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The Science of Public Health Surveillance THE TOOLS OF PUBLIC HEALTH SURVEILLANCE Public health surveillance is the ongoing, systematic collection, analysis, interpretation, and dissemination of health outcome-specific data for use by the public health sector to reduce morbidity and mortality and to improve health (Thacker and Berkelman, 1988~. Surveillance of many infections and intoxica- tions, including those that are foodborne, has been a fundamental public health activity for many years. Human foodborne disease surveillance is conducted for three principal reasons: (1) to identify, control, and prevent outbreaks of food- borne disease, (2) to monitor trends and determine the targets and efficacy of control measures, and (3) to determine the burden of specific diseases on public health (Potter et al., 2000). By detecting outbreaks and their sources quickly, surveillance can lead to control of an acute health hazard, for example, by removing a contaminated product from the market or by temporarily closing a hazardous kitchen. Outbreak investigations can also identify critical gaps in knowledge, leading to applied research and ultimately to better long-term prevention as unsafe food handling processes are corrected or new food hazards are identified and controlled. The information gathered through surveillance and subsequent investiga- tions of outbreaks and of sporadic cases can reveal the magnitude and trends of foodborne diseases, which helps policy makers target prevention strategies. This information is also critical to the design and evaluation of risk assessments. Improved understanding of foodborne diseases, in turn, can help researchers recognize new problems, such as entirely new hazards (e.g., microbes or toxins) 28

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29 Prevention Measures \ THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE Surveillance Applied Targeted Research FIGURE 2.1 The cycle of public health prevention. - Epidemiologic Investigation / or known hazards that may appear in foods not previously associated with them. Most foodborne pathogens were discovered during outbreak investigations, and much of the knowledge we have about specific hazards and how they enter the food supply also was gained during the course of investigations. As new foodborne disease sources and agents emerge, the efforts to control them through application of the Hazard Analysis and Critical Control Point (HACCP) system and other control strategies must constantly evolve. Surveillance is a keystone in the effort to define, control, and prevent foodborne diseases (Figure 2.1~. In the United States, foodborne disease surveillance is primarily conducted by local and state public health agencies. In fact, local surveillance for diseases of public health concern has been conducted for centuries. In the nineteenth century, fear of cholera led to the establishment of permanent municipal health depart- ments and disease surveillance, even before the microbe that caused it was iden- tified (Rosenberg, 1987~. Reporting of typhoid fever cases and deaths drove many improvements in water and food safety at the beginning of the twentieth century. Increased concern following the large Escherichia cold 0157:H7 out- break in 1993 associated with consumption of undercooked ground beef (Bell et al., 1994) stimulated enhancements in surveillance for foodborne infections (FSIS, 1998c). Strategies in Public Health Surveillance There are specific strategies to collect information that may serve as a basis for making food safety policy decisions. The surveillance strategies for outbreaks and sporadic cases of diseases that are often foodborne are:

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30 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD 1. Monitoring case reports of specific, notifiable infections 2. Investigating and reporting outbreaks of illnesses associated with events or establishments 3. Investigating and reporting unusual clusters of cases of specific infections 4. Vigilantly surveilling (termed sentinel site surveillance) for specific con- ditions that may or may not be notifiable 5. Laboratory subtyping of pathogens isolated from human infections 6. Surveying the population to measure trends in diarrhea! illness, consumer behavior, and food consumption One surveillance method may be more appropriate than another, and these methods may also be used alone or in combination, depending on the purpose. For example, subtyping of pathogens may be performed to confirm the source of an outbreak. The specific surveillance strategies are conducted either nationwide or in several sentinel sites that represent the whole population. Surveillance conducted to detect outbreaks and protect the public should cover the whole population, should include conditions most likely to appear in outbreak form, and in some instances, should focus on settings where outbreaks are likely to occur. Some outbreaks are not tightly clustered in time and space, and thus are not evident in surveillance conducted in one location. To detect dispersed outbreaks, it can be critical to compare specific markers of the infecting organisms, such as genetic "fingerprints," across many jurisdictions (Swaminathan et al., 2001~. Such com- parison of subtypes may reveal an unusual clustering of infections with a single strain of a pathogen that can then be further investigated. Public health laborato- ries use subtyping methods and are linked in a national network to permit rapid comparison of results and to provide warning of dispersed outbreaks. For example, the network of state public health laboratories detected a multistate cluster of Salmonella Newport infections that had the same pulsed-field gel electrophoresis profile. As a result of the investigation of genetic profiles, 78 infections in 13 states were linked to consumption of imported mangoes (Sivapalasingam et al., 2000~. If the purpose of surveillance is to measure the public health burden of disease or track long-term trends in the nation as a whole, more detailed data collected from a representative sample of sites around the country is likely to provide more accurate information (Angulo and Swerdlow, 1999~. This sentinel- site approach can provide data on important illnesses, such as Campylobacter or Vibrio infections, that are not well represented in national surveillance systems because they rarely appear in outbreak form and are not reportable in many jurisdictions. For the purpose of determining the food source of infections, surveillance based on outbreak investigations provides answers for those illnesses that fre- quently appear in outbreak form. For illnesses that rarely appear as outbreaks,

