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Institute of Medicine (US). Improving Food Safety Through a One Health Approach: Workshop Summary. Washington (DC): National Academies Press (US); 2012.

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Improving Food Safety Through a One Health Approach: Workshop Summary.

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Infections caused by microbes that contaminate the food supply are a frequent reminder of the complex food web that links us with animal, plant, and microbial populations around the world. In the United States, an estimated 46 million foodborne infections occur each year, along with 250,000 hospitalizations and 3,000 deaths (Scallan et al., 2011a, 2011b). While all are at risk, the consequences are the most severe in the vulnerable populations of the very young, the elderly, and those with compromised immune systems. Of the many pathogens that can contaminate food, some, like norovirus and Salmonella serotype Typhi, are sustained in human reservoirs and contaminate the food supply via the excreta of infected humans. Many others are sustained in animal reservoirs and contaminate our food supply because they are present in the flesh, milk, or eggs in the living animal, or because they are in the excreta of infected animals that subsequently contaminate the foods we eat. Some pathogens persist in the environment, or in multiple hosts, and can contaminate the foods we eat via pathways that reflect the variety of ecosystems that make up our food supply.

Food safety depends on understanding these pathways well enough to prevent them. In the United States, substantial progress during the 20th century in animal disease control efforts has greatly reduced the foodborne infections related to zoonotic diseases such as brucellosis and bovine tuberculosis (Tauxe and Esteban, 2006). At the same time, an increasing number of microbes have been recognized that can cause serious illness in humans, but rarely cause illness in the animals that carry them. The presence of these microbes is thus not apparent to the rancher or farmer, and the animal appears entirely healthy on inspection at slaughter; addressing these microbes requires a different prevention paradigm based on reducing levels of microbial contamination throughout the food chain. This effort starts on the farm or ranch where animals are raised, with attention to fodder, water, and biosecurity there. An early success was the virtual elimination of the parasite Trichinella from the nation's swineherds, and the prevention of pork-related trichinosis in people, through attention to the fodder fed to pigs (Schantz, 1983). Recent outbreaks show that plants can also be contaminated with human pathogens on the farm, through manures, water, and wild animal incursions (Lynch et al., 2009). The need to reduce and prevent contamination continues through harvest and slaughter, subsequent processing, and the food preparation steps in the final kitchen (Figure A14-1). Indeed, reducing the number of foodborne infections by making food safer is the result of efforts by many partners in the food safety system.

An illustration of the food production chain from farm to table


The food production chain from the farm to the table. SOURCE: Adapted from Tauxe (2006) Table 3-1, page 73. (accessed April 10, 2012).

Concentrated animal production has parallels with human urbanization, like the challenge of providing water, food, and fecal disposal for thousands of individuals every day. Just as the spread of many infections in human cities depends critically on treating the drinking water, and collecting sewage and keeping it out of the food and water supplies, and immunizing ourselves against many infections, so will the health of animals raised in virtual cities depend on attention to the safety of their water and food supplies, coupled with selective immunization.

New Pathogens and Problems

New food-borne pathogens emerge when previously unrecognized pathogens are identified and are linked to foodborne transmission from the beginning, or when foodborne transmission is documented for pathogens that are already well known. The list of foodborne agents that have emerged in the past three decades includes bacteria, viruses, parasites, biotoxins, and a prion (Table A14-1). They often emerge from animal reservoirs; 70 percent are sustained in animal populations and affect humans only incidentally. Many were identified in the course of outbreak investigations, when both their pathogenicity and association with food could be determined. Some common bacterial foodborne pathogens are adapted to particular reservoirs, making targeted control strategies feasible (Table A14-2). For example, Campylobacter are adapted to birds and particularly to poultry, among which they are commensal intestinal flora, and contaminate poultry meat by cross-contamination at slaughter. Some strains can also colonize cattle and are transmitted via raw cows' milk. Shiga toxin–producing E. coli O157:H7 can colonize the peri-rectal glands of ruminants and transfer from hides and feces to meat during the slaughter process. Strains of Salmonella serotype Enteritidis that spread around the world in the 1980s colonize the peri-ovarian tissues of the hen's reproductive tract, where they come in contact with the egg yolk as it forms, and contaminates the internal contents of normal-appearing eggs. If the egg is fertilized, these Salmonella then colonize the reproductive tissues of the chick embryo and reach the next generation, while in the unfertilized table egg, Salmonella can multiply in the yolk and infect the eater of a less than fully cooked egg.

TABLE A14-1. Major Pathogens Identified as Foodborne Since 1970.


Major Pathogens Identified as Foodborne Since 1970.

TABLE A14-2. Major Food-Animal Reservoirs for Human Foodborne Bacterial Pathogens.


Major Food-Animal Reservoirs for Human Foodborne Bacterial Pathogens.

