Food Safety and Foodborne Disease Surveillance Systems: Proceedings of an Iranian-American Workshop (2006)

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Overview of Food Safety Issues and of Diseases Arising from Food of Animal and Plant Origin in the United States Karl R. Matthews Department of Food Science, Rutgers University Food safety and foodborne diseases are topics of global concern. Food safe- ty encompasses many areas, including pesticide and antibiotic residues, the pres- ence of mycotoxins and foodborne pathogens, and all aspects of food production and preparation. Many issues associated with these topics are common to all countries. Decisions must be made by each nation to determine priority areas that should be addressed to ensure the health of its citizens. In the United States, despite significant strides in microbiological food safety, continued effort is re- quired to combat this complex human health issue. The Centers for Disease Control and Prevention (CDC) estimates that 76 million persons in the United States annually contract foodborne illness (Mead et al., 1999). Surveillance data from the Foodborne Disease Active Surveillance Network (abbreviated as FoodNet) suggest that the infection incidence for target foodborne pathogens in the year 2003 was lower than the average annual inci- dence in the United States for the years 1996-1998 (Vugia et al., 2004). FoodNet determines the burden and sources of specific foodborne diseases by surveying laboratories in selected states. The estimated incidence of several infections de- clined significantly during the evaluation period. Infections decreased 49 per- cent, 42 percent, 28 percent, and 17 percent for Yersinia, Escherichia coli O157:H7, Campylobacter, and Salmonella, respectively. The incidence of Cryptosporidium infection decreased 51 percent. The incidence of Listeria and Shigella varied considerably during the observation period but did not change significantly. Only the incidence of Vibrio infections increased. The changes in incidence of the above infections occurred during a period when control measures were implemented with new or renewed effort by gov- ernment agencies and the food industry. The U.S. Department of Agriculture 5 

6 FOOD SAFETY AND FOODBORNE DISEASE SURVEILLANCE SYSTEMS (USDA) through its Food Safety Inspection Service (FSIS) launched Pathogen Reduction/Hazard Analysis and Critical Control Point (PR/HACCP) regulations for meat and poultry slaughter operations and processing plants in 1996. The U.S. Food and Drug Administration (FDA) introduced several intervention strat- egies designed to control foodborne diseases in the products they regulate. These include the produce safety guidance of 1998 (http://www.foodsafety.gov/~dms/ prodguid.html), the sprout safety guidance of 1999 (http://www.isga-sprouts.org/ sprougd1.htm), the requirements for refrigeration and safety labeling of shell eggs in 2001 (http://www.foodsafety.gov/~dms/fs-toc.html), and implementation of HACCP regulations for the seafood industry in 1997 (http://vm.cfsan.fda.gov/ ~lrd/fr951218.html) and the juice industry in 2002 (http://www.cfsan.fda.gov/ ~lrd/fr01119a.html). Food safety policies and practices must continue to evolve as new technolo- gies, production practices, and food manufacturing processes are developed. The complex relationships among pathogens, the host, and the environment also ought to be taken into consideration when addressing foodborne illnesses. For the pur- poses of this paper, food safety and foodborne disease issues are categorized broadly as those of either animal or plant origin. The microbiological quality and safety of animal products is influenced by an array of factors. They include production practices, use of antibiotics, con- sumer demand, and the global nature of the marketplace. Meat animal produc- tion has increased significantly in the United States over the past 30 years. Con- currently, meat animal production practices have changed. Perhaps most notable is the change to higher-intensity production practices. Pathogenic microorgan- isms are more likely to spread among animals confined in a limited space (IFT, 2002). To ensure the health and promote the growth of livestock, antibiotics are often added to animal feed. Indeed, approximately one-half of the antibiotics produced today are added to animal feed (WHO, 2002). This may contribute to the development of antibiotic-resistant human pathogens that have animal reser- voirs (Smith et al., 2005). The microbiological safety of meat and meat products requires concerted effort from government agencies, livestock producers, and meat processors. A number of well-publicized outbreaks of foodborne illness and recalls of meat and meat products have occurred during the past decade. Many millions of kilograms of ground beef and luncheon meat have been recalled because of potential contamination with E. coli O157:H7 and Listeria monocytogenes, re- spectively. A large outbreak in the early 1990s due to E. coli O157:H7 contami- nated hamburgers resulted in four deaths and hundreds of illnesses; this prompt- ed the development of the USDA/FSIS PR/HACCP rule mentioned above. Indeed, a single foodborne pathogen has completely changed the beef industry in the United States. The cost of concerns about E. coli O157:H7 contamination in beef produc- tion in the United States was estimated at a staggering $2.7 billion in the past 10 

