Introduction

Food-borne diseases are an important public health problem [1]. Although it is impossible to estimate the worldwide burden of food-borne diseases [2], numerous food-borne disease outbreaks have been reported to the national surveillance and reporting systems in diverse countries such as the USA, European countries, China, and Japan [3–6]. In Korea 200–300 food- and water-borne disease outbreaks (FBDOs) are annually reported to the national surveillance and reporting system. However, there is little information to describe epidemiological characteristics of FBDOs in Korea including causal pathogens, causal vehicles, and outbreak places. Therefore, identifying epidemiological characteristics of FBDOs in Korea can provide additional epidemiological information of FBDOs in eastern Asia and contribute to finding global trends of FBDOs. Furthermore, considering that the epidemiological information is essential to make more efficient national policy to prevent infectious diseases, identification of epidemiologic characteristics of FBDOs is significant. Thus, this study aimed to identify the epidemiologic characteristics of FBDOs in Korea by analyzing epidemiologic data on FBDOs reported to the Korea Centers for Disease Control and Prevention (KCDC) during 2007–2012.

Materials and methods

2.1 Data collection

A total of 253 local public health centers are responsible for most of the epidemiological investigation of outbreaks caused by infectious diseases [7] in Korea. However, when large-scale outbreaks occur that cannot be controlled by local public health resources, Epidemiological Intelligence Service officers from the 16 provincial offices or KCDC usually conduct the epidemiological investigation [8]. Most epidemiological investigation reports and all the reports about FBDOs by microorganisms are submitted to the database electronically. All FBDOs reports were reviewed by EIS officers in KCDC to decide official results. The official results regarding causal pathogens and causal vehicles are based on the KCDC investigation report Epidemiological Investigation Guideline for Water and Food-borne Disease [7]. The database, the official results, and the epidemiological investigation summaries of the FBDOs are all available on the Internet [9]. In this study, we excluded FBDOs that occurred outside Korea.

2.2 Definition

An FBDO is defined as the occurrence of two or more cases of a similar illness resulting from a common food [7]. The causal pathogen is confirmed by standard laboratory confirmative criteria. If the laboratory results do not meet the confirmative criteria, the causal pathogen is suspected by reasonable assessment of the relevant epidemiological investigations such as checking incubation period [10,11]. The causal vehicle is confirmed when the same microorganism is isolated from the vehicles and illnesses. If the microorganism is not isolated from the illnesses, the causal vehicles are suspected by the results of statistical analysis or the laboratory results of the vehicles with an appropriate incubation period. Because most foods contained diverse ingredients, we simplified the causal vehicles into six groups by the main ingredient: meat, seafood, fresh vegetables, pickled vegetables, water, and others. In this study, positive results include both confirmed cases and suspected cases.

Results

3.1 National surveillance during 2007–2012

A total of 2862 FBDOs were reported between 2007 and 2012. Of these,1794 FBDOs affecting 48,897 patients occurred domestically and 1068 FBDOs occurred outside Korea. During 2007, 440 FBDOs and 9830 patients were reported. Thereafter, FBDOs and patient numbers steadily decreased over the next 2 years and then plateaued until 2011. However, in 2012, FBDOs increased slightly accompanied by a large increase in the number of affected patients: 350 FBDOs with 8543 illnesses in 2008; 224 FBDOs with 6827 illnesses in 2009; 256 FBDOs with 7259 illness in 2010; 236 FBDOs with 7039 illnesses in 2011; and 288 FBDOs with 9408 illnesses in 2012.

3.2 Epidemiological characteristics of the places where the FBDOs occurred

Over the study period FBDOs occurred most frequently in public restaurants (881 FBDOs with an average of 16.1 patients/outbreak). However, school catering services caused the greatest number of patients. Although only 293 FBDOs were reported in schools over the 6 years, the scale of FBDOs was much higher at 79.6 patients/outbreak. Reports of FBDOs in public restaurants decreased dramatically after 2009, whereas FBDOs in schools increased gradually with the largest numbers of patients occurring from 2010 onwards (Figure 1).

