lasts for a long time, and active ulcers can lead to limb amputation due to poor treatment (3-7). Diabetic foot complications are the most common causes of nontraumatic lower extremity amputations and are associated with a five-year mortality rate of 43% to 55%, which is even higher than some common types of cancer such as Hodgkin's disease, breast and prostate cancers (8-10).

Several pathogenic abnormalities, such as intrinsic flaws in the blood supply, angiogenesis, and other extrinsic factors, such as infections and continued trauma, contribute to failure of recovery from diabetic foot ulcers (11,12). Organisms causing diabetic foot infection (DFI) are not often identified completely by clinical laboratories. Although recent articles state that DFIs are usually polymicrobial, few papers from the literature report a low incidence of fungal isolation from the diabetic foot wound. Despite current treatment modalities for nonhealing diabetic foot ulcers, following systemic antifungal therapy will lead to improvement (13-21).

In spite of the evidence for fungal infection in diabetic foot lesions, clinicians and surgeons treat diabetic foot wounds as if they could only be bacterial infections and treat them with antibacterial agents. They often neglect fungal infections and do not routinely investigate deep tissue from the wound bed for fungal culture and sensitivity due to insufficient information in the literature. In this study, we aimed to evaluate fungal etiology of invasive fungal DFI which is rarely reported in the literature.

3. Results

Bone or deep tissue cultures were positive in 13 patients who were diagnosed with diabetic foot infection (ten females, three males, mean age 59.8 ± 9 years). Age, sex, diabetes type, HbA1c level, CRP, osteomyelitis, vasculopathy, neuropathy, response to antibacterial therapy, wound characteristics, treatment types and results, and bacteriology and mycology of the ulcers were summarized in Table. Six patients had a history of prior diabetic foot infection and decreased lower extremity arterial perfusion.

One of the patients refused amputation; therefore, only antifungal therapy was given. Five of the patients received antifungal therapy in addition to surgical treatment. Since two patients had died of cerebrovascular pathology before the culture results were available, antifungal therapy could not be started. Despite amputation, five patients had fungal growth in the culture. In spite of fungal growth in the culture, antifungal therapy was not given to these five patients thanks to adequate and clean surgical wound area at amputation level. Mixed infections were observed in 11 of 13 patients and pure fungal infections in two. The most common cause of fungal infections of diabetic foot ulcers was the Candida species (Table).

4. Discussion

Diabetes mellitus is the most common endocrine metabolic disease and its incidence is increasing rapidly. Foot ulcers and their complications are major causes of morbidity and mortality as are other complications in people with DM (12,22). Little is known about invasive fungal infections in the literature because there are only a few studies on osteomyelitis caused by fungal pathogens. The reasons are that clinicians do not routinely request fungal culture and sensitivity test for deep tissue from the wound bed due to lack of literature support and that fungi are neglected as causative agents after cultivating bacteria in the cultures. Patients with poorly-controlled diabetes are more prone to fungal infections (23). According to a brief overview of the literature, the rate of fungal isolation from diabetic foot ulcers varies from 5% to 27% (13-21,23). Chellan et al. (13) reported the incidence of fungal infections in patients with diabetic foot ulcer as 27.2%. The present study is retrospective and aims to reveal the fungal infections of diabetic foot ulcers analyzed from tissue biopsies in patients who did not recover despite proper antibacterial therapy. This is one of the large series that have been reported in the literature about invasive fungal infections as causative pathogens in diabetic foot infections.

Eckhard et al. (18) stated that fungal foot infection in patients with diabetes was correlated with age, sex, and duration of diabetes. Males were more frequently affected than females. Only HbA1c level was found to be significant in the incidence of fungal foot infection in the type-2 DM group. Although another study noted no difference in fungal foot infection rates among patients' age, sex, depth of wound, duration of diabetes, it was mentioned that poor and inadequate glycemic control among diabetes patients is a risk factor for fungal infection (13). Raiesi et al. (23) compared skin and nail fungal infections with diabetic foot ulcers. Only the type of diabetes was significantly different in diabetic foot ulcers, and no significance was revealed in the average age of patients and the duration of diabetes. Skin and nail lesions were more common in type-2 DM patients whereas diabetic foot ulcers were more common in type-1 DM patients. Although the ratio of fungal infection was 19.1% in diabetic foot ulcers, it was 28% in patients with skin and nail lesions. In this study, all cases suffered from type-2 DM (duration of 1-23 years, mean duration: 12-15 years). Most of the patients were male, only three were female. The mean age was 60.1 (50-79).

Diabetic foot infections are multifactorial processes involving neuropathy, peripheral vascular disease, and susceptibility to infection, all contributing to tissue damage. Vasculopathy and neuropathy often lead to nonhealing ulcers coupled with recurrent soft-tissue infections and subsequent osteomyelitis of foot bones (24). In this study, 11 of the 13 patients had vasculopathy, 10 of the 13 patients had neuropathy, and eight patients had both vasculopathy and neuropathy. Osteomyelitis was present in all cases except for two. Although vasculopathy and neuropathy play a central role, osteomyelitis was not observed in those two patients who had vasculopathy and neuropathy. It is suggested that some factors disrupting skin integrity should also be included in the development of diabetic foot infections.

Diabetic foot infections are often polymicrobial (25). Acute infections are usually caused by gram-positive cocci ( Staphylococcus aureus, B-hemolytic streptococci). However, gram-positive cocci and Enterobacteriaceae, diphtheroid species, Pseudomonas aeruginosa, other nonfermentative gram-negative bacilli and fungi are mostly observed in long-term nonhealing wounds, which are treated with long-term broad-spectrum antibiotic therapy. In the wounds, these are necrotic or ischemic and the most common causative agents are anaerobes (26-29). In line with the literature, concurrent bacterial infections were also detected in 11 of 13 patients with fungal diabetic foot infections. Seven patients responded to antibacterial therapy partially, whereas five patients did not benefit from it. In spite of the partial response to antibacterial therapy, six of them underwent surgical treatment. Despite the antifungal therapy, gram-negative bacteria accompanied fungi in the two patients who underwent amputation. Infection caused by the Candida species was observed only in two patients. Before the culture results were out, one of the patients had amputation and the other died. Four of six patients who had gram-negative bacterial infection also underwent amputation without culture results. Three of 13 patients, who were given antifungal therapy, recovered without surgery. Early initiation of therapy may reduce morbidity in cases when antibiotic treatment is not successful due to possible fungal infection.

In patients with diabetes, fungal foot infections like tinea pedis and onychomycosis are even more common inflammatory skin diseases compared to general population (23,26-31). The predisposing factors, which are high blood glucose, vasculopathy, neuropathy and various immunological disturbances, facilitate conditions for colonization of pathogen fungi, including Candida spp., Dermatophytes, Malassezia, Mucorales, Aspergillus, and Fusarium spp. (29). These fungi can also be caused by skin and soft tissue infections or onychomycosis in patients whose feet remain in moisture for a long time, or in cases of poor hygiene and trauma. Many studies show that fungal infections of the skin and nails including tinea infections are risk factors for cellulitis (31). The presence of superficial fungal foot infections could not be assessed and this was a limitation of our study. Many studies consistently identified fungal foot infection as a factor in the development of cellulitis, especially inter-digital rather than plantar and nail infections (31). Similar to our study, the most common pathogen in the literature is Candida spp. (13-21,23). Candida and other superficial fungal infections lead to a combination of higher humidity and thinner skin, which makes it more susceptible to infection (31). In DM, some pathogens other than bacteria like myiasis can cause delayed healing of the wound or even death of a patient because of distribution of integrity of the skin and immune system as well as poor self-care (32). Opportunistic fungi may invade deep into the wounds and contribute to delayed wound healing in some of the patients with diabetes who are otherwise immunocompromised when compared to the group without diabetes (11). If these infections are not noticed in time, these fungi colonize and damage the integrity of the skin, cause secondary infection through fissures, and increase the risk of soft tissue infections on the affected extremities. Although there is no evidence of fungal infection in the skin and nails of the patients, the infection is thought to develop after colonization.

Mold infections are less common but more progressive than Candida spp. However, factors such as uncontrolled diabetes, presence of other underlying diseases, trauma, poor foot care, and recurrent infections may predispose the development of mold infections. There are only a few case reports that present causative fungal pathogens: calcaneal osteomyelitis is caused by Aspergillus ochraceus and infections of flexor digitorum-peroneal tendon sheaths by Blastomyces (33,34). Osteomyelitis is caused by the Fusarium species, filamentous fungi present as saprophytes in soil and animals, was first reported in a patient with diabetes by Bader et al. (30). Fusarium spp. is also the cause of onychomycosis (30,35). It is stated that osteomyelitis caused by the progression of skin and soft tissue infections may be originated from patient's onychomycosis. Skin and nails are the main portals of entry, and cutaneous infections often develop after skin breakdown at the infection site and are present as necrotic lesions, cellulitis, chronic ulcers, and abscesses (30). In this study, only three patients had mold infections and the Fusarium species were causative; although one of the patients was amputated, the other two recovered after the antifungal treatment. Since the cases in this study were evaluated retrospectively, the presence of any fungal skin lesion or onychomycosis was not known before the diagnosis of diabetic foot infection.

The proper management of DFI needs appropriate antibiotic selection (22). Despite a proper surgical and antibacterial therapy, the outcome of patients could be poor and wound healing may be delayed up to 18 weeks (24,36,37). Several pathogenic abnormalities from intrinsic flaws in blood supply, angiogenesis, and matrix turnover to extrinsic factors such as infections and continued failure of recovery lead to diabetic foot ulcers trauma (11).

Chellan et al. (13) mentioned the importance of studying the pathogenicity of fungi in deep tissues of DFI and their possible contribution to delayed wound healing. They also revealed that the use of antifungal therapy besides antimicrobial therapy for invasive fungal infections in diabetic foot not only reduces the wound size rapidly but also leads the way to complete healing. It was shown that fluconazole and standard treatments were more effective than the standard treatment alone in diabetic foot patients with invasive fungal infections in terms of wound size reduction and complete wound healing. Hence, it is important to investigate all specimens from DFI for the presence of fungi in addition to bacteria. These patients should be treated with culture-specific antifungal agents along with antibacterial agents (13,21). Heald et al. (14) mentioned that the Candida species is associated with long term nonhealing wounds in diabetic foot which heals after systemic antifungal therapy.

In conclusion, it is important to suspect invasive fungal infections in patients with uncontrolled glucose levels and in patients unresponsive to antibacterial treatment. Although rare, invasive fungal infections can cause diabetic foot infections long before the detection of neuropathy and vasculopathy, which are first tested in order to prevent foot infections. Early detection of fungal infections in high‑risk individuals is critical for the prevention of severe consequences such as foot amputation. Diabetic foot infections require the utmost attention and a multidisciplinary foot care team including an infectious disease specialist and a medical microbiologist.

# data[].attributes.attachment_link.title
A neglected causative agent in diabetic foot infection: a retrospective evaluation of 13 patients with fungal etiology

# data[].attributes.attachment_link.description
Diabetes mellitus (DM) is the most common endocrine metabolic disease, and its prevalence has been increasing steadily all over the world with recently diagnosed cases (1,2). The most significant and devastating complications of diabetes are foot ulcers and other foot problems causing major morbidity and mortality in patients with DM.

# data[].attributes.body
Toe gaps and their assessment in footwear for people with diabetes: a narrative review | Journal of Foot and Ankle Research | Full Text (biomedcentral.com)

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As the official publication of the Australian Podiatry Association and The College of Podiatry (UK), Journal of Foot and Ankle Research provides an open ...

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00400-4

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Abstract

Background

Charcot foot arthropathy is a potentially limb-threatening condition that leads to progressive destruction of the bones and joints in the neuropathic foot. One of its main causes is diabetes mellitus whose prevalence is steadily increasing. The acute phase is often misdiagnosed thus leading to foot deformity, ulceration and increased risk of amputation. There is a paucity of literature on this condition from sub-Saharan Africa. This study aimed at determining the extent of Charcot foot arthropathy, the radiological patterns of Charcot foot arthropathy and patient's factors associated with Charcot foot arthropathy among adult patients with longstanding diabetes in an African setting.

