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"Farmers are leaving to follow the money." 

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"Farmers are leaving to follow the money." 

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This quote was in reference to the decline of the dairy industry. Many farmers are leaving the traditional industry to enter the raw milk industry. The raw versus pasteurized milk issue is highly controversial because raw milk is illegal and has been deems unsafe. The Infectious Diseases Society of America states that raw milk is a threat to public health. The issue had been almost eradicated but now with health food trends raw milk has found a market again (Angulo, 2009).

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Abstract

Although milk and dairy products are important components of a healthy diet, if consumed unpasteurized, they also can present a health hazard due to possible contamination with pathogenic bacteria. These bacteria can originate even from clinically healthy animals from which milk is derived or from environmental contamination occurring during collection and storage of milk. The decreased frequency of bovine carriage of certain zoonotic pathogens and improved milking hygiene have contributed considerably to decreased contamination of milk but have not, and cannot, fully eliminate the risk of milkborne disease. Pasteurization is the most effective method of enhancing the microbiological safety of milk. The consumption of milk that is not pasteurized increases the risk of contracting disease from a foodstuff that is otherwise very nutritious and healthy. Despite concerns to the contrary, pasteurization does not change the nutritional value of milk. Understanding the science behind this controversial and highly debated topic will provide public health care workers the information needed to discern fact from fiction and will provide a tool to enhance communication with clients in an effort to reduce the incidence of infections associated with the consumption of unpasteurized milk and dairy products.

Food available in the United States is plentiful, inexpensive, and, for the most part, safe. Advances in animal production, food processing and hygiene, and refrigeration have eliminated several foodborne diseases that plagued Americans in the past century. However, in the past 30 years, several previously unrecognized foodborne bacterial infections, including infection with Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli strain O157, have emerged as significant causes of human morbidity and mortality. Other infectious diseases once believed to be controlled have started to reappear. It is estimated that, each year, 76 million Americans become ill from eating contaminated food [ 1].

Milk and other dairy products, primarily from cows but also less frequently from goats and sheep, are important components of the American diet. The US Department of Agriculture recommends that people consume 2-3 servings of dairy products daily. Inclusion of these products in the diet aides in the prevention of certain diseases, such as obesity, hypertension, and diabetes, and they are a source of calcium-important for growing bones and the prevention of osteoporosis [ 2]. In addition, dairy products also provide dietary sources of protein, vitamins, and other minerals [ 3]. Notwithstanding the benefits, there are some individuals who believe that milk is inappropriate for inclusion in the human diet [ 4]. Moreover, it has long been recognized that milk is a vehicle for the transmission of numerous bacteria of both human and animal origin. Milk can be contaminated at any stage in the production-to-consumption continuum.

The Origin of Milk Contamination

Commensal microflora. Typically, unless there is an intramammary infection or an animal has a systemic disease, milk in the mammary gland at the site of its production does not contain bacteria. However, as milk is excreted, it can become contaminated with bacteria that live as commensal microflora on the teat skin or on the epithelial lining of the teat canal, the duct that conveys the milk from the mammary gland to the teat orifice. In cattle, bacteria of the genera Staphylococcus, Streptococcus, Bacillus, Micrococcus, and Corynebacterium and, occasionally, coliforms colonize this location [ 5]. Thus, even in a healthy animal, by the time the milk leaves the animal, it may contain numerous bacterial contaminants.

The single disease that has the most significant impact on milk quality is mastitis, the inflammation of the mammary gland. On the basis of bovine milk samples submitted to diagnostic laboratories during a period of several years in New York and Pennsylvania (1991-1995) and Wisconsin (1994-2001), the prevalence of intramammary infections was ∼50% [ 6, 7]. Staphylococcus and Streptococcus species were the most commonly isolated bacteria from bovine milk in these studies; ∼20% of the samples contained organisms of either group. The milk produced by animals with subclinical mastitis is not noticeably different from the milk produced by uninfected animals and frequently is added to the collection or storage tank on a farm. Milk from cows with clinical mastitis, however, typically has a changed appearance (i.e., it may contain flakes, clots, or blood or may have changed color) and is withheld from human consumption.

Other diseases and environmental contamination. Systemic disease can also result in localization of pathogens in the mammary gland or associated lymph nodes and consequent excretion of pathogens in milk. Bovine tuberculosis and brucellosis are classic examples of zoonotic milkborne diseases. The contribution of cattle to the epidemiology of these 2 diseases in humans was so important that enormous efforts were made to eradicate these infections among cattle in the United States. The programs have largely been successful, and Mycobacterium bovis and Brucella abortus are seldom found in domestic US cattle [ 8].

In contrast to M. bovis and B. abortus, several other organisms are commonly found today in the milk of asymptomatic US cattle and goats or contaminate milk from environmental sources. These include Coxiella burnetii; Listeria species; Mycobacterium avium subspecies paratuberculosis; Campylobacter species; coliforms, including E. coli; and Salmonella enterica [ 9-14]. Cattle can be a major reservoir of these organisms and still remain clinically healthy and maintain near-optimal milk production. For example, C. burnetii, the causal agent of Q fever, is not an important cause of clinical disease in cattle; however, its prevalence in pooled milk collected on farms in the United States was reported to be 94%, on the basis of PCR assays [ 15]. Similarly, a US Department of Agriculture 2007 dairy study estimated that at least 68% of all US dairy herds are infected with M. avium subspecies paratuberculosis, the causal agent of Johne disease, a chronic, progressive gastroenteritis of ruminants [ 16]. Although the association between M. avium subspecies paratuberculosis and Crohn disease, a similar condition of humans, is debated, the zoonotic potential exists [ 17-19].

The dairy farm environment is an important reservoir for many foodborne pathogens [ 20]. The frequency of contamination in pooled farm milk has been reported to be <1% to 8.9% for Salmonella species, 2.7% to 6.5% for L. monocytogenes, <1% to 3.8% for Shiga toxin-producing E. coli, <1% to 12.3% for C. jejuni, and 1.2% to 6.1% for Yersinia enterocolitica [ 21-24].

Moreover, the rich nutrient composition and neutral pH make milk a good vehicle for the survival and growth of bacteria. Generally speaking, if milk is maintained properly chilled, bacterial proliferation, with the exception of that of psychotropic organisms such as Listeria species, can be suppressed. Unfortunately, prevention of proliferation is not sufficient to ensure milk safety-even low numbers of contaminating pathogens may be adequate to result in human illness. Thus, simple survival of pathogens in milk is of major concern. Ultimately, the nature and complex interaction among microflora initially present in milk dictate how well pathogens will survive in milk [ 25-28].

In summary, there are 2 primary factors that contribute to the microbiological quality of milk: the inclusion of organisms in excreted milk (preharvest) and the contamination of milk at the time of collection, processing, distribution, and storage (postharvest). If pathogenic bacteria are among the contaminants, the product will pose a food safety threat. Several approaches have been used to minimize the possibility that milk contaminated with pathogenic organisms will reach the consumer. These include enhanced animal health, improved milking hygiene, and pasteurization.

Contamination Control Strategies

An overwhelming majority of dairy producers feel responsible for the safety and wholesomeness of the food products that leave their farms [ 29]. Good animal health and hygienic conditions on the farm are important for the welfare of the animals and the profitability of the producers, as well as for the quality and wholesomeness of the raw food products leaving the farms for human consumption. Nevertheless, many dairy producers are unaware of the zoonotic potential of the most common bacterial contaminants in milk. In a recent mail-based survey of 461 Ohio dairy farm respondants, 36% did not think Salmonella species caused disease in humans. Likewise, 81%, 88%, and 91% of farmers indicated that Listeria, Cryptosporidium, and Campylobacter species, respectively, were not associated with disease in humans (J.T.L., unpublished data).

Enhanced animal health. Over the past 100 years, veterinary care and diagnostic tests have improved, and many zoonotic diseases have been eliminated from the population of food-producing animals in industrialized nations. On the other hand, as mentioned above, there are a number of infections that may be present in animals and remain completely asymptomatic yet have serious public health implications.

