Surveillance for Foodborne Disease Outbreaks --United States, 1993-1997

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Sonja J. Olsen, Ph.D.
Linda C. MacKinon, M.P.H.
Joy S. Goulding
Nancy H. Bean, Ph.D.
Laurence Slutsker, M.D.

Problem/Condition: Since 1973, CDC has maintained a collaborative surveillance program for collection and periodic reporting of data on the occurrence and causes of foodborne disease outbreaks (FBDOs) in the United States.

Reporting Period Covered: This summary reviews data from January 1993 through December 1997.

Description of System: The Foodborne-Disease Outbreak Surveillance System reviews data concerning FBDOs, defined as the occurrence of two or more cases of a similar illness resulting from the ingestion of a common food. State and local public health departments have primary responsibility for identifying and investigating FBDOs. State, local, and territorial health departments use a standard form to report these outbreaks to CDC.

Results: During 1993-1997, a total of 2,751 outbreaks of foodborne disease were reported (489 in 1993, 653 in 1994, 628 in 1995, 477 in 1996, and 504 in 1997). These outbreaks caused a reported 86,058 persons to become ill. Among outbreaks for which the etiology was determined, bacterial pathogens caused the largest percentage of outbreaks (75%) and the largest percentage of cases (86%). Salmonella serotype Enteritidis accounted for the largest number of outbreaks, cases, and deaths; most of these outbreaks were attributed to eating eggs. Chemical agents caused 17% of outbreaks and 1% of cases; viruses, 6% of outbreaks and 8% of cases; and parasites, 2% of outbreaks and 5% of cases.

Interpretation: The annual number of FBDOs reported to CDC did not change substantially during this period or from previous years. During this reporting period, S. Enteritidis continued to be a major cause of illness and death. In addition, multistate outbreaks caused by contaminated produce and outbreaks caused by Escherichia coli O157:H7 remained prominent.

Actions Taken: Current methods to detect FBDOs are improving, and several changes to improve the ease and timeliness of reporting FBDO data are occurring (e.g., a revised form to simplify FBDO reporting by state health departments and electronic reporting methods). State and local health departments continue to investigate and report FBDOs as part of efforts to better understand and define the epidemiology of foodborne disease in the United States. At the regional and national levels, surveillance data provide an indication of the etiologic agents, vehicles of transmission, and contributing factors associated with FBDOs and help direct public health actions to reduce illness and death caused by FBDOs.

The reporting of foodborne and waterborne diseases in the United States began greater than 60 years ago when state and territorial health officers, concerned about the high morbidity and mortality caused by typhoid fever and infantile diarrhea, recommended that cases of "enteric fever" be investigated and reported. The purpose of investigating and reporting these cases was to obtain information regarding the role of food, milk, and water in outbreaks of intestinal illness as the basis for public health action. Beginning in 1925, the Public Health Service published summaries of outbreaks of gastrointestinal illness attributed to milk (1). In 1938, it added summaries of outbreaks caused by all foods. These early surveillance efforts led to the enactment of important public health measures (e.g., the Pasteurized Milk Ordinance) that led to decreased incidence of enteric diseases, particularly those transmitted by milk and water (2).

From 1951 through 1960, the National Office of Vital Statistics reviewed reports of outbreaks of foodborne illness and published annual summaries in Public Health Reports. In 1961, CDC -- then the Communicable Disease Center -- assumed responsibility for publishing reports concerning foodborne illness. During 1961-1965, CDC stopped publishing annual reviews but reported pertinent statistics and detailed individual investigations in the MMWR.