OVERVIEW OF FOOD SAFETY ISSUES 7 years (Kay, 2003). This cost is associated with recalls, lost consumer demand, implementation of food safety intervention strategies, and increased operating expenses. The poultry industry has also experienced greater production expenses to control Salmonella and Campylobacter associated with poultry products and eggs. Going beyond the egg refrigeration rule, the FDA proposed measures to prevent S. enteritidis contamination of shell eggs during egg production. Salmonella, Campylobacter, and E. coli O157:H7, more so than other patho- gens, are of significant concern in beef and poultry processing. Listeria monocy- togenes, ubiquitous in the environment, has caused several large outbreaks of foodborne illness linked to luncheon meats and hot dogs. Contamination of these products is generally thought to occur post-processing. Listeria monocytogenes can be found in a variety of foods; however, many outbreaks have been associated with ready-to-eat foods. In a continuing effort to prevent L. monocytogenes illness and control this pathogen, the FDA’s Center for Food Safety and Applied Nutrition (CFSAN) and the CDC developed the Listeria Action Plan (http://www.foodsafety.gov/~dms/lmr2plan.html). Six ar- eas for action have been identified at the government, processor, and consumer levels to reduce significantly the risk of illness and death caused by L. monocyto- genes in ready-to-eat foods. The FDA is also reexamining the U.S. regulatory policy on L. monocytogenes in food. A proposal has been put forth to eliminate the zero tolerance policy for food products that do not support the growth of L. monocytogenes. Clearly, no single measure can prevent contamination of animal products with microorganisms potentially hazardous to human health. In the United States, government programs are in place, guidance plans have been developed for in- dustry, and consumer education information is available to guide the public in the proper handling of animal products. Such strategies are also in use to ensure the safety of fresh fruits and vegetables. The microbial safety of fresh fruits and vegetables is of global concern with respect to human health (WHO, 1998). In the United States the number of out- breaks of human illness associated with the consumption of fresh produce has increased in recent years (Beuchat, 2002; Sivapalasingam et al., 2004). This has been attributed to a variety of factors, including increased consumption, changes in agronomic and harvesting practices, and increased importation (Beuchat, 2002). The increase in cases of foodborne illness linked to consumption of fresh fruits and vegetables has spurred research addressing the preharvest interactions between foodborne pathogens and growing plants. Recent studies by the USDA’s Economic Research Service and by the FDA’s CFSAN addressed issues of importation and contamination of imported produce (Jerardo, 2003; http://www.cfsan.fda.gov/~dms/prodsur6.html; http:// www.cfsan.fda.gov/~dms/ prodsur10.html). The percentage of fruits and vegeta- bles that were imported into the country more than doubled from 1985 to 2001. Import of fresh fruits went from 9 percent to 23 percent and for vegetables from 

8 FOOD SAFETY AND FOODBORNE DISEASE SURVEILLANCE SYSTEMS 8 percent to 17 percent (http://www.ers.usda.gov/publications/fau/july03/ fau7901/fau7901.pdf). During the 1990s, at least 12 percent of foodborne illness outbreaks were linked to fresh produce items. An FDA survey of domestic pro- duce indicated that approximately 1 percent (12 of 1028) of samples were posi- tive for target foodborne pathogens (http://www.cfsan.fda.gov/~dms/ prodsur10.html). Approximately 2.6 percent, 1.6 percent, and 1.8 percent of the cantaloupe, cilantro, and lettuce, respectively, were contaminated with Salmo- nella. In a survey of imported produce > 4 percent (44 of 1003) of samples were positive for either Salmonella (35 or 80 percent) or Shigella (9 or 20 percent) (http://www.cfsan.fda.gov/~dms/ prodsur6.html). Numerous avenues exist during the