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CiteScore: 5.8 ℹ CiteScore:
2019: 5.8
CiteScore measures the average citations received per peer-reviewed document published in this title. CiteScore values are based on citation counts in a range of four years (e.g. 2016-2019) to peer-reviewed documents (articles, reviews, conference papers, data papers and book chapters) published in the same four calendar years, divided by the number of these documents in these same four years (e.g. 2016 - 19).

Impact Factor: 3.242 ℹ Impact Factor:
2019: 3.242
The Impact Factor measures the average number of citations received in a particular year by papers published in the journal during the two preceding years.
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The Journal of Dentistry is the leading international dental journal within the field of Restorative Dentistry. Placing an emphasis on publishing novel and high-quality research papers, the Journal aims to influence the practice of dentistry at clinician, research, industry and policy-maker level on...

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The Journal of Dentistry is the leading international dental journal within the field of Restorative Dentistry. Placing an emphasis on publishing novel and high-quality research papers, the Journal aims to influence the practice of dentistry at clinician, research, industry and policy-maker level on an international basis.

Topics covered include the management of dental disease, periodontology, endodontology, operative dentistry, fixed and removable prosthodontics, dental biomaterials science, long-term clinical trials including epidemiology and oral health, technology transfer of new scientific instrumentation or procedures, as well as clinically relevant oral biology and translational research.

The Journal of Dentistry will publish original scientific research papers including short communications. It is also interested in publishing review articles and leaders in themed areas which will be linked to new scientific research. Conference proceedings are also welcome and expressions of interest should be communicated to the Editor.

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# data[].attributes.headline
Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: an observational cohort study

# data[].attributes.subject
Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: an observational cohort study

# data[].attributes.body
24.4 de Fator de impacto

Em dois hospitais diferentes pegaram pacientes covid-19 e coletaram amostras da saliva orofaríngea, sangue, urina e swabs retais e mediram a concentração do vírus ao longo do tempo.
Basicamente viram uma concentração maior da carga viral no inicio do quadro, testaram mutações e não encontraram. Enfatizam a importância de controlar a infecção e uso precoce de antivirais pra indivíduos de alto risco.

# data[].attributes.headline
Rapid In‐Vitro Inactivation of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS‐CoV‐2) Using Povidone‐Iodine Oral Antiseptic Rinse

# data[].attributes.subject
Rapid In‐Vitro Inactivation of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS‐CoV‐2) Using Povidone‐Iodine Oral Antiseptic Rinse

# data[].attributes.body
Testaram uma solução de povidone-iodine em corona virus in vitro pra ver se diminuía a atividade do mesmo.
Fator: 2.1

3 concentrações de pvp além de um controle negativo (agua) e outro positivo (etanol).
As três concentrações conseguiram inativar o vírus com 15s de contato. Entretanto o álcool só conseguiu com 30s.

# data[].attributes.attachment_link.readable_text
Avinash S. Bidra BDS, MS, FACP

Corresponding Author

E-mail address: avinashbidra@yahoo.com
https://orcid.org/0000-0001-8831-8096
Department of Reconstructive Sciences, University of Connecticut Health Center, Farmington, CT
Correspondence
Avinash Bidra, Department. of Reconstructive Sciences, University of Connecticut Health Center, 263 Farmington Ave., L7039, Farmington, CT 06030. E‐mail: avinashbidra@yahoo.com
Search for more papers by this author

First published:

The authors deny any conflicts of interest.

Abstract

Purpose

To investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice.

Materials and Methods

The severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) USA‐WA1/2020 strain, virus stock was tested against oral antiseptic solutions consisting of aqueous povidone‐iodine (PVP‐I) as the sole active ingredient. The PVP‐I was tested at diluted concentrations of 0.5%, 1%, and 1.5%. Test media without any virus was added to 2 tubes of the compounds to serve as toxicity and neutralization controls. Ethanol (70%) was tested in parallel as a positive control, and water only as a negative control. The test solutions and virus were incubated at room temperature (22 ± 2 °C) for time periods of 15 and 30 seconds. The solution was then neutralized by a 1/10 dilution in minimum essential medium (MEM) 2% fetal bovine serum (FBS), 50 µg/mL gentamicin. Surviving virus from each sample was quantified by standard end‐point dilution assay and the log reduction value (LRV) of each compound compared to the negative (water) control was calculated.

Results

PVP‐I oral antiseptics at all tested concentrations of 0.5%, 1%, and 1.5%, completely inactivated SARS‐CoV‐2 within 15 seconds of contact. The 70% ethanol control group was unable to completely inactivate SARS‐CoV‐2 after 15 seconds of contact, but was able to inactivate the virus at 30 seconds of contact.

Conclusions

PVP‐I oral antiseptic preparations rapidly inactivated SARS‐CoV‐2 virus in vitro. The viricidal activity was present at the lowest concentration of 0.5 % PVP‐I and at the lowest contact time of 15 seconds. This important finding can justify the use of preprocedural oral rinsing with PVP‐I (for patients and health care providers) may be useful as an adjunct to personal protective equipment, for dental and surgical specialties during the COVID‐19 pandemic.

Severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2 the virus resulting in the corona virus disease 2019, COVID‐19) is a novel coronavirus in the same family as the severe acute respiratory syndrome (SARS) and middle east respiratory syndrome (MERS) viruses that emerged in local outbreaks in 2003 and 2015. From the first cases recognized in late December 2019 by health care workers in China, it has rapidly spread across the globe. 1 The World health organization (WHO) declared the spread of COVID‐19 a global pandemic on March 11, 2020. This has significantly changed the way that dentistry is practiced around the world. The clinical workflow of dentists, especially prosthodontists, has been significantly altered due to the fact that the viral load is highest in the nasal cavity, nasopharynx and oropharynx related to the high expression of ACE2 receptor on goblet cells and respiratory epithelium used as fist entry into the body by SARS‐CoV‐2. 2, 2, 4, 5 3 As the mouth is also part of the oropharynx, it harbors bacteria and viruses from the nose, throat and the respiratory tract and contaminated saliva can easily result in spread of viral infections. 3 Viral shedding can be detected from nasal swabs before, during and after the onset of acute symptomatic disease including in seropositive antibody‐converted convalescent cases.

In a dental setting, well recognized terms related to microbiological risk are aerosol and splatter. 4- 7 Aerosols are generally defined as suspension of fine solid particles or liquid droplets in air and splatters are larger liquid particles in air that impact a surface and then break apart. In dentistry, aerosols are recognized as airborne particles smaller than 50 µm in diameter which are small enough to stay in air for extended periods and entail risk of environmental contamination, and entry into respiratory tracts. 4- 7 Most procedures in contemporary prosthodontics ranging from single unit restorations to complex implant surgery include aerosol production due to the use of handpieces and air‐water syringes. Additional dental maintenance procedures involving the use of ultrasonic scalers and air abrasion units produce even higher visible aerosols. 4 All these procedures involve aerosol production resulting in higher risk for clinicians, dental assistants, and patients. 7 Any dental procedure that can aerosolize contaminated saliva can significantly increase airborne contamination with microorganisms. 4‐7 On the other hand, splatters are denoted as airborne particles larger than 50 µm in diameter and too large to stay suspended in air for longer periods. Splatters are typically seen as droplets ejected forcefully in a ballistic manner similar to a bullet until they contact a surface.

Due to the COVID‐19 pandemic which has resulted in significant morbidity and mortality, it is imperative for clinicians to consider adjunctive protective measures that can add an additional barrier of safety in providing prosthodontics treatment. Understandably, there is no single method or agent, which can completely eliminate or minimize the risk of COVID‐19 infection to dental personnel and other patients. Harrel and Molinari have described 3 layers of defense against aerosols in a dental office. 4 The first layer is personal protective equipment (PPE) such as gloves, eye glasses and masks. The second layer is regular use of oral antiseptic rinse and the third layer is the use of high volume evacuator (HEV) ("high speed suction") and adjunctive high efficiency particulate air (HEPA) filters. The first and third layers of defense have received significant attention by dentists however, the second layer of defense has not received sufficient attention.