Improved milking hygiene. Complete control of microbiological hazards (i.e, zoonotic pathogens) is challenging, if not impossible, in the dairy farm environment, because these organisms may have multiple reservoirs; they do not always produce identifiable disease; their transmission pathways are incompletely known; and cost-efficient, sensitive diagnostic tests are not available. Dairy product food safety, however, can be enhanced by implementing excellent hygienic standards for housing and milking centers and cow cleanliness and through uniform adoption of milking practices that reduce contamination of milk [ 30].

Pasteurization. Because of the above-mentioned challenges related to preharvest eradication of pathogens and the ineffectiveness of environmental hygiene screening to adequately control microbial risks in milk, pasteurization has become the cornerstone of milk safety. Pasteurization is the process of heating milk for a predetermined time at a predetermined temperature to destroy pathogens ( table 1). The current guidelines for temperature and time combinations for pasteurization are based on the ability of the process to destroy C. burnetii. The thermal destruction process is logarithmic, and bacteria are killed at a rate that is proportional to the number of bacteria present. Pasteurization improves the safety and lengthens the shelf life of a product by destroying pathogenic and spoilage organisms; however, it is not the same as sterilization.

Guidelines, Regulations, and Laws Related to Milk Safety and Pasteurization

In the United States, the US Food and Drug Administration (FDA), under the Department of Health and Human Services, is responsible for providing oversight of quality standards for dairy products and dairy processing. The milk sanitation program of the US Public Health Service is one of its oldest activities. In 1924, the US Public Health Servic developed a model regulation known as the "Standard Milk Ordinance" for voluntary adoption by state and local milk-control agencies [31]. This regulation, known today as the "Grade 'A' Pasteurized Milk Ordinance" (PMO) was developed and is periodically reviewed and modified in cooperation with state and local governments, the dairy industry, and educational and research institutions. All 50 states have voluntarily adopted the PMO guidelines. These guidelines provide guidance pertaining to all aspects of production, handling, transportation, processing, testing, and sale of milk. The guidelines are expected to minimize microbial contamination of milk and relate to areas such as cow housing, milking barn hygiene, water supply, and sanitation methods. In addition, the PMO establishes maximum allowable bacterial limits in raw milk destined for pasteurization, as well as in pasteurized milk. The federal government and FDA, however, have no jurisdiction in the enforcement of milk sanitation standards within state borders, and individual states can establish regulations concerning adoption of specific PMO recommendations and can decide on the rules regarding the sale of unpasteurized milk within state borders. In 1987, the FDA prohibited the interstate shipment of raw milk for human consumption.

In 2006, the sale of raw milk was illegal in 26 states [32]. In states where raw milk sales are not allowed, various schemes have been developed to make raw milk available to the consumer. The marketing strategies designed to circumvent current laws include selling raw milk labeled as "animal or pet food" across state lines, publishing list of states where the sale of raw milk is allowed, and selling "shares" in cows or "leasing" cows. In buying shares of cows or leasing cows, consumers pay for the upkeep, care, and milking of their cows (or portion thereof) and, in return, receive raw milk from "their" animals, avoiding the buying and selling of raw milk per se. In the states where raw milk sales are legal, regulations vary-in some states, the sale of raw milk is allowed in retail outlets, whereas, in others, it is restricted to on-farm sales directly to consumers, and the volume of salable milk may be limited.

Trends in Consumption of Raw Milk and in Milkborne Diseases in the United States

Consumption of raw milk has always been common among farm families, currently varying from 35% to 60% [ 21, 22, 24]. Most farm families report taste and convenience as the main reasons for raw milk consumption [ 24]. A small portion of the general US population also consumes raw milk. According to the US Centers for Disease Control and Prevention's FoodNet Population Survey in 2002, 3.5% of respondents reported to have consumed unpasteurized milk in the past 7 days before the survey [ 33]. Demand for raw milk has considerably increased in recent years, despite the fact that public health officials consider the benefits of milk pasteurization to be undisputable. With the advent of mandatory pasteurization, the incidence of milkborne diseases dropped dramatically. In the United States in 1938, milkborne outbreaks constituted ∼25% of all disease outbreaks due to contaminated food and water. At the beginning of the 21st century, milk and milk products were associated with <1% of all such outbreaks [ 31].

Between 1880 and 1907, an average of 29 outbreaks of milkborne diseases were reported each year in the United States [ 34]. Headrick et al. [ 35] reported 46 outbreaks of milkborne disease in the 19-year period from 1973-1992; an average of 2.4 per year. A review of foodborne diseases reported to the CDC [ 36] that were suspected or confirmed to be associated with unpasteurized milk or milk products between 1993-2006 identified 68 outbreaks, an average of 5.2 per year ( figure 1). Although some of this increase may be a result of increased detection and reporting, it is clear that disease associated with the consumption of raw milk is still an important public health concern in the United States. Very young, aged, infirm, or immunocompromised persons are the most susceptible to the pathogens that may be present in raw milk. However, anyone can be affected, including healthy young adults, as described by Blaser et al. [ 37] in an outbreak of C. jejuni infection among 19 of 31 college students who consumed unpasteurized milk on a vist to a farm.

Recent disease outbreaks related to consumption of raw milk. Since 2005, several outbreaks of disease, including salmonellosis, campylobacteriosis, and E. coli O157:H7 infection, that were related to consumption of unpasteurized milk or dairy products have been reported. During the end of 2005, 18 cases of infection with E. coli O157:H7, mostly among children aged <14 years, occurred in Oregon and Washington states. Five patients, aged 1-13 years, were hospitalized, 4 with hemolytic uremic syndrome. Laboratory and risk factor analyses linked the cases to raw milk from a dairy participating in a cow-share program in Washington [ 38]. In 2007, 29 cases of S. enterica serotype Typhimurium infection were associated with consumption of raw milk or raw-milk products in Pennsylvania. A S. typhimurium strain isolated from a dairy selling raw milk to consumers at the farm matched the outbreak strain isolated from the case patients by PFGE. Sixteen of the 29 case patients were aged <7 years [ 39]. At least 87 people became ill in Kansas in 2 separate outbreaks of campylobacteriosis during the end of 2007. In both outbreaks, illness was associated with consumption of raw milk or raw-milk products [ 40]. In 2008, an outbreak of campylobacteriosis in California was associated with consumption of unpasteurized milk supplied from a farm operating a cow-share program. One of the patients consequently developed Guillain-Barre syndrome [ 41]. Intrastate sale of raw milk is legal in Washington, Pennsylvania, Kansas, and California.

Opposition to pasteurization. Despite the overwhelming scientific understanding of pathogens in milk and the public health benefits of pasteurization, there is considerable disagreement between the medical community and raw-milk advocates concerning the alleged benefits of consumption of raw milk and the purported disadvantages of pasteurization. Raw-milk advocates suggest that unpasteurized milk products are completely safe and that they can prevent and treat a wide spectrum of diseases, including heart disease, kidney disease, cancer, and lactose intolerance [ 42-45]. In addition to the contaminating microflora, milk contains substances that have bacteriostatic and antimicrobial properties. The presumed role of these substances and their heat stability after exposure to pasteurization temperatures are outlined in table 2. Scientific evidence to substantiate the assertions of the health benefits of unpasteurized milk is generally lacking [ 57]. Nevertheless, when the public is presented with a large body of conflicting information, their decision-making process does not always yield the same results as that of experts [ 58]. This problem is particularly complicated by the fact that individuals with established attitudes not only seek information that is supportive of their views [ 59, 60] but also unconsciously process information in a biased fashion [ 61]. This results in a population that is not easily persuaded by informational messages alone. Clinicians, therefore, are faced with the challenge of communicating health risks and promoting behavioral changes among individuals who hold strong opinions about their dietary selections. One possible strategy to overcome this obstacle is to better understand the values underlying their patients' decision-making processes and target these areas, rather than the disease-risk data, to influence healthier food choices among patients [ 62]. Other factors that motivate objective information processing include message clarity, message repetition, and source credibility [ 63, 64]. The last point is an area where clinicians have an enormous advantage and influence in communication of risks.