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THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE 31 case studies can give a general answer as to the source of illnesses that are strongly tied to specific sources, and case-control studies can provide information if the sources are complex. As described later, the committee feels that to con- struct a detailed quantification of the contribution of specific animal or food sources to foodborne diseases, systematic monitoring of pathogens in food and animal reservoirs using molecular subtyping and comparison of strains with iso- lates from human infections are urgently needed. The following sections describe how these strategies are utilized in both nationwide and sentinel site surveillance by public health agencies in the United States. Specialized surveys that relate the contribution of consumer behavior to the level of specific foodborne illness risk are described as well. Finally, several factors that limit the value of surveillance systems are discussed. Nationwide Surveillance of Notifiable Diseases Many counties and states have collected notifiable disease reports for more than a century, covering an ever-expanding list of illnesses. Since 1961, these reports have been voluntarily submitted to the Centers for Disease Control and Prevention (CDC), which publishes them as weekly and annual summaries (Thacker, 1994~. At its annual meetings, the Council of State and Territorial Epidemiologists decides which specific illnesses should be nationally notifiable. This general umbrella of reporting covers all areas of the United States; provides information useful to local, state, and national authorities; and is relatively inex- pensive. Most disease reporting is passive from the standpoint of the public health system, which means that clinicians and laboratories are asked to report cases on their own initiative. Basic case surveillance has been enhanced for some infections by further characterization of the infecting pathogen in public health laboratories. This voluntary case surveillance was first begun for Salmonella. Following large, multistate outbreaks of salmonellosis early in the 1960s, health department laboratories in states and large cities began to serotype strains of Salmonella isolated from humans; the results of this subtyping were shared with CDC as well in order to detect outbreaks affecting more than one state. Since 1962, national Salmonella surveillance has depended on this serotype-based reporting (Olsen et al., 2001~. These data have been critical to the detection of many outbreaks of salmonellosis each year. Since 1990, these data have been relayed electronically from states to CDC via the Public Health Laboratory Infor- mation System (Bean et al., 1992~. In addition, since 1995 these data have been routinely examined using an automated statistical outbreak detection algorithm that compares current reports with the preceding 5-year mean number of cases for the same geographic area and week of the year to look for unusual clusters of infection (Hutwagner et al., 1997~. The usefulness of the outbreak algorithm is limited by the timeliness of reporting and the high background rates of reporting for common serotypes such as S. Typhimurium and S. Enteritidis. The greatest