Harrel and Molinari recommended preprocedural oral rinsing with chlorhexidine gluconate a rinse with essential oils, but both of these are known to only be efficacious against bacteria, with no viricidal properties. 4 Therefore, the American Dental Association (ADA) interim guidelines from April 2020 have suggested preprocedural oral rinsing with 1.5% hydrogen peroxide (commercially available in the United States) or 0.2% povidone‐iodine PVP‐I (not commercially available in the United States). 8 The Centers for Disease Control and Prevention (CDC) have also recommended preprocedural rinsing with antimicrobial rinses such as chlorhexidine gluconate, essential oils, PVP‐I or cetylpyridinium chloride. 9 Presently, there are no clinical studies supporting the viricidal effects of any pre‐procedural oral rinse against SARS‐CoV‐2. 8 Additionally, there are no in vitro studies on the viricidal effect of the commercially available 1.5% hydrogen peroxide. However, PVP‐I solutions of 0.23% have effectively inactivated SARS‐CoV and MERS with contact times as low as 15 seconds in vitro. 10, 11 The SARS‐CoV‐2 virus resulting in the COVID‐19 pandemic is a novel coronavirus in the same family and is expected to be inactivated by PVP‐I in the same manner.

Therefore, the purpose of this study was to investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice. The null hypothesis was that there would be no difference in viricidal activity of PVP‐I at various concentrations and contact times as well as there would be no difference between PVP‐I and the positive and negative controls.

Materials and methods

All laboratory work with SARS‐CoV‐2 was conducted in biosafety level 3 (BSL‐3) laboratories at The Institute for Antiviral Research at Utah State University Logan, UT following established standard operating procedures approved by the Utah State University Biohazards Committee. The SARS‐CoV‐2, USA‐WA1/2020 strain, virus stock was prepared prior to testing by growing in Vero 76 cells. Culture media for prepared stock (test media) was minimum essential medium (MEM) with 2% fetal bovine serum (FBS) and 50 µg/mL gentamicin. The oral rinse antiseptic solution consisted of various concentrations of aqueous povidone‐iodine (PVP‐I) as the sole active ingredient (Veloce BioPharma; Fort Lauderdale, FL). The PVP‐I concentrations of each solution as supplied and after 1:1 dilution are listed in Table 1.

Test Product

PVP‐I Concentration (%) After 1:1 Dilution

Incubation Time (in seconds)

Virus Titera

LRVb

a Log10 CCID50 of virus per 0.1 mL. The assay lower limit of detection is 0.67 Log10 CCID₅₀/0.1 mL.

b LRV (log reduction value) is the reduction of virus compared to the virus control.

The test compounds were mixed directly with virus solution so that the final concentration was 50% of each individual test compound and 50% virus solution. A single concentration was tested in triplicate. Test media without virus was added to 2 tubes of the compounds to serve as toxicity and neutralization controls. Ethanol (70%) was tested in parallel as a positive control and water only as a virus control. The test solutions and virus were incubated at room temperature (22 ± 2 °C) for 15 and 30 seconds. The solution was then neutralized by a 1/10 dilution in MEM 2% FBS, 50 µg/mL gentamicin.

Surviving virus from each sample was quantified by standard end‐point dilution assay. The neutralized samples were pooled and serially diluted using eight log dilutions in test medium. Then 100 µL of each dilution was plated into quadruplicate wells of 96‐well plates containing 80% to 90% confluent Vero 76 cells. The toxicity controls were added to additional 4 wells of Vero 76 cells and 2 of those wells at each dilution were infected with virus to serve as neutralization controls, ensuring that residual sample in the titer assay plate did not inhibit growth and detection of surviving virus. Plates were incubated at 37 ± 2 °C with 5% CO ₂ for 5 days. Each well was then scored for presence or absence of infectious virus. The titers were measured using a standard endpoint dilution 50% cell culture infectious dose (CCID50) assay calculated using the Reed‐Muench equation and the log reduction value (LRV) of each compound compared to the negative (water) control was calculated. 12

Results

Virus titers and LRV of SARS‐CoV‐2 when incubated with various concentrations of the manufacturer's compounds for 15 seconds are shown in Table 1. After the 15‐second contact time, all of the PVP‐I oral rinse antiseptics tested were effective at reducing >3 log10 CCID50 infectious virus from, 3.67 log10 CCID50/0.1 mL to 0.67 log10 CCID50/0.1 mL or less. Table 2 shows the virus titers and LRV of SARS‐CoV‐2 when the virus was incubated for 30 seconds with each of the test compounds at 50/50 ratio. For the 30‐second contact time, once again all of the PVP‐I oral rinse antiseptics tested were effective at reducing >3.33 log10 CCID50 infectious virus from, 4.0 log10 CCID50/0.1 mL to 0.67 log10 CCID50/0.1 mL or less. No cytotoxicity was observed with any of the test compounds. The positive control and neutralization controls performed as expected.

Test Product

PVP‐I Concentration (%) After 1:1 Dilution

Incubation Time (in seconds)

Virus Titera

LRVb

a Log10 CCID50 of virus per 0.1 mL. The assay lower limit of detection is 0.67 Log10 CCID50/0.1 mL.

b LRV (log reduction value) is the reduction of virus compared to the virus control.

Discussion

The purpose of this study was to investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice. Data from this in vitro study rejected the null hypothesis, and showed the rapid viricidal activity of PVP‐I oral formulation. The minimum 15 seconds contact time proved to be sufficient for PVP‐I. This is similar to the results from previous studies where PVP‐I solutions of 0.23% inactivated SARS‐CoV and MERS with contact times as low as 15 seconds in vitro. 10, 13 11 Oral decontamination is an important adjuvant process along with PPE to reduce viral transmission among dental patients especially during aerosol generating procedures. A majority of prosthodontic procedures involve close physical contact with the patient and generate aerosols increasing the risk of viral transmission. In the absence of clinical studies, the residual challenge in oral antisepsis is to find the effective concentration and duration of topical preparations which are safe to administer. Several different protocols have been used anecdotally to dilute PVP‐I at a varying concentration ranging from 0.25% to 0.5% in an attempt to inactivate the virus from the nasal and oral cavity.

Oral use of PVP‐I antiseptic rinse is not novel to dentistry and has been used effectively in the past for oral decontamination, 14 periodontal therapy, 15 peri‐implant therapy 16 and post‐extraction therapy. 17 PVP‐I has proven safe for use in the oral cavity up to 5% concentration and nasal cavities at concentrations up to 1.25%. 18- 21 Thyroid stimulating hormone was shown to slightly increase within normal levels after oral use of 5% PVP‐I for 6 months, but no clinical thyroid disease was detected. 22 Nevertheless, at concentrations of 0.2% to 0.5% iodine absorption is minimal and below the total daily iodine intake for a healthy adult of 150 µg. Additionally, no change in taste or discoloration of teeth has been reported in the literature. 23 The substantivity (prolonged association between a topical material and a substrate) of oral PVP‐I antiseptic rinse has been reported to be as long as 4 hours. 24 However PVP‐I solutions are contraindicated for patients with anaphylactic allergy to iodine, pregnancy, active thyroid disease, and patients undergoing radioactive iodine therapy. 25- 27 20 At these concentrations, no change in olfaction or mucociliary clearance has been noted.

The alternative to oral PVP‐I solution is 1.5% hydrogen peroxide rinse, as recommended by the ADA interim guidelines. 8 Presently the CDC does not recommend this rinse due to absence of sufficient scientific evidence. 9 Though 1.5% hydrogen peroxide is known to be antibacterial, it is chemically more unstable. There are no published studies showing the inactivation of SARS‐CoV‐2 by this solution at 1 minute contact period. 28 The potential oral toxicity of routine use of this solution for 1 minute as well as its substantivity is unknown at this time. Additionally, alcohol is present in most oral rinses and results from this study showed that it required a longer time for viral inactivation than PVP‐I oral solutions tested.