Testing as an alternative to pasteurization. One method that has been proposed to ensure the safety of raw milk relies on product testing. The underlying premise is that if pathogens are not detectable in raw milk or the animals from which it is derived, then it should be safe for human consumption. It must be noted, however, that product testing cannot ensure safety. Testing schemes are limited by assay sensitivity-both of the sampling-collection strategy and the microbiological analysis. Microbiological assays have improved over time, and several rapid and sensitive methods are available to test for pathogens [ 65, 66]. Nevertheless, the problem of testing to ensure safety is complicated by several factors: (1) milk contamination occurs sporadically, (2) contamination may not be evenly distributed in a product, (3) extremely small amounts are infectious, and (4) extremely small numbers (below the detectable limit) of organisms present in the product may proliferate to levels that reach unacceptable risks after testing.

Summary and Conclusions

Despite the enormous advances in animal health, milking hygiene, and processing technology that have occurred during the past century, milkborne disease outbreaks continue to occur in the United States. Given that milk is derived from animals, it inherently carries the risk of being contaminated with pathogens from its source (cattle, goats, sheep, and the farm environment). The key factor in the prevention of milkborne disease is consumer avoidance of raw milk consumption. In an effort to protect human health, a number of organizations have published guidelines and statements concerning milk pasteurization. The American Medical Association (policy H-150.980) [ 67] clearly asserts that milk sold for human consumption should be pasteurized. Likewise, the American Veterinary Medical Association asserts that only pasteurized milk and milk products should be sold for human consumption [ 68]. Thus, physicians, veterinarians, and dairy farmers who promote, or even condone, the human consumption of unpasteurized milk and dairy products may be at risk for subsequent legal action [ 32, 69].

Acknowledgments

The authors thank Dr. John Sheehan for valuable discussions on the subject during the preparation of the manuscript.

Financial support. Funding in partial support of J.T.L. was provided by state and federal funds allocated to the Ohio Agricultural Research and Development Center, Wooster, Ohio.

Potential conflicts of interest. J.T.L. and P.J.R.-S.: no conflicts.

References

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Unpasteurized Milk: A Continued Public Health Threat | Clinical Infectious Diseases | Oxford Academic

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Although milk and dairy products are important components of a healthy diet, if consumed unpasteurized, they also can present a health hazard due to possible contamination with pathogenic bacteria. These bacteria can originate even from clinically healthy animals from which milk is derived or from environmental contamination occurring during collection and storage of milk.

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"From the day they are born to the day they are slaughtered; the chicken belongs to the poultry company." 

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"From the day they are born to the day they are slaughtered; the chicken belongs to the poultry company." 

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In this quote chicken farmers were not referred to as such and it was stated that it would be more correct to call them chicken growers. There are no wild chicken anywhere, every chicken is part of a farm growing system for consumption. Chicken growers are referred to as such because they have to do everything for the chicken like provide shelter, food, and water. One chicken grower stated that he feels more like a babysitter and spends more time with the chicken than he does his own children. Even though chicken grower put in all the work raising the chicken the big companies still own the chicken through contracts with the farmer that typically are unfair and demand a lot of the farmers (Moodie, 2017).

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Back in 2001, Alton Terry, his wife and two young children were living in San Jose, California, but they dreamed of a quieter, more rural life. Terry's grandparents had been farmers, and that inspired him to move his family to Shelbyville, Tennessee, to start a chicken farm.

Like the majority of chicken farmers in the US, Terry entered into an exclusive contract with a big producer, Tyson Foods. "The first couple of years we didn't have any problems," said Terry, "but then Tyson started asking us to put in extra equipment that we had to pay for."

Terry had taken out a $500,000 loan to build the chicken houses on his farm, and he wasn't willing to fork out more money for equipment that he said wasn't necessary, including extra feed bins and upgrades to the chicken houses.

"If we are independent contractors, then why does the company have the right to tell us what equipment to use?" said Terry. "We were independent in name only when it benefited the company."

Terry claims Tyson retaliated by giving him sick chicks. In 2005, Tyson didn't renew Terry's contract. Finding another big customer was difficult because Tyson was the only chicken company in the area.

Terry sued Tyson in 2008, alleging the company canceled his contract because he rallied farmers in the area to lodge complaints about the company with their congressional representatives and the US Department of Agriculture (USDA); he said Tyson mistreated him with tactics such as weighing his birds incorrectly while not allowing him to watch the weigh-in, a violation of USDA rules.

He lost the case in 2010 after a federal judge declared that the law required him to show that Tyson's actions had crippled competition for the entire poultry industry, not just him. The court ordered Terry to pay Tyson nearly $30,000 in legal fees. He was forced to declare bankruptcy.

"We lost the farm, our house, our horses and our dogs," said Terry, who now works as a handyman and carpenter.

Seven years later, a set of federal rules has emerged that aims to strengthen protection for farmers. But the new rules, drawn up in the final days of the Obama administration, are in limbo. The Trump administration suspended the enactment of any new federal rules for two months after inauguration, and just last week, the USDA announced that the new rules would remain on hold for another six months.

The new rules - a culmination of decades of effort by farmers and their advocates - would no longer require farmers to prove harm to competition within the industry owned largely by a handful of producers. The four largest chicken producers in the country, which include Tyson Foods and Pilgrim's Pride, control more than half of the chicken market and 57% of the turkey market, according to the USDA.

"It's really a story of unchecked corporate concentration," said Sally Lee, who works at family farmer advocacy nonprofit Rural Advancement Foundation International-USA and co-director of Under Contract, a documentary about farmers who suffered severe financial losses and emotional toll from what they said was unfair treatment by big chicken producers. "There are a few companies that control the market so they can exercise extreme power over farmers trying to work with them."

Clawing for control

More than 97% of chicken farmers in the US work under contract with a big producer. A farmer can choose to work independently and sell chickens to a company for processing or directly to retailers and consumers, but these farmers are at an "extreme disadvantage," said Lee, since most chicken processing plants are owned by producers.

The contract system offers chicken producers a consistent supply of products and guarantees a market for farmers, said Susan Schneider, director of the master's program in agricultural and food law at the University of Arkansas school of law.

Starting a chicken farm isn't cheap - one chicken house averages $250,000, and four houses are recommended to achieve a basic level of income. The startup cost sometimes requires farmers to mortgage their farms, Schneider said.

"Any objective legal analysis would find the typical poultry contract to be one-sided by design," added Schneider.

Farmers also often find there are additional mandates - such as upgrading a chicken house - that weren't included in the original contract. Investing in those changes could require farmers to take out new loans, and they often feel forced to comply or lose their only customer.

"The relationship between company and contract farmer has changed dramatically over time, to the point that the farmers are treated as employees in many ways, without receiving any of the benefits, yet retaining all the obligations and risk that independent contractors have," Lee said.

Mike Weaver, a poultry farmer in West Virginia, said his base pay hasn't changed since he entered the business in 2001.

"As long as they keep us in debt we have to keep raising their chickens. They don't want farmers to pay off their farms," Weaver said.

Worth Sparkman, a spokesperson for Tyson Foods, said the contract system is transparent and offers long-term stability to farmers.

"Our average contract farmer has been raising chickens for us for 15 years [and] the compensation we provide is set out clearly in contracts the farmers voluntarily enter into," said Sparkman. "The farmers are free to discuss the terms of their contracts with whomever they want, including other farmers, and are also free to switch to other chicken processors who operate in their area."

Unfair advantage?

Producers exert their influence in other ways, too. They supply farmers with baby chicks, feed and medication. A farmer typically has five weeks to raise them, after which the chickens are collected and weighed at a processing plant.

The farmers are paid according to a so-called "tournament system" that pits farmers against each other. The farmer that produces the most amount of meat with the least amount of feed comes out on top. A less efficient farmer will have money deducted from his base pay; that money is then be used to pay the farmers that produced more meat.

The problem, say the farmers, is that winning or losing is beyond their control. For example, they must take the chicks supplied by their producers and are out of luck if they receive a large number of unhealthy chicks.

"They say that if you work harder, you'll do better, but that's a lie," said Weaver. "If you don't get good chicks and feed from them, there's no way you can make a good chicken out of it."

The poultry industry says the tournament system is fair and ensures that the welfare of the chickens comes first.

"The performance-based contract structure of modern poultry production was instinctively designed to put the well-being of the birds as the top priority, as incentives are given to farmers who raise the healthiest birds, take risks and work hard," said Tom Super, a spokesperson for the National Chicken Council, a trade association. "It incentivizes farmers to do their best, to compete, just like every other business in America or any other free market."