The reservoirs where these pathogens persist, and the pathways by which they reach humans, are revealed in outbreak investigations. By epidemiological methods, the illnesses in an outbreak can often be associated with consuming a particular food, the food vehicle of infection. Between 2003-2008, the food vehicles identified in 1,565 outbreaks reported to the Centers for Disease Control and Prevention (CDC) with specific food vehicles are a broad spectrum of animal- and plant-derived foods (Figure A14-2). The list of implicated foods is regularly expanded as new ones are identified in outbreak investigations. Between 2006 and early 2012, 15 new specific food types were identified as food vehicles in outbreaks affecting the United States (Table A14-3). It is curious that while many of the pathogens have animal reservoirs, many new food vehicles are plant derived. This includes plant-derived processed foods, like peanut butter, peanut paste, and spinach powder; spices such as black and white pepper; tree nuts; and fresh produce items.

A pie chart showing the distribution of illnesses by food type reported to the CDC


Distribution of illnesses by food type in 1,565 foodborne outbreaks caused by a single food type and reported to CDC's National Foodborne Disease Outbreak Surveillance System, 2003-2008. SOURCE: CDC, unpublished data.

TABLE A14-3. Fifteen New Food Vehicles Identified from 2006 Through March 2012 in Foodborne Outbreaks Affecting the United States.


Fifteen New Food Vehicles Identified from 2006 Through March 2012 in Foodborne Outbreaks Affecting the United States.

The identification of new food safety problems has been accelerated by important improvements in surveillance and response. These new surveillance tools capture information about infections in humans as well as in animals and contamination of foods, providing important information that is integrated across sectors.

In the United States, public health surveillance that tracks the frequency of human infections with specific pathogens has expanded greatly since 1996 to capture different kinds of information that is needed for making public health decisions. FoodNet, the network for active surveillance of infections often transmitted through foods in 10 sentinel sites around the country, led by the CDC and supported by the Food Safety and Inspection Service of the U.S. Department of Agriculture (USDA) and the Food and Drug Administration (FDA), provides accurate tracking of what is diagnosed in human clinical laboratories, overcoming local variation in reporting requirements (Scallan, 2007). FoodNet data are fundamental to estimating the total number of illnesses that occur and to tracking trends over time. By 2010, FoodNet data showed that the incidence of E. coli O157 infections had declined by 44 percent since the baseline period of 1996-1998, that of Campylobacter by 27 percent, and that of Listeria infections by 38 percent, while those caused by Salmonella had not decreased at all (Figure A14-3) (CDC, 2011e). The substantial progress made in reducing E. coli O157, Campylobacter, and Listeria infections between 1996 and 2003 was largely the result of improvements in sanitation at slaughter and meat processing for meat and poultry. There has been little progress in more recent years.

Line graph showing trends in food-borne diseases from 1996-2010


Relative rates of laboratory-confirmed infections with Campylobacter, Shiga toxin–producing Escherichia coli O157, Listeria, Salmonella, and Vibrio, compared with 1996-1998 rates, by year, in the United States during 1996-2010, based on data from (more...)

A second surveillance enhancement is PulseNet, the national molecular subtyping network for bacterial foodborne pathogens, which has enhanced detection of outbreaks (Swaminathan et al., 2001). In each state, clinical laboratories send strains of Shiga toxin–producing E. coli (STEC), Salmonella, and Listeria monocytogenes isolated from ill persons to the public health laboratories where they are subtyped by molecular methods and added to a national database. To find clusters of infections that may be related, the database is scanned looking for surges in particular subtypes. Each state can review its own data and national data, and the CDC looks for multistate increases. The same laboratory methods are applied by the USDA to Salmonella and E. coli isolated from animals and meats, and by FDA to isolates from other foods, so that PulseNet can explore possible connections between animal reservoirs and foods, in addition to clusters of human infections. Epidemiological investigation of such clusters may reveal an exposure that the cases all have in common, such as eating a particular food, contact with an unusual pet, or travel to a particular place. The growth of this surveillance system, which now adds patterns of 50,000 isolates a year to the national database, and the increasingly sophisticated epidemiological approach to the clusters identified have led to a dramatic increase in the number of multistate outbreaks detected and investigated.

A third surveillance enhancement tracks the frequency of antimicrobial resistance in enteric bacterial pathogens (CDC, 2011c; Holmes and Chiller, 2004). The National Antimicrobial Resistance Monitoring System (NARMS) for enteric bacteria also depends on the submission of isolates to public health laboratories. For NARMS, a systematic subset of those isolates is tested at the CDC to determine their resistance to a panel of antimicrobial agents. In parallel, isolates from retail meats are tested at FDA, and isolates from animal carcasses are tested in USDA laboratories. These three arms of NARMS provide ongoing monitoring of the progression of resistance to specific agents that are used in agriculture and human health and have been important to promoting prudent use and regulation.

Finally, the National Outbreak Reporting System (NORS) collects reports of outbreaks of foodborne and waterborne illnesses that are investigated by public health departments, providing the summary information about frequency by pathogen and vehicle type (CDC, 2011d). In 2009, this system was expanded to include outbreaks of gastroenteritis caused by contact with animals and by person-to-person transmission. NORS thus captures information about a range of transmission events likely to lead to gastrointestinal disease.