Methods

This was a cross-sectional study that was carried at a national referral and university teaching hospital in Kampala, Uganda. One hundred patients with longstanding diabetes mellitus were consecutively recruited. Patients with a history of having diabetes mellitus for at least seven years since diagnosis were considered to have a longstanding disease. Clinical assessment of both feet was done. Weight-bearing radiographs of the selected foot were taken and evaluated using the Sanders and Frykberg and modified Eichenholtz classifications. A blood sample was taken for glycosylated haemoglobin (HbA1c). Data were summarized using descriptive statistics and student t-test.

Results

The proportion of Charcot foot arthropathy among patients with longstanding diabetes was 12% of which one-third (4 out of 12) were acute cases. Fifty percent of the lesions were in the forefoot and 50% in the midfoot. Seventeen percent of lesions were at the inflammatory stage of the modified Eichenholtz classification, 50% at the developmental stage, 25% at the healing stage, and 8% at the remodelling stage. An abnormal foot radiograph was significantly associated with Charcot foot arthropathy among patients with longstanding diabetes.

Conclusion

Charcot foot arthropathy is fairly common in patients with longstanding diabetes mellitus in these settings with one third of patients presenting in the early acute phase. An abnormal weight-bearing radiograph was an associated factor of Charcot foot arthropathy among this specific group of patients. To reduce on the morbidity and limb threatening sequelae of this condition, clinicians are therefore advised to routinely examine the feet of patients with diabetes and send those with suspicious signs and symptoms for radiographic assessment.

Peer Review reports

Background

Diabetes mellitus is the most prevalent non-communicable chronic disease worldwide [ 1], with Africa having the highest prevalence of undiagnosed diabetes [ 2]. The prevalence of diabetes mellitus in Uganda is on the increase and it is becoming a major public health problem that is being compounded by limited access to quality health care [ 3, 4, 5, 6]. Population-based studies in Uganda have reported diabetes prevalence rates ranging from 1.4 to 7.4% [ 3, 7]. Diabetes mellitus predisposes patients to foot complications that range from ulceration to gangrene that is associated with significant long-term disability and premature mortality [ 1]. Complication rates for foot complications in Africa vary from 4 to 19%; peripheral neuropathy, 4-84.4%; peripheral vascular disease, 2.9-78.7%; gangrene, 0.6-69%; and amputation rates of 0.3-45% [ 1]. However, very few studies from Africa have specifically addressed Charcot foot arthropathy (CA).

Charcot foot arthropathy (CA), is a condition affecting the bones and joints of the foot in patients with peripheral neuropathy of various origins, characterized in the earliest phase by non-infective inflammation of bones and joints of the foot [ 8, 9, 10] and in the later phases by progressive destruction of bones and joints in the weight-bearing neuropathic foot leading to acute fractures, dislocations and joint destruction [ 11, 12]. There are many reported aetiologies of CA, however, nowadays diabetes mellitus has become the leading cause [ 8, 12, 13, 14, 15].

Globally, several population-based studies have reported an estimated CA prevalence ranging from 0.08% of the general diabetes patient population to 13% of patients presenting at diabetic foot clinics [ 12, 14, 16, 17] though the exact prevalence of CA is unknown. This might partly be attributed to a high incidence of mistaken or delayed initial diagnosis [ 12, 14, 16]. Charcot foot arthropathy is associated with several complications [ 18, 19] yet there is a paucity of literature on CA from sub-Saharan Africa. We came across only one study from East Africa that was conducted in a Kenyan district hospital and reported foot complication rates as high as 29.2% in patients attending a diabetic clinic; with 95% of these having diabetic ulcers and 5% had CA or cellulitis [ 20]. To the best of the author's knowledge, no study related to CA in Uganda has yet been published.

The acute phase of CA is often misdiagnosed and can lead to permanent foot deformity, ulceration thus increasing the risk of lower extremity amputation [ 8, 12, 21, 22]. Early diagnosis and management of acute CA are therefore imperative to avoid progression towards permanent foot deformity and its associated complications [ 12, 13]. In patients with diabetes and an established CA, patients can present with foot ulceration secondary to foot deformity and therapeutic efforts tend to be focused on ulcers management rather than arresting the disease process [ 23].

There are 3 types of Charcot foot classification: clinical, anatomical and radiological [ 11, 12, 17, 24, 25, 26]. In clinical practice, Charcot foot can be classified into the acute and chronic stage [ 25]:

In the acute stage, the foot is remarkably red, warm and swollen; the midfoot is most affected and pain is not a prominent feature [ 25]. In the Chronic stage signs of local inflammation progressively recede [ 25, 27]; stable deformities may develop in this stage most commonly a rocker bottom deformity [ 25, 27]. The most frequently used anatomical classification was proposed by Sanders and Frykberg [ 11, 12, 17, 24, 25, 26]. It describes five different patterns of destruction. The radiological classification is based on the natural history of the disease and is divided into four stages based on Eichenholtz's work in 1966, and later modified in 1990 by Shibata et al. [ 17, 24, 25, 26, 27, 28].

Potential risk factors associated with CA include age, duration of diabetes, body mass index, history of an instigating event such as foot trauma or foot surgery and peripheral neuropathy [ 11, 12, 14, 29, 30]. In patients with diabetes, CA typically presents during the fifth or sixth decade of life [ 31]. A longstanding history, at least a decade with diabetes is usual [ 32, 33, 34]. Most commonly, at the time of onset patients with both Type 1 and Type 2 diabetes have been diagnosed for a period ≥10 years, however, for type 2 other studies found a diabetes duration of 5 to 9 years at the time of CA diagnosis [ 11, 12, 14, 29, 30]. The mean body mass index of Charcot patients, according to Pakarinen et al. [ 32] was 32.9 kg/m ² and 34.5 kg/m ² in men and women, respectively. A history of an instigating event (foot trauma, foot surgery) preceding the onset of Charcot's foot has been reported from 22 to 73% of the time [ 35]. Peripheral neuropathy is associated with all disorders that produce neuroarthropathy and is believed to be the prerequisite for the development of Charcot arthropathy, however not all patients with diabetes and peripheral neuropathy will develop Charcot foot arthropathy [ 8, 14, 17, 29, 30].

The prevalence of diabetes mellitus is currently increasing worldwide including Uganda, becoming, therefore, a major public health problem [ 3, 4, 5]. If not managed in time, CA leads to permanent foot deformities, which will progress to foot ulcers, thus increasing the risk for lower extremity amputation. Charcot foot arthropathy is a contributing factor in the 15 to 40-fold increase in the risk of lower-extremity amputations in the population with diabetes [ 36]. Screening for diabetic complications in Uganda urban diabetic clinics is suboptimal [ 37]. Among patients with diabetes, peripheral neuropathy, the main risk factor of CA estimated to have a prevalence of 9 to 32% among patients with diabetes [ 14, 38, 39], was found to be 46.4% in Uganda at the time of diagnosis [ 5].

Despite the facts mentioned above, there was no baseline data in terms of extent and patterns of that foot disease in these clinics, there were no established protocol for its early diagnosis and management. Charcot foot arthropathy is overlooked and misdiagnosed; hence the increased morbidity increased risk of foot amputations and high economic burden among these patients.

Therefore, this study aimed at determining the extent of CA, the radiological patterns of CA and patient's factors associated with CA among adult patients with longstanding diabetes attending MNRH.

Methods

Study design

This was a cross-sectional study that was conducted from June 2017 to April 2018.

Study site

The study was carried out in the weekly diabetic outpatient clinic at Mulago National Referral Hospital (MNRH). Mulago hospital, located in the Ugandan capital city Kampala, is the largest national referral hospital in the country and is also the teaching hospital for Makerere University.

Study participants

Participants included adult patients (at least 18 years) with long-standing diabetes mellitus who gave written informed consent. For this study, patients with a history of having diabetes mellitus for at least seven years since diagnosis were considered to have a longstanding disease. Patients with gangrene of the foot were excluded. Participants were consecutively recruited from a diabetic outpatient clinic. The sample size was 100 patients. We used an assumed prevalence of 7% based on Frykberg et al. [ 14] study that reported a CA prevalence of 0.08-13% and a precision of 5% (delta). To allow for adequate power, a confidence level of 95% was selected.

Data collection

Adult patients with long-standing diabetes were consented and consecutively enrolled in the study. Data collected on history included demographic characteristics, duration since diagnosis of diabetes mellitus, and previous foot surgery or foot trauma. Clinical assessment was done for both feet after which one foot, the most affected, was selected for a weight-bearing foot radiographs. The feet were examined for swelling, deformity, ulceration, peripheral neuropathy and warmth. Foot ulcers were examined to rule out osteomyelitis which was clinically suspected if the ulcer had been present for more than one week, the lesion extending more than 2cm ², and a positive probe to bone test. The probe to bone test was considered positive if the bone could be felt using a sterile blunt metallic probe through the ulcer [ 9, 40].

Peripheral neuropathy was assessed using the 5.07/10 g Semmes-Weinstein monofilament to test for sensation on the plantar aspect of the first, third, and fifth metatarsal heads. The monofilament was applied to the test site perpendicularly until it bent for about one second. The patients were instructed to say "yes" each time they sensed the monofilament. If the patient failed to sense the monofilament after bending, the test site was considered to be insensate. Patients unable to detect touch at one or more sites were considered to have abnormal sensation. Only patients able to feel all the examination sites were considered to have a normal sensation. [ 41, 42, 43, 44, 45]. The warmth was assessed using a handheld infrared dermal thermometer (Elektro™ Orb Genesis LLC, Istanbul, Turkey). The temperature was taken on the dorsal aspect of the midfoot or the most prominent site of the swelling. A difference of more than 2 °C between the two feet implied the presence of local inflammation, raising suspicion of the acute phase CA.

Radiographs were interpreted using Sanders and Frykberg anatomical classification [ 11, 12, 17, 24, 25, 26] and the modified Eichenholtz classification [ 17, 24, 25, 26, 27, 28].

Sanders and Frykberg anatomical classification:

Modified Eichenholtz classification:

Laboratory tests included glycosylated haemoglobin (HbA1C) for all research participants. For patients with clinical signs of suspected chronic foot osteomyelitis, total white blood cell count and Erythrocyte sedimentation rate (ESR) were as well requested. HbA1c was considered within the normal range if less than 7%. ESR of more than 70 mm/hr. was considered positive for osteomyelitis [ 40].

A final diagnosis of Charcot foot arthropathy was made by the PI based on both clinical findings and radiological findings. Three types of conclusion could arise from the examination: Acute CA, Chronic CA, CA associated with osteomyelitis.

Findings leading to confirmation of the diagnosis of acute CA should have all the followings: On observation: foot swelling/oedema/erythema, no single scratch, wound or ulcer. On neurologic examination: reduced or no foot sensation confirmed by a positive 5.07/10 g Semmes-Weinstein monofilament (peripheral neuropathy). On temperature examination: a difference of more than 2 °C with the opposite foot using an infrared dermal thermometer. On foot radiograph: normal radiograph or minimal abnormality different from the one of stages 1 (bony debris, fragmentation, fracture), 2 (coalescence, callus) and 3 (remodeling) of the modified Eichenholtz classification.

Findings leading to confirmation of Chronic CA should have all the followings: On observation: No or reduced swelling/oedema/erythema; no single scratch, wound or ulcer; bone deformity of various degrees. On neurologic examination: reduced or no foot sensation confirmed by a positive 5.07/10 g Semmes-Weinstein monofilament (peripheral neuropathy). On temperature examination: no difference of more than 2 °C with the opposite foot using an infrared dermal thermometer. On foot radiograph: abnormal radiograph showing one of the lesions of stages 1 (bony debris, fragmentation, fracture), 2 (coalescence, callus) or 3 (remodeling) of the modified Eichenholtz classification.

Findings leading to confirmation of the diagnosis of CA associated with osteomyelitis should have all the followings: the presence of a foot ulcer which had been present for more than one week, the lesion extending more than 2cm ², and a positive probe to bone test. On neurologic examination: reduced or no foot sensation confirmed by a positive 5.07/10 g Semmes-Weinstein monofilament (peripheral neuropathy). On foot radiograph: abnormal radiograph showing one of the lesions of stages 1 (bony debris, fragmentation, fracture), 2 (coalescence, callus) or 3 (remodeling) of the modified Eichenholtz classification plus other lesions of osteomyelitis. On laboratory investigation: an ESR more than 70 mm/h.