The present system of surveillance for foodborne and waterborne diseases began in 1966 when reports of enteric disease outbreaks attributed to microbial or chemical contamination of food or water were incorporated into an annual summary. Since 1966, the quality of investigative reports has improved greatly, with more active participation by state and federal epidemiologists in outbreak investigations. Outbreaks of waterborne diseases and foodborne diseases have been reported in separate annual summaries since 1978 because of increased interest and activity in surveillance for waterborne diseases. Previous summaries of data reported to the Foodborne-Disease Outbreak Surveillance System were published for 1983-1987 (3) and 1988-1992 (4). Surveillance has served three purposes:

• Disease prevention and control. The investigation of foodborne-disease outbreaks leads to prevention and control measures in the food industry. Public health officials identify critical control points in the path from farm to table that can be monitored to reduce contamination by foodborne pathogens. Changes at all levels of food production -- including the farm, slaughterhouse, and production plant -- have contributed to a cleaner food supply.
• Knowledge of disease causation. Outbreak investigations are a critical means of identifying new and emerging pathogens as well as maintaining awareness about ongoing problems. However, the pathogen is not identified in many outbreaks because of delayed or incomplete laboratory investigation, inadequate laboratory capacity, or inability to recognize a pathogen as a cause of foodborne disease. Prompt and thorough investigations of foodborne outbreaks aid in the timely identification of etiologic agents and lead to appropriate prevention and control measures.
• Administrative guidance. By analyzing several years of data on foodborne-disease outbreaks, epidemiologists can monitor trends over time in the prevalence of outbreaks caused by specific etiologic agents, food vehicles, and common errors in food handling. This information provides the basis for regulatory and other changes to improve food safety.

The objective of this report is to summarize epidemiologic data on foodborne-disease outbreaks (FBDOs) reported to CDC from 1993 through 1997.

Agencies use a standard form (CDC Form 52.13, Investigation of a Foodborne Outbreak) to report FBDOs to CDC. A revised form became effective October 1999; this report summarizes data collected with the old form (Appendix A). Most reports are submitted by state, local, and territorial health departments; however, they also can be submitted by federal agencies and other sources. CDC reviews data on the forms to determine whether a specific food vehicle and etiologic agent have been confirmed for an outbreak (Appendix B). In some instances, questions concerning etiology are referred back to the reporting agencies.

An FBDO is defined as the occurrence of two or more cases of a similar illness resulting from the ingestion of a common food.* Laboratory or clinical guidelines for confirming an FBDO outbreak vary for bacterial, chemical, parasitic, and viral agents (Appendix B, Table B). Outbreaks of unknown etiology are divided into four subgroups according to incubation period of the illness: less than 1 hour (probable chemical poisoning); 1-7 hours (probable Staphylococcus aureus or Bacillus cereus food poisoning); 8-14 hours (other agents); nd greater than or equal to 15 hours (other agents).

Several types of outbreaks are excluded from the Foodborne-Disease Outbreak Surveillance System such as outbreaks that occur on cruise ships (these are summarized and published periodically in scientific publications) (5); outbreaks in which the food was eaten outside the United States, even if the illness occurred within the United States; and outbreaks that are traced to water intended for drinking (these are reported to the Waterborne-Disease Outbreak Reporting System). A second limitation is the classification of food vehicles in the surveillance system. Food vehicles can be classified as individual food items (e.g., milk or eggs) or as food categories (e.g., ice cream or multiple vehicles). Therefore, the number of outbreaks attributed to a particular food item might fall under several food vehicle categories. For example, homemade ice cream containing milk and eggs is listed under "ice cream" rather than "milk" or "eggs." The category "Mexican-style food" includes vehicles containing beef, cheese, lettuce, and other ingredients. However, only one food vehicle is identified for each outbreak on the basis of the available epidemiologic and laboratory data. A third limitation is that FBDOs are not included in the surveillance system if the route of transmission from the contaminated food to the infected persons is indirect. For example, in 1988, chitterlings (pig intestines) were the ultimate source of a cluster of Yersinia enterocolitica infections among several infants; however, this outbreak was not included because the infants did not eat the chitterlings (6). A fourth limitation is that no standard criteria exist for classifying a death as being FBDO-related. This determination is made by the reporting agency.