Improving Preharvest Prevention: The Animal Sector

Long-term prevention of foodborne disease depends on actions of many partners in the food production chain, stretching from farm to table. Some critical prevention measures include quality assurance programs at egg farms; safe agricultural practices for produce farmers; inspection systems at meat processing plants; use of pasteurization, canning, cooking, irradiation, and other steps to kill pathogens in food processing; and food safety education for consumers and staff in the food industry. Much of the progress has been focused on safer processing of animals and plants after they are harvested, with less emphasis on the prevention that can be achieved before harvest or slaughter. Making food safer in the future will depend on reducing preharvest contamination.

Outbreak investigations show that contamination events often start with problems in production, that is, while growing the plants we harvest or raising food animals. Many factors throughout all stages of the food production and distribution system can affect food safety. For meat products, what happens on farms, in feedlots, during transport and lairage before slaughter, as well as during slaughter and further processing can have a major effect on human health (Miller and Griffin, 2012). Domesticated food animals can also serve as a source of contamination of nearby produce-growing fields and can lead to human infection through direct contact at petting farms and mail order hatcheries. Preventing such infections also means reducing the carriage and spread of human pathogens among live animals.

Bacterial and other microbial pathogens in animal feces can contaminate the environment in which animals are raised, where they roam, and where they are kept while awaiting slaughter. Because animal hides and intestinal contents may have pathogens, efforts at slaughter are focused on cleaning the hides, removing them with care, and preventing the contamination of meat with intestinal contents. Poultry farms with large populations of birds are a setting where infectious agents can spread rapidly. When birds are slaughtered, hot water dips help remove feathers but can spread intestinal contents to subsequent carcasses. Campylobacter jejuni/coli, a common cause of illness in the Unites States, contaminates at least 40 percent of chicken breasts at retail (FDA, 2011). As a result, poultry is a major source of Campylobacter infections in humans. People become infected by consuming inadequately cooked poultry or other foods that become cross-contaminated via contact with poultry. Even infants riding in shopping carts containing raw poultry are at increased risk (Patrick et al., 2010).

Control measures for Campylobacter focused on slaughter sanitation; chlorinating water baths and chiller tanks have been associated with a decrease in Campylobacter infections in the United States in the late 1990s, although there has been no progress since 2002 (Figure A14-3). In New Zealand, similar control measures implemented at slaughter led to a dramatic 50 percent decline in campylobacteriosis in 2008 and a parallel decline in Guillain-Barre syndrome cases (Baker et al., 2012; Sears et al., 2011). In Scandinavia, a new control strategy is “test and freeze,” developed first in Iceland and then adopted in Norway and Denmark, in which flocks are tested preslaughter for the presence of Campylobacter (Tustin et al., 2011). Birds from flocks that have Campylobacter must be frozen after slaughter, which reduces the level of Campylobacter contamination, while birds from poultry farms without Campylobacter can be sold fresh at a premium price. This provides farmers with an economic incentive to reduce Campylobacter contamination and may be a model for how to incentivize preharvest food safety measures. To make further progress, short of irradiating poultry, control measures will need to include a preharvest focus (Wagenaar et al., 2008). Such measures may include chlorinating the drinking water, probiotics, and vaccination (Wagenaar et al., 2008). In Denmark, field evaluations show that putting insect screens on henhouses can lead to a 70 percent decrease in Campylobacter flock prevalence (Hald et al., 2007).

Escherichia coli O157:H7 infection has emerged as an important cause of human illness ranging from simple diarrhea, to hemorrhagic colitis, to hemolytic-uremic syndrome, characterized by hemolytic anemia, thrombocytopenia, and renal injury (Griffin and Tauxe, 1991; Rangel et al., 2005). It was first recognized as a human pathogen in foodborne outbreaks associated with ground beef in 1982 (Riley et al., 1983). In 1993, after a large multistate E. coli O157 outbreak was linked to undercooked ground beef patties sold from a fast-food restaurant chain, E. coli O157 became broadly recognized as an important human pathogen (Bell et al., 1994). In 1994, officials at the USDA declared E. coli O157:H7 an adulterant of ground beef, so that finding these bacteria in ground beef resulted in its mandatory recall, and then implemented a new inspection procedure for beef carcasses based on hazard analysis critical control point strategies. In 2002, after a large multistate outbreak and recall of ground beef, regulators and slaughter and beef grinding companies focused more intensive effort on preventing the contamination of ground beef itself, including increased focus on hide removal, testing beef trim before it reached the grinder, and holding ground beef lots until they were found not to be contaminated. These efforts helped to reduce the contamination of ground beef and in turn may have led to the decrease in laboratory-confirmed E. coli O157:H7 cases measured in the U.S. FoodNet active surveillance system (See Figure A-14-3) (CDC, 2011e). However, beef remains the most frequently identified vehicle for E. coli O157:H7 infections, followed by produce-associated outbreaks (CDC, 2010a). Reducing these infections further will depend on preharvest interventions to decrease the shedding of E. coli O157 by cattle before they come to slaughter. E. coli O157 is common among cattle, particularly in the summertime, and reducing carriage may be achieved using a suite of interventions, including vaccines (two are currently available for evaluation), probiotics, and bacteriophage treatments, and microbicidal agents such as sodium chlorate (Loneragan and Brashears, 2005). Leveraging the need for safer meat with economic incentives for lower contamination rates in cows has yet to be achieved.