The new federal rules, opposed by lobbyists for the poultry industry, included criteria for ensuring a fair tournament system.

It's unclear whether the rules will take effect under the current administration. Republican members of Congress have generally opposed any effort to provide greater contract protections for poultry growers, said Schneider, and she doesn't see that changing.

"The Republican-controlled Congress has restricted USDA's efforts in the past, and I assume that this will carry over to the new Republican administration," said Schneider. "If so, I think that it is very likely that the new rules will be withdrawn, amended, or simply not enforced."

But Weaver said he and other farmers are optimistic that Trump will act in their best interests, since they helped him get elected.

"He claimed he's going to stand up for the little guy, that's why the farmers came out and voted for him and got him into office," said Weaver. "These multinational corporations have had way too much power over farming for too long."
Topics

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Fowl play: the chicken farmers being bullied by big poultry

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Back in 2001, Alton Terry, his wife and two young children were living in San Jose, California, but they dreamed of a quieter, more rural life. Terry's grandparents had been farmers, and that inspired him to move his family to Shelbyville, Tennessee, to start a chicken farm.

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"We need to double our yields by 2050." 

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"We need to double our yields by 2050." 

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This quote was in reference to the fourth episode of Rotten when talking about the chicken industry. The demand for chicken is on the rise everywhere and is forcing chicken farmers to create new ways to increase production. The Journal of Antimicrobial Chemotherapy states that chicken production has had a much higher demand in recent years partly because of the health and wellness industry deeming chicken as "healthy and a great source of lean protein." Even though the demand for chicken is growing everywhere Europe has banned the use of growth hormones in chicken production (Casewell, 2003).

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Abstract

Following the ban of all food animal growth-promoting antibiotics by Sweden in 1986, the European Union banned avoparcin in 1997 and bacitracin, spiramycin, tylosin and virginiamycin in 1999. Three years later, the only attributable effect in humans has been a diminution in acquired resistance in enterococci isolated from human faecal carriers. There has been an increase in human infection from vancomycin-resistant enterococci in Europe, probably related to the increased in usage of vancomycin for the treatment of methicillin-resistant staphylococci. The ban of growth promoters has, however, revealed that these agents had important prophylactic activity and their withdrawal is now associated with a deterioration in animal health, including increased diarrhoea, weight loss and mortality due to Escherichia coli and Lawsonia intracellularis in early post-weaning pigs, and clostridial necrotic enteritis in broilers. A directly attributable effect of these infections is the increase in usage of therapeutic antibiotics in food animals, including that of tetracycline, aminoglycosides, trimethoprim/sulphonamide, macrolides and lincosamides, all of which are of direct importance in human medicine. The theoretical and political benefit of the widespread ban of growth promoters needs to be more carefully weighed against the increasingly apparent adverse consequences.

Received 19 December 2002; returned 20 March 2003; revised 27 April 2003; accepted 28 April 2003

The bans on growth promoters and their immediate effects

Following the ban on all growth-promoting antibiotics in Sweden in 1986, and the ban on avoparcin and virginiamycin in Denmark in 1995 and 1998, the European Union (EU) banned the use of avoparcin in 1997 and the four remaining antibiotics used for growth promotion in 1999, on the basis of the 'Precautionary Principle'. These four antibiotics were bacitracin (a polypeptide), spiramycin and tylosin (macrolides), and virginiamycin (a streptogramin combination). The driving forces behind these bans were consumer and political opinion, and a scientific concern that resistance selected in animals might be transmitted to humans to the detriment of their health. Experience in Sweden had already shown that the bans might have adverse consequences for animal health and welfare, and economic consequences for farmers. 1 There were also suggestions that human health is unlikely to benefit and that it might even be adversely affected. 2,3 Careful perusal of the scanty published literature of events in Europe since the EU ban shows that these concerns were well founded.

The ban has resulted, as intended, in the complete removal of the banned compounds as growth promoters. In Denmark, for example, where over 105 metric tonnes of antibiotics were used for growth promotion in 1996, the usage fell to nil by 2000. 4 This was accompanied by a diminution of resistance to avoparcin, macrolides and virginiamycin among enterococci, studied as an 'indicator' species, in food-animal faeces, in Denmark and elsewhere, 4⁻6 although vancomycin-resistant Enterococcus faecium has persisted in samples from Danish broilers 7 and pork. 8 Nevertheless, the pool of antibiotic resistance genes in animal faecal enterococci appears, overall, to have diminished.

Consequences for human infections

The only attributable effect on humans has been some diminution in vancomycin resistance in enterococci isolated (VRE) from human faecal carriers. 6,9 However, despite the growth promoter ban and the reduction of carriage of resistant enterococci in animal and human faeces, there has been no diminution in the prevalence of resistant enterococcal infection in humans: little could be expected in Scandinavia where VRE infections have rarely been reported, 10,11 despite the widespread use since 1975 of avoparcin as a growth promoter. Rather, vancomycin resistance appears to be increasing in enterococcal infections in parts of Europe over the period of the ban, probably in relation to the increased prevalence of methicillin-resistant staphylococcal (MRSA) infection 12 necessitating the increased use of glycopeptides and streptogramins-mimicking the conditions found in the USA 13 where a high incidence of VRE infection has emerged in humans in the absence of the use of avoparcin in animals. The first vancomycin-resistant methicillin-resistant Staphylococcus aureus has recently emerged, not in Europe, but in the USA 14 and the most likely explanation is the acquisition of the VanA gene from a strain of vancomycin-resistant Enterococcus faecalis that was also present at the site of the patient's chronically infected foot ulcer. 15

The antibiotic susceptibility of salmonellae and campylobacters, responsible for the major zoonoses in Europe, could not have been expected to be affected by the ban to the benefit of human health (except possibly in relation to macrolides in the case of campylobacters) since they are Gram-negative organisms whereas the banned growth promoters had a Gram-positive spectrum of activity. However, human salmonellosis has not responded to control measures in some parts of Europe, and microbiologically confirmed infections actually increased in prevalence in Denmark in 2001 5 after they had declined for 3 years. 16 Increased antibiotic resistance in salmonella might be expected in response to the increased use of therapeutic antibiotics in animals consequent to the ban, and there is an increase in tetracycline and sulphonamide resistance in S. typhimurium isolates from pigs and from human domestic infections in Denmark in 2001. 5 The case of campylobacter appears to be worse: in Denmark, it has steadily increased in prevalence over the past decade 16 and there is more tetracycline and fluoroquinolone resistance in human than in animal isolates. 5 One possibility is that the persistence or even increase in prevalence of these two zoonoses might in part be related to the removal of growth-promoting antibiotics but so far as we are aware this hazard has not been explored. For example, the variation in size of broilers not given growth promoters leads to more frequent rupture of the gastrointestinal tract at slaughter, faecal spillage, and potential contamination with salmonella and campylobacter. 17 The possible contribution of increasing international travel to countries with poor food and water hygiene to the increased prevalence of campylobacter and salmonella infections has yet to be defined.

Consequences for animal health

Although originally approved for use as growth promoters, the sudden withdrawal of these antibiotics has revealed animal health promotional effects of growth promoters that are consistent with the prophylaxis of important food-animal infections. Thus, following the bans, the diminution of the resistance pool in animal and human faecal commensal enterococci has been at the cost of a deterioration in animal welfare. In Sweden, 16 years after their ban of growth promoters, the loss in production from pigs has not yet been fully recovered on a national basis. 1 From Denmark, there are reports of increased morbidity and mortality among pigs, 18 mostly associated with enteric infections; 19 11% of 'finishing' herds (weighing more than 35 kg) experienced permanent problems with increased frequency of diarrhoea or reduced weight gain. 20 However, in younger weaning pigs (7-30 kg weight) the problems of post-weaning diarrhoea and chronic infections due to Lawsonia intracellularis have persisted in Denmark 19,20 and in Spain (E. Marco, personal communication) leading to decreased weight gain and an increased mortality since the removal of growth promoters. 19,20 In poultry, it had been predicted that if bacitracin was withdrawn, clostridial necrotic enteritis, which is known to be suppressed by this growth promoter, 21 would emerge as a problem requiring therapy, and this has been reported to be the case in Denmark 22 and in France. A recent report from the Danish National Department of Poultry Production points out that since the late 1990s, the broiler industry has been "struggling with leg and skin problems" that may compromise broiler welfare and that, although not previously documented, "the exclusion of animal growth promoters and meat and bone meal from broiler diets has played a major role in the development of leg problems and deteriorated skin health". 23 Modifications in environmental conditions, such as light and feeding programmes, are being tested to improve food safety and customer acceptance of poultry meat.