3.3 Causal pathogens

The causal pathogens were identified in 1025 of the 1794 FBDOs (57%) over the 6 years. The main causal pathogens were as follow: norovirus, pathogenic Escherichia coli other than enterohemorrhagic E. coli (EHEC), Salmonella species, and Vibrio parahaemolyticus. The most common causal pathogen was norovirus, followed by pathogenic E. coli other than EHEC, Salmonella species, and V. parahaemolyticus.

In public restaurants, norovirus, which caused 28 FBDOs in 2007, became the most common causal pathogen in 2008 (33 FBDOs). However, it decreased rapidly and caused fewer than 10 FBDOs/year after 2009. Pathogenic E. coli other than EHEC caused 21 FBDOs in 2007 but after 2008 caused approximately 10 FBDOs/year. V. parahaemolyticus was the most common causal pathogen in 2007 and drastically decreased after 2008. Salmonella caused 10–20 FBDOs/year over the study period showing a fluctuation pattern.

In schools, norovirus outbreaks increased rapidly after 2010 and became the most common pathogen found in FBDOs. Pathogenic E. coli other than EHEC caused 5–15 FBDOs/year showing a fluctuation pattern during 2007–2011. Outbreaks caused by pathogenic E. coli other than EHEC rose to 25 FBDOs with a large number of patients in 2012. No outbreaks of V. parahaemolyticus were reported over the 6 years. Salmonella species, which caused four FBDOs in 2007, caused fewer than two FBDOs after 2008 (Table 1).

3.4 Causal vehicles of FBDOs

The causal vehicles of FBDOs were identified by epidemiological investigation in 24.1% of the FBDOs over the 6 years.

In public restaurants, FBDOs caused by seafood and meat were reported frequently. During 2007–2008, seafood caused more than 50 FBDOs. However, this number decreased by more than half after 2009. Meat caused approximately 5–10 FBDOs showing a fluctuating pattern. Water caused nine FBDOs during 2007–2008 and then decreased by two FBDOs during 2009–2010 and one FBDO during 2011–2012. Fresh vegetables were responsible for six FBDOs during 2007–2008 and decreased by three FBDOs in 2009–2010 and two FBDOs during 2011–2012. Pickled vegetables, which caused two FBDOs in 2008, did not cause any further FBDOs in public restaurants for the remainder of the study period (Table 2).

In schools, approximately one to three FBDOs were reported annually as being caused by seafood, meat, water, and fresh vegetables. One pickled vegetable-associated FBDO was reported during 2007–2008 but this number increased rapidly (Table 2). In 2012, a total of 18 pickled vegetable-associated FBDOs occurred: 13 FBDOs caused by pathogenic E. coli other than EHEC with 3152 illnesses, four FBDOs caused by norovirus with 427 illnesses, and one FBDO caused by Clostridium perfringens with 90 illnesses. Seven food factories that supplied pickled vegetables to schools were responsible for these FBDOs. Four out of the seven food factories caused pickled vegetable-associated FBDOs in more than two schools simultaneously.

Discussion

The number of FBDOs increased gradually in Korea until 2006 [12] and tended to decline after 2008. It was presumed that the decline of the FBDOs was associated with improved hygiene and continuous national efforts [13]. However, the number of illnesses by FBDOs increased drastically again in 2012 and we found that school catering service-associated outbreaks were responsible for that. It was interesting that public restaurant-associated outbreaks decreased at the same time. The pathogens involved in school catering service-associated outbreaks showed an increase in norovirus and pathogenic E. coli other than EHEC.

Norovirus is the main causal pathogen of FBDOs in the USA, European countries, China, and Japan. Norovirus was also reported as one of the most common causal pathogen of the FBDOs in Korea during 2007–2012. The norovirus outbreaks in public restaurants and schools decreased dramatically after 2009. It was presumed that the decline of the norovirus outbreaks was due to the national efforts to prevent the norovirus outbreaks including intensified inspection of seafood such as raw oysters and the norovirus surveillance system in underground water sources [14]. However, in 2012, the norovirus outbreaks emerged again in schools. The increases in norovirus outbreaks were also reported globally. Especially in the USA, UK, France, Australia, and Japan, the emergence of the new norovirus strain GII4, named the Sydney type, was reported as a cause of the increase of the norovirus outbreaks [15,16]. In Korea, norovirus GII-4 Sydney type was also detected in some of the norovirus outbreaks. However, more study is needed to establish whether the norovirus GII-4 Sydney type was a cause of the increase in norovirus outbreaks in schools in 2012.