Data analysis

Data were summarized using descriptive statistics. Bivariate analysis was performed using student t-test for continuous variables and Ranksum Mann Whitney U test categorical variables. A value of less than 0.05 was considered to be associated with CA.

Results

One hundred adult patients with longstanding diabetes were recruited of which the majority were female (79/100, 79%) and a half was above 50 years of age. Sixty-four patients (64%) were either overweight or obese. Forty-three patients (43%) had suffered from diabetes mellitus for more than 10 years. The mean diabetes duration, mean body mass index and mean HbA1c were respectively 12.8 years (± 5.9 SD), 27.6 (± 5.2 SD) and 6.7% (± 6.7 SD). Patient demographic characteristics are summarized in Table 1.

Table 1 Demographic characteristics of research participants

Clinical and radiological assessment

Twelve patients (12%, 7-20 95% CI) were diagnosed with Charcot foot arthropathy, one-third of which had the acute disease on clinical examination.

Using the Sanders and Frykberg anatomical classification of Charcot foot arthropathy, 2 among the 12 participants with CA had normal radiographs, 5 out of the remaining 10 participants (50%) had type 1 and 5 (50%) had type 3 disease.

Using the modified Eichenholtz classification, 2 out of 12 participants with CA (17%) had stage 0 lesions, 6 out of 12 participants with CA (50%) had stage 1 lesions, 3 out of 12 participants with CA (25%) had stage 2 lesions, and 1 out of 12 participants with CA (8%) had stage 3 lesions (Fig. 1).

Histogram showing the radiological classification of CA (modified Eichenholtz) among the 12 cases of CA. The different stages (with different colours) are on the x-axis and the number of cases for each stage is expressed on the y-axis and top of each histogram. Radiological classification of Charcot foot arthropathy (modified Eichenholtz) among the 12 patients with CA. 0: Inflammatory phase. 1: Development phase. 2: Healing phase. 3: Remodelling phase. 0 and 1 are early stages, 2 and 3 are late stages

Some feet with CA among the 12 patients and their features on weight-bearing radiographs are illustrated in Figs. 2 and 3.

The lateral view foot radiograph and the foot picture of the same patient with CA. The anatomical classification according to Sanders and Frykberg for this foot is type 1 (lesions in forefoot) and 3 (lesions in the tarsal bones). The modified Eichenholtz radiological classification for this foot is stage 1 (foot swelling, fragmentation of subchondral bones in the tarsus, periarticular fracture at the proximal interphalangeal joint of the 2nd toe, toe clawing)

The anteroposterior view foot radiograph and the foot picture of the same patient with CA. The anatomical classification according to Sanders and Frykberg for this foot is type 1 (lesions in forefoot) and 3 (lesions in the tarsal bones). The modified Eichenholtz radiological classification for this foot is stage 3 (callus, bone remodelling at tarsus and metatarsophalangeal joints)

Patient factors associated with Charcot foot arthropathy

Bivariate analysis of demographic characteristics showed no association between demographic characteristics (age, BMI, diabetes duration) and CA (Table 2).

Table 2 Bivariate analysis of demographic characteristics associated with CA among adult patients with longstanding diabetes

Bivariate analysis of clinical and paraclinical characteristics showed that an abnormal foot radiograph was associated with CA (Table 3).

Table 3 Bivariate analysis of clinical and paraclinical characteristics associated with CA among adult patients with longstanding diabetes

Discussion

This study aimed to determine the extent, the radiological patterns and associated factors of CA among adult patients with longstanding diabetes mellitus attending an outpatient's clinic in an African setting.

The majority of participants with CA were in their sixth decade of life. This is in concordance with other studies where CA presents during the fifth and sixth decade [ 14, 29, 30]. Age is an important risk factor for diabetic neuropathy [ 46] which is very crucial in the pathogenesis of CA [ 8, 14, 17, 29, 30].

The proportion of CA among patients with longstanding diabetes in this study was 12%. Several authors have reported varying prevalence rates for CA in different populations ranging from 0.08% to 13 [ 12, 14, 17, 23, 26]. The prevalence is low when considering the general population with diabetes and increases when considering a specific group among patients with diabetes such as those consulting a foot clinic for a foot problem [ 14, 17]. Charcot foot arthropathy is not a frequent complication in the general population with diabetes; however, when present it affects the quality of life, threatens the lower limb for amputation and its management is challenging [ 23, 26]. Routine examination of the feet is very crucial for patients with diabetes because it can avert catastrophic complications. One-third of the participants in this study were in the acute phase of CA. Diagnosis of CA in the acute phase is difficult because clinical features are non-specific and foot radiographs are often normal. Making a diagnosis at this stage reduces morbidity and facilitates proper management [ 8, 12, 17, 23]. Clinicians should not only have a clear understanding of diabetic foot disease but should also have a high index of suspicion.

In this study, there was an equal distribution of CA in the fore- and mid-foot. This pattern is similar to what has been reported by other authors [ 14, 23]. In addition to diabetes, the pattern of disease is influenced by other biomechanical factors that act on the foot. For example, a high BMI predisposes the middle arch to collapse culminating in a rocker-bottom foot; tightness of the triceps surae complex leads to abnormal plantar pressure distribution in the forefoot during walking thus exposing the forefoot bones to more strain [ 8, 17, 23]. Hence, addressing the biomechanics of the foot is also important in the management of these patients [ 8, 17, 23, 47, 48, 49].

Most of the lesions in this study were at the initial stages of the natural history of CA. The mainstay in the treatment of the initial stages (inflammatory and developmental) is non-operative management by offloading the limb in a total contact cast [ 17, 23, 50]. If these stages are treated judiciously, the achievement of a stable foot without surgery or skin breakdown is possible [ 17]. This shows the need for quick management intervention in the acute phase before latter stages where bone deformities are fixed and permanent, predisposing the foot to ulceration, infection and high risk of amputation [ 17]. Clinical symptoms in the inflammatory stage may precede radiographic changes by up to 1 year, hence treatment in this stage is critical in preventing the disease from progressing in further stages [ 14, 51].

The vast majority of patients in this study had abnormal weight-bearing foot radiographs with no obvious history of trauma. An abnormal weight-bearing foot radiograph in a patient with longstanding diabetes and peripheral neuropathy should raise suspicion of CA. When reading the film one must take time to confirm if the lesions seen are features of CA. Therefore clinicians should have a high index of suspicion and ought to routinely assess patient's feet for CA.

Strengths and limitations

This study was based on primary data gathered prospectively, hence allowing us to collect all intended parameters. To our knowledge this study is the first on CA in these settings, giving baseline data for further researches and planning in this field. This study also highlights the utility of corroborating clinical information with simple imaging techniques in making a diagnosis. This is especially important in settings, which only have basic diagnostic equipment; and disease diagnosis requires a high index of suspicion and good clinical acumen.

Results of this study may not be generalizable because of the cross-sectional design, relatively small sample size and the use of a consecutive sampling technique. We did not have access to more advanced imaging modality such as MRI to confirm acute cases of CA with normal foot radiographs.

Conclusion

Charcot foot arthropathy is a relatively common complication among patients with long-standing diabetes mellitus in our setting. Several cases present in the acute phase when there are no obvious pathological radiographic changes and diagnosis is relatively difficult. This notwithstanding, the majority of patients with a clinical diagnosis of CA may present with abnormal weight-bearing foot radiographs with the involvement of the mid-foot and forefoot. Therefore clinicians should have a high index of suspicion to enable early diagnosis and also prevent potentially disabling complications.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CA:

Charcot foot arthropathy

ESR:

Erythrocyte sedimentation rate

HbA1c:

Glycosylated hemoglobin

MNRH:

Mulago national referral hospital

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Acknowledgements

We thank the research assistants from Mulago National Referral Hospital who helped recruited participants and collected blood samples.

Funding

The study was self-funded.

Author information

Affiliations

1. Department of Orthopaedics, College of Health Sciences, Makerere University, P.O BOX 7072, Kampala, Uganda

Jean Paul Vwakya Wanzou & Patrick Sekimpi

2. Child and Family Foundation, Kampala, Uganda

Johnson Owonda Komagum

3. Department of Internal medicine, Endocrinology Unit, Mulago Hospital, P.O BOX 7051, Kampala, Uganda

Frederick Nakwagala

4. Department of Anatomy, College of Health Sciences, Makerere University, P.O BOX 7072, Kampala, Uganda

Erisa Sabakaki Mwaka

Contributions

VW conceived, designed the study, participated in the data collection and analysis, and drafted the manuscript. OJ critically analyzed the data and performed statistical tests. ME, FN and SP assisted in the study conception and design and critically reviewed the manuscript. All authors approved the manuscript for publication.

Authors' information

* Vwakya Wanzou: MBChB, MMed Orthopaedics, Makerere University, P.O Box 33595, Kampala, Uganda. Telephone: + 256753543573.

¹ Sekimpi Patrick: MBChB, M.Med Orthopaedics, FCS (ECSA), lecturer, Orthopaedic Department, Makerere University, Kampala, Uganda.

² Owonda Johnson Komagum: Statistician, Child and Family Foundation, Kampala, Uganda.

³ Nakwagala Frederick: MBChB, M.Med Internal medicine, Senior Consultant Physician, Endocrinology Unit, Mulago Hospital, Kampala, Uganda. Chair of Mulago Hospital Research and ethics committee.

⁴ Mwaka Erisa Sabakaki: MBChB, M.Med Orthopaedics, PhD (Fukui), Orthopaedic Surgeon and Senior Lecturer, School of Biomedical Sciences, Department of Anatomy, Makerere University, Kampala, Uganda. Chair school of biomedical sciences higher degrees and Research Ethics Committee.

Corresponding author

Correspondence to Jean Paul Vwakya Wanzou.

Ethics declarations

Ethics approval and consent to participate

The study was carried out after approval of school of medicine research and ethics committee (Ref: #REC REF 2017-090) and Mulago Hospital Research and ethics committee (MREC 18/10/2017). Written informed consent was obtained. Confidentiality from all the patients involved in the study was assured. Those diagnosed with CA were referred to the appropriate medical personnel.

Consent for publication

This paper is published with the approval of all the patients from which data were collected.

Competing interests

The authors declare that they have no competing interests.

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Charcot arthropathy of the diabetic foot in a sub-Saharan tertiary hospital: a cross-sectional study

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Charcot foot arthropathy is a potentially limb-threatening condition that leads to progressive destruction of the bones and joints in the neuropathic foot. One of its main causes is diabetes mellitus whose prevalence is steadily increasing. The acute phase is often misdiagnosed thus leading to foot deformity, ulceration and increased risk of amputation.

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Abstract

Background

Diabetes foot ulcer is a devastating and much-feared complication of diabetes. Diabetes foot ulcerations which developed gangrene can take weeks or months to heal and can sometimes not heal at all so that amputation for non-traumatic causes is a frequent outcome in the diabetic foot. Despite this, there is no finding on predictors of the amputation rate of diabetes foot ulcers in Ethiopia. Hence this study was aimed to identify factors associated with the amputation rate of diabetes foot ulcer patients in Nekemte referral hospital.

Patients and methods

A prospective observational study was conducted among adult diabetes foot ulcer patients admitted to Nekemte referral hospital from March 15 to June 15, 2018. A pus swab was obtained from the ulcers before any ulcer cleaning to conduct gram staining. The primary outcome was the amputation rate. Cox regression analysis was used to estimate the hazard ratios and time from study entry to healing was evaluated as censored event times by Kaplan-Meier curves.

Result

Over the study period, 115 diabetes foot ulcer patients were admitted to the NRH; of these patients, 64(55.65%) were males while the mean age of participants was 44.4 ± 14.7. A total of 34(29.57%) of the diabetes foot ulcer were overweight and 16(13.91%) were obese while the mean ± standard deviation of body mass index (BMI) was 24.94 ± 3.69 kg/m2 and a total of 56(48.69%) diabetic foot ulcer had a diabetic complication.

Of patients with diabetic foot ulcer, 35(30.43%) were undergone lower extremity amputations (LEA). Patients who were prescribed with inappropriate antibiotics were unlikely to heal. A total of 18(46.15%) of the patients who were taken inappropriate antibiotics were healed whereas 21(53.85%) were not healed ( P = 0.017). Besides, the higher the Wagner grade, the worse the outcome of healing. A total of 19(21.84%) and 16(57.14%) of patients with grade < 4 and grade ≥ 4, respectively, did not heal ( P  = 0.005).