Increased use of therapeutic antibiotics in food animals

This increase in infections since the ban has driven, at least in part, a substantial increase in the use of therapeutic antibiotics for food animals in Europe. 24⁻26 In the UK, the Veterinary Medicines Directorate published in 2002 the sales figures for veterinary antimicrobials up to the year 2000. 25 After the EU ban of growth promoters in 1999, there was an increase in sales of therapeutic antimicrobials from 383 tonnes in 1999 to 437 tonnes in 2000. This was due to increases in the sales of tetracyclines (by 36 tonnes), trimethoprim/sulphonamides (by12 tonnes) and macrolides (by 12 tonnes). There were increases of 7 tonnes in pigs, 13 tonnes in poultry and of 37 tonnes of therapeutics authorized for more than one species. It was thought that in the pig industry, the increase may well be ascribed to the EU ban in 1999 and to the presence of diseases such as porcine dermatitis, nephritis syndrome and post weaning multisystemic wasting syndrome. 25 In Denmark, there was an overall increase in therapeutic antibiotics from 48 tonnes in 1996 4 to 94 tonnes in 2001. 5 The main antibiotics involved in this increase have been tetracycline, mostly used in pigs, 26 whose usage increased from 12.9 to 27.9 tonnes (a 116% increase), macrolides and lincosamides (7.6 to 14.3 tonnes, 88%) and aminoglycosides (7.1 to 11.9 tonnes, 68%). 4,5 This has occurred despite attempts to improve other critical aspects of animal husbandry 27 to make up for the loss of the growth promoters. Experience in Sweden suggests that this may eventually be partially effective but with an increased financial burden; 1 it is far from clear that this will apply to the whole of Europe where farming conditions are different from those of Scandinavia.

Conclusion

The published evidence suggests that the growth-promoter bans have reduced overall antibiotic use in animals. It is increasingly clear, however, that the use of growth promoters was accompanied by other, previously unrecognized, health promotional or prophylactic effects. After the withdrawal of these antibiotics, animal welfare has suffered and despite efforts to improve other aspects of husbandry, the veterinary use of therapeutic antibiotics, which are identical to those used in human medicine, has increased, and this constitutes a theoretical hazard to human health in relation to resistance in salmonellae, campylobacters and zoonotic strains of E. coli. The efforts and expenditure involved in the imposition of the ban would have been better spent on achieving rational antibiotic use in humans and animals, and on much greater efforts to understand the complex epidemiology of resistant pathogens and resistance genes, as well as adequate risk assessments of both the ban, the 'precaution', in parallel with that of the 'threat', i.e. the continued use of growth promoters. The evidence suggests that the remaining growth promoting antibiotics still in use in Europe should not be banned until the relationship between growth promotion and prophylaxis is clarified, and the adverse consequences of the current ban can be remedied in Europe as a whole. The prediction in 1997 that "The elimination of these products will tend to increase the use of therapeutic antimicrobials" and that "animal production is likely to decline in countries which implement a unilateral ban on these products" 28 seems thus far to be supported by the evidence.

Acknowledgements

This review was prepared independently following a meeting sponsored by Elanco Animal Health, Basingstoke, UK.

Correspondence address. Department of Infectious Diseases, Guy's, King's & St Thomas's School of Medicine (King's College Hospital Campus), Bessemer Road, London SE5 9RS, UK. Fax: +44-20-7346-3404; E-mail: casewell@netcomuk.co.uk

References

Acar, J., Casewell, M., Freeman, J. et al. (

). Avoparcin and virginiamycin as animal growth promoters: a plea for science in decision-making.

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Heuer, O. E., Pedersen, K., Andersen, J. S. et al. (

). Occurrence and persistence of vancomycin resistant enterococci (VRE) in Danish broiler production after the avoparcin ban. In Abstracts of the International Invitational Symposium: Beyond Antibiotic Growth Promoters in Food Animal Production, Foulum, Denmark, 2002, p. 4. Danish Veterinary Institute, Copenhagen, and the Danish Institute of Agricultural Science, Tjele, Denmark.

Boel, J. & Andersen, S. (

). Effects of the termination of antimicrobial growth promoter use on antimicrobial resistance in bacteria from foods. In Abstracts of the International Invitational Symposium: Beyond Antibiotic Growth Promoters in Food Animal Production, Foulum, Denmark, 2002, pp.

-2. Danish Veterinary Institute, Copenhagen, and the Danish Institute of Agricultural Science, Tjele, Denmark.

Klare, I., Badstubner, D., Konstabel, C. et al. (

). Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from faecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry.

Microbial Drug Resistance

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Centers for Disease Control and Prevention. (

). Staphylococcus aureus resistant to vancomycin-United States, 2002.

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Wegener, H. C. (

). Banning antimicrobial growth promoters in Europe: where does it make a difference? In 42nd Interscience Conference on Antimicrobial Agents and Chemotherapy, San Diego, CA, 2002. Abstract for Session 195. American Society for Microbiology, Washington, DC, USA.

Tornee, N. (

). Consequences of terminating AGP use for broiler health and usage of antimicrobials for therapy and prophylaxis. In Abstracts of the International Invitational Symposium: Beyond Antibiotic Growth Promoters in Food Animal Production, Foulum, Denmark, 2002, p. 6. Danish Veterinary Institute, Copenhagen, and the Danish Institute of Agricultural Science, Tjele, Denmark.

Petersen, J. S. (

). Animal welfare and health as affected by management procedures in commercial broiler flocks. In The International Invitational Symposium: Beyond Growth Promoters in Food Animal Production, Foulum, Denmark, 2002. The Danish Veterinary Institute, Copenhagen, and the Danish Institute of Agricultural Science, Tjele, Denmark.

Larsen, P. B. (

). Consequences of terminating AGP use for pig health and usage of antimicrobials for therapy and prophylaxis. In Abstracts of the International Invitational Symposium: Beyond Antibiotic Growth Promoters in Food Animal Production, Foulum, Denmark, 2002, p. 7. Danish Veterinary Institute, Copenhagen, and the Danish Institute of Agricultural Science, Tjele, Denmark.

Author notes

1University of London, London; 4Poultry Health Services Ltd, Thirsk, North Yorkshire, UK; 2Royal Veterinary and Agricultural University, Copenhagen, Denmark; 3B & M Consulting, Barcelona, Spain

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European ban on growth-promoting antibiotics and emerging consequences for human and animal health | Journal of Antimicrobial Chemotherapy | Oxford Academic

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Following the ban of all food animal growth-promoting antibiotics by Sweden in 1986, the European Union banned avoparcin in 1997 and bacitracin, spiramycin, tylosin and virginiamycin in 1999. Three years later, the only attributable effect in humans has been a diminution in acquired resistance in enterococci isolated from human faecal carriers.

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"There has been a surge in food allergies especially among children. " 

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"There has been a surge in food allergies especially among children. " 

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This episode explored the issue of food allergies in children and why food allergies are a relatively new obstacle for farmers, chefs, and parents. The World Allergy Organization Journal states that it still is not clear as to why food allergies are on the rise, but some theories suggest that developed nations and children are more prone to food allergies because they have strayed farther from the traditional diet that humans ate thousands of years ago. This explains why children in Africa who do still eat a similar diet to that of humans thousands of years ago do not have a large issue with food allergies (Prescott, 2013).