production, harvesting, transport, and marketing of fresh produce for the introduction of pathogens (Beuchat, 2002). Contaminated manure, irrigation water, wash water, equipment, and farm work- ers are all potential vectors for the transmission of pathogens to fresh fruits and vegetables (Beuchat, 2002). A recent expert report from the Institute of Food Technologists (IFT) stated that “the complexity of the pre-harvest, harvest, and post-harvest environments makes it impossible to control all potential sources of microbial contamination” (IFT, 2002). The microbiological quality of water used for the irrigation and the washing and rinsing of vegetables post-harvest may be the single largest factor in contaminating produce. The USDA’s National Agricultural Statistics Service classifies irrigation methodologies into four categories: sprinkler systems, gravity-flow systems, drip or trickle methods, and subirrigation (USDA, 1998). Sprinkler systems apply water to crops from overhead pipes that are towed into position. Water droplets fall onto the edible portions of the plants as well as onto the soil surface. If the water is contaminated with a pathogen, the edible portion of the plant and the surrounding soil will likely also become contaminated. The advantage associat- ed with sprinkler systems is the potential for more exact water management than with surface irrigation. The remaining three irrigation techniques all involve the direct application of water onto the soil surface by a series of levees, furrows, and underground tubing. Here and throughout this paper these methods are collectively referred to as surface irrigation. With surface irrigation, water contacts primarily the roots of the growing plants. Data from the most recent census (1998) indicated that approximately 50 million acres of farmland were irrigated annually in the United States (USDA, 1998). Of that, 22.9 million acres were irrigated using sprinkler systems and the remainder by surface irrigation. For lettuce specifically, 58 per- cent of the annual harvest was sprinkler irrigated (USDA, 1998). Studies show that Salmonella and E. coli O157:H7 can survive for extended periods (> 40 days) in well, river, and lake water (Moore et al., 2003; Rice et al., 1999; Wang and Doyle, 1998). Therefore, a very real possibility exists for the contamination of crops in the field through exposure to contaminated irrigation water. 

OVERVIEW OF FOOD SAFETY ISSUES 9 At present, chlorine at a concentration of 50-200 ppm is the primary post- harvest sanitizing agent in routine use for fresh produce (Beuchat, 1998); how- ever, this level of chlorine has repeatedly been demonstrated to be ineffective at eliminating pathogens from fruits and vegetables (Beuchat, 2002; Weissinger et al., 2000). Indeed, chlorine is often added to the wash water to reduce the micro- bial load of the water, not necessarily to kill the specific pathogens that contami- nate the produce. While extremely effective against E. coli O157:H7 in aqueous systems (Rice et al., 1999), the efficacy of chlorine is greatly reduced on raw fruits and vegeta- bles. Beuchat et al. (1998) stated that the loss of activity likely occurs when chlorine interacts with organic material such as plant tissues. Numerous other sanitizers including ozone have been examined for use on fresh produce (Koseki et al., 2001), electrolyzed water (Kim et al., 2003), hydrogen peroxide (Lin et al., 2002), lactic acid (Lin et al., 2002), and chlorine dioxide (Han et al., 2000). Under the conditions studied and commercial practices, sanitizing agents are generally not able to reduce by more than 1 or 2 log10 CFU the levels of patho- gens on fresh produce (Beuchat et al., 1998). Although other sanitizing agents such as chlorine dioxide and ozonated water are available, chlorine remains the chemical sanitizer most widely used by the produce industry. The efficacy of sanitizers on fresh produce depends largely on the target pathogen’s accessibility. That foodborne pathogens can infiltrate plant tissues is of grave concern since microorganisms present within plants are protected from the actions of surface decontamination practices. Escherichia coli O157:H7 has been shown to localize preferentially on cut edges of lettuce leaves as opposed to intact leaf surfaces (Takeuchi and Frank, 2000). Seo and Frank (1999) demon- strated that cells of E. coli O157:H7 were able to penetrate the interior of cut tissue, becoming entrapped 20-100 µm below the surface. Cells present at these subsurface locations were protected from inactivation with chlorine (Burnett and Beuchat, 2002). The uptake of human pathogens by the root systems of growing crops has also been investigated (Guo et al., 2002; Solomon et al., 2002; Wachtel