Some disadvantages of the PVP‐I oral solutions include the absence of clinical research such as randomized clinical trials, and the current absence of commercially available formulation at lower concentrations for intra‐oral use. Therefore, dentists are required to dilute the commercially available antiseptic formulation of 10% PVP‐I, by 1:20, utilizing 0.5 ccs of 10% povidone iodine and 9.5 ccs of sterile water for routine clinical use at 0.5%. This compound typically contains suds which do not cause any adverse effects for topical usage. However, dentists should make freshly diluted solutions each day and refrigerate them during the day as diluted PVP‐I solutions are chemically unstable with respect to disproportionation into constituent equilibrium species. As the aqueous concentration of PVP‐I decreases from 10% to less than 1%, these solutions become unstable with respect to temperature, counterions, commercial packaging and pH value. In order to ensure that a diluted solution is safe for administration to the oral or nasal cavity, there should either be an analysis of the chemical ingredients of each freshly‐prepared solution or commercial preparations of PVP‐I at the appropriate dose (if available) should be used.

Conclusions

PVP‐I oral antiseptic preparations rapidly inactivated SARS‐CoV‐2 virus in vitro. The 70% ethanol control group was unable to completely inactivate SARS‐CoV‐2 after 15 seconds of contact, but was able to inactivate the virus at 30 seconds of contact. The viricidal activity of PVP‐I oral antiseptic solution was present at the lowest concentration of 0.5 %, and at the lowest contact time of 15 seconds. This important finding warrants the use of preprocedural oral rinsing with 0.5% PVP‐I for patients and health care providers. This solution serves as an adjunct to personal protective equipment for dental and surgical specialties during the COVID‐19 pandemic.

Funding

Sponsorship for this study was funded by Veloce Biopharma, Florida, USA. All authors had full access to all of the data in this study and take complete responsibility for the integrity of the data and accuracy of the data analysis.

Number of times cited according to CrossRef: 13

A. Vergara-Buenaventura, C. Castro-Ruiz, Use of mouthwashes against COVID-19 in dentistry, British Journal of Oral and Maxillofacial Surgery, 10.1016/j.bjoms.2020.08.016,

Mallesh Kurakula, G.S.N. Koteswara Rao, Pharmaceutical assessment of polyvinylpyrrolidone (PVP): As excipient from conventional to controlled delivery systems with a spotlight on COVID-19 inhibition, Journal of Drug Delivery Science and Technology, 10.1016/j.jddst.2020.102046, (102046), 60,

Jesse S. Pelletier, Kevin Stewart, Belachew Tessema, Reducing transmission of SARS-CoV-2 in ophthalmology with nasal and oral decontamination, Therapeutic Advances in Ophthalmology, 10.1177/2515841420951392, (251584142095139), 12,

Mubarak Muhamed Khan, Sapna Ramkrishna Parab, 0.5% povidone iodine irrigation in otorhinolaryngology surgical practice during COVID 19 pandemic, American Journal of Otolaryngology, 10.1016/j.amjoto.2020.102687, (102687),

Avinash S. Bidra, Jesse S Pelletier, Jonna B Westover, Samantha Frank, Seth M Brown, Belachew Tessema, Comparison of In Vitro Inactivation of SARS CoV‐2 with Hydrogen Peroxide and Povidone‐Iodine Oral Antiseptic Rinses, Journal of Prosthodontics, 10.1111/jopr.13220, 7, (599-603), 29,

PaulT Finger, Anthony Fam, AnkitS Tomar, Gaurav Garg, KimberlyJ Chin, COVID-19 prophylaxis in ophthalmology, Indian Journal of Ophthalmology, 10.4103/ijo.IJO_2459_20, 10, (2062), 68,

S. Abdulrab, B. Alkadasi, S. Al-maweri, E. Halboub, H. Alhadainy, G. Geerts, Statins-based prophylactic mouthwash and nasal spray may protect against coronavirus disease 2019, New Microbes and New Infections, 10.1016/j.nmni.2020.100751, (100751), 37,

L. Cegolon, M. Javanbakht, G. Mastrangelo, Nasal Disinfection for the Prevention and Control of COVID-19: A Scoping Review on Potential Chemo-preventive Agents., International Journal of Hygiene and Environmental Health, 10.1016/j.ijheh.2020.113605, (113605),

Eisha Imran, Zohaib Khurshid, Adam Ahmed M. Al Qadhi, Ahmed Adel A. Al-Quraini, Khaloud Tariq, Preprocedural Use of Povidone-Iodine Mouthwash during Dental Procedures in the COVID-19 Pandemic, European Journal of Dentistry, 10.1055/s-0040-1717001,

José G. B. Derraik, William A. Anderson, Elizabeth A. Connelly, Yvonne C. Anderson, Rapid Review of SARS-CoV-1 and SARS-CoV-2 Viability, Susceptibility to Treatment, and the Disinfection and Reuse of PPE, Particularly Filtering Facepiece Respirators, International Journal of Environmental Research and Public Health, 10.3390/ijerph17176117, 17, (6117), 17,

Shaur Sarfaraz, Juzer Shabbir, Muhammad Adeel Mudasser, Zohaib Khurshid, Ahmed Adel A. Al-Quraini, Maria Shakoor Abbasi, Jithendra Ratnayake, Muhammad Sohail Zafar, Knowledge and Attitude of Dental Practitioners Related to Disinfection during the COVID-19 Pandemic, Healthcare, 10.3390/healthcare8030232, 3, (232), 8,

Phulen Sarma, Hardeep Kaur, Bikash Medhi, Anusuya Bhattacharyya, Letter to the editor: Possible role of topical povidone iodine in case of accidental ocular exposure to SARS-CoV-2, Graefe's Archive for Clinical and Experimental Ophthalmology, 10.1007/s00417-020-04864-9,

Reza Eftekhar Ashtiani, Shabnam Tehrani, Marta Revilla‐León, Amirali Zandinejad, Reducing the Risk of COVID‐19 Transmission in Dental Offices: A Review, Journal of Prosthodontics, 10.1111/jopr.13261, 0, 0,

Abstract

Purpose

To investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice.

Materials and Methods

The severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) USA‐WA1/2020 strain, virus stock was tested against oral antiseptic solutions consisting of aqueous povidone‐iodine (PVP‐I) as the sole active ingredient. The PVP‐I was tested at diluted concentrations of 0.5%, 1%, and 1.5%. Test media without any virus was added to 2 tubes of the compounds to serve as toxicity and neutralization controls. Ethanol (70%) was tested in parallel as a positive control, and water only as a negative control. The test solutions and virus were incubated at room temperature (22 ± 2 °C) for time periods of 15 and 30 seconds. The solution was then neutralized by a 1/10 dilution in minimum essential medium (MEM) 2% fetal bovine serum (FBS), 50 µg/mL gentamicin. Surviving virus from each sample was quantified by standard end‐point dilution assay and the log reduction value (LRV) of each compound compared to the negative (water) control was calculated.

Results

PVP‐I oral antiseptics at all tested concentrations of 0.5%, 1%, and 1.5%, completely inactivated SARS‐CoV‐2 within 15 seconds of contact. The 70% ethanol control group was unable to completely inactivate SARS‐CoV‐2 after 15 seconds of contact, but was able to inactivate the virus at 30 seconds of contact.

Conclusions

PVP‐I oral antiseptic preparations rapidly inactivated SARS‐CoV‐2 virus in vitro. The viricidal activity was present at the lowest concentration of 0.5 % PVP‐I and at the lowest contact time of 15 seconds. This important finding can justify the use of preprocedural oral rinsing with PVP‐I (for patients and health care providers) may be useful as an adjunct to personal protective equipment, for dental and surgical specialties during the COVID‐19 pandemic.

Severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2 the virus resulting in the corona virus disease 2019, COVID‐19) is a novel coronavirus in the same family as the severe acute respiratory syndrome (SARS) and middle east respiratory syndrome (MERS) viruses that emerged in local outbreaks in 2003 and 2015. From the first cases recognized in late December 2019 by health care workers in China, it has rapidly spread across the globe. The World health organization (WHO) declared the spread of COVID‐19 a global pandemic on March 11, 2020. This has significantly changed the way that dentistry is practiced around the world. The clinical workflow of dentists, especially prosthodontists, has been significantly altered due to the fact that the viral load is highest in the nasal cavity, nasopharynx and oropharynx related to the high expression of ACE2 receptor on goblet cells and respiratory epithelium used as fist entry into the body by SARS‐CoV‐2. Viral shedding can be detected from nasal swabs before, during and after the onset of acute symptomatic disease including in seropositive antibody‐converted convalescent cases. As the mouth is also part of the oropharynx, it harbors bacteria and viruses from the nose, throat and the respiratory tract and contaminated saliva can easily result in spread of viral infections.