Better prevention can occur with multifaceted on-farm preharvest control measures and with test and diversion strategies. One example is egg safety in the United States. Shell eggs and poultry are common sources of human Salmonella serotype Enteritidis (SE) infections, which cause 6,000 to 7,000 laboratory-confirmed illnesses annually in the United States. These strains of SE increased dramatically in the 1980s in the United States and many other countries, causing egg-associated infections because they can silently infect the ovaries of healthy hens, resulting in internally contaminated eggs (St. Louis et al., 1988). In the United States, initial control measures included use of pasteurized liquid egg product for high-risk foods and institutions, refrigeration during transportation and sale, and voluntary programs of flock-based interventions. These egg safety programs typically included obtaining SE-free chicks from hatcheries, preventing spread among flocks by biosecurity, cleaning and disinfection, and testing henhouse environments with diversion of eggs to pasteurization if SE was found; these programs were associated with significant decreases in SE infections (Mumma et al., 2004). However, by themselves they are not enough. In July 2010, a nationwide increase in SE infections was identified in the most common pulsed-field gel electrophoresis (PFGE) pattern (CDC, 2010b). In PulseNet, this common PFGE pattern accounted for 30 to 40 percent of all SE isolates. In 2010, approximately 1,900 more laboratory-confirmed illnesses with this outbreak strain were reported than were expected; adjusting for underreporting approximately 55,000 illnesses likely occurred. Epidemiological investigations focused on 29 restaurant and event clusters in 11 states; egg suppliers were identified for 15 of these clusters. A single producer in Iowa was identified as a supplier of shell eggs in 92 percent of clusters with completed tracebacks, and a second Iowa producer supplied eggs to at least one cluster. The first producer was found to sell feed to the second; both producers shared the same source of pullets. Inspection of these producers identified 13 environmental samples matching the outbreak strain and found substantial potential for egg contamination. These producers recalled more than 550 million shell eggs in August 2010. Also in 2010, a year after publication, a new regulation titled “Prevention of Salmonella Enteritidis in Shell Eggs During Production, Transportation and Storage” was implemented for producers with 50,000 or more laying hens (FDA, 2009). The shell egg rule mandates what had previously been voluntary in egg safety programs to prevent SE contamination of eggs during production; to prevent further growth of SE during transportation and storage of shell eggs; and to require recordkeeping of testing results for SE. Shell eggs remain an important vehicle for SE infection, and this new rule is an important step toward enhancing egg safety.

A similar program was launched in the United Kingdom in 1998 to reduce SE infections. In the “British Lion” program, egg producers implemented measures voluntarily; including on-farm biosecurity, cleaning and disinfecting henhouses between flocks, vaccinating hens against SE, and monitoring them for the presence of infection (see Eggs from those producers were stamped with a red lion rampant and were thus differentiated from other eggs, including those imported from continental Europe. As with the Scandinavian Campylobacter program, this aligned the consumers' desire for local and safer eggs to support the cost of the flock-based control programs. Following this launch of this control program, the incidence of SE infections in the United Kingdom fell substantially (Figure A14-4).

A line graph showing the number of reported cases of salmonellosis in England and Wales


Number of reported cases of salmonellosis, by serotype, England and Wales, 2000-2010. SOURCE: Health Protection Agency, (accessed April 8, 2012) (more...)

SE infections are transmitted through chicken meat as well as through eggs. Recent sampling of retail chicken breasts as part of NARMS indicated that 2 percent are contaminated with SE (FDA, 2011). This is occurring despite efforts to improve slaughter hygiene and inspection processes. As with Campylobacter, it is likely that making further progress with poultry-associated SE and other types of Salmonella will require on-farm preharvest interventions. Indeed, it is notable that, despite the extensive efforts to reduce flock contamination of egg-laying flocks, virtually nothing similar has been done with broiler flocks. And as with Campylobacter, there is evidence that on-farm control measures for Salmonella may be effective. For example, parent flock vaccination, combined with hatchery sanitation and on-farm biosecurity in production flocks was recently documented to greatly reduce the Salmonella contamination of poultry carcasses at slaughter (Berghaus et al., 2011; Dorea et al., 2010). This suggests that Salmonella in poultry flocks may often be vertically acquired and that a focused program to reduce contamination in parent flocks may have value, although questions remain about the impact of concurrent immunocompromising infections on immune response to vaccines in chicken flocks (Hoerr, 2010). Aligning the benefit of less contaminated poultry meat with the cost to the producer of taking such measures could lead to their adoption.