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While food allergies and eczema are among the most common chronic non-communicable diseases in children in many countries worldwide, quality data on the burden of these diseases is lacking, particularly in developing countries. This 2012 survey was performed to collect information on existing data on the global patterns and prevalence of food allergy by surveying all the national member societies of the World Allergy Organization, and some of their neighbouring countries. Data were collected from 89 countries, including published data, and changes in the health care burden of food allergy. More than half of the countries surveyed (52/89) did not have any data on food allergy prevalence. Only 10% (9/89) of countries had accurate food allergy prevalence data, based on oral food challenges (OFC). The remaining countries (23/89) had data largely based on parent-reporting of a food allergy diagnosis or symptoms, which is recognised to overestimate the prevalence of food allergy. Based on more accurate measures, the prevalence of clinical (OFC proven) food allergy in preschool children in developed countries is now as high as 10%. In large and rapidly emerging societies of Asia, such as China, where there are documented increases in food allergy, the prevalence of OFC-proven food allergy is now around 7% in pre-schoolers, comparable to the reported prevalence in European regions. While food allergy appears to be increasing in both developed and developing countries in the last 10-15 years, there is a lack of quality comparative data. This survey also highlights inequities in paediatric allergy services, availability of adrenaline auto-injectors and standardised National Anaphylaxis Action plans. In conclusion, there remains a need to gather more accurate data on the prevalence of food allergy in many developed and developing countries to better anticipate and address the rising community and health service burden of food allergy.

Food allergy has emerged as an unanticipated 'second wave' of the allergy epidemic [], dramatically increasing the burden of allergic diseases in infants and preschool children [, ]. In some highly industrialized regions the prevalence of food allergy in infancy has reached 10% [] and there are now reports that rates of food allergy are now following the steep gradient of economic transition in rapidly developing countries []. While the rising global burden of asthma [], rhinitis [] and eczema [] has been well-documented over the past 20 years through world-wide epidemiological research programs such as the ISAAC Study (International Study of Asthma and Allergies in Childhood), there have been, as yet, no equivalent published data on food allergies on a global platform. Although several centres collected data enriched for food allergy in association with more ISAAC recent surveys [-] global trends have not been well studied, likely because in the early 1990's when ISAAC was established food allergy was relatively uncommon and more difficult to accurately ascertain than other allergic outcomes by questionnaire.

While there have been Systematic Reviews on food allergy prevalence, these largely capture data from Western Europe and North America where the majority of studies have been performed; many more than a decade ago []. The majority of these reports were based only on self-reported food reactions rather than objective measures of true IgE-mediated food allergy, and the few that used the gold standard, oral food challenges (OFC) did not have consistent or standardized criteria in defining outcomes []. New multi-centre well designed food allergy prevalence studies using OFC and IgE measures (notably the EuroPrevall birth cohort) are now underway and will more accurately determine the prevalence and cost food allergy []. The EuroPrevall study (more than 12,000 children) is also predominantly focused in Europe, although it has been extended east to examine an anticipated 37,000 children in the emerging economies of Russia, China, and India - countries comprising 40% of the global population and in transition from traditional to modern lifestyles []. However, the accurate determination of the food allergy burden in many other developing regions of the world remains an important unmet need.

The main purpose of this study was to utilize the global network of the World Allergy Organization (WAO) to provide a current 'snapshot' of the level of knowledge on the prevalence, patterns and burden of food allergens throughout the 93 national and regional member societies of WAO, and in particular reveal regions where more data is needed. We also sought to determine the level of service provision for food allergy, urban-rural preventionhealth-care access, availability of adrenaline auto injectors and standardized national food allergy anaphylaxis action plans in each country. This was also an opportunity to obtain some level of information about infant feeding practices in these diverse countries.

This was a collaborative project between the WAO and the Worldwide Universities Network (WUN). The Survey targeted the 93 peak national and regional member societies of WAO, with instructions to be completed by the most qualified experts in paediatric food allergy in each country. A working group from the WUN International Inflammation ( inFLAME) Network was established to develop the web-based questionnaire in February 2012. This included clinicians specialized in general paediatrics, paediatric allergy, neonatology, gastroenterology, nutrition and dietetics and epidemiology (each as members of both WAO and WUN). Questions were developed and discussed in a workshop format and then circulated to the wider inFLAME Network for comment. The resulting questionnaire was ratified by the WAO Special Committee on Food Allergy and Nutrition in June 2012, and disseminated through the WAO secretariat to the 93 regional/national societies in September 2012 (where possible data were also collected from neighboring non-WAO member countries). The respondents were identified by their own societies as the most qualified people to complete the questionnaire.

Each country was asked to provide any data to support any change in food allergy (both IgE and non-IgE forms as defined by WAO criteria [] provided) focusing on the last 10 years, and provide the source and level of evidence that their answer was based on, including published research, national data, changing health-care burden or to indicate if there was insufficient data in their region to provide an answer. Regions reporting a change in prevalence were asked to indicate the age group most affected (infants <1 year; 1-5 year olds; or children <5 years) again with the nature and source of data that this was based on. All were asked if there was published information of any kind available regarding the overall prevalence of food allergy in their country, and to provide any data available on the estimated percentage of children in their population who have food allergy (all ages and for preschool [<5 years] and for school aged children [<5 years], if data available). They were also asked to indicate the most common clinical presentations of food allergy including (1) acute IgE-mediated food allergy (i.e. onset generally within 1-2 hours with angioedema, urticaria, vomiting or anaphylaxis); (2) non IgE-mediated food allergies (i.e. more delayed gastrointestinal symptoms only e.g. reflux, constipation, colic, chronic diarrhea, blood in stool, without IgE associated symptoms) or (3) mixed IgE and non-IgE food allergy (children with features of both acute onset symptoms and more chronic symptoms, such as eczema, exacerbated by foods). Each country representative respondent was asked to indicate the 5 most common food allergen triggers in order of prevalence for infants and children younger than 5 years, and a separate list for children older than 5 years. For each answer the respondents were asked to provide the source of data, if any. Information was also collected on the availability of adrenaline auto-injectors for treatment of anaphylaxis in each country (including if these are subsidized by the health care system and whether they are available widely or only through selected health services or to selected patient groups). The use of National Anaphylaxis Action Plans was also determined for each country (i.e. whether patients with a risk of anaphylaxis because of known allergy are given the same nationally standardized management plan). General information was also collected about the population size of each country and the numbers of trained paediatric allergists in the region. Finally, respondents were asked to provide information on early infant feeding and weaning practices including average duration of breastfeeding, age of introduction of complementary feeding foods, kinds of solid foods first used and whether there were any specific allergy prevention guidelines in relation to infant feeding. A six-month period was allowed for all responses to be received. Where there was more than one respondent from a country (i.e. more than one national allergy society, or multiple responses for any other reasons) the data was selected based on the highest level of evidence provided. In each case a literature search was performed by the investigators to confirm the cited data source, and to look for any additional evidence. Where data were also provided and/or published for neighboring non-WAO member counties this has also been included. The findings are presented for each country separately and arranged by geographical region.

Data from 89 countries (Figure ) were compiled to formulate a global picture of food allergy, including 12 countries in Western Europe, 5 Nordic countries and 17 in Central/Eastern Europe, 18 countries in Asia and Oceania, 15 countries in the Americas, 10 in the Middle East and 12 countries in Africa (Additional file : Table S1, on line repository). This included 83 WAO member countries and 6 non-member countries (Figure ). These were categorized by the best level of evidence available for each country, with the highest level based in food allergy prevalence defined by oral food challenges (OFC) in unselected populations (Additional file : Table S1). The next best level of evidence was based on a suggestive clinical history confirmed by allergen skin prick testing (SPT) or other measures of food-specific IgE, also in unselected populations. Studies that relied only on self-reporting (such as questionnaire or phone survey data) were categorized as the lowest level of evidence for defining population food allergy prevalence.

Food allergy prevalence by level of evidence

Food allergy prevalence trends by country/region

Infant feeding patterns by region

Paediatric allergy services and anaphylaxis services by country/region

Each regional society was asked to provide the number of registered trained paediatric allergists (or equivalent) in their country, and based on the population size, that was used to determine the number of specialist service providers per million of total population (Additional file : Table S3). There were wide variations in the number of service providers, with some countries (such as the UK) with a reported high burden of food allergy having < 1 paediatric allergist per million of population (0.32/million). Similarly, other high-burden countries such as Australia, New Zealand and Canada, report ≤ 3 paediatric allergists per million population. The USA and European regions with relatively high food allergy burden are generally better serviced (such as Germany, Greece, Italy and Nordic countries) but this is highly variable. Other regions where food allergy is emerging as a new and growing problem have very few trained specialists per head of population. This is true in Asia (with the exception of Japan), South America (with the exception of Cuba) and the Middle East (with the exception of Israel), where there are generally ≤ 3 paediatric allergists per million of population. African nations have very few trained paediatric specialist, although there is a general lack of data on both the burden of disease and service provision in that region. In the most populous regions (China and India), there were also no accurate data available.