In a dental setting, well recognized terms related to microbiological risk are aerosol and splatter. Aerosols are generally defined as suspension of fine solid particles or liquid droplets in air and splatters are larger liquid particles in air that impact a surface and then break apart. In dentistry, aerosols are recognized as airborne particles smaller than 50 µm in diameter which are small enough to stay in air for extended periods and entail risk of environmental contamination, and entry into respiratory tracts. 4‐7 On the other hand, splatters are denoted as airborne particles larger than 50 µm in diameter and too large to stay suspended in air for longer periods. Splatters are typically seen as droplets ejected forcefully in a ballistic manner similar to a bullet until they contact a surface. Any dental procedure that can aerosolize contaminated saliva can significantly increase airborne contamination with microorganisms. Most procedures in contemporary prosthodontics ranging from single unit restorations to complex implant surgery include aerosol production due to the use of handpieces and air‐water syringes. Additional dental maintenance procedures involving the use of ultrasonic scalers and air abrasion units produce even higher visible aerosols. All these procedures involve aerosol production resulting in higher risk for clinicians, dental assistants, and patients.

Due to the COVID‐19 pandemic which has resulted in significant morbidity and mortality, it is imperative for clinicians to consider adjunctive protective measures that can add an additional barrier of safety in providing prosthodontics treatment. Understandably, there is no single method or agent, which can completely eliminate or minimize the risk of COVID‐19 infection to dental personnel and other patients. Harrel and Molinari have described 3 layers of defense against aerosols in a dental office. The first layer is personal protective equipment (PPE) such as gloves, eye glasses and masks. The second layer is regular use of oral antiseptic rinse and the third layer is the use of high volume evacuator (HEV) ("high speed suction") and adjunctive high efficiency particulate air (HEPA) filters. The first and third layers of defense have received significant attention by dentists however, the second layer of defense has not received sufficient attention.

Harrel and Molinari recommended preprocedural oral rinsing with chlorhexidine gluconate a rinse with essential oils, but both of these are known to only be efficacious against bacteria, with no viricidal properties. Therefore, the American Dental Association (ADA) interim guidelines from April 2020 have suggested preprocedural oral rinsing with 1.5% hydrogen peroxide (commercially available in the United States) or 0.2% povidone‐iodine PVP‐I (not commercially available in the United States). The Centers for Disease Control and Prevention (CDC) have also recommended preprocedural rinsing with antimicrobial rinses such as chlorhexidine gluconate, essential oils, PVP‐I or cetylpyridinium chloride. Presently, there are no clinical studies supporting the viricidal effects of any pre‐procedural oral rinse against SARS‐CoV‐2. Additionally, there are no in vitro studies on the viricidal effect of the commercially available 1.5% hydrogen peroxide. However, PVP‐I solutions of 0.23% have effectively inactivated SARS‐CoV and MERS with contact times as low as 15 seconds in vitro. The SARS‐CoV‐2 virus resulting in the COVID‐19 pandemic is a novel coronavirus in the same family and is expected to be inactivated by PVP‐I in the same manner.

Therefore, the purpose of this study was to investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice. The null hypothesis was that there would be no difference in viricidal activity of PVP‐I at various concentrations and contact times as well as there would be no difference between PVP‐I and the positive and negative controls.

Materials and methods

All laboratory work with SARS‐CoV‐2 was conducted in biosafety level 3 (BSL‐3) laboratories at The Institute for Antiviral Research at Utah State University Logan, UT following established standard operating procedures approved by the Utah State University Biohazards Committee. The SARS‐CoV‐2, USA‐WA1/2020 strain, virus stock was prepared prior to testing by growing in Vero 76 cells. Culture media for prepared stock (test media) was minimum essential medium (MEM) with 2% fetal bovine serum (FBS) and 50 µg/mL gentamicin. The oral rinse antiseptic solution consisted of various concentrations of aqueous povidone‐iodine (PVP‐I) as the sole active ingredient (Veloce BioPharma; Fort Lauderdale, FL). The PVP‐I concentrations of each solution as supplied and after 1:1 dilution are listed in Table 1.

The test compounds were mixed directly with virus solution so that the final concentration was 50% of each individual test compound and 50% virus solution. A single concentration was tested in triplicate. Test media without virus was added to 2 tubes of the compounds to serve as toxicity and neutralization controls. Ethanol (70%) was tested in parallel as a positive control and water only as a virus control. The test solutions and virus were incubated at room temperature (22 ± 2 °C) for 15 and 30 seconds. The solution was then neutralized by a 1/10 dilution in MEM 2% FBS, 50 µg/mL gentamicin.

Surviving virus from each sample was quantified by standard end‐point dilution assay. The neutralized samples were pooled and serially diluted using eight log dilutions in test medium. Then 100 µL of each dilution was plated into quadruplicate wells of 96‐well plates containing 80% to 90% confluent Vero 76 cells. The toxicity controls were added to additional 4 wells of Vero 76 cells and 2 of those wells at each dilution were infected with virus to serve as neutralization controls, ensuring that residual sample in the titer assay plate did not inhibit growth and detection of surviving virus. Plates were incubated at 37 ± 2 °C with 5% CO ₂ for 5 days. Each well was then scored for presence or absence of infectious virus. The titers were measured using a standard endpoint dilution 50% cell culture infectious dose (CCID50) assay calculated using the Reed‐Muench equation and the log reduction value (LRV) of each compound compared to the negative (water) control was calculated.

Results

Virus titers and LRV of SARS‐CoV‐2 when incubated with various concentrations of the manufacturer's compounds for 15 seconds are shown in Table 1. After the 15‐second contact time, all of the PVP‐I oral rinse antiseptics tested were effective at reducing >3 log10 CCID50 infectious virus from, 3.67 log10 CCID50/0.1 mL to 0.67 log10 CCID50/0.1 mL or less. Table 2 shows the virus titers and LRV of SARS‐CoV‐2 when the virus was incubated for 30 seconds with each of the test compounds at 50/50 ratio. For the 30‐second contact time, once again all of the PVP‐I oral rinse antiseptics tested were effective at reducing >3.33 log10 CCID50 infectious virus from, 4.0 log10 CCID50/0.1 mL to 0.67 log10 CCID50/0.1 mL or less. No cytotoxicity was observed with any of the test compounds. The positive control and neutralization controls performed as expected.

Discussion

The purpose of this study was to investigate the optimal contact time and concentration for viricidal activity of oral preparation of povidone‐iodine (PVP‐I) against SARS‐CoV‐2 ('corona virus') to mitigate the risk and transmission of the virus in the dental practice. Data from this in vitro study rejected the null hypothesis, and showed the rapid viricidal activity of PVP‐I oral formulation. The minimum 15 seconds contact time proved to be sufficient for PVP‐I. This is similar to the results from previous studies where PVP‐I solutions of 0.23% inactivated SARS‐CoV and MERS with contact times as low as 15 seconds in vitro. Oral decontamination is an important adjuvant process along with PPE to reduce viral transmission among dental patients especially during aerosol generating procedures. A majority of prosthodontic procedures involve close physical contact with the patient and generate aerosols increasing the risk of viral transmission. In the absence of clinical studies, the residual challenge in oral antisepsis is to find the effective concentration and duration of topical preparations which are safe to administer. Several different protocols have been used anecdotally to dilute PVP‐I at a varying concentration ranging from 0.25% to 0.5% in an attempt to inactivate the virus from the nasal and oral cavity.

Oral use of PVP‐I antiseptic rinse is not novel to dentistry and has been used effectively in the past for oral decontamination, periodontal therapy, peri‐implant therapy and post‐extraction therapy. PVP‐I has proven safe for use in the oral cavity up to 5% concentration and nasal cavities at concentrations up to 1.25%. At these concentrations, no change in olfaction or mucociliary clearance has been noted. Thyroid stimulating hormone was shown to slightly increase within normal levels after oral use of 5% PVP‐I for 6 months, but no clinical thyroid disease was detected. Nevertheless, at concentrations of 0.2% to 0.5% iodine absorption is minimal and below the total daily iodine intake for a healthy adult of 150 µg. Additionally, no change in taste or discoloration of teeth has been reported in the literature. The substantivity (prolonged association between a topical material and a substrate) of oral PVP‐I antiseptic rinse has been reported to be as long as 4 hours. However PVP‐I solutions are contraindicated for patients with anaphylactic allergy to iodine, pregnancy, active thyroid disease, and patients undergoing radioactive iodine therapy.