et al., 2002). The reported uptake of E. coli O157:H7 by the roots of growing lettuce plants (Solomon et al., 2002; Wachtel et al., 2002) and Salmonella by hydro- ponic tomato plants (Guo et al., 2002) has led to the hypothesis that foodborne pathogens may exist as endophytes within growing plants. It is most likely that internalized bacteria are protected from sanitation by virtue of their inaccessi- bility. Harvesting practices and equipment can have a significant impact on the microbiology of fresh produce. Approximately 90 percent of fruits and vegeta- bles are harvested by hand (USDA, 2001). Farm workers may transfer pathogens from their hands to the crop or from crop to crop during the harvesting process. The tools used for harvesting (e.g., knives and machetes) and containers used for storage and transport (bins, buckets, and trailers) should be properly washed and 

10 FOOD SAFETY AND FOODBORNE DISEASE SURVEILLANCE SYSTEMS sanitized; however, reports indicate that washing and sanitizing, respectively, are done only about 75 percent and 30 percent of the time (USDA, 2001). A relatively new segment of the produce industry, “Fresh Cut,” has emerged in the last 15 years in the United States. Fresh-cut products have been physically altered from the original form, but remain in a fresh state. Products include, for example, salad mixes, sliced or diced tomatoes, and papaya halves. Some pro- cessors have moved the early stages of processing lettuce to the field. For exam- ple, heads of lettuce are cut at their stems, exterior leaves and core are removed, and the heads are immersed in wash water containing up to 200 ppm chlorine. The lettuce heads are then loaded by conveyor belt into bins lined with a plastic bag and cooled within two hours. There is concern that bringing processing onto the farm could increase the likelihood for microbial contamination. The USDA and the FDA have developed guidelines to minimize foodborne illness associated with fresh produce consumption (http://vmcfsan.fda.gov/~dms, http://www.foodsafety.gov/~dms/prodplan.html). These guidelines include the implementation of Good Agricultural Practices (GAPs), Good Manufacturing Practices (GMPs), and HACCP systems. GAPs encompass irrigation water qual- ity, manure handling, equipment cleaning, and worker education. Other areas being addressed focus on increased communication among growers, packers, and consumers, and increased support of research relevant to fresh produce. Microbial food safety issues with fresh fruits and vegetables will likely always exist since the products are consumed raw; however, contamination can be minimized through comprehensive control strategies from the farm to the table. GAPs must be coupled with GMP and HACCP programs at the post- harvest stage to limit contamination of a product with foodborne pathogens. Such control practices must be implemented not only in the United States but also in countries from which the fresh produce has been imported. Safety of the food supply throughout the world is a major concern as new pathogens emerge and known pathogens reemerge. The foodborne pathogens E. coli O157:H7 and Shigella present significant problems for the food industry and the consumer in part because of their ability to survive under a broad range of conditions. Although these pathogens traditionally have been linked to animal products (eggs, poultry, beef, and dairy products), more recent outbreaks have been associated with water (well and municipal), produce, and processed foods that likely were cross-contaminated. Characterization of these target pathogens has also demonstrated that they are often resistant to one or more antibiotics (Aarestrup and Wegener 1999; Bower and Daeschel, 1999; Bryan et al., 2004). Transmission of pathogens to food occurs at various levels: in the field; during harvesting, processing, and shipping; or in the home. Routes of contami- nation include water used to irrigate fields, contaminated feed, colonized ani- mals, cross-contamination from fecal matter, the use of improperly composted manure, improper sanitation of processing equipment, and human handling (Beuchat and Ryu, 1997; Wang et al., 1996). Methods employed to enhance the 