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32 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD sensitivity for Salmonella serotyping to detect meaningful clusters is for the rare serotypes, whereas further differentiation is necessary for the most common sero- types. The utility of serotyping as an international designation for Salmonella sub- types has led to its widespread adoption. In a recent survey, 61 countries reported that they used Salmonella serotyping for public health surveillance (Herikstad et al., 2002a). A new World Health Organization (WHO) website (WHO, 2002) collects and presents the results of this serotyping. This website is a new mecha- nism for the global surveillance of foodborne diseases. Molecular subtyping is now expanding the power of surveillance to detect outbreaks that appear as sporadic cases and is improving the ability of public health authorities to investigate outbreaks by comparing the molecular "finger- print" of bacterial strains associated with sporadic cases of a foodborne disease. These new techniques can define subtypes within a single species or serotype and provide useful strain differentiation for a growing number of pathogens (Swaminathan et al.,2001~. State public health laboratories began using an assay standardized at CDC for E. cold 0157:H7 after it proved useful in the 1993 West Coast outbreak associated with the consumption of undercooked ground beef; they have now expanded the use of this technique to common serotypes of Salmonella such as Typhimurium and Enteritidis, and to Listeria monocytogenes (Swaminathan et al., 2001~. Developing this capacity at the state level also en- hanced rapid detection of multicounty clusters within the state (Bender et al., 1997, 2001~. Standardized subtyping protocols have now been developed for seven pathogens; next-generation, gene-based technologies are under develop- ment. Recently, PulseNet, a national network formed by linking all state public health laboratories via the Internet, with a national database maintained by CDC, made it possible to rapidly identify and investigate multistate clusters. Once a cluster of infections caused by strains with the same fingerprint is identified, rapid epidemiological investigation can determine whether the cluster is a true outbreak with a common source. Laboratories at the Food and Drug Administra- tion (FDA) and the U.S. Department of Agriculture (USDA) also participate in this network so that isolates from foods and animals can be compared within the system. It is noteworthy that Canada has already adopted a compatible system and that the European network for laboratory-based surveillance of foodborne infections, EnterNet, has similar plans. The participation of Canada, Europe, Asia, and other regions could make it possible to detect multiregional clusters of foodborne disease (Swaminathan et al., 2001~. Monitoring levels of antimicrobial resistance in foodborne pathogens is an- other form of subtype-based surveillance. Since 1996, the National Antimicrobial Resistance Monitoring System (NARMS) for enteric bacteria, a collaborative effort of CDC, USDA, and FDA, has been monitoring the prevalence of resis- tance in Salmonella, Campylobacter, and other foodborne bacterial pathogens

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THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE 33 isolated from humans, animals, and foods (Marano et al., 2000~. This type of surveillance provides information about the trends in microbial resistance to specific drugs, identifies the emergence of new resistance threats, and permits the comparison of strains identified in various locations. This information is useful to public health officials who are involved in controlling highly resistant strains, to clinicians making treatment decisions, and to regulators who can better evaluate the association between antibiotics used in animals or the environment and resis- tance developed in human pathogens. In summary, nationwide surveillance systems for cases of foodborne infec- tion are valuable tools for defining trends, identifying outbreaks, and evaluating food safety programs. In some situations, serotyping and subtyping of pathogens, coupled with nationwide surveillance, provide an ideal system to link a cluster of cases. Considering that state and local public health systems provide the only nation- wide population-based surveillance for foodborne diseases, and that outbreak investigations are critical to identify new pathogens and new food safety hazards, the committee recommends that foodborne outbreak investigation and reporting by state and local health departments be enhanced. Training and personnel and laboratory support should be provided to enable rapid, thorough, and accurate investigation and reporting of foodborne outbreaks by local and state health departments, with performance evaluated through systematic review of outbreak reports. In addition, timely analysis and dissemination of results to regulators, industry, and the public is essential. Time series analysis (as discussed in Chapter 3) would also be a valuable analysis technique in this area. Sentinel Site Surveillance In contrast to the national umbrella of routine notifiable disease surveillance supplemented with public health laboratory subtyping, a different strategy, senti- nel site surveillance, can provide more detailed information about specific ill- nesses that are likely to be foodborne. This strategy was first developed for monitoring cases of hepatitis, for which detailed laboratory and epidemiological data are crucial (Bell et al., 1998~. A more recent example of this type of surveillance is the Foodborne Disease Active Surveillance Network (FoodNet), a collaborative program of CDC, senti- nel sites (currently nine sites), USDA, and FDA under the aegis of CDC's Emerging Infections Program (Angulo and Swerdlow, 1999~. The establishment of FoodNet was stimulated by a request from USDA's Food Safety and Inspec- tion System (FSIS) for a system to ascertain the public health impact of USDA's Pathogen Reduction; Hazard Analysis and Critical Control Point Final Rule (PR/HACCP rule). FoodNet began with an initial five-site area in 1996 and expanded to nine sites by 2001. The current surveillance area covers 37.8 million persons, or approximately 13 percent of the U.S. population (CDC, 2002a).

