Analysis of foodborne disease outbreaks for improvement of food safety programs in Seoul, Republic of Korea, from 2002 to 2006.

Introduction

Food safety management has been an important public health issue in every country. Foodborne diseases (FBD) have posed growing public health threats and caused economic impacts to many countries during the past three decades. Foodborne diseases are not only a primary concern of public health in developing countries; they also pose a significant public health threat in developed countries (Tauxe, 1997).

Lack of intensive FBD surveillance often hampers measuring the magnitude of impacts of FBD on public health, which is particularly true in developing countries. As many occurrences of FBD are undiagnosed or unreported, the true dimension of FBD impacts on public health is unknown. It has been estimated that in 2005 alone 1.8 million people died from diarrheal diseases (Rocourt, Moy, Vierk, & Schlundt, 2003). It is suggested that each year more than 10% of the population suffers from FBD in industrialized countries (Kaferstein, Motajemi, & Bettcher, 1997). For example, it is estimated that each year FBD causes approximately 76 million cases, 325,000 hospitalizations, and 5,000 deaths in the U.S. (Schlundt, 2002).

Seoul, Republic of Korea, is one of the world's largest cities, with a population of 10.3 million. It hosted the summer Olympic Games in 1988 and the World Cup soccer tournament in 2002 (Seoul City, 2007). South Korea (Republic of Korea) has been a member country in the Organization for Economic Cooperation and Development (OECD) since 1996. The OECD facilitates further economic, environmental, and social developments in the country.

Many factors have contributed to the increase in FBD. Industrialization and urbanization have led to revolutionary changes in the food supply system, as well as mass production and an increase in the number of food service establishments and food outlets (Collins, 1997; Kaferstein, Motajemi, & Bettcher, 1997). The globalization of food trade and international travel have increased the risk for cross-border transmission of infectious diseases. South Korea has increased its trade with neighboring countries. Since the Asian economic crisis in 1997-1998, much of South Korea's agricultural products have been imported from neighboring countries such as China, Thailand, and Vietnam. Foreign laborers have increased in manufacturing, farming, and construction as well.

Recent changes in the social and economic environments of Korea have changed patterns of food consumption and have increased the risk of foodborne illnesses, which therefore requires improvements in food safety programs. Hence, recent FBD occurrences in Seoul were analyzed to identify focus areas in order to improve the efficiency of food safety programs.

Materials and Methods

This report summarizes data on the outbreaks and human cases of FBD reported to Seoul City from 2002 through 2006. Foodborne diseases are reportable diseases in South Korea. Laboratory confirmation of human cases was made in, and related data were obtained from, the Seoul Metropolitan Government Institute of Health and Environment. An FBD outbreak is defined as the occurrence of a gastrointestinal illness among two or more people in which an investigation links the consumption of a common meal or food items. For botulism, however, even one case is considered an outbreak. The number of cases is defined as the number of laboratory-confirmed cases.

The protocol in FBD outbreak investigations is to collect fecal samples from suspected cases when FBDs are reported. Samples are not collected if the person had been treated with antibiotics before sampling. All the collected samples of FBD outbreak cases were tested according to the infectious disease guideline of Korea Center for Disease Control and Prevention (KCDCP). The collected samples were tested for bacterial and viral organisms and parasites. Bacterial tests included Salmonella spp., pathogenic E. coli, Staphylococcus aureus, Vibrio parahaemolyticus, Listeria monocytogenes, Campylobacter jejuni, Clostridium perfringens, Yersinia enterocolitica, and Bacillus cereus. The viruses examined were norovirus, rotavirus, astrovirus, and enteric adenovirus. Stool specimens were also tested for Cryptosporidium parvum, Giardia lamblia, and Entamoeba histolytica.

Statistical analysis was conducted with SAS version 9.1. The statistical significance of comparisons among groups was assessed with analysis of variance (ANOVA).

Results

FBD Outbreaks and Cases in Seoul from 2002 to 2006

The number of outbreaks varied year to year (F [Fisher's F ratio] = 3.21, p = .019) (Table 1). The highest number of average outbreaks per month (5.1) occurred in 2006 and the lowest (0.8) in 2002. Both 2003 and 2006 had average monthly case numbers of 209.4 and 213.3, respectively, about 10 times greater than the lowest case number (17.8 per month) in 2002. Compared to 2002, a marked increase of FBD outbreaks was reported in 2003 but there after occurrences seemed to decrease until 2006, when the highest numbers occurred (Table 1).

TABLE 1
Mean Number of Outbreaks and Cases of Foodborne Disease per Month in
Seoul, Republic of Korea, 2002-2006

Year     Outbreaks/Month (SD)  Cases/Month (SD)

2002           0.8 (1.2)           17.8 (30.8)

2003           2.8 (4.0)          209.4 (435.9)

2004           1.6 (1.8)           98.9 (208.9)

2005           1.9 (1.4)           61.1 (97.4)

2006           5.1 (5.2)          213.3 (416.8)

F-Value          3.21                 1.11

p-Value          .019                  .359

Facilities Involved in FBD Outbreaks

During the period of 2002 to 2006, restaurants were associated with an average of 12.4 outbreaks per year, followed by schools (10.0), workplaces (2.4), others (3.4), and unknown (1.2) (F = 2.86, p = .052) (Table 2). In number of cases, the school lunch outbreaks involved 1,054 per year. Restaurant and workplace outbreaks averaged 173.8 cases and 137 cases per year, respectively (F = 4.62, p = 008) (Table 2).