The alternative to oral PVP‐I solution is 1.5% hydrogen peroxide rinse, as recommended by the ADA interim guidelines. Presently the CDC does not recommend this rinse due to absence of sufficient scientific evidence. Though 1.5% hydrogen peroxide is known to be antibacterial, it is chemically more unstable. There are no published studies showing the inactivation of SARS‐CoV‐2 by this solution at 1 minute contact period. The potential oral toxicity of routine use of this solution for 1 minute as well as its substantivity is unknown at this time. Additionally, alcohol is present in most oral rinses and results from this study showed that it required a longer time for viral inactivation than PVP‐I oral solutions tested.

Some disadvantages of the PVP‐I oral solutions include the absence of clinical research such as randomized clinical trials, and the current absence of commercially available formulation at lower concentrations for intra‐oral use. Therefore, dentists are required to dilute the commercially available antiseptic formulation of 10% PVP‐I, by 1:20, utilizing 0.5 ccs of 10% povidone iodine and 9.5 ccs of sterile water for routine clinical use at 0.5%. This compound typically contains suds which do not cause any adverse effects for topical usage. However, dentists should make freshly diluted solutions each day and refrigerate them during the day as diluted PVP‐I solutions are chemically unstable with respect to disproportionation into constituent equilibrium species. As the aqueous concentration of PVP‐I decreases from 10% to less than 1%, these solutions become unstable with respect to temperature, counterions, commercial packaging and pH value. In order to ensure that a diluted solution is safe for administration to the oral or nasal cavity, there should either be an analysis of the chemical ingredients of each freshly‐prepared solution or commercial preparations of PVP‐I at the appropriate dose (if available) should be used.

Conclusions

PVP‐I oral antiseptic preparations rapidly inactivated SARS‐CoV‐2 virus in vitro. The 70% ethanol control group was unable to completely inactivate SARS‐CoV‐2 after 15 seconds of contact, but was able to inactivate the virus at 30 seconds of contact. The viricidal activity of PVP‐I oral antiseptic solution was present at the lowest concentration of 0.5 %, and at the lowest contact time of 15 seconds. This important finding warrants the use of preprocedural oral rinsing with 0.5% PVP‐I for patients and health care providers. This solution serves as an adjunct to personal protective equipment for dental and surgical specialties during the COVID‐19 pandemic.

Funding

Sponsorship for this study was funded by Veloce Biopharma, Florida, USA. All authors had full access to all of the data in this study and take complete responsibility for the integrity of the data and accuracy of the data analysis.

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# data[].attributes.attachment_link.title
Rapid In‐Vitro Inactivation of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS‐CoV‐2) Using Povidone‐Iodine Oral Antiseptic Rinse

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Avinash S. Bidra BDS, MS, FACP Corresponding Author E-mail address: avinashbidra@yahoo.com https://orcid.org/0000-0001-8831-8096 Department of Reconstructive Sciences, University of Connecticut Health Center, Farmington, CT Correspondence Avinash Bidra, Department. of Reconstructive Sciences, University of Connecticut Health Center, 263 Farmington Ave., L7039, Farmington, CT 06030.

# data[].attributes.headline
Efficacy of mouthwashes pre-procedural in the reduction of microorganisms in the aerosol: a systematic review

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Efficacy of mouthwashes pre-procedural in the reduction of microorganisms in the aerosol: a systematic review

# data[].attributes.body
Testaram a influencia de enxaguantes bucais pré-procedimentos odontologicos no aerosol expelido naturalmente durante
fator de impacto: 2.8

Pra ver se isso afetava a quantidade de microorganismos expelidos durante o procedimento, esse estudo foi de revisão sistematica para estudar a redução do numero de unidades formadoras de colonias (UFc) no aerossol dentario
Essas UFC parecem ter seu numero significativamente reduzido com uso de alguns enxanguantes pré-procedimentos.
É um estudo bem inicial, mas interessante.

# data[].attributes.attachment_link.title
Eficácia de enxaguatórios bucais pré-procedimento na redução de microrganismos no aerossol: uma revisão sistemática | São Paulo; s.n; 20180000. 70 p. | LILACS | BBO

# data[].attributes.attachment_link.description
Eficácia de enxaguatórios bucais pré-procedimento na redução de microrganismos no aerossol: uma revisão sistemática / Efficacy of mouthwashes pre-procedural in the reduction of microorganisms in the aerosol: a systematic review

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Is the oral cavity relevant in SARS-CoV-2 pandemic?

# data[].attributes.subject
Is the oral cavity relevant in SARS-CoV-2 pandemic?

# data[].attributes.body
Pesquisa na literatura (pubmed incluindo SARS-CoV-2, COVID-19, oral cavity, and antimicrobial agents) fator: 2.8

Basicamente argumentam que a carga viral presente na boca do individuo pode agravar seu quadro, e também faz com que sua infecção seja menos ou mais transmissível uma vez que a principal rota carreadora do vírus é a saliva.
Também citam que na busca que fizeram há evidencias de um maior risco de severidade de covid-19 em pacientes periodontais.
Levantam a hipótese de que enxaguantes bucais anti-sépticos podem ser capazes de diminuir a transmissão e patogenecidade de COVID-19.

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Abstract

Keywords: SARS-CoV-2, COVID-19, Antiseptic, Oral health, Transmission

COVID-2019 and oral cavity

Coronavirus 2 of severe acute respiratory syndrome (SARS-CoV-2), previously known 2019 novel corona virus (2019-nCoV), a member of the Coronaviridae family is the responsible agent of the disease referred as 2019 coronavirus disease (COVID-2019). This disease was first identified in Wuhan (China), and from there, it has spread to more than 185 countries, acquiring pandemic characteristics, with more than 2.8 million of confirmed cases and almost 0.2 million of dead, on April 25, 2020 [ 1].

Most patients with COVID-19 present a mild disease, with fever, myalgia or fatigue, and dry cough as main symptoms [ 2]. However, almost 14% present signs and symptoms of a severe disease, requiring hospitalization and oxygen support, and 5% need to be admitted to intensive care units [ 3]. These severe cases usually include impairment of the function of different organs such as acute kidney injury, cardiac injury, and liver dysfunction and grave complications as severe acute respiratory syndrome (SARS), sepsis, and septic shock [ 4]. The risk factors associated with this severe systemic impact of COVID-19 in a small proportion of patients infected with SARS-CoV-2 have not been properly identified, although it has been suggested that the presence of other comorbidities, such hypertension, diabetes, coronary disease, aging, and obesity may play a significant role [ 5].

The role of the oral cavity, as the entrance to the body of SARS-CoV-2, and its possible role as protective/aggravating factor in the infectivity and in the progression of this viral infection have been controversial, although recent scientific evidences suggest a relevant role of the oral cavity and its mucosae in the transmission and pathogenicity of SARS-CoV-2. In addition, the demonstrated chronic systemic inflammation associated with periodontitis may presuppose a higher risk of increased severity of COVID-19 in periodontitis patients. This predicate is supported by the available scientific evidence supporting the relevance of oral health, and specifically, of periodontal health, on systemic health [ 6, 7] and, again, emphasizing the importance of oral health in the overall systemic health [ 8, 9].

It was, therefore, the objective of the present short communication to evaluate the importance of the oral cavity and the possible impact of using oral antiseptics to reduce the transmission and pathogenicity of SARS-CoV-2.

Methods

A literature search was performed in PubMed, up to April 30, 2020, focusing on SARS-CoV-2, COVID-19, oral cavity, and antimicrobial agents.

Is the oral cavity relevant in the transmission and pathogenicity of SARS-CoV-2?

The infectivity of SARS-CoV-2 depends on the ability of this virus to enter the cells, and there is clear evidence that the transmembrane protein angiotensin-converting enzyme (ACE2) is the primary receptor and portal of entrance of this virus into the cell. Besides the lungs, intestines, heart, and kidneys, which have shown expression of ACE2, recent evidence has also demonstrated that epithelial cells in different oral cavity mucosae, especially in the tongue mucosa, show a high expression of ACE2. Since the oral cavity is one of the first interfaces between the exterior and body, there is a high potentiality that this pathway of viral colonization and infection is critical for the onset of COVID-19 [ 10, 11].