Another emerging challenge for food safety officials is multidrug- resistant Salmonella infections. In the United States, many outbreaks of multidrug-resistant Salmonella infections have been investigated in recent years. Because infections with multidrug-resistant Salmonella may be associated with an increased risk of hospitalization and antibiotic treatment failure, these illnesses are especially concerning (Anderson et al., 2005). In 2011, an outbreak of 136 laboratory-confirmed infections with Salmonella serotype Heidelberg infections were identified in 32 states (CDC, 2011b). Epidemiological and traceback investigations linked these illnesses with consumption of ground turkey from a common production facility, resulting in a recall of 36 million pounds of ground turkey, the largest USDA Class I recall in U.S. history. Antibiotic resistance profiles of patient and environmental samples matched an identical multidrug-resistant pattern, which included several clinically relevant antibiotics. These outbreaks of multidrug-resistant salmonellosis highlight the importance of preharvest food safety programs to reduce the need for antibiotic usage in animals, and for considering further measures to reduce contamination with multidrug-resistant Salmonella.

Traditional animal disease control measures, such as those for trichinosis and brucellosis, have had important impacts on the reduction of infections. Presently, concern exists for agents that may be less pathogenic in animals but can cause serious human disease. Often these animals appear asymptomatic, but they can be shedding bacteria and other agents that cause disease in humans. One example of a recurring public health issue involving human illness linked to contact with asymptomatic animals is the problem of human Salmonella infections linked with live poultry (chicks, ducklings, chickens, ducks, turkeys, and geese) (Loharikar et al., 2012). Since 1990, at least 35 such outbreaks of human Salmonella infections have been reported in the United States (CDC, 2011a). Various Salmonella serotypes have been associated with these outbreaks, and specific outbreak strains have been linked to single mail-order hatcheries over several years (CDC, 2006a). These illnesses are especially severe among young children who account for the majority of infections. Chicks and ducklings appear healthy and clean, but their bodies and areas where they live and roam can be contaminated with Salmonella, leading to human illness. For example, since 2004, Salmonella serotype Montevideo infections having the same genetic fingerprint profile have been reported annually and linked to a single mail-order hatchery. Starting in late 2007, this hatchery implemented numerous interventions to reduce Salmonella transmission in its birds, including biosecurity measures and introduction of an autogenous vaccine specific to the outbreak strain. As of 2011, these measures reduced, but did not eliminate, corresponding human Salmonella infections associated with live poultry from the implicated mail-order hatchery.

Human contact with animals of many types and in various settings carries a risk of infectious illnesses. Petting zoos and similar venues that feature animals like goats, sheep, cattle, pigs, and poultry can be particularly risky for high-risk individuals including children, elderly, and those with weakened immune systems, especially when handwashing facilities are also inadequate. Since the 1990s, more than 150 outbreaks linked to animals displayed in public settings have been reported in the United States (CDC, 2011a). Cultures of specimens from patients, animals, and animal environments have yielded the outbreak strain in numerous investigations. These animals usually appear healthy but can be shedding zoonotic pathogens that also contaminate the areas where the animals are displayed, leading to infections in people who do not directly contact an animal (Friedman et al., 1998). Strategies that reduce contamination of live animals used for food could also help prevent transmission by direct contact.

Improving Preharvest Prevention: The Plant Sector

Large outbreaks of human infections linked to fresh produce consumed after minimal processing have been more frequently identified in recent decades (Lynch et al., 2009; Sivapalasingam et al., 2004). There is little that consumers can do to protect themselves because these foods are not cooked, washing them has little effect on contamination, and the contamination itself is undetectable, so it is particularly important to prevent such contamination from happening in the first place.

Outbreak investigations have revealed direct links between produce and animal reservoirs. Several recent produce-associated outbreaks have followed wildlife intrusion into growing fields or fecal contamination from nearly animal production facilities that likely led to produce contamination. In 2006, a multi-state outbreak of approximately 200 illnesses with E. coli O157:H7 infection from 26 states was linked to the consumption of fresh spinach (CDC, 2006b). An environmental investigation identified E. coli O157:H7 isolates with a PFGE pattern indistinguishable from the outbreak strain in samples obtained from river water, cattle manure, and wild pig feces in and around a field used to grow one brand of spinach from the implicated lot (Wendel et al., 2009). The investigation team also found evidence that wild pigs had been in the spinach fields (FDA, 2006). In August 2006, FDA launched a lettuce safety initiative to address recurring outbreaks of E. coli O157 infections. After this outbreak, the initiative was expanded to include all leafy greens.