OVERVIEW OF FOOD SAFETY ISSUES 11 safety of food along the production and processing path should focus not just on slowing or preventing the growth of pathogens but also on eliminating them. Such methods include the use of antibiotics on the farm, sanitizers in the pro- cessing plant to prevent cross-contamination, the use of preservatives in foods to prevent and retard growth, and various processes, including pasteurization, to eliminate pathogens. Antibiotics are used in plant and fruit production for disease control and in animal agriculture for therapy, prophylaxis, and growth promotion (Gustafson and Bowen, 1997). A wide range of antibiotics is used (-lactams, sulfonamides, and macrolides) in animal agriculture and, depending on the type of animal (dairy cattle, beef cattle, sheep, poultry, or fish), the target may be treated indi- vidually or as a group (herd or flock). Reports indicate that a greater percentage of E. coli O157:H7 and Shigella isolates and other pathogens are antibiotic resis- tant today compared with 10 to 15 years ago (Sahm et al., 2001; Tollefson and Miller, 2000; Van den Bogaard and Stobberingh, 1999), with many strains ex- hibiting multiple antibiotic resistance (Kim et al., 1994; Mevius et al., 1999). Antibiotic use on the farm has come under increased scrutiny in light of an increase in the emergence of antibiotic-resistant pathogens. Broad-spectrum an- tibiotics are typically used for livestock at subtherapeutic levels to promote feed efficiency and growth as well as to control disease (Gustafson and Bowen, 1997). An increase in pathogens resistant to antimicrobials, including E. coli O157:H7 and Shigella, may contribute to the higher prevalence of such resistant bacteria in commensal flora and vice versa. Widespread use of antimicrobials in com- mercial farming may result in the release of antimicrobial agents into the envi- ronment, subsequently causing the emergence of resistant commensal bacteria. Antibiotics excreted by farm animals or incorporated into feed or drinking water can ultimately be dispersed into the environment through the fertilization and irrigation of fields. Often farm wastes (manure, bedding, and feed) are collected in lagoons and pit systems and spread or sprayed onto fields. A range of micro- organisms—including Staphylococcus aureus, nongroupable streptococci, enter- obacter, enterococci, and E. coli—isolated from farm workers were significantly more resistant to antibiotics than when isolated from other individuals (Aubry- Damon et al., 2004). Resistant bacteria present on food crops intended for human consumption may prove to be a major route of infection. Enterobacteriaceae are not only found in abundance in the environment but are pathogens and commensals of the human gastrointestinal tract. A Finnish study investigated the potential for raw vegetables to serve as a source of resistant strains of Enterobacteriaceae (Oster- blad et al., 1999). The researchers concluded that bacteria from vegetables were not responsible for the high prevalence of resistant Enterobacteriaceae in fecal flora in Finland. Transfer of antibiotic-resistant determinants may occur in vivo between en- teric microorganisms. Gene transfer between pathogens is not a new concern and 

12 FOOD SAFETY AND FOODBORNE DISEASE SURVEILLANCE SYSTEMS has been reported in both humans and animals. Interspecies gene transfer in vivo occurred in association with an outbreak of shigellosis in 1983 (Tauxe et al., 1989). The Shigella isolate associated with this outbreak carried a plasmid that encoded resistance to ampicillin, carbenicillin, streptomycin, sulfisoxazole, tet- racycline, and trimethoprim/sulfamethoxazole; this was identical to the antimi- crobial resistance of an E. coli isolated from a case patient’s urinary tract infec- tion that had occurred prior to the onset of shigellosis. Others have investigated the potential for transfer of an apramycin-resistant plasmid from E. coli to S. typhimurium in calves (Hunter et al., 1992). E. coli O157:H7 strains initially associated with human illness were suscep- tible to most antibiotics used against Gram-negative pathogens. During the last two decades the antibiotic susceptibility profile of E. coli O157:H7 has changed drastically. Only 2 of 200 strains of E. coli O157:H7 collected by the CDC between 1983 and 1985 were resistant to antibiotics (Bopp et al., 1987). Subse- quent screening of 125 E. coli O157:H7 (n = 118) and O157:NM (n = 7) re- vealed that 24 percent were resistant to at least one antibiotic and 19 percent were resistant to three or more antibiotics (Meng et. al., 1998). In a longitudinal study of beef cattle feedlots, E. coli O157:H7 isolates were resistant to six of the eight antibiotics that are used to treat E. coli infections in food animals (Galland et. al., 2001). Perhaps surprisingly, less than one-half of the isolates were resis- tant to tetracycline, one of the most extensively used antibiotics on feedlots. Compared with other foodborne pathogens or with other E. coli isolates, the level of antibiotic resistance of E. coli O157:H7 is generally low and basically limited to tetracycline, streptomycin, and sulfamethoxazole. Shigella, although associated with foodborne illness, accounts for only a fraction of