Pathogenic E. coli other than EHEC has become a significant causal pathogen in Korea. Its significance is greater than norovirus because the scale of FBDOs caused by pathogenic E. coli other than EHEC was much larger than the scale of FBDOs caused by norovirus in school catering services. This is a unique epidemiologic characteristic of FBDOs in Korea compared with the USA, European countries, Japan, and China [3–6]. It has not been definitively established why pathogenic E. coli other than EHEC was the cause of such large-scale FBDOs in Korea.

It was presumed that pickled vegetables was an emerging causal vehicle in Korea. Most school catering services usually serve pickled vegetables sourced from food factories. One catering factory may supply pickled vegetables to a large number of schools, so that, if the pickled vegetables are contaminated in the factory, FBDOs can occur in multiple schools simultaneously. In the epidemiological investigations of food factories providing pickled vegetables in 2012, the causes of contamination were identified in only three of the seven factories. Underground water contaminations occurred in two factories and ingredient contamination in one. In Korea, 1077 food factories providing pickled vegetables were legally registered in 2013 and 228 catering factories used underground water [17]. Furthermore, where tap water is available, the catering factories still prefer to use underground water because of its low cost. According to national research in 2011, 16.2% of the underground water specimens tested was not safe for use [18,19]. Therefore, political support is needed to ensure that the factories use tap water instead of underground water. Although underground water is suspected as one of the main causal factors of pickled vegetable contamination, there are still factors that remain unknown. Epidemiological investigations and current monitoring of underground water in the food factories were not sufficient to control pickled vegetable-associated FBDOs. Hence, taking strong and specific actions including intensified inspection of the ingredients and monitoring of the cooking process of pickled vegetables are needed. For this, the Ministry of Food and Drug Safety recommends the application of Hazard Analysis and Critical Control Points (HACCP) for food factories and has a plan to apply mandatory HACCP to factories that make some kinds of pickled vegetable [20].

This research was significant in identifying emerging pathogens and causal vehicle using the analysis of FBDOs from 2007 to 2012. However, we acknowledge a number of potential limitations. First, it is easier to identify causal pathogens and causal vehicles in large-scale than in small-scale FBDOs. It is therefore possible that the pathogens and agents causing small-scale FBDOs may have been underestimated. Second, small-scale FBDOs may also be under-reported. Third, most human specimens collected were not stool samples but rectal smear samples. Therefore, rigorous tests for parasites could not be conducted in most of the FBDOs. Fourth, this study excluded FBDOs experienced in Korea but caused by exposure in other countries.

In conclusion, the decrease in the total number of FBDOs over the study period can be attributed to national efforts and general improvements in hygiene. However, large-scale FBDOs in schools increased rapidly in 2012. This increase was associated with pickled vegetable, an emerging causal vehicle, which has led to the emergence of norovirus and pathogenic E. coli other than EHEC. We recommend intensified inspections of food factories that supply pickled vegetables, including monitoring of underground water, ingredients, and the cooking process, as well as the strengthening of laboratory surveillance for norovirus and pathogenic E. coli.

Conflicts of interest

None of the authors have any conflicts of interest to disclose.

Acknowledgements

Acknowledgments

We express our gratitude to our colleagues in the local public health centers and EIS officers in the provincial office and KCDC for their help and co-operation in this project. This study was supported by a grant from the Korea Centers for Disease Control and Prevention (No. 4800-4838-300).