An instructive outbreak of produce-related illness linked to wildlife intrusion was identified in Alaska in 2008, when there was a sharp increase in the incidence of Campylobacter infections around Anchorage (Gardner et al., 2011). Raw peas had been suspected as the source of a small cluster in 2005, and a larger increase in 2008 was rapidly shown to be associated with eating raw peas, from one local farm, which was adjacent to a nature preserve for the Sandhill Crane, Grus canadensis. Peas were harvested mechanically and washed in a tank without added chlorine. After harvest, shelled peas were bagged and labeled with directions for blanching, though they were often repacked in bags without this advice, and eaten without blanching. Cranes were observed feeding on peas in the growing fields at the time of harvest, and molecular subtyping studies confirmed that some Campylobacter bacteria isolated from patients were indistinguishable from strains isolated from peas, and from crane feces. Harvest was halted that year, and resumed the following year with scarecranes in the fields, chlorination in the wash water, and clearly visible advice on the packages to blanch the peas before eating. To date, the outbreak has not recurred. This investigation shows that wild birds may be an underrecognized source of produce contamination, and that some basic prevention measures may make it safer. Animal intrusions have also been suspected as the likely source of contamination of apples in cider orchards by cattle or deer with E. coli O157 and Cryptosporidium (Besser et al., 1993; CDC, 1997), strawberries by deer with E. coli O157 (Laidler and Keene, 2012), and lettuces by wild animals with Yersinia pseudotuberculosis in Finland (Nuorti et al., 2004).

Water contaminated with animal feces and then used to irrigate plants has also been a route connecting plant production with animal reservoirs. In 2006, an outbreak of approximately 80 persons with E. coli O157:H7 infection was linked to lettuce served at locations of a Mexican-style fast food restaurant chain in Iowa and Minnesota (CDPH, 2006). An investigation identified dairy farms near lettuce fields in California that provided lettuce to the restaurants where ill persons had eaten. Environmental samples from the dairy farm and water in soil samples in close proximity to the growing fields identified E. coli O157 indistinguishable from the outbreak strain. The irrigation system was connected to the dairy wastewater blending and distribution system, with inadequate backflow protection devices, presenting a possible route for contaminated water to be used on fields adjacent to the lettuce-growing fields associated with this outbreak. These findings indicated that the nearby dairy farm was the likely source of this outbreak. Contaminated water used for irrigation or for processing has been suspected as the likely source of contamination of outbreaks of E. coli O157 infections traced to lettuce (Hilborn et al., 1999), and tomatoes, mangoes, and cantaloupes with Salmonella (Bowen et al., 2006; Greene et al., 2008; Hedberg et al., 1999; Sivapalasingam et al., 2003).

Sprout-associated outbreaks represent a special scenario, in which the presence of even a few bacterial cells on seeds can be amplified to a large number as a result of the sprouting process itself (Taormina et al., 1999). As seeds are a raw agricultural commodity rather than a food, they may not be expected to be free of pathogens, and their transformation into a food (the sprouts themselves) actually increases the risk, unless special measures are taken to decontaminate the seeds before sprouting and to regularly test the sprouting environment for contamination.

Observations of the biology of human pathogens on plants suggest that interactions between pathogens and produce may sometimes lead to internalization of the pathogen into edible parts of the plant, where it cannot be washed off or eliminated by surface treatments (Berger et al., 2010; Erickson, 2012). This internalization can occur via different mechanisms. Human bacterial enteric pathogens can enter cut or bruised surfaces of leaves and fruit and then multiply in the interior. Air spaces in many fruits contract with a sudden decease in temperature, and this contraction can draw in water and pathogens from the outside of a fruit, as shown for apples, mangoes, and tomatoes (Burnett et al., 2000; Penteado et al., 2004; Rushing et al., 1996). The interactions may be active as well as passive. In the case of sprouts, grown hydroponically without accompanying soil flora, E. coli O157 and Salmonella present in seeds can enter via the young sprouts' root hairs and are rapidly found thoughout the entire plant (Itoh et al., 1998; Jaquette et al., 1996). The interactions may be complex. For example, in the dark, Salmonella distribute randomly over the surface of fresh lettuce leaves, but when light stimulates photosynthesis, they concentrate at the stomatal openings that are the respiratory pores on the leaf, as though drawn to products of photosynthetic metabolism (Kroupitski et al., 2009). Some pathogens may be able to manipulate the stomata directly, with a type 3 secretion system that targets the guard cells that ordinarily hold stomata closed in the presence of Gram-negative flagellated bacteria (Saldaña et al., 2011).

These observations raise the question of whether some enteric bacterial pathogens have a life cycle with plant as well as animal hosts. An enteric organism that colonizes herbivores and that also can enter and persist in the plants the herbivores eat gains ready access to the next generation of herbivores. Transfer events from herbivore to plant and plant to herbivore are frequent in prairie or pasture. If enteric pathogens cycle between animal and plant hosts, then the omnivorous human can encounter them on both sides of the cycle. This suggests that, just as food animals may need safer water, fodder, and environments, so food plants may be safer with further attention to the water, soil amendments, and environments used to grow them.

Emerging Foodborne Infections Around the World

Major changes in the global food trade in the past several decades have led to a transformation in the patterns of food production (Florkowski, 2008). The food we eat is sourced from around the globe and distributed over larger distances than ever before. This global trade provides opportunities for exporting countries to earn foreign exchange and drives increases in the standard of living in developing countries. Not only have supply chains become longer, but also the global trade in food has become more specialized. Higher-income countries export grains and processed food to low- and middle-income countries, which in turn export labor-intensive horticultural and fishery products to higher-income countries. Finally, there has been a move toward integration and consolidation of agriculture and food industries, and large corporations have ownership and control across all stages of food production and distribution.