In this report, 1993-1997 data on foodborne-disease outbreaks are presented as follows:

• Outbreaks, by state, for each of the 5 years (Figures 1-5).
• Outbreaks, cases, and deaths, by etiology, for the 5-year period (Table 1) and for each of the 5 years (Tables 2-6).
• Outbreaks, by etiology and month of occurrence, for each of the 5 years (Tables 7-11).
• Outbreaks, by etiology and place here food was eaten, for each of the 5 years (Tables 12-16).
• Outbreaks, cases, and deaths, by vehicle of transmission, for each of the 5 years (Tables 17-21).
• Outbreaks, by etiology and vehicle of transmission, for each of the 5 years (Tables 22-26).
• Outbreaks, by etiology and contributing factors, for each of the 5 years (Tables 27-31).

From 1993 through 1997, 878 (32%) of the 2,751 outbreaks reported to CDC had a known etiology; these outbreaks accounted for 50,788 (59%) of 86,058 infections (Table 1). Of the 878 outbreaks with a known etiology, 75% (86% of infections) were caused by bacterial pathogens, 17% (1% of infections) by chemical agents, 6% (8% of infections) by viruses, and 2% (5% of infections) by parasites. In most (68%) outbreaks, the etiology was not determined. The incubation period was reported for 1,406 (75%) of the 1,873 outbreaks that had an unknown etiology; in 44 (3%) outbreaks, the incubation period was less than 1 hour; in 428 (30%) outbreaks, 1-7 hours; in 285 (20%) outbreaks, 8-14 hours; and in 649 outbreaks (46%), greater than or equal to 15 hours.

Local investigators may report factors they believe contributed to the outbreak. For each of the years from 1993 through 1997, the most commonly reported food preparation practice that contributed to foodborne disease was improper holding temperature; the second most commonly reported practice was inadequate cooking of food (Tables 27-31). Food obtained from an unsafe source was the least commonly reported factor for the 5 years combined. In most outbreaks caused by bacterial pathogens, the food was stored at improper holding temperatures.

The annual number of outbreaks reported during 1993-1997 ranged from 477 to 653 (Tables 2-6). These numbers are comparable with those in previous years (3,4). During this period, multistate outbreaks caused by ground beef contaminated with Escherichia coli O157:H7 (7,8) and fresh produce contaminated with Salmonella or E. coli O157:H7 (9) were frequently reported (Tables 22-26). A massive outbreak of Salmonella serotype Enteritidis infections was linked to commercially distributed ice cream made from a liquid premix that had been transported in tanker trucks used previously to haul liquid raw eggs (10). Unexpected vehicles of transmission (e.g., alfalfa sprouts [11], apple cider [12], and orange juice [13]) were also reported. Several outbreaks involved imported food items.

Salmonella caused 357 (55%) of the 655 bacterial FBDOs with a known etiology during 1993-1997; 55% of these 357 outbreaks were caused by S. Enteritidis. S. Enteritidis was the most frequently reported cause of FBDOs, accounting for 7% of all outbreaks and 22% of outbreaks for which an etiology was determined. S. Enteritidis also resulted in more deaths than any other pathogen; of the 10 persons who died as a result of S. Enteritidis, four (40%) were residents of nursing homes.

As in previous years, bacterial pathogens caused most outbreaks and infections with a known etiology (3,4). However, 68% of reported FBDOs were of unknown etiology, a finding that highlights the need for improved epidemiologic and laboratory investigations. Approximately 50% of these outbreaks had an incubation period of greater than or equal to 15 hours, indicating that many were of viral etiology. Viruses (e.g., Norwalk and Norwalklike viruses) are probably a much more important cause of foodborne disease outbreaks than is currently recognized. Although local and state public health laboratories have often lacked the resources and expertise to diagnose viral pathogens, methods to diagnose these agents are now increasingly available in some state laboratories. Thus, outbreaks of viral etiology might be more likely to be identified and reported in the future.