Article information

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

References

• 1. World Health Organization. Foodborne disease outbreak guidelines for investigation and control. [Internet]. 2008. Available from:. http://www.who.int/foodsafety/publications/foodborne_disease/outbreak_guidelines.pdf. [accessed 13.07.13].
• 2. World Health Organization. WHO initiative to estimate the global burden of foodborne diseases. Summary document. [Internet]. 2008. Available from:. http://www.who.int/foodsafety/foodborne_disease/ferg/en/index7.html. [accessed 13.07.13].
• 3. Centers for Disease Control and Prevention. Surveillance for foodborne disease outbreaks - United States, 2009-2010. MMWR Morb Mortal Wkly Rep 62(SS02). 2013 Jun 28;41−47.
• 4. European Centers for Disease Control and Prevention. EU summary report on zoonoses, zoonotic agents and foodborne outbreaks. ESFA J 11:2013;193−239.
• 5. Chen Y., Gou Y., Wang Z.. [Foodborne disease outbreaks in 2006 Report of the national foodborne disease surveillance network. China.] Wei Sheng Yan Jiu 39(3). 2010 May;331−334.
• 6. Shinagawa K.. [Foodborne disease outbreaks reported in Japan, 1952–2009—outbreaks of microbial foodborne disease.]. J Food Hyg Soc Japan 51(6). 2010;274−278.Article
• 7. Korea Centers for Disease Control and Prevention. Epidemiological investigation guideline for food and waterborne diseases 2012. 2012. Korea Centers for Disease Control and Prevention; Osong.
• 8. Kwon G., Moon S., Kwak W.. Epidemic intelligence service officers and field epidemiology training program in Korea. Public Health Res Perspect 4(4). 2013 Aug;215−221.Article
• 9. http://www.cdc.go.kr/CDC/info/CdcKrInfo0519.jsp?menuIds=HOME001-MNU0003-MNU0072-MNU0073.
• 10. Korea Centers for Disease Control and Prevention. Epidemiological investigation guideline for food and waterborne diseases 2013. 2013. Korea Centers for Disease Control and Prevention; Osong.
• 11. Lynch M., Painter J., Woodruff R.. Surveillance for foodborne disease outbreaks—United States, 1998–2002. MMWR Surveill Summ 55(SS10). 2006 Nov 10;1−42.
• 12. Kwun J.W., Lee C.H.. [Trends of recent foodborne disease outbreaks in Korea.]. J Korean Med Assoc 50:2007;73−81.Article
• 13. Gwack J., Lee K.C., Lee H.J.. Trends in water and foodborne disease outbreaks in Korea. Public Health Res Perspect 1:2010;50−54.Article
• 14. Korea Food and Drug Safety Administration. Guideline for management of food safety, 2009. 2009. Korea Food and Drug Safety Administration; Seoul: pp 323−328.
• 15. van Beek J., Ambert-Balay K., Botteldoorn N.. Indications of worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill 18(1). 2013 Jan;8−9. PubMed
• 16. Centers for Disease Control and Prevention. Note from the field: emergence of new norovirus strain GII.4 Sydney-United States, 2012. MMWR Morb Mortal Wkly Rep 62(3). 2013 Jan 25;55
• 17. Korea Ministry of Food and Drug Safety. [Official report on surveillance of food manufacturers that use underground water, 2013.] [Internet]. 2013. Available from:. http://www.mfds.go.kr/daejeon/index.do?mid=27&seq=20188&cmd=v. [accessed 13.07.13].
• 18. Korea Ministry of Environment. 2011 waterworks statistics. 2012. Korea Ministry of Environment; Sejong: pp 3−5.
• 19. Korea Ministry of Land. Transport, and Maritime Affairs. Annual report on surveillance for underground water. 2012. Korea Ministry of Land, Transport, and Maritime Affairs; Daejeon: pp 361−363.
• 20. Korea Ministry of Food and Drug Safety. Guideline for management of food safety, 2003. 2013. Korea Ministry of Food and Drug Safety; Cheongwon: pp 63−76.

Figure 1

Total numbers of food- and water-borne disease outbreaks and illnesses by location and year during 2007–2012.