Changes in the globalization of the food trade have important implications for food safety (Tauxe et al., 2010). More imported foods and food ingredients means we depend on food safety systems in other countries. Centralized production of foods means when a problem occurs, it can lead to a widespread outbreak. In this setting, a contaminated food can rapidly cause a geographically widespread or “dispersed scenario” type of foodborne disease outbreak. In these outbreaks, there are a small numbers of cases in many jurisdictions, typically detected by lab-based subtype surveillance, leading to a multistate or country investigation, and they are usually a result of an industrial contamination event with broad implications. Effective investigations of these types of outbreaks are key to reducing the burden of foodborne disease as we identify food vehicles and factors that lead to outbreaks.

A recent example of a dispersed scenario outbreak was an outbreak of Salmonella serotype Montevideo infections in the United States associated with salami products from one company made with contaminated imported black and red pepper (Julian et al., 2010). A total of 272 cases were identified from 44 states and the District of Columbia during 2009 and 2010. In a multistate case-control study, consumption of salami was associated with illness. The outbreak strain was identified in salami products, one company facility environmental sample, and sealed containers of black and red pepper used to produce the salami products. Pepper tracebacks revealed that the pepper originated from Asian countries, although the locus of contamination was not determined.

Multicontinental outbreaks have been recognized when the same subtype of a pathogen is recognized as a simultaneous source of infection in widely separated populations as a result of global trade in foods and feeds. Detecting such events depends on using the same subtyping strategies in many countries, and on collaboration and information sharing when possible links are recognized, and it is likely that many are missed. For example, a global pandemic of Salmonella serotype Agona in the early 1970s was the result of contaminated anchovy meal shipped from Peru and used in chicken feed around the world. This was first recognized as a restaurant-associated outbreak in Arkansas traced back to one poultry farm and was subsequently linked to sudden increases in Salmonella Agona infections in many countries (Clark et al., 1973). In 1995, simultaneous outbreaks of sprout-associated Salmonella serotype Stanley infections in Arizona, Michigan, and Finland were all linked to seeds from one shipper in the Netherlands, who obtained and blended seeds from many other countries (Mahon et al., 1997). In 1998, a savory snack produced in Israel caused Salmonella serotype Typhimurium infections in the United Kingdom and North America and was subsequently shown to be a common source of infections in Israel itself; contamination had apparently occurred at the factory where the snack was made (Killalea et al., 1996; Shohat et al., 1996). In 2001, contaminated peanuts from China caused outbreaks of Salmonella serotype Stanley infections in Canada, the British Isles, and Australia (Kirk et al., 2004). In 2010, semi-dried tomatoes from Turkey were recognized as the source of similar hepatitis A virus infections in Australia, France, and the Netherlands (Donnan et al., 2012; Petrignani et al., 2010). These events are surely the tip of the proverbial iceberg and are likely to become more frequently recognized as subtype-based surveillance networks increase worldwide (Swaminathan et al., 2006). They illustrate how a foodborne pathogen arising in one part of the world can be rapidly disseminated if it is introduced into the global trade networks.

New and unusual foodborne infections continue to arise around the world, as the expanding ecologies of human food production provide niches for the emergence of foodborne pathogens. Two striking examples are described elsewhere in this symposium: Nipah virus encephalitis in Bangladesh, and Shiga toxin–producing E. coli O104 infections in Germany (See Burger, 2011, and Luby et al., 2011, in this volume). In Brazil, Chagas disease, a parasitic infection caused by Trypanosoma cruzi, transmitted by the feces of the triatomid bug, and carried by the opossum, is a classic vectorborne infection, long associated with primitive rural thatched housing. An urban foodborne outbreak occurred in 1986, linked to consumption of fresh sugar cane juice, apparently contaminated by triatomids or opossum feces present in the cane as it was crushed to extract the juice (Shikanai-Yasuda et al., 1991). Since then, such outbreaks have been more frequently recognized, particularly with production of fresh juice of the açai berry, a jungle fruit that is now being grown in orchards to satisfy consumer demand (Nobrega et al., 2009). The transmission may depend on the intersection of this production with Amazonian ecology (Valente et al., 2009). Such outbreaks may be due to the direct contamination of freshly processed juice with bugs; illness has not been reported from commercial pasteurized product.

In western China, between 2006 and 2009, public health officials investigated several foodborne outbreaks of infection with toxigenic Vibrio cholerae O139, a variant strain of the dominant V. cholerae O1 that first appeared in India in 1995 and spread through Southeast Asia (Li et al., 2008; Tang et al., 2010; Xia et al., 2010). In these outbreaks, the food vehicle has been the soft-shelled turtle, steamed and served at banquet celebrations. These turtles are brought from sources in other parts of China or Asia, where they are produced commercially. A survey of such turtles in Hunan markets found that 7 of 437 had toxigenic V. cholerae O1 or O139 (Xie et al., 2009). The traditional virtues of the long-lived turtle may make it an attractive delicacy for banquets. As with the crab-associated cholera in the United States, future control for this problem may depend on better understanding of circumstances where the turtles are harvested, as well as on better cooking practices (Lowry et al., 1989).