Conclusion

The amputation rate of diabetes foot ulcers was rapid for patients prescribed inappropriate antibiotics and higher grades of the foot ulcer. Therefore, the presence of clinical pharmacists plays a pivotal role to promote the appropriate use of antibiotics and besides the daily care, special attention should be given for patients having an advanced grade of diabetes foot ulcer.

Peer Review reports

Background

Diabetes mellitus is a chronic disease that needs long-term medical attention to prevent the development of its complications [ 1]. The development of diabetes foot ulcers increases a patient's risk of mortality [ 2].

Different treatment protocols which include applying vascular intervention, anti-infection treatment, surgical operation, and postoperative wound care have been performed to increase the healing rate of the diabetes foot ulcer. Despite these, the reported diabetic foot ulcer healing rates from multiple series were poor [ 3].

Amputation of the lower extremities is the commonly occurred outcome for the DFU [ 4]. Approximately, more than half were progressed to infections that may result in amputations, disability, prolonged hospitalization, and death [ 5]. Due to prolonged healing time, many patients will need to be hospitalized for treatment [ 6]. For people with diabetes who have an active ulcer, the final healing rates are 65-75% for those attending a hospital, while around 15-20% of all people with an ulcer undergo amputation, depending on the duration of follow-up [ 7].

The size of the ulcer was greater in the amputation group compared to healed ulcers which can predict diabetes foot ulcer healing [ 8]. Despite this, the feet of diabetes patients were ignored by health care providers which could have an economic impact on the patient and health care system as a result of long-term in-hospital treatment and/or amputation [ 1, 9].

Determinants of ulcer healing in diabetes patients are generally essential in establishing management strategy in addition to their routine application as predictors of the outcome. Therefore, they are useful in the early identification of diabetes patients with high risk for foot ulcers to decrease the risk of amputation [ 10].

Diabetes mellitus patients whose ulcer progressed to Chronic do not show the well-defined sequence of ulcer healing. An increase in wound size and surface may empirically be determinants of poor healing [ 2]. In Ethiopia, patient behavior of poor diabetes foot ulcer treatment practice, and the absence of good quality service of diabetes foot ulcer may have led to foot infections which result in limb amputation. Only a few pharmacists were assigned to avoid the inappropriate use of antibiotics in the Nekemte referral hospital by intervening problems at only dispensing levels. Despite this, no study has been conducted on the amputation rate of diabetic foot ulcers in NRH. Therefore, this study was tried to determine the factor that affect the amputation rate of diabetes foot ulcer patients.

Methods

Study design, period and area

A prospective observational study was conducted at NRH from March 15 to June 15, 2018 to assess the amputation rate of diabetes foot ulcers. The hospital is found in Nekemte town, which is located 330 km to the west of Addis Ababa, the capital city of Ethiopia. The hospital is a referral hospital and gives health services for more than 10 million people living in western Ethiopia. There were about 2420 diabetic patients who have been following the diabetic clinics annually.

Study participants and eligibility criteria

Patients ≥18 years who were admitted to the hospital due to no- traumatic chronic diabetes foot ulcer with visible foot lesions were included.

Study variables and outcomes

The primary outcome was the amputation rate. Independent variables included were sex, age, residence, educational level, marital status, type of diabetes mellitus, antibiotic given, previous history of ulcer, grade of diabetes foot ulcer, and presence of co-morbidity. The Wagner classification of diabetes foot ulcers was used to assess the grades of foot ulcers. The magnitude of foot ulcer was determined by multiplying the largest by the second largest diameter perpendicular to the first [ 11]. The etiology of diabetes foot infection was identified by using gram stains. Amputation and healing status was measured using a checklist and assessed by close followed of the patient through a telephone interview of the patient/ caregiver/ proxy on a weekly basis. The ulcer of different sites which includes, dorsal/inter-digital toes, plantar fore foot/mid foot/hind foot, plantar toes, dorsal foot, and heel were recorded to identify the location of diabetes foot ulcer.

Sample size and sampling technique

Single population proportion formula was used to calculate the required sample size by considering the incidence of amputation which is 29% [ 12]. Accordingly, a sample of 316 was obtained. The expected number of source population in the study period, based on the average number of patients coming to the hospital was 156. Finally, by using correction formula a total of 115 patients were included. Conveniently all patients during the study period full filling the eligibility criteria and willing to respond were included in the final analysis.

Data collection process and management

Data was collected using data abstraction format which was developed after reviewing different literature and adopting [ 5, 7, 8, 9, 10, 11, 12]. One medical doctor, one nurse and one pharmacist were selected as data collectors. One medical doctor working in a medical ward who had not been involved in data collection was assigned to supervise the collected data. A pus swab was obtained from the ulcers before any ulcer cleaning and avoiding other contamination. The samples were delivered to the laboratory immediately and a thin smear was prepared on grease or oil free slides. Appropriateness of antibiotics was identified based on infectious diseases society of America (IDSA) standard guidelines for diagnosis and treatment of diabetes foot infection [ 13], which is based on the most likely coverage of antibiotics for treatments of diabetic foot infection for identified gram stain results and their correct dosage regimens. Five percent of the sample was pre-tested to check the acceptability and consistency of the data collection tool 2 weeks before the actual data collection.

Data processing and analysis

The data was entered into the computer using EPI-manager 4.0.2 and analysis was done using statistical package for social sciences (SPSS) 24. Descriptive data was explained by frequency and percentage. The obtained results were explained by means and standard deviations (SD). Cox regression analysis was used to estimate the hazard ratios and Time from study entry to time to healing was evaluated as censored event times by Kaplan-Meier curves. The variables with a p-value of less than 0.05 had a statistically significant association with the healing of diabetic foot ulcers.

Operational definitions

Result

Socio-demographic and clinical characteristics

During the study period, 115 diabetes foot ulcer patients were admitted to the NRH; of these patients, 64(55.65%) were males. A total of 26(22.61%) of them were in the age range of 58-67, and 56(48.69%) of them had hypertension as comorbidity (Table 1). A total of 34(29.57%) of the diabetes foot ulcer were overweight and 16(13.91%) were obese while the mean body mass index (BMI) was 24.94 ± 3.69 kg/m ². From the sites of ulcers involved, a total of 67(58.26%) of them were developed over plantar toes/foot whereas, 31(26.96%) of ulcers were located on dorsal/interdigital toes, 9(7.83%) of the diabetes foot ulcers were located in the dorsal foot and 8(6.96%) of the ulcers were developed over heel [ 16]. The mean fasting blood glucose level among diabetic patients with foot ulcers was 147.93 ± 45.03 mg/dl and a total of 56(48.69%) diabetes foot ulcers had a diabetes complication.

Table 1 Demographic and clinical patient characteristics of diabetes foot ulcer patients in Nekemte referral hospital, west Ethiopia, 2018

Healing time of diabetes foot ulcer and associated factors

Over the study period, a total 35(30.43%) patients were undergone lower extremity amputations (LEA) and 80(69.57%) were healed. Regarding the rate of wound healing (in cm ²/week): a total of 20(17.39%) were healed < 1 cm ²/week, 22(19.13%) were1-2 cm ²/week and 38(33.04%) were > 2 cm ²/week whereas, the overall mean time to healing was 42 ± 5.592 days.

From the total diabetes foot ulcer patients, a total of 77(67%) of ulcers were progressed to infection and 38(33%) of them did not. From the patients who developed an infection, gram- positive organisms were identified in 42(54.55%), gram-negative were identified in 20(25.97%) and polymicrobial were seen in 15(19.48%) [ 16].

From the total patient's given antibiotics, a total of 38(49.35%) of them were prescribed appropriately and 39(50.65%) were prescribed inappropriately whereas, 38 (49.35%) of the diabetic foot ulcer patients were never given antibiotics. Individual antibiotics prescribed includes; cloxacillin 56 (34.15%), metronidazole 43 (26.22%), ceftriaxone 33 (20.12%), ampicillin 9(5.49%), chloramphenicol 8(4.88%), gentamycin 5 (3.05%),ceftazidime 4(2.44%), ciprofloxacin 3 (1.83%), vancomycin 2 (1.22%), and amoxicillin 1(0.61%).

Neither age nor gender had an association with the outcomes of foot ulcers whereas; advanced grade of ulcer and inappropriate antibiotics use had an association with the healing of diabetes foot ulcers. Patients prescribed with inappropriate antibiotics were 2 times more likely to be amputated as compared to the patients given appropriate antibiotics (AHR = 2.14;95%CI:1.64,10.63). The higher grades of foot ulcers, the worse the outcome of healing. Diabetes foot ulcer patients presented with grade ≥ 4 were 1.6 times more likely to be amputated as compared to the patients having grade < 4(AHR = 1.59;95%CI:1.49,7.48) (Table 2).

Table 2 Predictors of amputation rate of diabetes foot ulcer and associated factors in Nekemte referral hospital, west Ethiopia, 2018

The Kaplan-Meier survival analyses of the patients who were given appropriate and inappropriate antibiotics showed that the healing time of diabetes foot ulcer patients who were given inappropriate antibiotics were prolonged than diabetes foot ulcer patients who were given appropriate antibiotics (Fig. 1).

Kaplan-Meier curves for amputation-free survival of diabetes foot ulcer patients over 60 days, depending on the appropriateness of antibiotics prescribed

The Kaplan-Meier survival analyses of the patients who were on Wagner grade less than 4 and grade 4 and above showed that the healing time of diabetes foot ulcer patients who were on the advanced stage of diabetes foot ulcer was prolonged than diabetes foot ulcer patients who were at an earlier stage (Fig. 2).

Kaplan-Meier curves for amputation-free survival of diabetes foot ulcer patients over 60 days, depending on the grades of diabetic foot ulcers

Discussion

The study was aimed to identify the amputation rate of diabetes foot ulcer and its predictors. Appropriate anti-microbial therapy is essential for diabetes foot ulcers that progressed to infection, unlike this; prescribing antibiotics for uninfected foot ulcers can results in unnecessary therapy, increase cost, and risk of antibiotic resistance [ 17]. Therefore, appropriate use of antibiotics is a very crucial problem for clinicians. Duration of antibiotic therapy for a diabetes foot infection should be based on the severity of the infection and clinical response to therapy, and antibiotic therapy can generally be discontinued when the patients don't show any clinical presentation of infection [ 13]. One medical doctor, one nurse were selected as data collectors as they had experience in treatment of DFU.

The study conducted by Fatma I. Abo El-Ela et al. showed appropriate treatment of diabetes foot infection by amoxicillin and doxycycline help to prevent bacterial growth and ulcers that heal the wounds within a short period [ 18]. According to the study done in China by Chu et al., for moderate/severe infection, the healing rate was rapid in patients given appropriate antibiotic therapy [ 17]. This is similar to our study in which appropriate antibiotics prescription can fasten the healing rate of diabetes foot ulcers. This is because in China and the Nekemte referral hospital the antibiotics were started when the patients reach the advanced stage of grade. In our study, almost half of the antibiotics were prescribed inappropriately due to a lack of clinical pharmacy service that can improve the rational antibiotics prescription. Therefore, because of excessive and inappropriate use of antibiotics for treating diabetes foot infections, resistance to the usually employed bacteria wills possibly increasing to alarming levels in the study area unless tackled. The International Working Group on the Diabetic Foot Also recommends selecting antibiotic agents for treating diabetic foot infection from among those that have demonstrated efficacy for diabetic foot infection in clinical studies [ 19].

On the contrary, the study conducted in Denmark revealed that the antibiotics given were not significantly associated with the healing rate of diabetes foot ulcers [ 20]. This was in agreement with our study.

In our study, the rate of healing of almost half of the patients' wounds was very rapidly, i.e., greater than 2 cm ²/week. On the contrary, in Saudi Arabia the rate of healing of more than three-fourths of patients' wounds was very slow, i.e., less than 1 cm2/week [ 1]. The rapid healing rate of diabetes foot ulcers in our study was due to initial Wagner's grades of the majority of diabetes foot ulcer patients.