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34 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD FoodNet conducts active case ascertainment for foodborne diseases, accompa- nied by epidemiological studies designed to help better understand the epidemi- ology of foodborne diseases in the United States. Active case ascertainment means that public health authorities regularly contact clinical laboratories to obtain case reports of diagnosed illnesses; therefore, the results do not depend on which infections are locally notifiable or on local resources available for surveil- lance. Thus, because reporting is more uniform and complete, active case ascer- tainment yields better data than passive reporting systems. However, it is also more expensive and limited in geographic scope. In addition to case ascertain- ment, FoodNet surveys laboratory, physician, and patient practices that cause an individual case to be diagnosed. Also, FoodNet has been a platform for conduct- ing case-control studies of sporadic infections in order to identify general risk factors for infection that distinguish the persons who get ill from those who stay healthy. This information has been used to better define the burden of foodborne illness (Mead et al., 1999), to evaluate the risk factors for specific infections (e.g., in the Campylobacter case-control study [Friedman et al., 2000bj), and to track the trends in major foodborne infections (CDC, 2002a). To provide real-time tracking of human case surveillance, the committee recommends that the capacity of the sentinel sites of FoodNet to rapidly inter- view (i.e., as soon as possible after the case is diagnosed, as opposed to two to three weeks later when active surveillance contacts with the laboratory detect the case, a cluster is identified, or some other event shows the need for follow-up) individual illness cases that are potentially foodborne, to track real-time inter- views, and to collect and subtype Listeria, E. cold 0157:H7, and Salmonella isolates from human infections, be enhanced as soon as feasible. (Although sev- eral subtyping schemes exist for Campylobacter, none has yet been shown to be useful and practical in the public health setting for routine testing of all isolates.) All cases of infection from pathogens covered by FoodNet surveillance should be interviewed. In addition, the committee believes that international collaboration and the sharing of methods and microbiological and illness surveillance data between the United States and other surveillance systems such as WHO's Global SalmSurv (WHO, 2002) and Europe's EnterNet must be strongly supported. Foodborne Outbreak Reporting A foodborne outbreak is a cluster of two or more similar infections that are shown by investigation to result from ingestion of the same food (Olsen et al., 2000~. Local and state health departments conduct most foodborne outbreak investigations. Since 1967, CDC has collected reports of outbreaks of foodborne illnesses investigated by local, state, and national public health authorities (Olsen et al., 2000~. Reports of outbreaks include the nature of the pathogen or toxin, the type of food that caused the outbreak, and some information about factors that contributed to the outbreak. Before 1998, these reports were collected on paper

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THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE 35 and slowly reviewed and compiled. The system is now being overhauled with an improved form, the active solicitation of reports from states, the introduction of Internet-based reporting (Electronic Foodborne Outbreak Reporting System), and the more rapid analysis and dissemination of results (FDDB, 2002a). The foodborne outbreak surveillance system has provided useful informa- tion on long-term trends for many pathogens for which surveillance otherwise does not exist, as well as summaries of the outbreaks caused by a particular pathogen, hazard, or food (Bean and Griffin, 1990~. In the future, it may provide more systematic detection of clusters of outbreaks, based on both laboratory testing and epidemiological assessment of the outbreak presentation (Hall et al., 2001~. The committee considers the systematic analysis of information on out- breaks gathered through this system as an effective tool for allocating the burden of many infections and other hazards across broad food categories. Specialized Surveys of Behavior FoodNet and other surveillance efforts also provide systematic data on be- havior of the population and exposure to specific risks. Studies conducted through the CDC Behavioral Risk Factor Surveillance System (BRFSS) documented the high frequency of risky food behavior (Yang et al., 1998~. More recently, FoodNet population surveys have provided population-based data on the incidence of diarrhea! illness and the likelihood of seeking medical care for a diarrhea! illness; this information was critical to develop a general estimate of the burden of foodborne disease (Herikstad et al., 2002b; Mead et al., 1999~. The surveys also provided general population-based data on the frequency of exposure to a wide variety of foods and other potential sources of intestinal infection (Consumer Studies Branch, 2002; FDDB, 2002b). Another potential source of information is the complaint systems maintained by local and state health departments to which individuals can report illnesses or hazardous conditions they believe may be related to food (Samuel et al., 2001~. While such systems are far less specific than systems built on diagnosed cases of illness, they may provide an early warning of problems. Limitations of Surveillance One limitation inherent in all surveillance systems is that many cases go unrecognized for a variety of reasons. For example, cases may not be detected because people who are ill do not seek medical care, physicians and laboratories may not make a specific diagnosis, diagnosed cases may not be reported to authorities, and authorities with limited resources may not investigate or report cases. This last factor becomes especially significant if the surveillance program is voluntary, as is the case with outbreak reporting by local and state agencies.

