How Do Animals Transmit Diseases Through The Food Chain?
Bacterial Contamination of Beast Feed and Its Relationship to Human Foodborne Affliction
John A. Crump, one Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases , Atlanta, Georgia two Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office, Centers for Disease Control and Prevention , Atlanta, Georgia Reprints or correspondence: Dr. John A. Crump, Foodborne and Diarrheal Diseases Co-operative, Div. of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, MS A-38, Centers for Disease Control and Prevention, 1600 Clifton Rd., Atlanta, GA 30333 (jcrump@cdc.gov). Search for other works by this author on: 1 Foodborne and Diarrheal Diseases Co-operative, Sectionalization of Bacterial and Mycotic Diseases, National Heart for Infectious Diseases , Atlanta, Georgia Search for other works by this author on: 1 Foodborne and Diarrheal Diseases Co-operative, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases , Atlanta, Georgia Search for other works by this author on:
Revision received:
30 May 2002
Published:
01 October 2002
Abstruse
Animal feed is at the beginning of the food safety concatenation in the "farm-to-fork" model. The emergence of variant Creutzfeldt-Jakob disease has raised awareness of the importance of contaminated animal feed, but less attention has been paid to the function of bacterial contagion of animal feed in human being foodborne disease. In the United States, animal feed is frequently contaminated with non-Typhi serotypes of Salmonella enterica and may lead to infection or colonization of nutrient animals. These bacteria can contaminate animal carcasses at slaughter or cross-contaminate other food items, leading to human affliction. Although tracing contamination to its ultimate source is hard, several large outbreaks have been traced dorsum to contaminated animal feed. Improvements in the safety of creature feed should include strengthening the surveillance of animal feed for bacterial contamination and integration of such surveillance with human foodborne affliction surveillance systems. A Gamble Assay and Critical Control Point program should be instituted for the animal feed industry, and a Salmonella-negative policy for feed should be enforced.
Bacterial enteric pathogens are estimated to crusade ∼5 million illnesses, 46,000 hospitalizations, and 1458 deaths in the U.s.a. each year [1]. Food-producing animals (east.chiliad., cattle, chickens, pigs, and turkeys) are the major reservoirs for many of these organisms, which include Campylobacter species and non-Typhi serotypes of Salmonella enterica, Shiga toxin—producing strains of Escherichia coli, and Yersinia enterocolitica [1]. Food-producing animals acquire these pathogens by ingestion. Contamination of beast feed before inflow at and while on the farm contributes to infection and colonization of food-producing animals with these pathogens. Pathogens can then be transmitted through the nutrient chain to humans and cause homo foodborne illness. Concern about the contribution of contaminated animal feed to homo foodborne illness has been heightened by the recent emergence of variant Creutzfeldt-Jakob illness in humans in the Britain. Variant Creutzfeldt-Jakob disease is a prion disease thought to be associated with the feeding of cattle with meat and bone meal derived from sheep infected with transmissible spongiform encephalopathies [two].
The Brute Feed Manufacture
There has been major transformation and intensification of agronomics in the The states and elsewhere during the past 50 years. This has led to increasing reliance on a wide range of manufactured feed products every bit food for animals destined for human consumption. Firms of several types are involved in animal feed production. Rendering plants procedure animals, meat trimmings, and other slaughter by-products into creature feed ingredients. Protein blenders obtain animal and vegetable protein from various sources and mix or redistribute it as animal feed [3]. Feed mills combine ingredients of animate being and plant origin to produce a feed mix suited to animals of a particular species and/or age. For older animals, the combined and basis product of feed mills, sometimes called "ration," may be used as feed, or it may be heat-treated and compressed into formed pellets (effigy 1). For young mammals, protein is used as an ingredient in the industry of milk replacer. Some farms that raise food-producing animals are large plenty to process their own feed and are often referred to as "mixer-feeder" operations.