We found the average duration for ulcer healing in our study was 42 days, which was a relatively short time compared to the study of Saudi Arabia of 3 months, Denmark of about 6 months and the USA of 133 days [ 10, 20, 21], and in the UK the healing rate was 2 months which was almost similar to our study [ 22]. The accelerated healing times might be due to the superficial infections of foot ulcer in majority of cases in our study.

The finding was not similar to those of Markuson et al., who identified a difference with in the type of diabetes and healing time. More patients in type one diabetes mellitus had rapid healing rate than type two diabetes mellitus [ 21]. In UK the healing rate was similar in both type one and two diabetes mellitus patients [ 22]. This is similar to our study in which type of diabetes couldn't affect the healing rate.

Advanced Wagner grades (≥ grade 4) predicted the amputation rate of diabetes foot ulcers in our study. This is because gangrene was developed at an advanced grade of foot ulcer which finally results in amputation. Similarly, Sung Hun Won, et al. showed that advanced grade of ulcer had a risk of amputation [ 23], similar to our study. This is due to the patients at a higher levels of Wagner's grade seek hospital after gangrene was developed in our study.

The amputation rates of foot ulcers were higher than the study done by Morbach et al. [ 24]. This is because all amputation levels (minor and major) were included in our study over the study period of 3 months. The study conducted in Brazil revealed that about 11.7% of the diabetic foot ulcer patients were undergone amputation [ 25], which was lower than our study. This may be due to a lack of quality of health service, inadequate healthcare professionals to provide care for the patients in our study. The healing rate was comparable with the study conducted by Akturk A, etal, in which 67% of the DFU were healed [ 26].

Strength and limitation of the study

As strength, the study was conducted among DFU patients as the foot complication of diabetes mellitus patients is increasing in the developing world and may be used as baseline information for other researchers. As limitations, culture, and sensitivity tests were not done to identify the specific strains of the pathogen. Further the follow-up period was short, thus failing to take into account any non- healing ulcers after 3 months and patients were followed by telephone not by face to face interviews. Despite the mortality was not reported in our study, further research should be conducted to identify the mortality rate. Lastly, there might be selection bias due to convenience sampling technique of the study.

Conclusion

The healing rate of diabetes foot ulcers was rapid and the majority of them were healed within 2 months. The amputation rate of diabetes foot ulcers was rapid for patients prescribed inappropriate antibiotics therapy and an advanced grade of foot ulcers. Therefore, the presence of clinical pharmacists plays a pivotal role to facilitate and promote the appropriate use of antibiotics by intervening different problems in prescribing, dispensing, and providing necessary advice for the patients, and health care professionals regarding the overall issues related to drugs. Besides the daily care, special attention should be given for patients having advanced grades of diabetes foot ulcers.

Availability of data and materials

The datasets used during the study are available from the corresponding author on a reasonable request.

Abbreviations

AHR:

Adjusted hazard ratio

BMI:

Body mass index

CHR:

Crude hazard ratio

CI:

Confidence interval

DFU:

Diabetic foot ulcer

DM:

Diabetes mellitus

IDSA:

Infectious Diseases Society of America

IWGDF:

International Working Group on the Diabetic Foot

LEA:

Lower extremity amputation

NRH:

Nekemte referral hospital

SD:

Standard deviation

SPSS:

Statistical package for social sciences

UK:

United Kingdom

References

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Acknowledgments

We thank Jimma University for funding this study. We are grateful to health care professionals of NRH, data collectors, and study participants that extended their helpful hands toward the study.

Funding

The study was funded by Jimma University.

Author information

Affiliations

1. Department of Pharmacy, College of Health Science, Mettu University, Mettu, Ethiopia

Firomsa Bekele

2. School of Pharmacy, College of Health Science, Addis Ababa University, Addis Ababa, Ethiopia

Legese Chelkeba

Contributions

FB contributes to the proposal preparation, study design, and writes up the manuscript. LC contributed to the design of the study and edition of the manuscripts. Both authors made substantial contributions to conception, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; gave final approval of the version to be published; and agree to be accountable for all aspects of the work.

Corresponding author

Correspondence to Firomsa Bekele.

Ethics declarations

Ethics approval and consent to participate

Ethical clearance was obtained from the Institutional Review Board (IRB) of Jimma University, with a reference number of IHRPGC/104/208. The ethics waiver was not applicable since the study was not a randomized clinical trial so that the study subjects never have been divided into experimental and control groups. Permission was obtained from the medical director of the NRH to access diabetes patients and conducts the study. The benefit and risks of the study were explained to each participant included in the study and written consent were obtained from each patient involved in the study. To ensure confidentiality, name and other identifiers of patients and health care professionals were not recorded on the data collection tools.

Consent for publication

Not applicable. No individual person's personal details, images, or videos were being used in this study.

Competing interests

No competing interests exist.

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# data[].attributes.attachment_link.title
Amputation rate of diabetic foot ulcer and associated factors in diabetes mellitus patients admitted to Nekemte referral hospital, western Ethiopia: prospective observational study

# data[].attributes.attachment_link.description
Diabetes foot ulcer is a devastating and much-feared complication of diabetes. Diabetes foot ulcerations which developed gangrene can take weeks or months to heal and can sometimes not heal at all so that amputation for non-traumatic causes is a frequent outcome in the diabetic foot.

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Highlights

*

Heels height influences the motion of the pelvis and the spine during walking.

*

Lumbar and thoracic curvatures decrease during gait with high heels.

*

Low-heeled walking influenced the pelvis and the spine less than with high-heels.

*

No difference between the level of expertise was observed.

Abstract

An estimated 78% of women regularly walk in high heels. However, up to 58% complain about low back pain, which is commonly thought to be caused by increased lumbar lordosis. However, the extent to which a subject's posture is modified by high-heeled shoes during dynamic activities remains unknown. Therefore, we sought to evaluate whether low- or high-heeled shoes influence the kinematics of the pelvis and the spine during walking. Twenty-three inexperienced women, and seventeen women experienced in wearing high-heeled shoes, all aged 20-55 years, were measured barefoot and while wearing low- (4 cm) and high-heeled (10 cm) shoes during gait at a self-selected speed. A 22-camera motion capture system was used to assess the gait patterns for each condition.

No significant inter-experience-group kinematic differences were found. In contrast to the results of some studies, our results show that the heels' height does indeed influence the motion of the pelvis and the spine during walking, whereby low-heeled shoes influenced the subjects' trunk kinematics during gait less than high-heeled shoes compared to barefooted walking. However, inexperienced high-heel wearers showed less thoracic curvature angle while wearing high-heels than while wearing low-heels. Importantly, both groups exhibited significantly lower maximum and minimal lumbar and thoracic curvature angles when wearing high-heeled shoes compared to the barefoot condition. As a result, it seems that low back pain might be associated with other factors induced by high-heels.

View Abstract

# data[].attributes.attachment_link.title
High-heeled walking decreases lumbar lordosis

# data[].attributes.attachment_link.description
Heels height influences the motion of the pelvis and the spine during walking. * Lumbar and thoracic curvatures decrease during gait with high heels. * Low-heeled walking influenced the pelvis and the spine less than with high-heels. * No difference between the level of expertise was observed.

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-1-6

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Foot symmetry and change in foot structure as a function of weight bearing status have not been investigated in a large cohort study. The foot structure of 1,054 incoming cadets at the US Military Academy (172 female, 18.5±1.1 years, 24.5±3.0 kg/m ²) was examined. Arch Height Index (AHI) was assessed in sitting and standing condition, and its value was used to classify each foot into 3 foot types as previously described [ 1].

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Foot type symmetry and change of foot structures from sitting to standing conditions

# data[].attributes.attachment_link.description
Foot symmetry and change in foot structure as a function of weight bearing status have not been investigated in a large cohort study. The foot structure of 1,054 incoming cadets at the US Military Academy (172 female, 18.5±1.1 years, 24.5±3.0 kg/m 2) was examined.

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00433-9

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00433-9

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00433-9

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/1757-1146-6-20.pdf

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00428-6

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-4-S1-I11

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00433-9

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00426-8

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Van Puyvelde Lobke

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Journal of Foot and Ankle Research 13, Article number: 9 (2020) Cite this article

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Abstract

Background

Fifth metatarsal base fracture are a common occurrence in the orthopaedic practice. Literature on the epidemiology of such fractures is scarce. The aim of this analysis was to study the relationship between Body Mass Index (BMI) and the zone of the fifth metatarsal base involved by the fracture.

Methods

Data on adult patients who have been diagnosed with isolated fifth metatarsal base fracture were gathered at our Institution (blinded for review). Age, sex, height, weight and injury mechanism were collected from electronic medical records. Fractures were classified according to the Lawrence and Botte classification (Zone 1, 2 and 3) by three independent reviewers.

Results

From March 2016 to December 2018, 149 patients (109 women and 40 men) have been diagnosed with fifth metatarsal base fracture. Average age and BMI at the time of injury were 51.9 (SD 17.1, range 18-84) and 24.0 (SD 3.8, range 16.4-36.7) respectively. Fracture distribution was 63.8% in zone 1, 23.5% in zone 2, 12.7% in zone 3. 12.1% of patients had a BMI < 20 kg/m ², 57.7% between 20 and 24.9 kg/m ², 22.2% between 25 and 29.9 kg/m ² and 8.0% over 30 kg/m ². No statistically significant differences attributable to sex ( p = 0.774) or age ( p = 0.379) were found between different zones of fracture. Average BMI was found to be higher in the zone 3 (26.1 ± 4.7 kg/m ²) fracture group than in zone 1 (23.7 ± 2.9 kg/m ²) ( p = 0.031).

Conclusion

The prevalence of proximal diaphysis (zone 3) fractures rises proportionally with BMI in our sample study. BMI appears to have an impact on fifth metatarsal base fractures pattern.

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Background

Fifth metatarsal base fracture are common in routine orthopaedic practice [ 1, 2, 3, 4, 5, 6]. Lawrence and Botte [ 7] proposed a classification based upon the position of the fracture line (zone 1: tuberosity, zone 2: meta-diaphyseal junction, zone 3: proximal diaphysis). Pathomechanically, injury patterns develop in different ways: in zone 1, a traction injury caused by peroneus brevis tendon and the lateral band of the plantar fascia determine an avulsion fracture of the tuberosity, also called "pseudo-Jones' "fracture; in zone 2, forced foot adduction and excessive plantar flexion determine a fracture in the metaphyseal-diaphyseal junction, also called Jones' fracture [ 8, 9]; in zone 3, acute over-bearing onto the area or chronic overload determine a fracture in the proximal portion of the diaphysis, distal to the intermetatarsal joint [ 10, 11].

To the best of the Authors' knowledge, no study has been published to date on the relationship between the value of Body Mass Index (BMI) and the prevalence of fractures in a specific portion of the fifth metatarsal base. The aim of this study was to define the impact of BMI on fifth metatarsal base fractures location according to Lawrence and Botte classification [ 7].

Methods

A retrospective observational analysis was performed. Patients diagnosed with fifth metatarsal base fractures between March 2016 to December 2018 were selected. Inclusion criteria were: age at presentation between 18 to 85 years-old and a twisting-type injury as a causative mechanism. Patients with additional fractures involving the foot and/or ankle, forefoot and/or hindfoot deformity, connective-tissue and/or rheumatic diseases, primary tumor or secondary localization, state of pregnancy were excluded. Electronic medical records were searched for sex, age, height, weight, mechanism of injury. Plain radiograph study (Anteroposterior, Oblique and Lateral view) were obtained and classified according to Lawrence and Botte classification (Fig. 1). Patients were classified based on BMI: < 20 kg/m ²: underweight, between 20 and 24.9 kg/m ²: normal weight, between 25.0 and 29.9 kg/m ²: overweight, 30 kg/m ² and above: obese [ 6]. Statistical analysis was conducted using R V 3.4.4 (R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [ 12]. Continuous variables were reported as mean ± standard deviation. Repeated measures design Analysis of Variance (ANOVA) and Tukey's Honest Significant Difference test were used to compare BMI across groups. ANOVA was finally used to investigate the presence of statistically significant differences attributable to age, and Chi squared test was used to investigate the presence of statistically significant differences attributable to sex.