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36 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD Data collected in this voluntary manner do not correspond to a nationally representative sample of the population because reporting depends on other vari- ables, such as local resources or whether a particular disease is notifiable (CDC, 2001~. Even in active surveillance programs, such as FoodNet, the number of cases is underestimated because people do not seek medical care or because cases are reported only when they are confirmed by a laboratory. Therefore, the actual number of cases that occurs is likely to be substantially greater than the number of cases reported. For example, it has been estimated that 38 cases of salmonellosis occur for every 1 that is reported (Voetsch et al., 1998~. Many outbreaks are also likely to be unrecognized. A common-source outbreak in a restaurant may not be recognized because patrons were exposed in small groups that were unknown to each other. For some foodborne infections, the incubation period may be long enough to obscure the relationship with the meal unless persons attending a large gathering, such as a banquet or wedding reception, have some reason to compare their experiences afterwards. A second limitation is the difficulty in attributing a specific case to a specific food. Many infections can be transmitted by a variety of foods and by routes other than food. In the sporadic case of illness, the person may have consumed many foods and may have had other potentially risky exposures in the days preceding illness, making it difficult to determine the source of the illness. In an outbreak setting, where careful comparison of food consumption patterns of a group of ill persons with those of a group who remained well can identify the immediate food vehicle, it is still difficult sometimes to determine which of the various ingredients was the source of the illness. However, many outbreak inves- tigations are definitive, and comparison of patterns observed among groups of outbreaks can help define patterns. Finally, surveillance can only count what is measurable and known. Because diagnosis of Norwalk-like virus (recently designated "Noroviruses") infections is not routinely performed in clinical laboratories, for example, this extremely com- mon illness cannot be monitored with the same type of case-based surveillance that is conducted for infections caused by Salmonella or Campylobacter, for which routine diagnostic tests are available. The importance of Norwalk-like virus infections can be defined from outbreaks where the typical combination of signs, symptoms, incubation period, and duration of illness can be documented and where specimens reach specialized laboratories that can make the diagnosis (Bresee et al., 2002~. Similarly, enterotoxigenic E. colt, the cause of much travelers' diarrhea, is increasingly recognized as a cause of outbreaks in the United States, but may also be an unrecognized common cause of sporadic cases because the specialized tests to detect it are rarely applied (Dalton et al., 1999; Guerrant et al., 1990~. It is likely that there are many foodborne disease agents yet to be dis- covered which, consequently, are not currently tested for in any laboratory (Tauxe, 1997~.

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THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE 37 Similarly, behavioral risk-factor surveillance is subject to limitations. This type of surveillance depends on what people can and will report. People may overestimate how often they perform socially desirable behaviors such as hand washing. Questions about risk exposures also depend on what the consumer observes. People are not likely to know if the food they ate was cross-contaminated in the kitchen, even if they prepared it themselves. The observations individuals can make may be a less-than-perfect measure of risk. Although the FoodNet population survey used consumption of pink ground beef as an assessment of cooked meat doneness and safety, research has clearly demonstrated that cooked meat color is not an acceptable indicator for these parameters (Berry et al.,1998; FSIS, 1998a, 2000; Hunt et al., 1999~. Premature browning and a persistent pink color are two conditions that can occur in ground beef patties, influencing inter- nal beef patty color, whether or not a patty has been cooked to an internal temperature of 160F (Hunt et al., 1999; Killinger et al., 2000~. In a nationwide evaluation, Berry and coworkers (1998) found 47.4 percent of hamburgers cooked to 160F retained some pink color, and 15.8 percent still retained some pink color when cooked to 175F. In addition, more than 25 percent of fresh-cooked ham- burgers (meat was never frozen) were brown or nearly brown internally although hamburgers were only cooked to 150F. RESULTS FROM PUBLIC HEALTH SURVEILLANCE The Burden of Disease An estimation of the burden of disease is very useful when regulatory agen- cies make decisions about the focus and allocation of resources. The burden of disease attributable to foods has only been estimated in a general way; if the estimate of this burden was specific for particular foodborne diseases and food groups, more informed decisions could be made by regulatory agencies. Information from surveillance has recently been integrated into a general estimate of the overall burden of foodborne disease in the United States (Mead et al., 1999~. This estimate included the number of cases, hospitalizations, and deaths that were attributed to specific pathogens and to the large number of illnesses that remain unaccounted for. These pathogen-based point estimates can provide a benchmark for assessing the economic impact of foodborne diseases, such as the $6.9 billion estimated cost to society from the diseases caused by the major foodborne bacterial pathogens (Buzby and Roberts, 1996~. Some foodborne infections can also cause chronic complications in a small percentage of cases; for example, kidney failure related to E. cold 0157:H7 has been reported in 4 to 8 percent of cases (Griffin et al., 2002), and Guillain Barre syndrome paralysis may complicate 1 in 1,000 Campylobacter infections (Nachamkin et al., 2000~. There may be other complications of and sequelae from foodborne diseases. For ex- ample, it has recently been reported that people infected with multiresistant