Figure 1
Effigy 1
The global trade in animate being feed and fauna feed ingredients is substantial and far-reaching. More than 100 countries reporting to the Un Food and Agronomics Organisation recorded importing a total of 2 million tons of meat meal lonely in 1999 [four]. In the U.s., the beast feed industry is big. During the year 2000, 119 million tons of animal feed were produced, and farmers spent ∼$25 billion on animal feed [five]. In 2000, the leading 85 feed companies alone operated >850 mills and had a combined almanac feed product capacity of >54 million tons [6]. Information technology is estimated that in that location are a total of ∼8000 feed mills and 264 poly peptide renderers in the United States [vii]. There is considerable potential for contaminated animate being feed or animal feed ingredients to motility between and within countries. This could result in the widespread and rapid broadcasting of a pathogen to geographically dispersed animal herds —and, in turn, to a range of man food products.
Responsibilities and Legislation Relating To Safety of Fauna Feed
Several federal agencies are responsible for the different components of fauna feed safety. Nether the Federal Nutrient, Drug, and Cosmetic Human action of 1906, as amended, the US Food and Drug Administration (FDA) has the authorization to ensure that animal feed is properly labeled, is safe for its intended use, and produces no human wellness hazards when fed to food-producing animals. In addition, the US Department of Transportation has the authority under the Germ-free Nutrient Transportation Human action of 1990 to prescribe regulations to safely transport creature feed. The United states of america Department of Agriculture'south Animal and Plant Health Inspection Service is responsible for ensuring the health and care of animals and for improving agronomical productivity while contributing to the nation's economy and public wellness [3].
Nutrient-producing animals are the major reservoir of non-Typhi serotypes of Due south. enterica, which cause an estimated 1,412,498 human being illnesses, 16,430 hospitalizations, and 582 deaths annually in the Usa [1]. To illustrate the potential importance of bacterial contamination of animal feed, we review the evidence that contagion of animal feed with non-Typhi serotypes of S. enterica can contribute to the burden of human salmonellosis.
Evidence That Animal Feed is Frequently Contaminated with Bacterial Pathogens
There is considerable bear witness that animal feed is frequently contaminated with foodborne bacterial pathogens. Not-Typhi serotypes of South. enterica were reported in The states poultry feed as early on as 1948 [eight, 9]. Studies from around the earth take documented the presence of S. enterica in a wide multifariousness of animal feeds [10–19].
In the United States, the FDA periodically conducts surveys of feed ingredients and feed. In 1993, the FDA tested for the presence of S. enterica in samples from 78 rendering plants that produced animal protein—based fauna feed and in samples from 46 feed mills that produced vegetable poly peptide—based animate being feed. Southward. enterica were detected in 56% of the 101 animal protein—based samples and 36% of the 50 vegetable poly peptide—based samples [20]. In 1994, the FDA tested 89 finished feed samples collected from feed mills and from farms where animal feed is mixed and found that 25% of the samples were contaminated with South. enterica (D. K. McChesney and G. Kaplan, unpublished data). Surveys done by the rendering industry [21], although limited in their scope, likewise show that animal protein—based beast feed is oftentimes contaminated with Southward. enterica.
Evidence That Contaminated Creature Feed Results in Infection or Colonization of Food Animals
It has long been known that infectious agents can be transmitted to animals through contaminated feed. For example, in 1948, workers in the United Kingdom demonstrated that non-Typhi serotypes of South. enterica could exist transmitted to chicks through feed contaminated by the carrion of infected rodents [22].
Experimental studies ostend that animals given feeds artificially contaminated with not-Typhi serotypes of S. enterica develop colonization or infection with that organism [23]. Furthermore, at that place are numerous examples of outbreaks of Salmonella infections in animals that were traced to contaminated feeds. These include cattle [13, 24, 25], pigs [26], chickens [27], turkeys [28, 29], and mice [30]. Although it is less well documented, bacteria that can cause human being infections but may not cause illness in animals tin also be readily transmitted to nutrient animals via contaminated feed and announced on animal carcasses destined for human consumption [31].