In Israel, where Tilapia species have been raised in fish farms for more than 30 years, a new pathogen emerged in the 1990s, after marketing practices changed. The previous practice had been to market the fish frozen, but in 1996, some began to sell them alive. In 1996-1997, 62 cases of severe Vibrio vulnificus biotype 3 infections were reported, among persons handling the live fish (Bisharat et al., 1999). These infections were food-associated, although not caused by eating the fish itself. They typically started as local wound infection in the person buying the fish, after a penetrating injury from the many spines on the dorsal fin, and rapidly progressed to bacteremia; 41 required surgical wound debridement. Unlike infections with Vibrio vulnificus biotype 1, which cause severe wound infections in persons who have poor immune systems, and primary bacteremia in oyster eaters with serious liver disease, the patients in Israel were previously healthy. The implicated fish were also healthy and came from a variety of farms. Biotype 3 is a novel recombination of biotype 1 and biotype 2, a pathogen of eels (Bisharat et al., 2005). In 1998, the marketing policy was changed back to selling fish frozen, although cases still occur among those who handle the live fish (Zaidenstein et al., 2008). While it remains unclear where the recombination first occurred, the event is an example of how a pathogen can expand in an agricultural niche and reach the consumer if the circumstances are right.

In Taiwan, since 2000, extremely resistant strains of Salmonella serotype Choleraesuis have caused serious infections in humans and have also been detected in local swineherds (Chiu et al., 2002). This highly invasive serotype has a predilection in humans for endothelial tissues. Most hospitalized patients were admitted with primary bacteremia, sepsis, aortitis, and aortic valve infections (Jean et al., 2006). Human strains have high levels of resistance to ampicillin, chloramphenicol, trimethoprim-sulfamethoxazole, and ciprofloxacin (Chang et al., 2005). More recently, some have been resistant to extended-spectrum cephalosporins as well, due to a transmissible plasmid with blaCMY2 that has recently been found in four other common Salmonella serotypes in addition to Choleraesuis (Su et al., 2011). Indistinguishable strains have been reported from pigs, for which Choleraesuis is a host-adapted pathogen, and it was noted that 40 percent of pig farmers used fluoroquinolones to treat their herds (Hsueh et al., 2004). It seems likely that many of the human infections come from the porcine source, and full control is likely to require changes in agriculture practices to control the infection in pigs.

The challenge of global emerging foodborne infections underlines our inter-dependence on the public health and food safety systems around the world. Several collaborative programs are actively improving basic public health capacity, promoting standard laboratory identification and subtyping methods, and providing rapid communication. For example, the Training Programs in Epidemiology and Public Health Interventions Network, and the European Program for Intervention Epidemiology Training provide long-term training and practical experience in more than 56 countries (Anonymous, 2006; Moren et al., 1996). The World Health Organization (WHO) Global Foodborne Infections Network (formerly known as WHO Global Salm-Surv) has held 73 short-term multinational multidisciplinary courses to train microbiologists and epidemiologists together from public health, food, and animal medicine sectors (WHO, 2010). PulseNet International has training laboratories in all regions of the world, members in more than 75 counties who have been trained in standardized methods for molecular subtyping, and a global platform for evaluating and introducing new standard methods as they are developed (CDC, 2010c; Swaminathan et al., 2006). The WHO INFOSAN communication channel can link food safety authorities in all countries, so that information about newly identified hazards can be rapidly disseminated (WHO, 2007). Managing international foodborne outbreaks relies on robust investigations in the countries where disease occurs, and in the countries where the implicated food is grown or manufactured (Tauxe et al., 2008). In many of these investigations, close collaboration with the exporting country authorities and with the food industry can lead to better prevention strategies for the long term.


The complex and changing biological web of the human food supply means that we can expect new pathogens to emerge and novel food vehicles to be identified. Many of these will start in animal reservoirs and may reach us through both animal- and plant-derived foods. Much of the recent progress that has occurred in food safety has been the result of focused efforts to reduce contamination after harvest, for example with better sanitation and process control for meat and poultry at slaughter and in subsequent processing, and better control of processed foods to reduce contamination with Listeria. Contamination can start well before harvest or slaughter, and interventions that focus on the live animal or plant are needed to make further progress in making food safer. Such intervention will depend on understanding the biology of pathogens in the field, their life cycles, and the points at which contamination can be prevented or interrupted. Detecting the new problems will depend on robust capacity for public health surveillance and investigation and on multidisciplinary understanding of the ecologies that sustain them. With our global food supply, problems that arise in one part of the world can spread rapidly, if they enter the global food trade. Improving the safety of the food supply thus depends on stronger public health capacity around the world, better understanding of new challenges wherever they are identified, and translating that understanding into effective prevention from farm to table.


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Division of Foodborne, Waterborne and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA.

Copyright © 2012, National Academy of Sciences.
Bookshelf ID: NBK114501


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