TABLE 2
Mean Number of Outbreaks and Cases of Foodborne Disease by Facility,
Seoul, Republic of Korea, 2002-2006

Facility Type  Outbreaks (SD)     Cases (SD)

School           10.0 (10.3)   1054.0 (990.3)

Restaurant       12.4 (10.0)     173.8(85.4)

Workplace         2.4 (2.1)     137.0 (149.5)

Others            3.4 (2.3)      55.4 (35.7)

Unknown           1.2 (1.3)      21.0 (28.1)

F-Value             2.86            4.62

p-Value             .052            .008

Temporal Distribution of the FBD Outbreaks and Cases in Seoul

The temporal distribution of FBD outbreaks and cases from 2002 to 2006 is shown in Figure 1. The average number of outbreaks per year was highest (6.8) in June. July and March had the second highest number (3.8), followed by September (3.4), August (2.6), and May (2.4). The FBD outbreaks from October to February occurred rarely and ranged from 0.4 to 1.6. The monthly variation of outbreak occurrences was not statistically significant (F = 1.57, p = .1389).

[FIGURE 1 OMITTED]

The highest number of cases per year was reported in June (498.6). March had the second highest case numbers (341.2), followed by May (180.8), September (112.8), December (83.2), and November (61.2). Unlike the number of outbreaks, July and August had the lowest numbers of cases (40.8 and 43.8, respectively) other than January and February. The monthly variation of case numbers was not statistically significant (F = 1.51, p= .1587).

Causative Agents of the FBD Outbreaks in Seoul from 2002 to 2006

The etiologic agents that were responsible for the outbreaks and the cases are shown in Table 3. Among the identified agents, norovirus was responsible for an average of 6.4 outbreaks (F = 3.72, p = .003) and 584 cases per year (F = 3.22, p = .007) and was the most significant etiologic agent. Staphylococcus aureus caused the second highest average number of outbreaks (6.2) and cases (414.8), followed by Salmonella spp. (4.2 outbreaks, 95 cases) and pathogenic E. coli (one outbreak, 85.6 cases) (Table 3). The number of outbreaks from Staphylococcus aureus gradually increased during this period. No parasites were responsible for any of the FBD outbreaks during this period. An average of nine outbreaks and 215.4 cases per year were from unidentified causative agents (Table 3).

TABLE 3
Mean Number of Outbreaks and Cases of Foodborne Disease per Year by
Causative Agents, Seoul, Republic of Korea, 2002-2006

Causative Agent       Outbreaks (SD)    Cases (SD)

Salmonella spp.         4.2 (1.9)      95.0 (51.2)

S. aureus               6.2 (3.7)     414.8 (292.9)

V. parahasemolyticus    1.8 (2.2)      18.8 (34.0)

Pathogenic E. coli      1.0 (0.7)      85.6 (137.4)

Norovirus               6.4 (8.6)     584.0 (639.8)

Rotavirus               0.2 (0.4)       2.2 (4.9)

Astrovirus              0.4 (0.5)      17.2 (26.8)

Other                   0.2 (0.4)       8.2(18.3)

Unknown                 9.0 (5.7)     215.4 (290.9)

F-Value                   3.72            3.22

p-Value                   .003            .007

Discussion

Food safety is an important part of public health, involving agriculture and other food production sectors. Technological developments in food production and new control policies have contributed to safer food production and the decrease of foodborne illnesses in most developed countries (Altekruse & Swerdlow, 1996). FBD still remains an important public health threat, however. In addition, changing consumer lifestyles as well as increasing global food trades are altering patterns of FBD occurrences, which necessitates a periodic analysis of FBD outbreak patterns and assessment of the current food safety program.

To improve the food safety programs, FBD outbreaks and the associated cases from 2002 to 2006 were analyzed. Significant yearly variation of FBD outbreaks was observed (F = 3.21, p= .019). More FBD outbreaks occurred in 2003 and 2006 than the other three years, and the case numbers in those years increased as well. The yearly variation of FBD occurrences and case numbers could be explained by the facilities associated with FBD outbreaks. Our study shows that FBD outbreaks mainly occurred in restaurants (42.2%) and schools (34%), followed by the workplace (8.2%) (F = 2.86, p = .052) (Table 2). A majority (73.1%) of FBD cases occurred in schools and 12.1% in restaurants (F = 4.62, p = .008). Students in primary and secondary schools used to eat their own homemade lunch. In 2002, no FBD outbreaks related to school lunches were reported. The sudden increase of school lunch-related FBD outbreaks and cases in 2003 and thereafter is largely due to the full-scale operation of the new school lunch program in Seoul. The new program uses catering services to prepare and deliver lunches foe primary and secondary schools. Intensive and consistent food safety trainings and inspections, targeting catering services, might have reduced FBD outbreaks.