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38 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD salmonellae are more likely to die in the 6 months following the infection than uninfected individuals (Helms et al., 2002~. The full impact of illnesses includes acute morbidity and mortality, as well as the impact of subsequent complications and of long-term effects, such as life-long impairments from congenital toxoplas- mosis or early childhood diarrhea! illnesses in impoverished areas (Guerrant et al., 2002~. With more information about the frequency, duration, and disability caused by these complications, the burden of foodborne illness could be reesti- mated on a basis such as Disability Adjusted Life Years, a measure used to characterize the burden of many other public health problems (Murray and Lopez, 1997). Surveillance data can subdivide the burden of a specific infection. For ex- ample, the contribution of specific Salmonella serotypes to the overall burden of salmonellosis can be derived from their frequency. More specifically, the three most common serotypes of Salmonella, Typhimurium, Enteritidis, and Newport, together accounted for nearly half of all reported cases of salmonellosis in 2001, and thus of the burden of salmonellosis (Table 2.1~. The burden of reported foodborne outbreaks can also be measured. National foodborne outbreak reporting from 1998 through 2000 gave a combined annual incidence of 4.8 outbreaks per 1 million persons in the population (FDDB, 2002a). However, in addition to the limitations mentioned above, measuring the burden of disease due to outbreaks presents special challenges. For example, small out- breaks are particularly likely to go unrecognized and unreported, and it is likely that outbreak surveillance undercounts the true frequency of events for the rea- sons noted earlier. Moreover, a substantial fraction of outbreak investigations do not determine either the causative agent (the etiology) or the specific food that TABLE 2.1 The Top Ten Salmonella Serotypes Reported from Humans in 2001 Rank Serotype Number of Reported Cases Percentage of the Total 1 Typhimurium 6,999 22.1 2 Enteritidis 5,614 17.7 3 Newport 3,158 10.0 4 Heidelberg 1,884 5.9 5 Javiana 1,067 3.4 6 Montevideo 626 2.0 7 Oranienburg 595 1.9 8 Muenchen 5 8 3 1.8 9 Thompson 514 1.6 10 Saint Paul 469 1.5 Subtotal 21,509 67.9 Total 3 1,675 SOURCE: FDDB (2002c).