Apparently, in the first 10 days after the transmission, when the patient usually remains asymptomatic but is highly contagious, the virus accumulates at the nasal, oral, and pharyngeal mucosa, and only later will further accumulate in the lungs [ 12]. It has also been shown that the number of ACE2 receptors in the salivary glands is higher than in the lungs that has been suggested could be a reservoir area for SARS-CoV-2 in asymptomatic patients [ 11].

Two major routes of transmission have been described, on through Flügge droplets (> 5 μm in size), expelled when breathing, talking, sneezing, coughing, etc., which normally will not remain in the air but immediately settle down on different surfaces or on the floor and, from there, indirectly, the virus may be transmitted through contract by the hand or contaminated objects if they contact the subject mucosae. In the other route, viruses will be transmitted directly person to person, via Wells droplet nuclei (≤ 5 μm), expelled by breathing, talking, sneezing, coughing, etc., since they remain suspended in air for significant periods of time, allowing them to be transmitted over distances > 1 m [ 11, 13].

This possible role of the oral cavity both as portal of entrance of the virus in the body and as virus reservoir may be impacted at two levels:

By decreasing the viral load SARS-CoV-2 that has been associated with a reduced severity of COVID-19 [ 14].

By decreasing the viral load, the amount of virus expelled by the carrier could be temporarily reduced and, therefore, the risk of transmission will be lesser. This is supported by different reasons: (i) during the first 10 days, the virus mainly accumulates at the nasal, oral, and pharyngeal area [ 12]; (ii) the number of ACE2 receptor is greater in the salivary glands as compared with the lungs [ 11]; and (iii) salivary droplets represent the most relevant transmission route [ 11, 13].

This proposed beneficial impact could become even more relevant under the light of the foreseen evolution of the pandemic, which suggest that in spite of the implementation of hygienic measures and social distance, SARS-CoV-2 may not be eradicated up to 2024 [ 15]. This positive impact may specifically be even more relevant in the context of the clinical practice of dentistry [ 16], since due to the frequent generation of aerosols, the associated risk of virus transmission may be enhanced during the different dental procedures [ 11, 17].

Could oral antiseptics have an impact on the transmission and pathogenicity of SARS-CoV-2?

Some oral antiseptics, used as a pre-procedure rinsing, have shown efficacy to reduce the amount of bacteria in aerosols, hence significantly reducing the risk of cross-infection. This outcome has been demonstrated when rinsing with chlorhexidine before dental procedures [ 18- 20]. Similar outcomes, albeit in lesser extent, have also been demonstrated with the use of essential oil mouth rinses [ 21]. A recent systematic review, with meta-analysis that evaluated the efficacy of preoperative mouth rinses in the reduction of the number of microorganisms produced by aerosols during dental procedures, concluded that mouth rinses containing chlorhexidine and cetylpyridinium chloride, among others, were efficacious to reduce the bacterial load in the aerosols [ 22]. There is, however, no direct evidence of the possible impact of preoperative rinsing with oral antiseptics on the SARS-CoV-2 viral load. Furthermore, the likely impact of a daily use of these antiseptics for limited periods of time (e.g., when being a carrier of the virus) on the viral transmissivity has not been explored. However, the possible beneficial effect of using oral antiseptics during this viral infection may be assessed indirectly by evaluating the in vitro antiviral activity of most common active agents.

Povidone-iodine

Pre-procedural rinsing with povidone-iodine has been frequently recommended in protocols specifically applied for dental settings in the control of SARS-CoV-2 [ 16]. However, it has very limited substantivity in oral use [ 23], and its use may present some risks, including allergic reactions or thyroid dysfunction in long-term use [ 24]. The recommendation of mouth rinse/gargling with povidone-iodine in the COVID-19 context is based on its virucidal activity, shown against both enveloped and non-enveloped viruses including ebola, Middle East respiratory syndrome (MERS) and SARS coronavirus, influenza, and hand, foot, and mouth disease (HFMD) viruses (Enterovirus 71 and Coxsackievirus A16) [ 24]. These recommendations have been partially based on a series of German studies from one research group showing that:

There is virucidal activity of 1% povidone-iodine (formulation for rinsing) against MERS-CoV, within 15 s of exposure, shown in an in vitro study [ 25].

Better virucidal activity (against murine norovirus) was shown when using 7.5% povidone-iodine when compared with 4% chlorhexidine gluconate [ 26].

Povidone-iodine (7.5%), formulated as gargle/mouthwash but diluted 1:30 to a final concentration of 0.23% for in vitro rapidly inactivated (15 s of exposure) SARS-CoV, MERS-CoV, influenza virus A (H1N1), and rotavirus [ 27].

In another narrative review on the virucidal activity of povidone-iodine [ 28], different Japanese in vitro studies were evaluated:

Inactivation of adenovirus, mumps, rotavirus, poliovirus (types 1 and 3), Coxsackievirus, rhinovirus, herpes simplex virus, rubella, measles, influenza, and human immunodeficiency virus (HIV) [ 29]

Efficacy against a SARS coronavirus strain, with rapid inactivation of the virus after 2 min of treatment [ 30, 31]

Virucidal activity against avian influenza viruses [ 32]

Virucidal efficacy, including when use as gargle, against swine influenza viruses [ 33]

Cetylpyridinium chloride

N-hexadecyl pyridinium chloride or cetylpyridinium chloride (CPC) is a cationic quaternary ammonium compound soluble in water and in aqueous solutions, non-oxidant or corrosive, and highly cationic at neutral pH. These compounds belonging to the group of tensioactive agents have been frequently used as detergents and antiseptics. As antiseptic, its antibacterial, antiplaque, and antigingivitis properties have been demonstrated in different randomized clinical trials [ 34], and its efficacy has been summarized in several systematic reviews [ 35- 37].

In vitro studies have shown that it is able to eliminate/inactivate different strains of influenza virus (AH3N2, A H1N1, B, oseltamivir-resistant A). The antiviral mechanism of action of CPC resides in its ability to disrupt the lipid envelope, hence interfering with the capacity of the virus to enter the cell. Due to this mechanism of action, it has been suggested that CPC may also act against other viruses with envelope, such as respiratory syncytial virus (RSV), parainfluenza virus, and coronavirus [ 38]. In a preclinical in vivo investigation using mice adapted to an influenza strain (A H1N1), a statistically significant lower mortality and morbidity were shown in the group of mice using the CPC formulation.

In humans, in a pilot double-blinded, placebo-controlled, randomized clinical trial, assessing a CPC-based formulation for inhalation, in the prevention of upper respiratory tract infections (usually associated with influenza virus, RSV, human metapneumovirus (hMPV), rhinovirus, and adenovirus), it was observed that patients in the test group suffered viral infections with less severity and duration, when compared with those included in the placebo group [ 39].

Most recently, in a high-throughput screening aiming to identify broad-spectrum inhibitors of coronaviruses, CPC was rated as the 9th most relevant, out of 36, against the four viruses tested, which included MERS-CoV [ 40].

CPC products are widely available in the market, formulated as only active agent in different concentrations, but also in combination with other active agents, being of special relevance the formulation together with 0.12% chlorhexidine, which has shown an important microbiological impact as single rinse [ 41] or with a 2-week use [ 42], and also at different concentrations [ 43], such as 0.05% evaluated for 6 months [ 44] or as 0.03% evaluated for 1 year [ 45].

Chlorhexidine

Chlorhexidine is a biguanidic antiseptic and disinfectant, with a widely demonstrated antimicrobial activity against bacteria (gram-positive and gram-negative, anaerobic and aerobic), some viruses, and yeast. As antiseptic, its antibacterial, antiplaque, and antigingivitis properties have clearly established, as summarized in systematic reviews [ 35- 37]. In regard to its antiviral activity, although the use of chlorhexidine has been suggested to reduce the viral transmission via aerosols in recent narrative reviews [ 46, 47], its efficacy is controversial. In a systematic review, it was reported that chlorhexidine rapidly inactivates lipophilic viruses (e.g., herpes simplex virus, HIV, influenza virus, cytomegalovirus) but not small non-enveloped viruses (enteroviruses, polio viruses, papilloma viruses) or enveloped human coronavirus [ 48].