Changes in Korean family structures have been implicated in altering patterns of food consumption, due to an increased number of women in the workforce (Schmid et al., 2007). Since the Asian economic recession of 1997-1998, job security and the male workforce have declined sharply in Korea. As a result, the divorce rate and the number of working women have increased (National Statistical Office, Korea, 2005). The increase in single heads of households and working women has probably resulted in less time for cooking and food preparation at home and more dependency on restaurants and catering services. With these changes in food consumption patterns, an increased potential for restaurant-associated FBD occurrences is to be expected. Our study showed that FBD occurrences sharply increased in 2005 and 2006 suggesting the need for an intensive restaurant food safety program, where trainings and inspections are devised on the basis of restaurant-specific risk factors.

The workplace was the third type of facility implicated in FBD outbreaks. Considering the numerous workplaces in Seoul, one of the biggest cities in the world, the number of FBD outbreaks and cases is low (Table 2). This is probably because a majority of workplaces have their own cooking facilities managed by at least a licensed nutritionist and food hygienist in order to provide hot food to employees. Other facilities involved in FBD outbreaks during the 2002-2006 period were funeral facilities, though the numbers were low. In traditional Korean culture, visitors to a funeral are expected to stay overnight in the facility to console the bereaved. The visitors are usually served catered foods. Foods are sometimes improperly held due to lack of attention. Though the tradition has been gradually changing, it is still prevalent in Korean society.

More FBD outbreaks occurred in the summer months. Warmer temperatures increase bacterial FBD occurrences (D'Souza, Becker, Hall, & Moodie, 2004; Fleury, Charron, Holt, Allen, & Maarouf, 2006). Out of 147 outbreaks in our study, 64.6% occurred from May to September. The school year in South Korea also likely affects the temporal trend of FBD occurrences, because schools had the most FBD case numbers and the second largest number of FBD outbreaks. Unlike in the U.S., a school year in Korea starts with the spring semester, from early March until mid-July, followed by the fall semester, from early September until mid-December. For this reason, along with temperature, June had the highest number of outbreaks and cases, although July and August are the hottest months of the year in Korea. High FBD occurrences in March and September correspond to the beginning of each school semester, indicating that intensive food safety trainings and inspections at the beginning of each semester might have reduced the FBD outbreaks and the associated cases.

FBD outbreaks in the winter--from December through February--increased in 2005 and 2006. This outcome is open to various interpretations. One possibility is that Seoul City Laboratory testing capability has been enhanced since 2003, when the city added Reverse Transcriptase Polymerase Chain Reaction (RT-PCR) food-borne virus testing (Seymour & Appleton, 2001; Widdowson et al., 2005) to the routine testing battery. The increase of laboratory capability might have encouraged more reports, especially in the winter when bacterial FBD occurrences are less likely. Regardless, occurrences of winter FBD outbreaks highlight the need not only for sensitive FBD surveillance but also for active food safety programs even in the winter months.

During the study period, bacterial agents were responsible for more outbreaks (44.9%) than viral agents (23.8%) but both types of pathogens caused a similar numbers of cases, i.e., 42.6% of cases were bacterial and 41.9% of cases were viral. Among the FBD pathogens identified, norovirus and Staphylococcus aureus caused 61.7% of outbreaks and 81.5% of cases. The future food safety training and inspection programs should adequately address risk factors associated with contamination of food items by these two primary FBD agents.

Unidentifiable causes were responsible for 30.6% of FBD outbreaks and 14.5% of cases, suggesting a need to further improve protocols of FBD investigation and surveillance.

Conclusion

A total of 147 FBD outbreaks and 7,206 cases were reported in Seoul, Korea, from 2002 to 2006. A majority (73.1%) of the FBD cases were associated with school lunch programs. The highest number of outbreaks and cases occurred in June. Among the identified FBD pathogens, norovirus and Staphylococcus aureus were responsible for 61.7% of outbreaks and 81.5% of cases, and were the two main FBD pathogens in Seoul. This study indicates that critical control points in the school lunch program should be identified and incorporated into the food safety training and inspection. Risk factors for food contamination by norovirus or Staphylococcus aureus should also be indentified. To increase efficiency of food safety programs in school lunches, timely and intensive trainings and inspections would be helpful to achieve a reduced number of cases.

Acknowledgements: The authors are grateful to Terry Gratton, Dr. P.H., of University of North Texas School of Public Health for his review and comments on the manuscript. This work was a collaborative effort of the Seoul Metropolitan Government Institute of Health and Environmental and Department of Environmental & Occupational Health at University of North Texas.

Corresponding Author: Joon-Hak Lee, Assistant Professor, Department of Environmental and Occupational Health, School of Public Health, University of North Texas-Health Science Center at Fort Worth, 3400 Camp Bowie Boulevard, Fort Worth, TX 76107. E-mail: [e-mail].

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