Evidence That Consumption of Infected Or Colonized Food Animals and Their Products Results in Man Illness
It has been well established that bacteria from colonized food animals tin be transmitted to humans through the food supply. Humans become infected when they ingest contaminated meat or poultry products, raw produce contaminated with animal feces (e.g., from contaminated streams used for irrigation), or other foods, particularly uncooked foods, that have been cross-contaminated by contact with uncooked meat or poultry products. For example, Due east. coli O157:H7 is shed in the manure of cattle and contaminates beefiness during slaughter. Eating undercooked hamburger, a widespread practice, can lead to East. coli O157:H7 infection [32, 33]. Campylobacter jejuni, carried by poultry, tin can be spread to many poultry carcasses during the water-bath dressing process. Man infections occur when undercooked craven or cross-contaminated food is consumed [34]. Cattle, poultry, pigs, and other food animals are colonized with non-Typhi serotypes of South. enterica, which have multiple routes into the nutrient supply. Consumption of meat or poultry products contaminated during slaughter leads to human salmonellosis [35, 36]. Consumption of produce grown next to herds of animals colonized with bacterial pathogens may issue in homo infections if the ingather is contaminated with animal carrion [37].
The Foodborne-Affliction Outbreak Surveillance Arrangement of the U.s. Centers for Disease Control and Prevention collects data on foodborne disease outbreaks reported by state and local wellness departments. During 1993–1997, 23% of outbreaks of human foodborne illness in which a food vehicle was identified were attributed to eating meat, dairy, and poultry products [38]. That figure does not include outbreaks in which meat and poultry were among several items possibly linked to illness and outbreaks due to cantankerous-contamination of foods by meat or poultry products. In addition to causing outbreaks of illness, meat and poultry products also contribute to a big proportion of sporadic affliction [39–41].
Outbreaks of Homo Salmonella Infections Traced To Contaminated Animal Feed
Several incidents have been reported in which human affliction was traced back to contaminated animal feed. In 1958, an outbreak of infection with foodborne S. enterica serotype Hadar in Israel was linked to consumption of chicken liver. An investigation of the chicken farm found that os meal fed to the chickens was contaminated with the same serotype of Salmonella [15]. A milkborne outbreak of infection due to S. enterica serotype Heidelberg in England in 1963 resulted in 77 homo illnesses and was traced to a cow with bovine mastitis due to the aforementioned organism. Investigation revealed that meat and bone meal fed to the cow was contaminated with the same organism [42]. During 1968, frozen chickens from a packing station in Cheshire, England, were implicated in a large outbreak of infection with S. enterica serotype Virchow [43]. Investigation showed that the hatchery and the majority of rearing farms that supplied the packing station independent chickens colonized with South. enterica serotype Virchow, and the organism was isolated from feed fed to the chickens [44].
In 1970, S. enterica serotype Agona emerged as a public wellness problem in several countries. In the United states, before 1970, Due south. enterica serotype Agona infection of humans had been reported simply twice, once in 1967 and again in 1968. Past 1972, 507 isolates from humans had been reported, and S. enterica serotype Agona had risen to be the eighth most oft isolated S. enterica serotype. Human infections occurred predominantly in states with poultry-raising operations that used feed derived from Peruvian fish meal. An epidemiological investigation in Arkansas implicated chickens served at a eating place. The chickens were traced to a subcontract in Mississippi that used animal feed derived from Peruvian fish repast. The Peruvian fish meal had been contaminated with S. enterica serotype Agona before the animals were infected [11] and was plant to be the ultimate source of the increase in the number of infections with Due south. enterica serotype Agona in the United States every bit well as in the United Kingdom, Israel, and the Netherlands.