Many countries reported perceived urban-rural differences in paediatric allergy health care services (Additional file : Table S3). The main exceptions are smaller developed countries or states (such as Singapore, Hong Kong and smaller European regions) or regions where services are equally poor in urban and rural regions (such as Mongolia).

Adrenaline autoinjectors and allergy action plans

There are wide variations in the availability of adrenaline auto-injectors and many countries do not yet have standardized national Food Allergy/Anaphylaxis Action Plans (Additional file : Table S3). Adrenaline auto-injectors are readily available in countries with the higher service burden of allergy, such as North America, Western Europe, Nordic countries and Oceania, and are generally subsidized by healthcare systems. Most, but not all, of these countries have standardized national anaphylaxis action plans. However, in some countries with a very high service burden of allergy (such as in New Zealand) adrenaline auto-injectors are still not subsidized by the healthcare system. There is a reported lack of general availability of adrenaline auto-injectors (very difficult to access and/or not subsidized) in the Middle East, many areas of Asia and South America, Africa (although data more limited) and some regions of Eastern Europe.

The main purpose of this survey was to provide a global 'snap shot' of current trends in food allergy including the quality of evidence available and regions where more information is needed. Because the rise in food allergy is believed to have been relatively recent as 'a second wave' of allergy after the rise in asthma and rhinitis [, ], most regions do not have accurate or current prevalence data, particularly in infants and young children under 5 years of age who are most commonly affected. Many estimates are based on parent- or self-reported questionnaires or surveys and very few objectively confirm the prevalence of food allergy through the gold standard of oral food challenge. Even those few studies undertaking food challenges until recently have been hampered by poor challenge participation rates resulting in potential for substantial allergic bias.

The findings reveal a general paucity of quality data on food allergy prevalence, even in high prevalence areas of North America and Western Europe. In Europe this will be addressed to a large extent by the large-scale multicentre 'Europrevall Study'. Extending this to study an additional 37,000 children in the emerging economies of Russia, China, and India [] will be very helpful. However, there remains a need for similar studies in South America, South East Asia, the Middle East and Africa where very little information is available. To address this in South Africa there are plans for a cross-sectional, observational study of IgE-mediated food allergy in an unselected population of children aged 12-36 months. This will include both urban and rural communities and all children with a positive SPT of any size (≥1 mm) will be referred to the Allergy clinic for OFC to determine the clinical significance. Similar studies are also needed in other emerging economies.

A recent meta-analysis commissioned by the National Institute of Allergy and Infectious Disease concluded that the prevalence of food allergy across all age groups is likely to be between 1% and 10%, with higher prevalence in younger age groups []. The more recent well designed Australian HealthNuts study supports this, with 10% of 1 year old infants demonstrating challenge-proven IgE-mediated food allergy with even higher rates of food sensitisation []. The design of HealthNuts provides a good model for future food allergy prevalence studies. The cohort was not selected on the basis of a family history of atopy, and children with positive tests irrespective of SPT wheal size proceeded to hospital-based food challenge to confirm the clinical food allergy. Oral food challenges were the first to be undertaken with predetermined objective stopping criteria. Prevalence was adjusted for participation bias, both at the point of initial population screening and at invitation for food challenge, and nonparticipants were also surveyed to allow for any bias towards allergy. This study was clearly labor-intensive and it is acknowledged that, although OFC are the gold standard in diagnosing food allergy, this is not feasible in many low and middle-income countries.

Another key observation is that rapidly developing regions such as China are showing significant rates of food allergy [, ]. Thus, despite common notions that food allergy is less prevalent in Asia, these prevalence figures from various studies in Asia are comparable to those reported from western populations (Additional file : Table S1). Published studies on food allergy time-trends confirm the rising prevalence in Asia [], and a gradient of food allergy with progressive economic development also provides indirect evidence that food allergy is associated with westernisation; with higher rates of food allergy in Chinese born in Hong Kong (4.8%) compared with those born in mainland China (2.4%) []. This is consistent with recent reports showing a rise in non-food allergic diseases such as asthma and allergic rhinitis in developing countries that are adopting a more "westernised" lifestyle [-]. Eczema prevalence has also increased significantly in Asia []. This has major global implications, as the heavily populated regions of Asia are becoming rapidly urbanised, westernised and industrialised.

In this context it is important to note preliminary evidence that Asian and other non-Caucasian populations may be even more susceptible to the adverse effects of 'Westernisation' than Caucasians [, ]. Earlier studies of respiratory disease observed that both allergic symptoms and sensitisation were more common in Asian Australians than non-Asians Australians []. Rates were also higher in Australian-born Asians than Asian immigrants, with the prevalence increasing with length of stay in Australia [] and this was echoed recently in data from the Healthnuts study on eczema prevalence. More recent US studies have similarly noted that non-white races are more susceptible to food allergy, particularly Asian populations [], suggesting a strong genetic propensity that is amplified by a western environment. Thus, as urbanisation inevitably progresses we can anticipate a major rise in the global burden of food allergy.

Many countries (n = 45) already report an increase in food allergy prevalence, although only 6 based this on published evidence and the remainder based this on reported increased health care burden. Only 9 countries reported a stable prevalence, and none reported a decline in food allergy burden. However, many (n = 35) could/did not provide any data (either published or based on health care burden). We did not collect data on the changing prevalence of specific allergies, however, it has been recently noted that while peanut allergy has increased dramatically in the USA [], UK [, ] and Australia [], this is less evident in Asia although data are more limited (reviewed recently in []).

Although there is some variation in the patterns of food allergy, there is surprising consistency in the most common allergen triggers, particularly in infants and younger children. In most regions egg and milk are among the most common allergens in preschool children, generally listed as the two most common. Although these are typically considered as 'transient' allergies, it is interesting that these were also noted among the most common allergens in older children (<5 years) in almost all regions. It is not clear how this might relate to emerging evidence that egg and milk allergies are now commonly persisting into late childhood and adolescence [, ]. Peanut, tree nuts and seafood were also common allergen triggers in almost all regions for both preschool and older children. Across continental Europe, fruits appear to be more common allergens than in the UK, Australia and North America, particularly in older children and this is likely related to tree pollen cross sensitisation. In Asia, seafood including shrimp and shellfish feature commonly, even in preschool children. There was a similar trend in South America although there is less data to support this. Sesame was more frequently listed among common allergens in the Middle East.

Although it was beyond the scope of this survey to examine the relationship between early feeding patterns and food allergy, we collected very basic information on the patterns of early infant formula use, the age at which infants most commonly start complementary foods, and the level of parental concern about allergy prevention in each region. As noted above, there were regional differences in the likelihood that complementary formula milk are used in the perinatal period (but hospital staff prior to discharge) and in the early postnatal period by parents, however there was general uniformity in the age at which other complementary foods are most commonly introduced (typically reported to be between 4-6 months in most regions). As anticipated, parental concern about allergy prevention was more common in the high prevalence regions, but is an emerging issue in some developing regions. We acknowledge that this is qualitative data, based on the experience and knowledge of experts in each region, rather than more accurate population-level census data, and should be interpreted as such.

The burden of food allergy and eczema also has major economic implications for health care provision of specialist allergy services worldwide. Our survey reveals wide inequities in health service provision, even in developed regions where the disease burden is already well recognised. Based on current trends in emerging economies the health burden of food allergy and eczema is anticipated to rise substantially in the next decade, and the greatest impact is likely to be in the more populated regions of the developing world. Currently, emerging economies generally have the fewest trained medical staff with expertise in paediatric allergy. Investment in training, which can take many years, is particularly important as these regions might anticipate a substantial increase in disease burden.

There were also wide variations in the reported access to emergency treatments for potentially life threatening food allergy (anaphylaxis). Experts from many emerging economies report that adrenaline auto-injectors are not readily available. In other countries, cost is reported to be a significant barrier because of lack of government subsidies, even in some highly industrialised countries where a high burden of food allergy is recognised. Many countries still do not have nationally-standardised Food Allergy/Anaphylaxis Action plans, even where auto-injectors are available, with the choice of plan remaining at the discretion of each individual treating clinician. This has implications for the consistency and training for teachers and other community carers supervising children with food allergies. These observations generally suggest the need for greater awareness among governments and health policy makers of the significance and impact of food allergy particularly in children.