Table 1

Total numbers of food- and water-borne disease outbreaks (FBDOs) and illnesses by causal vehicle, location, and year during 2007–2012

Causal pathogens	Total No. of FBDOs by year (total patients)
	2007	2008	2009	2010	2011	2012
Total FBDOs
Norovirus	72 (1704)	64 (2465)	28 (553)	28 (1918)	26 (1300)	50 (1784)
Pathogenic Escherichia coli other than EHEC	64 (2615)	27 (1911)	34 (2460)	22 (1857)	32 (2088)	34 (4390)
Vibrio parahaemolyticus	27 (542)	28 (377)	9 (88)	17 (297)	8 (130)	12 (195)
Salmonella species	38 (1213)	21 (376)	17 (455)	26 (669)	23 (937)	10 (157)
Others	51 (1553)	63 (1753)	32 (1947)	65 (1558)	50 (1509)	47 (1672)
Public restaurants
Norovirus	28 (316)	33 (532)	5 (33)	6 (159)	2 (17)	8 (139)
Pathogenic E. coli other than EHEC	29 (996)	13 (539)	4 (88)	8 (321)	10 (315)	3 (32)
V. parahaemolyticus	21 (485)	19 (288)	7 (77)	9 (186)	6 (112)	12 (195)
Salmonella species	20 (708)	10 (219)	8 (279)	20 (510)	18 (910)	7 (102)
Others	23 (333)	35 (675)	8 (447)	24 (278)	19 (463)	15 (189)
Schools
Norovirus	15 (475)	18 (1120)	9 (388)	8 (1280)	12 (970)	27 (1366)
Pathogenic E coli other than EHEC	16 (1222)	6 (1030)	18 (2130)	9 (1369)	10 (933)	25 (4182)
V. parahaemolitycus	0	0	0	0	0	0
Salmonella species	4 (164)	0	2 (28)	0	1 (2)	0
Others	9 (865)	9 (604)	7 (856)	9 (569)	10 (564)	11 (862)

EHEC = enterohemorrhagic E. coli.

Table 2

Total numbers of food- and water-borne disease outbreaks (FBDOs) and illnesses by location and year during 2007–2012

Causal vehicles	Total numbers of FBDOs by year (total patients)
	2007–2008	2009–2010	2011–2012
Public restaurants	476 (6708)	174 (2961)	213 (3397)
Pickled vegetables	2 (222)	0	0
Fresh vegetables	6 (141)	3 (136)	2 (17)
Seafood	54 (814)	17 (211)	15 (337)
Water	9 (131)	1 (54)	2 (66)
Meat	11 (480)	11 (516)	14 (512)
Others	32 (494)	21 (838)	17 (826)
Unknown	362 (4426)	121 (1206)	163 (1639)
Schools	103 (6685)	77 (7213)	113 (9435)
Pickled vegetables	0	4 (216)	21 (4300)
Fresh vegetables	1 (467)	3 (572)	3 (122)
Seafood	3 (498)	4 (232)	4 (174)
Water	8 (1135)	2 (759)	6 (261)
Meat	1 (84)	4 (497)	2 (445)
Others	6 (368)	7 (663)	4 (277)
Unknown	84 (4133)	53 (4274)	73 (3856)