Of the FBDOs with a known etiology, multistate outbreaks caused by contaminated produce and outbreaks caused by E. coli O157:H7 remained prominent. S. Enteritidis continued to be a major cause of illness and death. Approximately 40% of persons who died as a result of S. Enteritidis were residents of nursing homes -- a finding that reflects the seriousness of S. Enteritidis infections in elderly persons, many of whom might be immunocompromised. Persons can decrease their risk for egg associated infections caused by S. Enteritidis by not eating raw or undercooked eggs. Nursing homes, hospitals, and commercial kitchens should use pasteurized egg products for all recipes requiring pooled or lightly cooked eggs (14).

Several outbreaks reported during 1993-1997 involved imported food items. This finding demonstrates the role of food production and distribution in FBDOs.

Foodborne diseases cause an estimated 76 million illnesses and 5,000 deaths in the United States each year (15). Although foodborne diseases are common, only a fraction of these illnesses are routinely reported to CDC because a complex chain of events must occur before a foodborne infection is reported; a break at any point in the chain will result in a case not being reported. In addition, most reported foodborne illnesses are sporadic in nature; only a small number are identified as being part of an outbreak and thus are reported through the Foodborne-Disease Outbreak Surveillance System. For example, Salmonella infection causes an estimated 1.4 million foodborne illnesses annually (15). However, from 1993 through 1997, a total of 189,304 Salmonella infections (approximately 38,000 annually) were reported through the National Salmonella Surveillance System (16-20), which is a passive, laboratory-based system. In contrast, during the same period, 357 recognized outbreaks of Salmonella infection resulting in 32,610 illnesses were reported through the Foodborne-Disease Outbreak Surveillance System. Thus, the system greatly underestimates the burden of foodborne disease.

Moreover, the number of outbreaks summarized in this report represents a small proportion of the outbreaks that actually occurred during the period under surveillance. Most outbreaks are never recognized, and those that are recognized frequently go unreported. The likelihood that an outbreak is brought to the attention of public health authorities depends on many factors, including consumer and physician awareness, interest, and motivation to report the incident as well as the resources and disease surveillance activities of state and local public health and environmental agencies. Outbreaks that are most likely to be brought to the attention of public health authorities include those that are large, interstate, or restaurant associated or that can cause serious illness, hospitalization, or death. Therefore, this report should not be used to draw conclusions about the absolute or relative incidence of foodborne-disease outbreaks related to specific causes. For example, foodborne diseases characterized by short incubation periods (e.g., those caused by a chemical agent or staphylococcal enterotoxin) are more likely to be recognized as common source FBDOs than are diseases with longer incubation periods (e.g., hepatitis A). Outbreaks involving less commonly identified pathogens (e.g., B. cereus, enterotoxigenic E. coli , or Giardia lamblia) are less likely to have a confirmed etiology because these organisms are not always considered in clinical, epidemiologic, and laboratory investigations of FBDOs.

Current methods to detect FBDOs are improving. For example, two new tools that enhance detection of FBDOs are the Salmonella Outbreak Detection Algorithm (SODA) and PulseNet. SODA applies a statistical algorithm to data reported through CDC s National Salmonella Surveillance System to identify significant increases over a historical baseline for any given serotype (21). This technology, now employed at state health departments, can be used to help identify clusters or outbreaks. PulseNet is a national network of public health laboratories that perform pulsed field gel electrophoresis (PFGE) on bacteria that might be foodborne (22). The network permits rapid comparison of PFGE patterns through an electronic database at CDC; closely related PFGE patterns suggest a common source. PulseNet is helpful in epidemiologic investigations, particularly those that involve many states.

Several changes to improve the ease and timeliness of reporting are occurring. In October 1999, CDC issued a revised FBDO reporting form to simplify reporting by state health departments. In addition, electronic reporting methods such as fax, e-mail, and the Internet are being increasingly used to make reporting more timely.