Radiographic classification of the fractures according to Lawrence and Botte ⁷. The three different zones are based on anatomic landmarks (far left): proximal to the meta-diaphyseal junction involving the tuberosity (zone 1, centre left), between the lines of the intermetatarsal joint between fourth and fifth metatarsal bones involving the meta-diaphyseal junction and the intermetatarsal articular facet (zone 2, centre right), distal to the meta-diaphyseal junction involving the proximal diaphysis (zone 3, far right)

Results

One hundred forty-nine patients were included in the analysis. 109 (73.1%) patients were female, 40 were male. Mean age was 51.9, with a Standard Deviation (SD) of17.2 years. Mean BMI was 24 (SD = 3.8) kg/m ² (Table 1). According to Lawrence and Botte classification [ 7], 95 patients (63.8%) suffered a fracture involving Zone 1, 35 (23.4%) involving Zone 2 and 19 (12.8%) involving Zone 3. Data distribution based on BMI and zone of fracture are shown in Fig. 2. No statistically significant differences attributable to sex ( p = 0.774) between different zones of fracture. ANOVA analysis found no statistically significant differences attributable to age ( p = 0.379) between different zones of fracture. ANOVA analysis and post hoc Tukey test, found BMI to be significantly higher in the zone 3 (26.1, SD = 4.7 kg/m ²) fracture group than in zone 1 (23.7, SD = 2.9 kg/m ²) ( p = 0.031).

Table 1 Demographic data of study population and divided according to Lawrence and Botte Classification

BMI-stratified fracture distribution. Data in the histogram represent the ratio between fracture zone over the total of a weight class (\( \frac{\mathrm{N}\ \mathrm{patients}\ \mathrm{with}\ \mathrm{fracture}\ \mathrm{in}\ \mathrm{zone}\ \mathrm{n}}{\mathrm{Total}\ \mathrm{patients}\ \mathrm{in}\ \mathrm{considered}\ \mathrm{weight}\ \mathrm{class}} \)). Data in the table represent the ratio between weight class over the total of fractures zone \( \left(\frac{\mathrm{N}\ \mathrm{patients}\ \mathrm{in}\ \mathrm{considered}\ \mathrm{weight}\ \mathrm{class}}{\mathrm{Total}\ \mathrm{patients}\ \mathrm{with}\ \mathrm{fracture}\ \mathrm{in}\ \mathrm{zone}\ \mathrm{n}}\right) \). Note the growing distribution of proportion of zone 3 fractures with growing BMI (gray-coloured area)

Discussion

The most important finding of this study is the relationship between the prevalence of specific patterns of fifth metatarsal base fractures and BMI. The relative prevalence of fracture zones in this study reflects a trend which was already evident in the literature [ 6, 13]. The role of some demographic features (i.e. age, sex etc.) was investigated in its association with fifth metatarsal base fracture. While Kane et al. [ 6] found a statistically significant correlation between female sex and zone 1 fracture ( p < 0.001), no such result attributable to age ( p = 0.379) or sex ( p = 0.774) was evident in this study sample despite the similar proportions of patients for each variable considered. In their sample, patients were stratified according to etiology into five categories: "twisting", "fall", "crush", "indirect trauma", "unknown"; the two most represented categories were "twisting" (57.2%) and "fall" (22.1%). Patients whose mechanism of injury was clearly identifiable as "twisting" were exclusively included in the study: this was done by directly questioning each patient and explicitly asking if they "fell from any kind of height". This choice was dictated by the difficulty in discerning two "different but similar" pathomechanical categories ("twisting" and "fall") and was done in order to minimize bias. In both studies, patients were stratified according to BMI using the same threshold values. The same boundaries were used in order to facilitate comparative analysis with the only published study which categorizes its population of fifth metatarsal base fracture patients according to BMI.

In this study a statistical analysis of data regarding BMI was performed, which showed a statistically significant difference between increasing BMI and increasing prevalence of zone 3 fractures. Despite the smaller sample, its results confirm a trend which is already visible in the analysis performed by Kane: a rising trend of obesity can be seen as the fracture moves more distally on the fifth metatarsal base. The same trend is not obvious here, but a statistically significant difference is evident. In future research, statistical analysis in larger samples can provide enough power to either confirm or disprove this trend and determine if a statistical correlation is present.

The relationship between BMI and fractures was investigated in the recent literature. It was traditionally thought that higher BMI in overweight and obese patients correlated with a lowered fracture risk due to increased Bone Mineral Density (BMD) [ 14, 15, 16]. On the other hand, the protective effect of higher BMI through increased BMD displays a ceiling-effect [ 17] and is possibly counteracted by metabolic and systemic proinflammatory effects [ 18], questioning several aspects of said protective factor. Therefore, even if present, it might not be able to compensate for the stronger vectors of forces at play in obese individuals [ 19]. Court-Brown et al. [ 20] investigated the relationship between fractures and obesity in the general population: no association was found between metatarsal fractures and BMI. However, neither the ordinal number nor the fractured area of the metatarsal bone were specified. In fact, the Authors are not aware of any other published study who subclassified and analysed proximal fifth metatarsal fractures in relation to BMI Since no established protective effect attributable to increased BMD is known to take place in the fifth metatarsal, the results of this study could be partially explained by acute excessive bearing onto the foot [ 10], further exacerbated by excess weight.

Three factors can contribute to muscle and tendon degeneration in the patient with a higher-than-normal percentage of body fat: peroneus brevis muscle dynapenia, microvasculopathy, systemic and localized chronic low-grade inflammation. Muscle mass infiltration by excess fat can lead to a combination of "sarcopenic" [ 21] and "dynapenic" [ 22] obesity, which in turn leads to a reduction of strength in the affected muscles. Also, dynapenia can contribute to poorer muscle control while falling [ 16], which could lead to a lack of defensive contraction of the peroneus brevis. Pathomechanically, overabundant adipose tissue can influence fracture in the overweight/obese patient by acting both on bone and on soft tissue: it is possible that not only excess weight alters the way the bone responds to weight-bearing, but also that proinflammatory factors associated to systemic dysmetabolic disorders trigger tendon degeneration [ 23]. The higher rate of formation of advanced glycation end-products increases the number of stable covalent cross-links within collagen fibres, which in turn alter their structure and functionality. Finally, systemic (adipokine-mediated) and localized (metalloproteinase-mediated) chronic low-grade inflammation can cause tendon damage in the long term. While it might be difficult to disentangle the impact of each factor, a combination of these might explain the lower incidence of obese patient in the zone 1/2 fracture group fractures compared to zone 3 in this study sample.

The results of this study might also have implications regarding treatment and prognosis. High BMI might have an impact in zone 3 fractures non-union, which are known to have an intrinsic risk of non-union per se [ 24, 25]. In fact, high BMI is a known factor for fracture non-union in the general population [ 26]. As current literature suggest operative treatment of zone 3 fractures either in the athlete [ 11, 27], in case of significant displacement [ 28] or established non-union [ 29], the treating orthopaedic surgeon might choose to warn these patients of their increased chance of non-union and suggest modifications to the treatment plan accordingly.

This study has several limitations: firstly, the sample size is small, especially when compared to other series published in the literature. Secondly, data on weight and height was gathered retrospectively through inquiry and self-report. Thirdly, despite the conscious effort to include only fractures which were a result of a "twisting-type" motion, the retrospective fashion of the study did not allow for a more thorough analysis of the injury mechanism. Lastly, results were not adjusted according to BMD or any underlying metabolic disorders: as the behaviour of BMD in the fifth metatarsal was not studied in literature or investigated by us, this aspect was not included it in the analysis.

Conclusions

The results of this study show that BMI might play a role in the prevalence of specific fracture patterns in the fifth metatarsal base: overweight and obese patients are most numerous in the zone 3 fracture group and the risk of incurring in such fracture increases with higher BMI values. A possible explanation can be found in the secondary biomechanical and metabolic effects of excessive adipose tissue. Despite the several limitations, this study can lay ground for future research in this field: statistical analysis on larger sample size can confirm or disprove these findings, with further implications on treatment and prognosis.

Availability of data and materials

Please contact author for data requests.

Abbreviations

BMD:

Bone Mineral Density

BMI:

Body Mass Index

SD:

Standard Deviation

References

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Ding BC, Weatherall JM, Mroczek KJ, Sheskier SC. Fractures of the proximal fifth metatarsal keeping up with the joneses. Bull NYU Hosp Jt Dis. 2012;70:49-55.

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Author information

Affiliations

1. Department of Anatomical, Histological, Forensic Medicine and Orthopaedic Science, Sapienza University of Rome, Piazzale A. Moro 3, 00155, Rome, Italy

M. Pugliese, D. De Meo, E. Sinno, V. Pambianco, P. Persiani & C. Villani

2. Department of Orthopaedics and Traumatology, Policlinico Umberto I, Rome, Italy

M. Pugliese, D. De Meo, E. Sinno, V. Pambianco, P. Persiani & C. Villani

3. Division of Diagnostic and Interventional Radiology, University Hospital Policlinico "Tor Vergata", Rome, Italy

A. U. Cavallo

Contributions

MP, ES and DDM designed the study and wrote the paper. VP, PP and AUC gathered the data and classified the fractures, CV contributed to the study design and critical revision, giving the final approval of submitted version. AUC conceived and performed statistical analysis. All authors read and approved the final manuscript.

Corresponding author

Correspondence to M. Pugliese.

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Not applicable (In light of the Italian law, authors are not required to ask for approval of an institutional review board or ethical committee for this type of study).

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The authors declare that they have no competing interests.

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Pugliese, M., De Meo, D., Sinno, E. et al. Can body mass index influence the fracture zone in the fifth metatarsal base? A retrospective review. J Foot Ankle Res 13, 9 (2020). https://doi.org/10.1186/s13047-020-0374-6
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Can body mass index influence the fracture zone in the fifth metatarsal base? A retrospective review

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Fifth metatarsal base fracture are a common occurrence in the orthopaedic practice. Literature on the epidemiology of such fractures is scarce. The aim of this analysis was to study the relationship between Body Mass Index (BMI) and the zone of the fifth metatarsal base involved by the fracture.

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-5-9

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This study did not find a significant difference between the foot and internal shoe length in diabetic and non-diabetic subjects. A significant number of participants did, however, have a gap between the toe and shoe that lay outside Chantelau and Gede's [ 21] suggested 10 to 15 mm range (p = 0.009). Therefore, according to Chantelau and Gede, the majority of the participants (72%) in our study were wearing footwear of incorrect length. In particular, 82% of participants with diabetes were wearing shoes of incorrect length and 35% and 36% of the diabetic and the non-diabetic populations respectively wore shoes that were too short. In our study, 47% of the diabetic population and 31% of the non-diabetic population wore shoes that were too long.

Given the fitting mismatches apparent between foot and internal shoe-length, it is possible that participants may have developed footwear purchasing habits before being diagnosed with diabetes. For example, it is possible that people had their feet measured once as an adult and then continue to purchase the same size shoe over many years without being re-measured, whether or not they have been diagnosed with diabetes. It is also possible that people do not have their feet measured at all, basing their purchases on subjective feelings of fit adequacy alone; a habit that would establish the perceived fit required, and which could continue after receiving a diagnosis of diabetes.

The foot and shoe length differences were significantly greater in terms of overall length in the diabetic group compared to the non-diabetic group. This could relate to a finding by Burns et al [ 20] who reported that some people purchase a larger shoe size than their foot in order to achieve a wider width fitting, with this practice resulting in a commensurate increase in length. In Chantelau and Gede's study [ 21], the foot to shoe length matched well with the (continental) shoe size system used, whilst the width sizes did not, which may be another characteristic of an ill-fitting shoe.

Width measurements from a shoe fitting perspective should, however, involve a three-dimensional assessment. Width measurement with a calliper or calliper-like device alone, such as undertaken by Chantelau and Gede [ 21] and Harrison et al, [ 22], does not take into consideration the depth needed to accommodate the foot - a consideration that is closely related to the width. As such, shoe width fitting involves a balance between the actual shoe width, foot width, foot depth and available shoe depth and this complexity makes the width dimension more difficult to measure. Therefore, width fitting may be an important factor in correct shoe fitting, but to achieve an acceptable width fitting, the length fitting may need to be compromised.