Other products

Very limited evidence is available for other products that are frequently recommended in cross-contamination preventive protocols in viral infections:

Hydrogen peroxide [ 16] is frequently recommended as part of measures of control of COVID-19, despite the limited available evidence, very limited substantivity [ 49], or limited impact on dental biofilms [ 50].

Essential oil mouth rinses, since there are suggestions of their possible benefits in controlling viral contamination, at least for herpes viruses [ 51]. However, its use has seldomly been suggested in the COVID-19 context.

Beta-cyclodextrin and citrox [ 52] have also been suggested as possible candidates for evaluation.

Comparisons of different agents in non-oral scenarios

Some information can also be extracted from a narrative review, including 22 articles, that evaluated the relative efficacy of different disinfectant products in other settings, such as disinfection of inanimate surfaces (metal, glass, or plastic), in which different human coronaviruses, including SARS-CoV and MERS-CoV, or endemic human coronaviruses (HCoV) can persist for up to 9 days. Effective inactivation of the viruses was observed with 62-71% ethanol, 0.5% hydrogen peroxide, or 0.1% sodium hypochlorite within 1 min. Other biocidal agents, such as 0.05-0.2% benzalkonium chloride or 0.02% chlorhexidine digluconate, were considered as less effective [ 53].

More recently, and specifically in relation with SARS-CoV-2, the in vitro virucidal effect was considered similar with ethanol (70%), povidone-iodine (7.5%), chloroxylenol (0.05%), chlorhexidine (0.05%), or benzalkonium chloride (0.1%), when used as disinfectants [ 54].

Summary

The recommendations of different health authorities in different countries of the world are indicating the need to perform pre-procedure rinsing with antiseptic agents in dental clinical settings, both during and after the pandemic period. The most frequently recommended agents are povidone-iodine, hydrogen peroxide, and cetylpyridinium chloride, although the scientific support behind these recommendations is still weak and mostly derived from indirect evidence.

The information presented in this narrative review supports the use of antiseptic mouth rinses, both as a single pre-procedural use and as daily use during a limited period of time, to impact the transmission and/or pathogenicity of SARS-CoV-2, since they have shown to reduce the oral viral load and, therefore, they may reduce the severity of the disease in an infected subject and may reduce the risk of transmission, by reducing the viral load in aerosols, expelled during dental procedures, or in droplets generated when breathing, talking, sneezing, coughing, etc. However, these recommendations must be validated with well-designed clinical trials that evaluate their efficacy.

Authors' contributions

All authors participated in the search, selection of relevant articles, analysis of the evidences provided, and preparation of the manuscript.

Funding information

The present work was prepared as part of the activities of the Extraordinary Chair Dentaid in Periodontal Research ( Cátedra Extraordinaria Dentaid en Investigación Periodontal), University Complutense of Madrid, Spain.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study, formal consent is not required.

Footnotes
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References

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Is the oral cavity relevant in SARS-CoV-2 pandemic?

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Keywords: SARS-CoV-2, COVID-19, Antiseptic, Oral health, Transmission Coronavirus 2 of severe acute respiratory syndrome (SARS-CoV-2), previously known 2019 novel corona virus (2019-nCoV), a member of the Coronaviridae family is the responsible agent of the disease referred as 2019 coronavirus disease (COVID-2019).

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Predicting the response of the dental pulp to SARS-CoV2 infection: a transcriptome-wide effect cross-analysis

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Predicting the response of the dental pulp to SARS-CoV2 infection: a transcriptome-wide effect cross-analysis

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Neste relato os pesquisadores analisaram dados de estudos publicados anteriormente. Através dos seus cálculos foi possível mensurar a expressão de enzima conversora de angiotensina 2 (ACE2) e sua protease serina celular associada TPMRSS2 na polpa dentária tanto em condições normais como inflamadas. E associaram esses conhecimentos aos dados recentes sobre genes interativos ou não com o SARS-CoV-2.

Analisando dados já sequenciados do interatoma humano e genes expressados na pulpite, foram identificados 75 genes com regulação negativa ou positiva. Notou-se que ACE2 e TMPRSS2 são expressos em tecidos bucais normais e inflamados. Há uma subexpressão de ACE2 durante a infecção de SARS-CoV2 e segundo os pesquisadores esse fator poderia influenciar negativamente na gravidade da pulpite.

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Introduction

SARS-CoV2 is a highly aggressive coronavirus, which has infected over 6 million people to date [ 1]. Most infections (81%) produce only mild symptoms or are asymptomatic. Fifteen percent of infections are severe and require hospitalization. Transmission of this disease is produced by asymptomatic carriers, symptomatic patients, as well patients who are in the incubation period. Human-to-human transmission occurs via close contact of respiratory droplets, direct contact with infected individuals, or by contact with contaminated objects and surfaces.

Viral entry into the target cells requires angiotensin converting enzyme 2 (ACE2) and its associated cellular serine protease TPMRSS2 [ 2]. ACE2, a negative regulator of the renin-angiotensin system, functions as the key SARS coronavirus receptor and stabilizer of neutral amino acid transporters [ 3]. Viruses found to use this protein for cell entry include Influenza virus and the human coronaviruses HCoV-229E, MERS-CoV, SARS-CoV, and SARS-CoV-2. It is postulated that the pattern of expression of ACE2 in human respiratory epithelia and oral mucosa explains the rapid human-human transmission [ 4]. TMPRSS2, a serine protease, facilitates entry of viruses into host cells by proteolytically cleaving and activating viral envelope glycoproteins. While a number of studies have examined the expression of ACE2 and TPMRSS2 in various tissues, their expression in the dental pulp is yet to be examined.

Pulpitis, inflammation of the dental pulp, is a disease that often necessitates emergency dental care. Over 90% of dental emergency visits are due to pulpitis pain [ 5]. In the United States alone, over 22 million procedures are performed annually to treat diseased dental pulps [ 6]. While pulpitis is considered to be a microbial disease primarily caused by bacteria [ 7], viruses have also been implicated in its pathogenesis [ 8]. The complex interaction between the 31 SARS-CoV2 and human proteins has been recently reported [ 9], but the correlation between this interactome and pulpitis is yet to be explored.

Here, we first used existing gene expression data (53,000 genes) from our previously published study on pulpitis (GEO NCBI accession number GSE77459; ID: 20007745) [ 10]. Then, with the data and methods used in a recently published study on the transcriptome-wide effects on coronavirus infection in human cells [ 11], a master regulator analysis (MRA) [ 12] was performed to identify genes whose expression values are correlated (upregulated or downregulated) in both the human interactome [ 11] and pulpitis datasets [ 10]. With these techniques, we endeavored to answer two important questions: how would the dental pulp respond to SARS-CoV2 infection, and how would ACE2 and TPMRSS2 expression change during SARS-CoV2 infection?

Results and discussion

We identified 75 relevant genes whose expression values are either upregulated or downregulated in both human interactome and pulpitis datasets (Table 1). Of particular interest amongst these genes are ACE2 and TMPRSS2, which were shown to be exploited by SARS-CoV-2 for cell entry and for spike (S) protein priming, respectively [ 9].

Table 1 Master regulator analysis (MRA) between the gene microarray datasets of inflamed human dental pulp tissue cells and SARS-Cov2 transcriptome in human lung tissue cells.

In the human dental pulp, both ACE2 and TMPRSS2 are expressed consistently in biopsies of normal and inflamed tissues (Fig. 1a, b). The expression levels of both ACE2 and TMPRSS2 remain unchanged under conditions of inflammation. These findings are similar to expression patterns in other tissues. For example, both of these viral entry molecules are expressed in the ileum and colon and, expression levels in mucosal biopsies of these tissues do not differ between patients with active Irritable Bowel Disease and those of control patients [ 13]. Similarly, the expression level of ACE2 in lung tissues does not differ between biopsies taken from patients with chronic respiratory diseases such as chronic obstructive pulmonary diseases and asthma compared to those from healthy volunteers [ 14].

Differences in RMA log2 signal intensity between samples were analyzed using Student's t test. No statistical difference was found in the expression of both genes in normal and inflamed dental pulps.