Figure & Data

References

Citations

Citations to this article as recorded by  

• Measures for preventing norovirus outbreaks on campus in economically underdeveloped areas and countries: evidence from rural areas in Western China
  Huali Xiong, Fengxun Ma, Dayi Tang, Daiqiang Liu
  Frontiers in Public Health.2024;[Epub]     CrossRef
• Phage biocontrol of zoonotic food-borne pathogen Vibrio parahaemolyticus for seafood safety
  Jung Hyen Lee, Minjin Oh, Byoung Sik Kim
  Food Control.2023; 144: 109334.     CrossRef
• Vibrio-infecting bacteriophages and their potential to control biofilm
  Ana Cevallos-Urena, Jeong Yeon Kim, Byoung Sik Kim
  Food Science and Biotechnology.2023; 32(12): 1719.     CrossRef
• Antibiotic Resistance Profiles of Bacteria Isolated from Hotspot Environments in Bahir Dar City, Northwestern Ethiopia
  Kindu Geta, Mulugeta Kibret
  Journal of Multidisciplinary Healthcare.2022; Volume 15: 1403.     CrossRef
• Inhibitory Effects of Crude Fucoidan Extract from Hizikia fusiformis against Norovirus Causing Foodborne Disease
  Hyojin Kim, Mi Sook Chung
  Korean Journal of Food and Cookery Science.2018; 34(5): 519.     CrossRef
• High level of drug resistance by gram-negative bacteria from selected sewage polluted urban rivers in Addis Ababa, Ethiopia
  Teshome Belachew, Amete Mihret, Tesfaye Legesse, Yihenew Million, Kassu Desta
  BMC Research Notes.2018;[Epub]     CrossRef
• Inhibitory Effects of Allium chinense and Its Dimethyl Disulfide against Murine Norovirus as a Surrogate for Foodborne Virus
  Mi Sook Chung
  Korean Journal of Food and Cookery Science.2018; 34(2): 222.     CrossRef
• Inactivation of norovirus surrogates by kimchi fermentation in the presence of black raspberry
  Garam Bae, Jeongwon Kim, Hyojin Kim, Jong Hyeon Seok, Dan Bi Lee, Kyung Hyun Kim, Mi Sook Chung
  Food Control.2018; 91: 390.     CrossRef
• Metagenomic Sequencing for Surveillance of Food- and Waterborne Viral Diseases
  David F. Nieuwenhuijse, Marion P. G. Koopmans
  Frontiers in Microbiology.2017;[Epub]     CrossRef
• Prevalence, antimicrobial resistance and multiple-locus variable-number tandem-repeat analysis profiles of diarrheagenic Escherichia coli isolated from different retail foods
  Lili Wang, Hiromi Nakamura, Eriko Kage-Nakadai, Yukiko Hara-Kudo, Yoshikazu Nishikawa
  International Journal of Food Microbiology.2017; 249: 44.     CrossRef
• Complete genome sequence ofVibrio parahaemolyticusFORC_023 isolated from raw fish storage water
  Han Young Chung, Eun Jung Na, Kyu-Ho Lee, Sangryeol Ryu, Hyunjin Yoon, Ju-Hoon Lee, Hyeun Bum Kim, Heebal Kim, Sang Ho Choi, Bong-Soo Kim, David Rasko
  Pathogens and Disease.2016; 74(4): ftw032.     CrossRef
• An outbreak of norovirus infection associated with fermented oyster consumption in South Korea, 2013
  H. G. CHO, S. G. LEE, M. Y. LEE, E. S. HUR, J. S. LEE, P. H. PARK, Y. B. PARK, M. H. YOON, S. Y. PAIK
  Epidemiology and Infection.2016; 144(13): 2759.     CrossRef
• Molecular epidemiology of norovirus in South Korea
  Sung-Geun Lee, Han-Gil Cho, Soon-Young Paik
  BMB Reports .2015; 48(2): 61.     CrossRef
• Three Gastroenteritis Outbreaks in South Korea Caused by the Consumption of Kimchi Tainted by Norovirus GI.4
  Ji-Hyuk Park, Sunyoung Jung, Jaeseung Shin, Jeong Su Lee, In Sun Joo, Deog-Yong Lee
  Foodborne Pathogens and Disease.2015; 12(3): 221.     CrossRef
• Environmental monitoring of bacterial contamination and antibiotic resistance patterns of the fecal coliforms isolated from Cauvery River, a major drinking water source in Karnataka, India
  Sinosh Skariyachan, Arpitha Badarinath Mahajanakatti, Nisha Jayaprakash Grandhi, Akshatha Prasanna, Ballari Sen, Narasimha Sharma, Kiran S Vasist, Rajeswari Narayanappa
  Environmental Monitoring and Assessment.2015;[Epub]     CrossRef
• Detection of viable murine norovirus using the plaque assay and propidium-monoazide-combined real-time reverse transcription-polymerase chain reaction
  Minhwa Lee, Dong Joo Seo, Jina Seo, Hyejin Oh, Su Been Jeon, Sang-Do Ha, Jinjong Myoung, In-Soo Choi, Changsun Choi
  Journal of Virological Methods.2015; 221: 57.     CrossRef
• Emergence of Norovirus GII.4 variants in acute gastroenteritis outbreaks in South Korea between 2006 and 2013
  Han-Gil Cho, Po-Hyun Park, Sung-Geun Lee, Ju-Eun Kim, Kyung-A Kim, Hyeun-Kyong Lee, Eun-Mi Park, Myong-Ki Park, Sun-Young Jung, Deog-Yong Lee, Mi-hye Yoon, Jong-Bok Lee, Soon-Young Paik
  Journal of Clinical Virology.2015; 72: 11.     CrossRef