The gap required between foot and overall internal shoe length of 10 to 15 mm as suggested by Chantelau and Gede is greater than others quoted in the literature (e.g. the 8.5 mm quoted by DiMaggio and Vernon [ 23]). Both values are intended to allow the foot to extend whilst standing and walking, however these values have also been stated within different fitting contexts. Continental shoe sizing systems are used across mainland Europe, where Chantelau and Gede are based, while US and UK shoe size systems apply to the working context of DiMaggio (US) and Vernon (UK). The US and UK systems half size availability of 4.25 mm allows a greater range of fitting choice between sizes than the Continental system, which allows 2/3 cm (6.66 mm) between size options [ 29]. As such, with fewer size options in the Continental system, there may be no option other than to recommend a wider allowance from the distal end of the toe to the shoe in order to allow adequate extension of the foot within the shoe. This may explain the reason for Chanteleau and Gede's larger value.

Alternately, it is possible that Chantelau and Gede's value is erroneous. They refer to their 10 -15 mm value as an example of the gap between foot and shoe-length. However, the data tables presented by Chantelau and Gede appear to indicate gaps predominantly in the order of 6-11 mm, with a modal value of 9 mm - a lower range than his suggested example and more in line with the 8.5 mm allowance.

Whichever reason accounts for the differences between Chanteleau and Gede's value and those suggested by others, there is a need for an appropriate standardised measurement and sizing system. Such a system should consider all relevant factors to ensure that a baseline of agreement exists in relation to length and width measurements in the context of foot health.

One inconsistency in the literature is in the measurement of foot to internal shoe-length. The current study used a calibrated internal shoe size gauge (mm)® (SATRA, UK), whilst others have used the following disparate methods, a motorised measuring apparatus [ 21]; a calibrated (in centimetres) measuring stick and conversion to shoe size [ 22]; nurse-clinician thumb size to determine end of foot to shoe gap [ 15]; internal calliper measurements and shoe size [ 20]; and the use of English shoe size to calibrated measuring stick [ 19].

In a previous descriptive study of one hundred participants with diabetes, the foot length was measured with the use of a commercial shoe company's measuring device [ 22]. The foot length was measured both seated and standing, and the shoe length was measured in centimetres with the use of a calibrated stick, with differences between shoe and foot length being calculated and recorded. The authors concluded that about 33% of patients were more than a half size out in shoe length when seated. One particular finding was that there was no relationship between footwear size and the presence of sensory neuropathy [ 22]. It is not clear from this article what allowances were made in the study for movements such as slippage when comparing measurements of overall foot and internal shoe-lengths.

The criteria for 'ill-fitting' footwear and the methods for measuring the foot and shoe differ widely. This compromises the determination of the prevalence of ill-fitting footwear in a diabetic population as considered in this study. Our study has attempted to determine the relationship of the foot length to the shoe length by taking a standardised approach to both foot and shoe measurements and this approach has highlighted the discrepancies and lack of standardisation in both the measurement techniques and allowances made in shoe fitting.

It is important to note that loose fitting shoes can also potentially cause those pathologies that are related to increased levels of dynamic friction forces between the foot and shoe (e.g. blisters and callus formation), which in the diabetic population can have more serious sequelae. There is sufficient compelling evidence that footwear contributes to foot ulceration [ 14]. One study [ 15], investigated the role of footwear in the prevention of foot lesions in people with type 2 diabetes and reached a controversial conclusion that there was no interaction between neuropathy and footwear in the aetiology of foot wounds. However, this was challenged by Chantelau and Gede [ 21] who suggested that a significant number of people with diabetic neuropathy developed shoe induced foot ulcers.

Despite the studies in this area using different methodologies and taking place within different operating contexts, they have reached similar conclusions; a significant number of people with and without diabetes do not wear appropriately sized shoes. However, the objective identification of specific characteristics of a good fitting shoe remains elusive. A trained shoe fitter can identify characteristics of a shoe that indicate poor fit, but this is very much a craft skill, much of which is not currently supported by research evidence.

This study needs to be viewed in light of a few limitations. Firstly, participant characteristic data, such as height, age and weight, were not recorded, so we were unable to compare the two groups for differences in these variables. There is the possibility that some of these variables (e.g. height) may have had an effect on foot length. If the example of height is explored further, then the significant difference we found in foot length may have simply been due to a difference in height between the two groups. We were, however, primarily interested in the difference between foot length and shoe length, not foot length alone. Secondly, a power calculation (i.e. a sample size calculation) was not performed prior to the study commencing recruitment and the sample size estimate we did make was not reached. This may have affected whether we had sufficient statistical power to detect clinically worthwhile differences between shoe length and foot length. Finally, it was not anticipated that the majority of participants with diabetes and neuropathy would already have bespoke footwear, which resulted in lower numbers of eligible patients being able to enter the study. Further research in this area should consider a longer recruitment time and include more than one centre to ensure that enough participants are able to take part.

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Comparison of shoe-length fit between people with and without diabetic peripheral neuropathy: a case-control study

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Amongst the many identified mechanisms leading to diabetic foot ulceration, ill-fitting footwear is one. There is anecdotal evidence that people with diabetic peripheral neuropathy wear shoes that are too small in order to increase the sensation of fit. The aim of this study was to determine whether people with diabetic sensory neuropathy wear appropriate length footwear.

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00415-x

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00410-2

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Lien:
https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00431-x

Helene:
https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00428-6

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Thibaud Michiels

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Esther Van Snick

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Highlights

*

Heels height influences the motion of the pelvis and the spine during walking.

*

Lumbar and thoracic curvatures decrease during gait with high heels.

*

Low-heeled walking influenced the pelvis and the spine less than with high-heels.

*

No difference between the level of expertise was observed.

Abstract

An estimated 78% of women regularly walk in high heels. However, up to 58% complain about low back pain, which is commonly thought to be caused by increased lumbar lordosis. However, the extent to which a subject's posture is modified by high-heeled shoes during dynamic activities remains unknown. Therefore, we sought to evaluate whether low- or high-heeled shoes influence the kinematics of the pelvis and the spine during walking. Twenty-three inexperienced women, and seventeen women experienced in wearing high-heeled shoes, all aged 20-55 years, were measured barefoot and while wearing low- (4 cm) and high-heeled (10 cm) shoes during gait at a self-selected speed. A 22-camera motion capture system was used to assess the gait patterns for each condition.

No significant inter-experience-group kinematic differences were found. In contrast to the results of some studies, our results show that the heels' height does indeed influence the motion of the pelvis and the spine during walking, whereby low-heeled shoes influenced the subjects' trunk kinematics during gait less than high-heeled shoes compared to barefooted walking. However, inexperienced high-heel wearers showed less thoracic curvature angle while wearing high-heels than while wearing low-heels. Importantly, both groups exhibited significantly lower maximum and minimal lumbar and thoracic curvature angles when wearing high-heeled shoes compared to the barefoot condition. As a result, it seems that low back pain might be associated with other factors induced by high-heels.

View Abstract

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High-heeled walking decreases lumbar lordosis

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Heels height influences the motion of the pelvis and the spine during walking. * Lumbar and thoracic curvatures decrease during gait with high heels. * Low-heeled walking influenced the pelvis and the spine less than with high-heels. * No difference between the level of expertise was observed.

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Elena Daelman

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Journal of Foot and Ankle Research 13, Article number: 47 (2020) Cite this article

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Abstract

The current study investigated the effects of shoes of different weights on calf individual muscle contributions during a running cycle. Twenty male runners ran on a force platform with shoes of four different weights (175 g, 255 g, 335 g, and 415 g). The study evaluated runners' lower extremity muscle forces under the four shoe weight conditions using a musculoskeletal modeling system. The system generates equality and inequality constraint equations to simulate muscle forces. The individual muscle contributions in each calf were determined using these muscle forces. Data were compared using one-way repeated-measure ANOVA. The results revealed significant differences in the contributions of the gastrocnemius lateralis. Post hoc comparisons revealed that running in the 175 g shoes resulted in a larger contribution of the gastrocnemius lateralis than running in the 415 g shoes during the braking phase. Therefore, wearing lightweight shoes while running may promote fatigue in the gastrocnemius muscle during the braking phase. The calf muscle activation results may indicate that an adaptation period is warranted when changing from heavy to lightweight shoes.

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Background

Shoe weight can be used to categorise running shoes. Shoes with a weight of 150-200 g are called light shoes, shoes with a weight of 200-300 g are called minimalist shoes and shoes with a weight of 360 g or greater are called heavy shoes [ 1]. Minimalist shoes have been speculated to strengthen foot muscles and arches, which may help prevent injuries [ 2]. The reasons for this phenomenon may be that impact force on the ground acts as an input signal to trigger muscle tuning [ 3], and runners use their own comfort mechanisms to maintain their preferred movement path and reduce the risk of injury [ 4].

Previous studies have noted that reducing the weight of shoes has been found to improve running economy [ 5]. Previous studies have also observed that adding 100 g of weight per shoe increases the submaximal VO2 (increases oxygen consumption) by ~ 1% [ 6]. Hoogkamer et al. also found that adding 100 g of mass per shoe increases metabolic rate by 0.75% at a velocity of 3.5 m·s-1 during the 3000 m time-trial running [ 7]. This concept of compensation for additional shoe weight implies decreased movement efficiency when performing in heavy shoes [ 8]. Runners with heavy shoes produce more oxygen and consume more energy than those with lightweight shoes, resulting in a low running efficiency [ 9]. Reducing the weight of shoes increases the efficiency of running because less force must be generated by muscles, and less mechanical work is required. When muscles perform mechanical work, they consume energy. Therefore, shoes of different weights and configurations can change a runner's foot muscles and energy consumption.

The lack of arch support in minimalist running shoes have been shown to increase the strength of foot muscles [ 10]. This concept is reflected by an increase in the cross-sectional areas of both intrinsic and extrinsic foot muscles after a period of running in minimalist shoes that mimic barefoot running [ 11]. Further, use of Vibram FiveFinger minimalist shoes have been shown to increase the intrinsic muscle thickness and strength of the abductor hallucis muscle [ 12]. These effects have been proposed to reduce the risk of muscle injury.

Different shoes (i.e. different shoe masses) may change a runners foot strike patterns [ 13], which in turn may affect muscle activation in the lower extremities. Musculoskeletal models may be used as generic models or subject-specific models. The generic models made by generic data measurements from cadaveric quantity information [ 14, 15]. To date, these effects have not been reported during running with shoes of different weights focus on calf individual muscle contributions.

Therefore, the aim of the current investigation was to examine forces produced by muscles and contributions of calf muscles during the braking phase. The hypotheses were that a large shoe mass would result in increased calf muscle activation during the braking phase of a running cycle. This study may provide important information regarding the extent of the recruitment of key muscles when running with shoes of different weights.

Methods

Participants

Twenty males with a mean (SD) age of 21.8 (1.2) years, height of 1.72 (0.03) m and weight of 68.00 (4.32) kg were recruited from a university. The participants had no experience wearing the running shoes used in this experiment (running shoe, model 1208, Xinwei, China). None of the participants reported having any musculoskeletal or ligamentous injuries to the lower extremities at the time of participation or during the 6 months prior to the experiment. Prior to data collection, each participant gave informed consent, as stipulated by the Antai Medical Care Corporation Memorial Hospital (Pingdong, Taiwan; IRB no. 15-066-B1).

Experimental protocol

All participants wore identical running shoes throughout the data collection period to minimize variability. Lead weights were attached to the four outer sides of each shoe to reach the required total weight. Four of the same shoes of different weights were used, and the additional weights were evenly distributed over the length of the shoes in this study (Fig. 1): shoe only (175 g +/− 5 g), shoe alone with an additional 4 × 20 g lead weight (255 +/− 5 g), shoe alone with an additional 4 × 40 g lead weight (335 +/− 5 g), and shoe alone with an additional 4 × 60 g lead weight (415 +/− 5 g). The lead weights were covered with tape, so the participants were blinded to the different footwear conditions. The participants were instructed to warm up for 20 min (by raising their knees high and lowering their jaw) and to practice running five times at a comfortable, controlled, self-selected running velocity with each shoe weight condition for familiarization before data collection [ 16]. A rest period of 2 min separated the trials. The shoe weight condition order was randomized for each participant.