the total cases of foodborne illnesses that occur in the United States (Mead et al., 1999; Shiferaw et al., 2004). A large outbreak in 1987 was likely the result of transmission by food, water, and person to person (Wharton et al., 1990). The outbreak strain was resistant to ampicillin, tetracycline, and trimetho- prim-sulfamethoxazole. Contamination of crops with Shigella through application of contaminated manure to fields or contaminated irrigation water may occur. Fresh raw agricul- tural ingredients associated with prepared foods are also often implicated as the source of Shigella (CDC, 1999). In 2000 a nationwide outbreak of shigellosis involving 406 persons was traced to a commercially prepared five-layer dip (Kimura et al., 2004). The outbreak was probably the result of a food handler shedding the pathogen since the guacamole and salsa used were also sold as stand-alone products, and in that context were not linked to illnesses. The potential for the spread of antibiotic-resistant Shigella from one country to another should not be ignored. A recent study from South Asia indicates that all Shigella isolates evaluated were resistant to ampicillin, tetracycline, nalidixic acid, and ciprofloxacin (Bhattacharya et al., 2003). Perhaps most alarming is that small outbreaks of shigellosis due to ciprofloxacin-resistant strains have been 

OVERVIEW OF FOOD SAFETY ISSUES 13 detected (Bhattacharya et al., 2003). These reports underscore the potential role that food handlers and agricultural production practices in one country may have on the occurrence of Shigella that are multiply resistant to antimicrobials in countries with which they trade. Indeed, a recent study conducted in Karaj, Iran, indicated that approximately 91 percent and 88 percent, respectively, of Shigella isolates were resistant to one or more antimicrobial agents and 88 percent were multidrug resistant (MoezArdalan et al., 2003). The issue of vancomycin-resistant Enterococcus faecium (VREF) is worri- some. Reservoirs for VREF include food and other sources, such as cattle, swine, poultry, minced pork or beef, and pet food. The concern stems from the use of streptogramin antibiotics as growth promoters and therapeutic agents in farm animals, and the use of streptogramins to treat patients with VREF infections. Streptogramin-resistant organisms are now common in the food supply, although factors associated with foodborne transmission need to be clarified (McDonald et al., 2001). Sampling of chicken carcasses revealed that 237 of 407 carcasses were positive for streptogramins-resistant E. faecium (McDonald et al., 2001). Risk modeling recently suggested that banning the use of virginiamycin in chick- ens would have little impact on human morbidity and mortality (Cox and Pop- ken, 2004). However, carriage of resistance by commensal bacteria and transfer of resistance is unpredictable; therefore the effects of agricultural use of antibiot- ics on human health remains uncertain (Smith et al., 2005). The continued safety of the U.S. food supply requires a proactive approach. Science-based means must be used to establish food safety guidance and regula- tions. Greater funding must be made available to support needed research and the development of expert panels to aid in establishing food safety objectives. Food safety objectives may focus on anything from the use of antibiotics in agriculture to distribution of resources by public health organizations. Since there is no all-encompassing solution to foodborne disease, establishing objectives will permit the allocation of limited resources that have the greatest impact on food safety. Human foodborne disease surveillance systems, use of microbiolog- ical risk assessment, and statistical process control are scientific tools that regu- lators can use when developing compliance with regulations. Programs such as GAPs, GMPs, and HACCP must be further developed to prevent contamination of food during its journey from the farm to the table. International coordination is required to develop effective food safety mea- sures. In a global society and marketplace it is possible for people, food, and pathogens to circle the world in a single day. To combat the spread of pathogens, greater consumer participation is required. For example, practicing personal hy- giene (e.g., hand washing) and proper food handling will reduce the spread of foodborne pathogens and help to control or kill pathogens in foods prior to consumption (i.e., cook the food thoroughly in order to kill potentially harmful bacteria). Food safety will be realized through the melding of science and com- mon sense, ultimately protecting consumers throughout the world. 

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