A variety of factors probably contribute to the contempo small number of cases of human being foodborne illness and lack of outbreaks that have been traced to contaminated fauna feed. Although the nutrient vehicle is identified in many foodborne disease outbreaks and although many such outbreaks are attributed to eating contaminated meat or poultry, few investigations trace the source of contamination dorsum through the food supply to the farm of origin. The reasons for this include limited resources and the difficulty of tracing food and animals because of express identification of animals and express farm record-keeping. Furthermore, when epidemiological studies of human foodborne disease outbreaks include an investigation to trace back the source of infection to farms, they rarely extend to microbiological evaluation of the quality of creature feed. In addition, surveillance of creature feed for bacterial contagion is non sufficiently developed nor is it integrated with the surveillance of food-producing animals, food, and human illness to detect outbreaks that may be owing to contaminated brute feed.
Significance of Salmonella Contamination of Animal Feed for Human Foodborne Illness
Because S. enterica serotype Agona was rare in the U.s.a. before its introduction in animal feed, the increase in the number of infections due to this pathogen was detected by human Salmonella surveillance, and its source in creature feed was adamant by a series of studies. It is likely that introductions of more-mutual serotypes occur merely are not detected and remain uninvestigated. Determining the overall contribution of contaminated animal feed to man disease, relative to other sources of contamination, is difficult with currently available data. Similarly, it would be difficult to bear a precise, quantitative take chances assessment of the contribution of contaminated beast feed to human affliction. Yet, bear witness presented here and elsewhere [35, 45, 46] suggests that the contribution of contaminated animal feed to human foodborne illness is probable to be important.
The potential magnitude of the problem can exist examined by studying the increase in S. enterica serotype Agona infection more closely. Since its remarkable expansion after being introduced in animal feed, Due south. enterica serotype Agona has persisted in the United States, resulting in a substantial disease burden. Between 1970 and 2000, there were 28,322 human S. enterica serotype Agona infections reported to the US National Salmonella Surveillance Arrangement (figure 2). Of these, 40% occurred in infants and children aged <x years, and 1.v% of isolates were recovered from the bloodstream, a mark of severe disease [47]. It is estimated that merely 1 in 38 Salmonella infections in humans are reported through the national surveillance system [one]. Therefore, S. enterica serotype Agona has probably caused >1 meg human being illnesses in the United States since it was introduced in brute feed in 1968.
Figure ii
Figure ii
Differences in the S. enterica serotypes isolated from sick humans and the serotypes isolated from animal feed are sometimes used as an argument that contaminated animal feed does non contribute substantially to man foodborne disease. For example, of the 15 serotypes most ordinarily isolated from humans in the United States during 1987–1997 [48], but iii (S. enterica serotypes Enteritidis, Agona, and Montevideo) were also recovered from finished feed, as reported in the 1993 FDA study of finished feed [20]. However, the spectrum of S. enterica serotypes isolated from fauna feed would not be expected to friction match the spectrum of serotypes isolated from sick humans, because organisms multiply in feed after testing, because the infectious doses of dissimilar serotypes of S. enterica are different for animal species and humans, and because multiple sources of Due south. enterica contribute to colonization of animals and infection of humans. Furthermore, only limited microbiologic surveys of creature feed have been done, and, when S. enterica has been isolated, non all isolates take been serotyped. For case, simply 35 (23%) of 151 of South. enterica isolates collected from animal feed in the 1993 FDA survey of finished feed had their serogroups or serotypes adamant [20]. Additional sampling of animal feed would exist peculiarly useful to monitor trends in Southward. enterica contamination. Information regarding such trends could contribute to the cess of the bear on of animal feed interventions and further elucidate the relationship between contaminated feed and human illness. In add-on, the recovery of S. enterica isolates from beast feed indicates failure to control contamination early in the man food concatenation.