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58 SCIENTIFIC CRITERIA TO ENSURE SAFE FOOD and the major seed distributors put these instructions on the seed packages. Since then, outbreaks of salmonellosis have been linked to a sprout producer that reported disinfecting the seeds following those guidelines (Proctor et al., 2000), as well as to a sprout producer using less chlorine than recommended (Winthrop et al., 2003~. Another recent outbreak involved a single lot of clover seed shipped to two sprout producers in Colorado (Brooks et al.,2001~. The first did not disinfect the seed before sprouting and caused 1.13 documented infections per 50 lb-bag of seed sprouted, whereas the second did disinfect the seeds and caused only 0.29 infections per bag of seed. These outbreaks show that the disinfection strategy works partially, but is by itself insufficient to completely protect the public. In addition to disinfection, FDA also recommended lot-by-lot testing of the irriga- tion water for Salmonella (FDA, l999~. One outbreak occurred that was linked to sprouts that had passed such a test, suggesting that false negative tests may occur (Winthrop et al., 2003~. Continued surveillance and investigation indicate that the challenge of preventing outbreaks of salmonellosis from sprouts has been par- tially met, but complete prevention has still not been achieved. Multidrug-Resistant Salmonella Newport and Foods of Bovine Origin One of the latest food hazards to emerge in the United States is a new and highly resistant strain of S. Newport (Zansky et al., 2002~. This strain was first identified through NARMS surveillance in 1998, and its detection increased rapidly in 1999 and 2000. The strain is resistant to at least nine antibiotics because it possesses a large plasmid bearing several resistance genes, including an unusual gene, the AmpC cmy2 gene, which confers resistance to most cephalosporins. In 2001, a retrospective study of these strains in Massachusetts identified the same strains in ill and dying dairy cattle, and showed that visiting or working on dairy farms was a risk factor for illness (Gupta et al.,2001~. Later that year, an outbreak in Connecticut was traced to traditional cheese made from insufficiently pasteur- ized milk from Massachusetts dairy farms (McCarthy et al., 2002~. In 2002, an investigation of a multistate cluster of cases in the Northeast linked the illness to eating ground beef traced to meat from a single slaughter plant (Zansky et al., 2002~. Surveillance of human infections indicates a sharp increase in S. Newport infections, which in 2001 represented 10 percent of human salmonellosis (FDDB, 2002c). Many of the S. Newport strains are multidrug resistant (CDC, 2002b). The same organism has been detected since 1998 among isolates from animals, including bovines (Fedorka-Cray et al., 2002~. Among S. Newport isolated from cattle in 2000,74 percent had the AmpC multidrug resistance profile (ARS, 2002~. The evidence to date indicates that this strain has spread in epidemic fashion among cattle herds and that it affects the animals themselves, persons in contact with the animals, and consumers of bovine products (including meat, cheese, and other foods). Once control measures begin, success can be measured by monitor- ing animals and meat for this strain, by trends in human illness, and by outbreak

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THE SCIENCE OF PUBLIC HEALTH SURVEILLANCE 59 surveillance. Surveillance activities in animals, meat, and poultry can also pro- vide early warning of the spread of this strain or its plasmid to other food-animal populations. ANTICIPATING THE FUTURE In the future, it can be expected that new pathogens and new foodborne modes for transmission of such pathogens will continue to be recognized. New diagnostic strategies will identify some pathogens that currently are often or completely missed. Globalization of the food supply and concentration of food production, in turn, will create new challenges for detection, investigation, con- trol, and prevention of microbial foodborne hazards. The committee concludes that enhanced public health surveillance for human foodborne illnesses will be vital to identify and investigate these new challenges. In addition, it believes that a flexible monitoring system is needed that permits comparison of information from multiple points in the food supply. Just as moni- toring individual cattle at slaughter is an important strategy for documenting the continuing absence of bovine spongiform encephalopathy, a system for docu- menting the frequency of microbial or other foodborne hazards at the point of slaughter or processing could be critical to assessing and controlling these haz- ards in the future. Systematic surveys of potential hazards, such as the appearance of antibiotic resistant microbial strains in live animals in production, already provide information useful to industry, regulators, and the public health sector. In the future, similar systematic surveys of microbial contamination in various cat- egories of processing plants and at various points along processing lines could be equally useful for risk assessors. Preventing or minimizing contamination early in the chain, as well as identifying foods at higher risk of being contaminated so that they can be diverted out of the raw product market and into safer processing, may become the norm. For some foods, irradiation and other terminal microbial decontamination steps hold great potential (Tauxe, 2001~. High-pressure process- ing, for example, is already commercially available. Preventing foodborne dis- ease means preventing contamination before food reaches the consumer. Risk- management policies applied throughout the food system on farms, fisheries, and orchards; in slaughter facilities and processing plants; during transportation and storage; and in retail food stores, food service establishments, and homes- are all key parts of food safety. For certain products, it may be possible to define varying levels of process- ing depending on microbiological and other markers of the risk that they are contaminated. Already, eggs that are cracked or that come from farms contami- nated with S. Enteritidis are routinely approved for marketing after pasteuriza- tion; milk for manufacturing purposes meets standards that are different from Grade A milk; and an occasional carcass is passed for cooking rather than being

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