Experimental shoes. a 175 g shoe, b 255 g shoe, c 335 g shoe, and d) 415 g shoe

Data analysis

A motion capture system (Qualisys Track Manager [QTM], Oqus 100, Sweden) consisting of seven infrared video cameras recorded the marker trajectories at a sampling rate of 200 Hz. Whole-body motion data were collected with a total of 40 reflective markers (19 mm in diameter) placed on bony landmarks (Fig. 2). To form a 10-m-long straight path, two force plates (BP600900, AMTI Inc., Watertown, MA, USA) that measured ground reaction force (GRF) data at a sampling rate of 1000 Hz were embedded in the path. GRF measurements were normalized to the body mass to facilitate interindividual comparisons. The motion and force data were time synchronized with the Qualisys 64-channel interface. The marker trajectories and GRF data were imported into MATLAB (version 7.0; Mathworks Inc., Natick, MA) from QTM software for data reduction and analysis. The kinematic and force data were low-pass filtered with fourth-order Butterworth filters and 12 Hz and 50 Hz cutoff frequencies, respectively. The average data per participant were used for analysis. The dominant leg was defined as the leg used by the participant to kick a ball. The trials were normalized to 100% of the gait cycle on the dominant side for analysis [ 16]. Muscle simulations are commonly used for the analysis of load during body movements [ 14, 15, 17]. In this study, the specific muscles used in the comparisons of calf muscle's contributions during the braking phase among the different shoe weight groups were considered. A musculoskeletal modeling system was adopted to determine muscle forces. Simulations of the muscle forces were generated using the Biomechanics of Bodies (BoB) biomechanical modeling package [ 18]. The BoB musculoskeletal modeling system was used to generate the equality and inequality constraint equations for a full-body model in a number of arbitrary poses subject to an arbitrary set of external forces. The musculoskeletal model consisted of 508 muscle forces and 30 joint torques [ 18]. The moments generated by the calf muscle were calculated using inverse dynamics. External forces acting from the ground, gravitational force and inertial forces acting on the participants' bodies were analyzed and used to calculate the forces in the calf muscle [ 19]. The individual muscle's contributions in each calf were determined using these muscle forces. A muscle force optimization approach was utilized in which a solution was sought that minimizes the sum of the square of the activations of the muscles, with activation being defined as the instantaneous force divided by the maximum isometric force of the muscle [ 20, 21]. The individual calf muscle contributions during the braking phase were calculated using the following formula:

$$ \mathrm{Individual}\kern0.3em \mathrm{muscle}\kern0.3em \mathrm{contributions}\%=\frac{\mathrm{Muscle}\kern0.3em \mathrm{force}}{\mathrm{Total}\kern0.3em \mathrm{muscle}\kern0.3em \mathrm{force}}\ast \% $$

Marker set used to record whole-body motion

Muscle forces were defined based on the following conditions: (1) the preactivation phase: 50 ms before the foot lands on the force plate; (2) the stance phase: from heel strike (vGRF > 10 Newtons) to when the toe leaves the force plate (vGRF < 10 Newtons); (3) the braking phase: from heel strike to when the anterior-posterior GRF value becomes negative; and (4) the push-off phase: from when the anterior-posterior GRF values are negative and increase to when the foot leaves the force plate (Fig. 3).

Experimental setup and muscle activations of the lower extremities during the running trials. The following timepoints are represented: ( a) T1: toe off, ( b) T2: prelanding, ( c) T3: contact, ( d) T4: converse, and ( e) T5: toe off. The preactivation phase was from T2 to T3, the breaking phase was from T3 to T4, and the push-off phase was from T4 to T5. The stance phase was from T3 to T5

Statistical analysis

The distribution of data were evaluated from skewness statistic for equality of variances. Statistical analysis was performed using SPSS statistics software version 14.0 (SPSS, Inc., Chicago, IL, USA). Repeated-measure one-way ANOVA was used to determine whether muscle forces were higher when participants wore lightweight shoes. The least significant difference (LSD) test was used as a post hoc test [ 16]. The significance level was set at α = 0.05.

Results

The results showed that the contribution rate of the lateral gastrocnemius muscle during the braking phase was 5.7% in 175 g shoes, 4.0% in 255 g and 335 g shoes, and 3.1% in 415 g shoes (Table 1). The results indicated that the lateral gastrocnemius contribution of the calf muscle was significantly different during the braking phase.

Table 1 Individual calf muscle contributions during the braking phase

The lateral gastrocnemius muscle contributions results showed significant differences between the shoe weight groups ( p = 0.043). The post hoc comparisons revealed that the lateral force contributions of the gastrocnemius muscle during the braking phase was larger in the 175 g shoe condition than in the 415 g shoe condition ( p  = 0.023). There were no other significant differences in other muscle contributions throughout the gait cycle.

Discussion

This study assessed the differences in the forces produced by skeletal muscles and activation patterns of calf muscles during the braking phase while participants ran wearing shoes of different weights. A previous study showed that compared to running while wearing shoes, running barefoot results in higher activation of the gastrocnemius muscle [ 22]. Similarly, another study found that in the time of peak activity of the lateral gastrocnemius, running with heavy shoes significantly delayed the gait cycle by approximately 4% [ 23]. However, J Becker, BJJoE Borgia and Kinesiology [ 24] found no difference in lateral gastrocnemius muscle activation during the whole gait cycle. In this study, differences were found in the braking phase, which may indicate that different shoe weights can change muscle activation during the braking phase. The inter-joint coordination risk of running injuries usually occurs in the braking phase [ 16]. The increasing muscle activity leads to an increasing load on that muscle [ 22], and an increasing load might cause injury to the Achilles tendon, which is highly vulnerable to repetitive overload during running activities [ 25, 26]. Therefore, wearing a light shoe that results in the excessive activation of the gastrocnemius lateralis during the braking phase may increase the incidence of muscle injuries.

Minimalist running shoes can influence the role each muscle has in controlling the motion of the body, with a trend towards higher muscle forces in the gastrocnemius and soleus muscles and higher energy transfers [ 27]. An appropriate shoe affects the landing impact force when running, which can trigger muscle tuning [ 3] to allow the skeleton to move in its preferred path through self-determined comfort mechanisms [ 4]. Minimalist shoes are lighter than traditional shoes, so when people run in minimalist shoes, the gastrocnemius lateralis activates more during the braking phase. The lightest shoes are designed to mimic barefoot conditions. A previous study compared muscle simulations of running in shoes and running barefoot and found that the peak muscle forces of the vastus medialis, vastus lateralis, rectus femoris, and tibialis anterior were larger in the barefoot condition. When barefoot running was simulated, the gastrocnemius had a large peak muscle force [ 13]. In this study, shoes with the same structure and different weights were compared, and the gastrocnemius lateralis was found to have the largest muscle contributions. Therefore, a light shoe may also cause fatigue in the gastrocnemius lateralis.

Minimalist and lightweight shoes are associated with decreased knee extensor individual muscle contributions and increased ankle joint angles [ 28]. These factors increase the load on the ankle joint and increase the contribution of the triceps surae muscles [ 28]. The 175 g shoes may cause greater activation of the gastrocnemius lateralis. A previous study showed that running extreme distances requires more training of the gastrocnemius muscles to prevent muscle fatigue and reduce the risk of injury [ 29]. The results of this study show that the lightest shoes resulted in the largest muscle contributions, so wearing lightweight shoes likely results in more gastrocnemius fatigue compared to wearing heavy shoes. Participants showed more FFS when wearing the 175 g shoes than when wearing the 415 g shoes [ 30]. Medial and lateral gastrocnemius activity increases during FFS running, and these heightened activity levels may lead injury because of the overuse of the medial and lateral gastrocnemius muscle [ 31]. Therefore, wearing lightweight shoes without training may increase the likelihood of injury. This is consistent with previous research which found that transitioning form a RFS to a non-rearfoot strike will reduce running economy and increase loads at the ankle and ankle plantarflexors [ 32]. Therefore, as wearing lightweight shoes may change a runners strike pattern, it may also increase the risk of injury at these sites. Immediate changes lightweight shoes may cause muscle damage due to the excessive fatigue of the ankle joint muscles during the initial wear period. There are limitations to this study, including the use of simulated muscle models rather than EMG data. Furthermore, an attempt was made to blind the participants, as stated in the methods; however, the runners were clearly not blinded to the weights of the shoes since they could see the weights attached. This factor could have introduced performance bias.

Conclusion

This study explored the differences between running shoes with the same structure but different weights. The contribution of the gastrocnemius lateralis, i.e., the integral of the force generated, increased for lightweight shoes. Therefore, wearing lightweight shoes may promote muscle fatigue in the gastrocnemius during the braking phase. Calf muscle activation may be indicative that an adaptation period is warranted when changing from heavy to lightweight shoes.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Abbreviations

RFS:

rearfoot strike

MFS:

midfoot strike

FFS:

forefoot strike

GRF:

ground reaction force

COM:

center of mass

References

1. 20.
Brand RA, Crowninshield RD, Wittstock C, Pedersen D, Clark CR, Van Krieken F. A model of lower extremity muscular anatomy. J Biomech Eng. 1982;104(4):304-10.

2. 32.
Anderson LM, Bonanno DR, Hart HF, Barton CJJSM. What are the benefits and risks associated with changing foot strike pattern during running? A systematic review and meta-analysis of injury, running economy, and biomechanics. J Sports Med. 2020;50(5):885-917.

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Acknowledgments

We thank Jilin Sport University students for participating in the training, testing and data collection for this project and AJE ( www.aje.com) for English language editing.

Funding

This research was supported by Research on Higher Education Teaching for the Jilin Province-Anatomy course on skeletal muscle simulations and teaching construction [grant number [2018] 40] and Research on Teaching Reform of Vocational Education and Virtual Simulation Experiment Teaching in Colleges and Universities of Jilin for post activation potentiation and enhanced training with weight training for skeletal muscle simulations and teaching construction [grant number [2018] 45].

Author information

Affiliations

1. College of Physical Education, Hubei Normal University, No. 11, Cihu Road, Huangshi, 435002, Hubei Province, China

I-Lin Wang & Yi-Ming Chen

2. Graduate College, Jilin Sport University, No. 2476 Ziyou, Changchun, 130022, Jilin Province, China

Ke-Ke Zhang

3. Sports Department, Southwest University of Political Science and Law, No.301 Baosheng, Chongqing, 401120, China

Ming Gou

4. Health Technology College, Jilin Sport University, No. 2476 Ziyou, Changchun, 130022, Jilin Province, China

Jia-Qi Li & Yu-Hong Jiang

Contributions

ILW and YMC designed the experiments. ILW, YMC, YHJ, KKZ and JQL performed the laboratory experiments and compiled the supplementary material. YHJ and KKZ analyzed the data, interpreted the results and prepared the figures. All authors read and approved the final manuscript. ILW, YMC, YHJ, KKZ and JQL provided the materials and analysis platforms.

Corresponding author

Correspondence to I-Lin Wang.

Ethics declarations

Ethics approval and consent to participate

The Antai Medical Care Corporation Memorial Hospital granted approval, and informed consent was obtained for all participants included in the study (No. 15-066-B1).

Consent for publication

Participants' consent to publish was granted.

Competing interests

The authors declare that they have no competing interests.

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Wang, I., Chen, Y., Zhang, K. et al. Effects of the weight of shoes on calf muscle simulation. J Foot Ankle Res 13, 47 (2020). https://doi.org/10.1186/s13047-020-00415-x
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Keywords

Running

Individual muscle contribution

Kinematics

Biomechanics

Footwear

# data[].attributes.attachment_link.title
Effects of the weight of shoes on calf muscle simulation

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The current study investigated the effects of shoes of different weights on calf individual muscle contributions during a running cycle. Twenty male runners ran on a force platform with shoes of four different weights (175 g, 255 g, 335 g, and 415 g). The study evaluated runners' lower extremity muscle forces under the four shoe weight conditions using a musculoskeletal modeling system.

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00433-9

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# data[].attributes.body
https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-018-0260-7#Tab2

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-020-00410-2

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effects of the weight of shoes on calf muscle simulation

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https://jfootankleres.biomedcentral.com/articles/10.1186/s13047-018-0260-7#Tab2

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https://jfootankleres.biomedcentral.com/track/pdf/10.1186/s13047-020-0374-6

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https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-4-S1-O25

https://jfootankleres.biomedcentral.com/articles/10.1186/1757-1146-5-S1-O13

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en Marieke Bizet