In summary, this survey highlights food allergy as a significant paediatric health issue that is likely to increase globally in the coming decade. In some developed economies 1 in 10 infants now have challenge-proven IgE-mediated food allergy, following substantive increase in the last 10 years [, ]. Similar trends are now apparent in the developing countries of Asia and other regions. The survey also reveals the paucity of quality data in many regions, and the need to obtain more accurate information about food allergy prevalence and impact, even in developed countries. Unlike asthma, food allergy has been relatively neglected area of allergy research. This is important to address this as part of promoting awareness of food allergy for health policy and health care system to better anticipate the growing impact and growing need for better services, community education and training to cope with this rising global health issue.

Acknowledgement

Members of the WAO Special Committee on Food Allergy and Nutrition:

Alessandro Fiocchi, Hugh Sampson, Motohiro Ebisawa, Susan Prescott, Wesley Burks, Kirsten Beyer, Gideon Lack, Bee Wah Lee, Kangmo Ahn, Andrea Vereda-Ortiz.

Electronic supplementary material

Competing interests

Authors' contributions

SP coordinated the study, chaired questionnaire design workshops. She also analysed the data and drafted the manuscript. RP provided genera advice for the study, logistic support and advice on the questionnaires and data analysis. KA, DC, JS and SP all assisted with the questionnaire development and manuscript content and review. AF, ME, HS KB and BL reviewed the process and 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
A global survey of changing patterns of food allergy burden in children

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While food allergies and eczema are among the most common chronic non-communicable diseases in children in many countries worldwide, quality data on the burden of these diseases is lacking, particularly in developing countries.

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"30 years ago it [food allergies] did not exist, if it did it was never discussed." 

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"30 years ago it [food allergies] did not exist, if it did it was never discussed." 

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This quote actually comes up multiple times in episode two of Rotten. Whether it be peanut farmers commenting on the issue or restaurant chefs it shows that food allergies are relatively new and are increasing rapidly causing many industries to have to adapt to consumers' needs. A study in Proceedings of the National Academy of Sciences compared the gut bacteria from 15 children in Florence, Italy, with gut bacteria in 14 children in a rural African village in Burkina Faso. It was found that many children in Western societies have less rich in gut bacteria and this may be a reason why food allergies are increasing so sharply in more developed nations (Landau, 2010).

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(CNN) -- Two-year-old Ethan Wily had a cold recently, so at first it wasn't surprising that he started coughing last week after eating some pistachio gelato.

But he started coughing up mucus, and then gasping for air. His parents gave him an antihistamine, but it didn't stop the reaction. By the time the boy's parents brought him to their local hospital, he could barely breathe.

"His face was really swollen. He looked like an alien," said Ethan's father, Preston Wily of Lehi, Utah. "We didn't have any idea an allergy could be so bad."

He said the child had shown only a somewhat mild reaction to peanuts before this.

It seems like more and more children in the U.S. are developing food allergies, and there's data to back that up. The number of kids with food allergies went up 18 percent from 1997 to 2007, according to the U.S. Centers for Disease Control and Prevention. About 3 million children younger than 18 had a food or digestive allergy in 2007, the CDC said.

Scientists are still trying to figure out why food allergies seem to be on the rise, especially in industrialized countries such as the United States. Are children not getting exposed to enough bacteria? Should they eat common allergens such as nuts and shellfish at an earlier age?

A recent study in the Journal of Allergy and Clinical Immunology found that visits to the emergency room at Children's Hospital Boston for allergic reactions more than doubled from 2001 to 2006. Although this is just one hospital, the findings reflect a rise in food allergies seen in national reports, said Dr. Susan Rudders, lead author and pediatric allergist-immunologist in Providence, Rhode Island.

Researchers took a look at thousands of cases in the emergency department. They did not rely on the diagnosis given at that time, but made their own determination about whether an allergic reaction had occurred based on symptoms such as hives. That means the rise in reactions probably did not have to do with an increased awareness among doctors, Rudders said.

This also suggests that previous reported numbers of allergy-related hospital visits are underestimates, Rudders said. For all adults and children in the U.S., there are 30,000 ER visits because of food allergies each year. But that is based on a report that is about 10 years old, and this figure is likely higher now, Rudders said.

Doctors in other parts of the country have also noticed an increase in children coming in with severe food allergies. Dr. Ronald Ferdman at the Children's Hospital of Los Angeles said his hospital has seen a rise of these cases, based on anecdotal evidence.

Dr. Joseph Zorc at the Children's Hospital at Philadelphia cautioned that there may have been situational factors that influenced the Boston hospital's experience -- for example, if another hospital in the area stopped taking cases, resulting in more people at Children's Hospital Boston. But he agreed that food allergies are causing more significant reactions in U.S. emergency departments in general.

One theory is that the Western diet has made people more susceptible to developing allergies and other illnesses.

A study in Proceedings of the National Academy of Sciences compared the gut bacteria from 15 children in Florence, Italy, with gut bacteria in 14 children in a rural African village in Burkina Faso. They found that the variety of flora in these two groups was substantially different.

The children in the African village live in a community that produces its own food. The study authors say this is closer to how humans ate 10,000 years ago. Their diet is mostly vegetarian. By contrast, the local diet of European children contains more sugar, animal fat and calorie-dense foods. The study authors posit that these factors result in less biodiversity in the organisms found inside the gut of European children.

The decrease in richness of gut bacteria in Westerners may have something to do with the rise in allergies in industrialized countries, said Dr. Paolo Lionetti of the department of pediatrics at Meyer Children Hospital at the University of Florence. Sanitation measures and vaccines in the West may have controlled infectious disease, but they decreased exposure to a variety of bacteria may have opened the door to these other ailments.

"In a place where you can die [from] infectious diseases, but you don't get allergy, obesity, asthma, inflammatory bowel disease, autoimmune disease, the flora is different," Lionetti said.

This study only looked at a small number of children, but the findings support the widespread notion of the "hygiene hypothesis" -- the idea that cases of allergies are increasing in number and severity because children grow up in environments that are simply too clean.

"That our immune system is skewed away from fighting infections, and toward fight things that it's not supposed to be fighting, like things in the environment or foods -- that's one thing that people think may be in play," Rudders said.

Still, this is only speculation.

Another theoryis that children need to get exposed to common allergens, such as nuts and shellfish, from a much earlier age, to avoid developing allergies. Some doctors have been recommending waiting until 2 or 3, but Ferdman at Children's Hospital Los Angeles is a proponent of giving kids nuts very early.

An oft-cited 2008 study in the Journal of Allergy and Clinical Immunology compared peanut allergies among Jewish children living in Israel and the United Kingdom. Peanut allergies were more common among the children in the U.K. than in Israel. This was associated with the fact that 69 percent of the Israeli children received peanuts by 9 months of age, compared with 10 percent of the infants in the U.K.

This pitfall, however, is that it was not a controlled experiment, and other factors may have influenced the allergies. More research needs to be done to support giving peanuts and other common allergens to infants. But according to Ferdman, more doctors are questioning recommendations to delay these foods.

These issues about when to introduce allergens are crucial for Preston Wily and his wife, Jen, who are expecting a second child next month. The parents are planning to wait on introducing nuts until their daughter is old enough to get tested for allergens, Preston said.

But hearing about recent research does make the father wonder whether delaying nuts could have influenced Ethan's allergies.

The boy isn't the only one in his peer group with allergies. Ethan goes to a nursery program at church where there's a wall of children's photos with each kid's personal list of food allergies. The teacher has been trained in how to use an epinephrine auto-injector in case of emergency.

Ethan's father knows now to administer an epinephrine injection as soon as the child begins to have a sign of anaphylaxis.

"There are a lot of kids here with allergies -- everywhere. It just seems more common now than when I was little," Wily said.

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(CNN) -- Two-year-old Ethan Wily had a cold recently, so at first it wasn't surprising that he started coughing last week after eating some pistachio gelato. But he started coughing up mucus, and then gasping for air. His parents gave him an antihistamine, but it didn't stop the reaction.