The investigation and reporting of FBDOs by state and local health departments are important steps in efforts to better understand and define the epidemiology of foodborne disease in the United States. At the regional and national levels, surveillance data provide an indication of the etiologic agents, vehicles of transmission, and contributing factors associated with FBDOs and help direct public health actions.

References

1. Public Health Service. Annual report of the surgeon general on the Public Health Service of the United States for the fiscal year 1924-1925. Washington, DC: Government Printing Office, 1925:34-5.
2. Potter ME, Kaufmann AF, Blake PA, Feldman RA. Unpasteurized milk: the hazards of a health fetish. JAMA 1984;252:2048-52.
3. CDC. Foodborne disease outbreaks, 5year summary, 1983-1987. MMWR 1990;39(No. SS1):15-57.
4. CDC. Surveillance for foodborne-disease outbreaks -- United States, 1988-1992. MMWR 1996;45(No. SS5):1-66.
5. Koo D, Maloney K, Tauxe R. Epidemiology of diarrheal disease outbreaks on cruise ships, 1986 through 1993. JAMA 1996;275:545-7.
6. Lee LA, Taylor J, Carter GP, et al. Yersinia enterocolitica O:3: an emerging cause of pediatric gastroenteritis in the United States. J Infect Dis 1991;163:660-3.
7. Bell BP, Goldoft M, Griffin PM, et al. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic syndrome from hamburgers: the Washington experience. JAMA 1994;272:1349-53.
8. CDC. Escherichia coli O157:H7 infections associated with eating a nationally distributed commercial brand of frozen ground beef patties and burgers -- Colorado, 1997. MMWR 1997;46:777-8.
9. Tauxe R, Kruse H, Hedberg C, Potter M, Madden J, Wachsmuth K. Microbial hazards and emerging issues associated with produce: a preliminary report to the National Advisory Committee on Microbiologic Criteria for Foods. J Food Protect 1997;60:1400-8.
10. Hennessy TW, Hedberg CW, Slutsker L, et al. A national outbreak of Salmonella Enteritidis infections from ice cream. N Engl J Med 1996;334:1281-6.
11. Mahon BE, Ponka A, Hall WN, et al. An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J Infect Dis 1997;175:876-82.
12. Cody SH, Glynn MK, Farrar JA, et al. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann Intern Med 1999;130:202-9.
13. Cook KA, Dobbs TE, Hlady WG, et al. Outbreak of Salmonella serotype Hartford infections associated with unpasteurized orange juice. JAMA 1998;280:1504-9.
14. Levine WC, Smart JF, Archer DL, Bean NH, Tauxe RV. Foodborne disease outbreaks in nursing homes, 1975 through 1987. JAMA 1991;266:2105-9.
15. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607-25.
16. CDC. Salmonella surveillance: annual tabulation summary, 1993. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, CDC, 1994.
17. CDC. Salmonella surveillance: annual tabulation summary, 1994. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, CDC, 1995.
18. CDC. Salmonella surveillance: annual tabulation summary, 1995. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, CDC, 1996.
19. CDC. Salmonella surveillance: annual tabulation summary, 1996. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, CDC, 1997.
20. CDC. Salmonella surveillance: annual tabulation summary, 1997. Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service, CDC, 1998.
21. Hutwagner LC, Maloney EK, Bean NH, Slutsker L, Martin SM. Using laboratory-based surveillance data for prevention: an algorithm for detecting Salmonella outbreaks. Emerg Infect Dis 1997;3:395-400.
22. Tauxe RV. Emerging foodborne diseases: an evolving public health challenge. Emerg Infect Dis 1997;3:425-34.

* Before 1992, three exceptions existed to this definition; only one case of botulism, marine toxin intoxication, or chemical intoxication was required to constitute an FBDO if the etiology was confirmed. The definition was changed in 1992 to require two or more cases to constitute an outbreak.

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