It is important to note that the consistent expression of both ACE2 and TMPRSS2 in the dental pulp confers its vulnerability to SARS-Cov2 infection. The oral cavity stands at the entry of the respiratory system where its fluids like saliva have been reported to harbor and transmit SARS-CoV2 [ 15]. This vulnerability may also increase the risk of infection in dental personnel. While several studies have documented the risk of COVID-19 in health care workers, they have been mostly limited to those in medicine and surgery. To our knowledge the risk of acquiring SARS-CoV2 or developing COVID-19 in dental personnel is yet to be documented.

The MRA correlation analysis between the pulpitis microarray dataset and the human SARS-Cov2 transcriptome-wide effects shows that both ACE2 and TMPRSS2 values are underexpressed (Table 1). SARS-CoV infection in other tissues have shown marked decrease in ACE2 expression [ 16]. Furthermore, underexpression of ACE2 was associated with worse outcomes of SARS-CoV2 infection in patients with inflammatory bowel disease [ 17].

One of the advantages of studies like the present one is that by using omic tools, one can answer several biological questions, without the need of collecting more samples. Our original studies on gene expression in inflamed human pulps was conducted several years ago. We then took advantage of having the sequenced data to explore expression of ACE2 and TPMRSS2 in inflamed and normal human pulps. This was an efficient and quick way to answer a time-sensitive question [ 10].

Taken together, our results suggest that the dental pulp is vulnerable to SARS-CoV2 infection. The predicted underexpression of ACE2 during SARS-CoV infection in the dental pulp may contribute to worse outcomes of pulpitis.

Materials and methods

Our analysis started by assessing a published study that utilized a dataset describing the transcriptome-wide effects of coronavirus infection in human cells [ 11]. The study employed a system [ 18] that probed the transcriptome-wide effects of SARS-CoV2 and its implication on human interactome by applying a MRA, which was performed by comparing infected and mock samples in both MERS and SARS datasets separately with the corto algorithm [ 18]. With these tools, an MRA correlation analysis of the gene microarray dataset of pulpitis [ 10] can be performed using a known platform in managing microarray binary data [ 19].

We first calculated a gene-by-gene signature of differential expression of genes caused by viral infections. In brief, a gene-by-gene signature of viral-induced differential expression is generated, and combined value for each coexpression network is generated by weighting every gene's likelihood in the network, providing a final Normalized Enrichment Score for each genes of the human/Sars-Cov2 integrated interactome. The value is positive when the network is unregulated by the infections, and vice-versa. In this study, we hypothesized that the effects of the viral infection are the same for the dental tissue, therefore we merged the data published in human airway cells [ 11] with that in dental pulp tissue cells [ 10]. Consequently, we were able to predict a possible regulator effect for the same genes. This study may therefore suggest some possible effects that should be tested in the future by extracting dental tissue samples from Covid-19 infected patients.

Gene expression analysis of ACE2 and TMPRSS2 in normal and inflamed dental pulps were from our previous study's existing public gene expression database on pulpitis (GEO NCBI accession number GSE77459). Differences in RMA log2 signal intensity between samples were analyzed using Student's t test. Statistical significance was set at 0.05.

Acknowledgements

We are grateful to Dr. Xiaoyuan Han for her assistance with statistical analysis

Author information

Affiliations

1. Department of Endodontics, Arthur A. Dugoni School of Dentistry, University of the Pacific, San Francisco, CA, 94103, USA

Johnah C. Galicia

2. Department of Surgical and Medical Sciences, Magna Graecia University, Campus S. Venuta, Catanzaro, 88100, Italy

Pietro H. Guzzi

3. Department of Pharmacy and Biotechnology, University of Bologna, Bologna, 40126, Italy

Federico M. Giorgi

4. Department of Endodontics, School of Dentistry, University of Texas Health and Sciences Center, San Antonio, TX, 78229, USA

Asma A. Khan

Corresponding author

Correspondence to Asma A. Khan.

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The authors declare that they have no conflict of interest.

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Galicia, J.C., Guzzi, P.H., Giorgi, F.M. et al. Predicting the response of the dental pulp to SARS-CoV2 infection: a transcriptome-wide effect cross-analysis. Genes Immun (2020). https://doi.org/10.1038/s41435-020-00112-6
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# data[].attributes.attachment_link.title
Predicting the response of the dental pulp to SARS-CoV2 infection: a transcriptome-wide effect cross-analysis

# data[].attributes.attachment_link.description
Pulpitis, inflammation of the dental pulp, is a disease that often necessitates emergency dental care. While pulpitis is considered to be a microbial disease primarily caused by bacteria, viruses have also been implicated in its pathogenesis.

# data[].attributes.headline
Could there be a link between oral hygiene and the severity of SARS-CoV-2 infections?

# data[].attributes.subject
Could there be a link between oral hygiene and the severity of SARS-CoV-2 infections?

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Fator de impacto baixo (1.3) mas apareceu na nature e gostei.

Considerações gerais:
A hipótese dos pesquisadores aqui é que superinfecção por bacterias pode agravar a severidade dos sintomas de coronavírus. Filamentos do vírus mostraram capacidade de aumentar a aderência estreptocócica às células epiteliais ao longo do trato respiratório, causando complicações como pneumonia e danos inflamatórios nos pulmões que inibem a eliminação de bactérias.

O estudo referência 21 cita uma comparação entre pacientes com sitomas graves e pacientes com infecção leve. Pacientes com sintomas severos - poucos leucócitos e muitos neutrofilos comparados ao pacientes leves, alta taxa de neutrofilo = comum em infecções bacterianas
O uso de antibioticos em pacientes parece aumentar a chance de cura.

Pela data de escrita eles referenciam positivamente o estudo feito com cloroquina e azitromicina, que é um ponto a desconsiderar, mas interessante ver o impacto que aquele artigo teve em outros estudos.

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Author information

Affiliations

1. Dentistry, 38 Devonshire Street, London, W1G 6QB, UK

Victoria Sampson

2. Centre for Nutrition Education & Lifestyle Management, London, RG40 1DH, UK

Nawar Kamona

3. Orthodontics, Cambridge University Hospital Trust, Cambridge, CB1 00Q, UK

Ariane Sampson

Corresponding author

Correspondence to Victoria Sampson.

Ethics declarations

The authors declare no conflicts of interest related to the study.

About this article

Cite this article

Sampson, V., Kamona, N. & Sampson, A. Could there be a link between oral hygiene and the severity of SARS-CoV-2 infections?. Br Dent J 228, 971-975 (2020). https://doi.org/10.1038/s41415-020-1747-8
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Could there be a link between oral hygiene and the severity of SARS-CoV-2 infections?

# data[].attributes.attachment_link.description
On 30 January 2020, the World Health Organisation identified COVID-19, caused by the virus SARS-CoV-2, to be a global emergency. The risk factors already identified for developing complications from a COVID-19 infection are age, gender and comorbidities such as diabetes, hypertension, obesity and cardiovascular disease.

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Oral saliva and COVID-19

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Highlights

*

ACE-2 is a critical COVID-19 receptor can be found in salivary gland epithelial cells.

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COVID-19 can be transmitted through saliva droplets.

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SARS-CoV-2 might induce acute and chronic sialadenitis.

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Salivary diagnostics testing can be a convenient tool for early-diagnosis of Covid-19.

Abstract

Outbreak pneumonia announced in Wuhan, China, in December 2019, had its causative factor classified as a new coronavirus (SARS-CoV-2). Since saliva can host several viruses including SARS-CoV-2, the transmission chance of viruses through saliva, particularly those causing respiratory infections, is unavoidable. COVID-19 can be detected through salivary diagnostic testing which has lots of advantages for medical care professionals and patients. It should be noted that not only does saliva offer an ecological niche for the colonization and development of oral microorganisms, but it also prevents the overgrowth of particular pathogens such as viral factors. The aim of this study is to gather all the information about saliva and its association with COVID-19 for the whole health care professionals across the world.

View Abstract

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ACE-2 is a critical COVID-19 receptor can be found in salivary gland epithelial cells. * COVID-19 can be transmitted through saliva droplets. * SARS-CoV-2 might induce acute and chronic sialadenitis. * Salivary diagnostics testing can be a convenient tool for early-diagnosis of Covid-19.