Lessons from Typhoid Fever Control in The Usa
The trends in reported human South. enterica infections in the United States for 1920–1998 indicate substantial declines in typhoid fever and the rising importance of not-Typhi serotypes of Due south. enterica [36]. Typhoid fever, which is caused by S. enterica serotype Typhi, was common during the early on 1900s. Humans are the reservoir of Due south. enterica serotype Typhi, which is shed by infected persons in their stool. Typhoid fever was mutual during the early 1900s, simply its incidence declined with the implementation of pasteurization of milk, chlorination of h2o, and safe canning practices. These interventions controlled the entry of human stool from the human food and water supply. Since the mid-1900s, non-Typhi serotypes of Southward. enterica take emerged every bit a major crusade of human foodborne illness. Food-producing animals are reservoirs for non-Typhi serotypes of S. enterica, which infected animals shed in their feces [49]. A sanitary revolution in food-animal production could pb to a pass up in the incidence of non-Typhi salmonellosis in humans that would be similar to the turn down in the incidence of typhoid fever subsequently the early 1900s. Such a decline would be possible if contagion of animal feed, also every bit human nutrient and water, by not-Typhi serotypes of S. enterica from animals was reduced or eliminated.
"Farm-To-Fork" Control of Man Foodborne Illness in Sweden
Sweden has a comprehensive so-chosen "farm-to-fork" Salmonella surveillance and command system that recognizes the importance of each stride in the feed-animate being-food-human chain. Notably, Sweden implemented a Hazard Analysis and Critical Control Point (HACCP) program for animal feed in 1991. Approximately 7000 samples from feed mills are analyzed annually, and twoscore% of samples are obtained before heat treatment. On average, during 1995–1999, 5 samples per yr that were collected at critical control points after heat treatment were institute to be positive for non-Typhi serotypes of South. enterica. Detection of any such positive sample generates more-all-encompassing sampling and corrective activity. Sweden's integrated surveillance of feed, animals, food, and humans allows investigators to track trends and monitor the bear upon of interventions [50]. This multifaceted surveillance and control program has been highly successful: it has virtually eliminated S. enterica from domestically produced animal feed [51] and ruby and white meat [52], and it has been associated with a decline in the almanac incidence of domestically acquired homo salmonellosis from 14 cases per 100,000 population in 1991 to 8 cases per 100,000 population in 2000 [50, 53].
Addressing Safe Animal Feed in The United States
The 2001 Nutrient Safety Strategic Program of the President's Council on Food Safe calls for condom command efforts at every phase "from subcontract to fork," including enhancement of national, systematic monitoring of food brute diseases and testing of feeds and feedstuffs for microbial, chemical, and other hazards that pose a food prophylactic hazard [54]. Three major measures are needed to address animal feed prophylactic in the United States. Outset, surveillance of animal feed for microbial contagion is necessary, which must be integrated with surveillance systems for food animals, nutrient, and humans. This mensurate volition monitor and meliorate our understanding of the period of feed contaminants through the food chain, volition inform policy, and will rail the affect of interventions. 2d, a HACCP plan is needed in the fauna feed industry to minimize Salmonella contamination by identifying and controlling sources of feed contamination. HACCP is an approach that applies 7 principles to place, rectify, and prevent issues in food production that could result in foodborne illness. It was initially developed 30 years ago to reduce the gamble of contamination of food for consumption by astronauts [55]. Finally, a Salmonella-negative standard for fauna feed should be implemented. A Salmonella-negative policy for animal feed was appear past the FDA in 1991, but it has not been implemented or stringently enforced.
Microbial contamination of animal feed is a significant potential pathway for entry of pathogens into the human being food supply, and now, there is no comprehensive program that addresses information technology in the United states food safety program. Ensuring that creature feed is free of bacterial pathogens should help reduce homo foodborne illness.
Acknowledgments
We give thanks Dr. George Graber, Segmentation of Animal Feeds, Function of Surveillance and Compliance, Eye for Veterinary Medicine, Food and Drug Administration, for his comments and suggestions.
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