Skip Navigation
Skip to contents

Epidemiol Health : Epidemiology and Health


Author index

Page Path
HOME > Browse articles > Author index
Inyeong Hwang 1 Article
A large outbreak of Salmonella enterica serovar Thompson infections associated with chocolate cake in Busan, Korea
Youngduck Eun, Hyesun Jeong, Seungjin Kim, Wonseo Park, Byoungseon Ahn, Dongkeun Kim, Eunhee Kim, Eunhee Park, Sunhee Park, Inyeong Hwang, Hyunjin Son
Epidemiol Health. 2019;41:e2019002.   Published online January 9, 2019
  • 17,729 View
  • 417 Download
  • 31 Web of Science
  • 35 Crossref
AbstractAbstract AbstractSummary PDFSupplementary Material
This study aimed to reveal the epidemiologic characteristics of the outbreak of gastroenteritis caused by Salmonella enterica serovar Thompson in Busan Metropolitan City and to identify points for improvement to prevent of food-borne disease outbreak.
This was a case-control study. The control group comprised asymptomatic students in the same classes of the cases. The presence or absence of symptoms, ingestion of each food provided by school meal service, and commonly ingested foods in addition to those foods in meal service were investigated. Moreover, specimens collected from rectal swab, preserved foods, and environmental surface were tested.
Of the 6,092 subjects, 1,111 (1,083 students, 22 school personnel, and 6 foodservice employees) were included in the case group; this corresponded to an 18.4% attack rate. Symptoms included diarrhea (n=1,051, 94.6%), abdominal pain (n=931, 83.8%), febrile sensation (n=502, 45.2%), and vomiting (n=275, 24.8%). The epidemic curves of each 10 schools were unimodal. Investigation of food intake showed a significantly high odds ratio for chocolate cake in 5 out of the 10 schools. Laboratory test detected Salmonella enterica serovar Thompson both in rectal swab specimens of 9 schools and in collected preserved chocolate cakes of 9 schools. Pulsed-field gel electrophoresis test result showed that Salmonella enterica seorvar Thompson isolated from human and foods were the same.
The source of infection for the Salmonella enterica serovar Thompson outbreak in the 10 schools of Busan Metropolitan City is chocolate cake. Traceback investigation for origin of contaminated food in food-borne disease outbreak and safety control during food production should be more enhanced.
Korean summary
이 연구는 2018년 9월 부산광역시 10개 학교에서 급식으로 제공된 초콜릿 케익으로 인해 발생한 살모넬라 톰슨 감염증 대규모 유행의 역학 조사 결과이다. 학교 급식과 같은 대규모 집단급식은 원재료에서 급식 제공까지 안전하게 관리되어야 하며 식품매개감염병 집단 발생 역학조사에 있어 오염원에 대한 체계적 역추적 조사와 기관 간 협업의 중요성을 강조하였다.


Citations to this article as recorded by  
  • Salmonella prevalence in raw cocoa beans and a microbiological risk assessment to evaluate the impact of cocoa liquor processing on the reduction of Salmonella
    Xingchen Zhao, Liesbeth Jacxsens, Vesela Tzeneva, Michiel Kokken, Anett Winkler, Cécile Vadier, Nicolau de Toledo, Tomasz Seliwiorstow, Mieke Uyttendaele
    Journal of Food Protection.2024; : 100327.     CrossRef
  • Nontyphoidal Salmonella Outbreaks Associated With Chocolate Consumption: A Systematic Review
    Zacharie Patà, Pietro B. Faré, Sebastiano A. G. Lava, Gregorio P. Milani, Mario G. Bianchetti, Simone Janett, Isabella Hunjan, Lisa Kottanattu
    Pediatric Infectious Disease Journal.2024; 43(5): 420.     CrossRef
  • Emergence and genomic characteristics of multi-drug-resistant Salmonella in pet turtles and children with diarrhoea
    Wei Wang, Feng Liu, Hui Li, Menghan Li, Yujie Hu, Fengqin Li, Jing Xiao, Yinping Dong
    Microbial Genomics .2024;[Epub]     CrossRef
  • Epidemiology and genetic characterization of tet(X4)-positive Klebsiella pneumoniae and Klebsiella quasipneumoniae isolated from raw meat in Chengdu City, China
    Weishuai Zhai, Yiqing Wang, Honghu Sun, Bo Fu, Qidi Zhang, Congming Wu, Jianzhong Shen, Dejun Liu, Yang Wang
    Biosafety and Health.2024; 6(2): 116.     CrossRef
  • Dissemination of IncC plasmids in Salmonella enterica serovar Thompson recovered from seafood and human diarrheic patients in China
    Zengfeng Zhang, Dai Kuang, Xuebin Xu, Zeqiang Zhan, Hao Ren, Chunlei Shi
    International Journal of Food Microbiology.2024; 417: 110708.     CrossRef
  • Characterization of Salmonella species from poultry slaughterhouses in South Korea: carry-over transmission of Salmonella Thompson ST292 in slaughtering process
    Yewon Cheong, Jun Bong Lee, Se Kye Kim, Jang Won Yoon
    Journal of Veterinary Science.2024;[Epub]     CrossRef
  • Rapid identification and absolute quantitation of zero tolerance-Salmonella enterica subsp. enterica serovar Thompson using droplet digital polymerase chain reaction
    Eiseul Kim, Chang Hun Choi, Seung-Min Yang, Min-Ki Shin, Hae-Yeong Kim
    LWT.2023; 173: 114333.     CrossRef
  • Prevalence and characterization of Staphylococcus aureus in raw eggs and it's growth and enterotoxin a production in egg contents
    Pengfei Zhang, Panpan Wang, Xueting Fu, Xu Xu, Fuqian Ruan, Ting Wang, Guanhong Chang, Yangli Wan, Yao Zhang, Xin Wang
    LWT.2023; 174: 114379.     CrossRef
  • An Extensive Review on the Exploration of Non-Typhoidal Salmonella and its Associated Infections
    Pallavi Rawat, Vidya Chauhan, Juhi Chaudhary, Neha Chauhan
    Journal of Pure and Applied Microbiology.2023; 17(1): 112.     CrossRef
  • Rapid detection of Salmonella enterica subsp. enterica serovar Thompson by real-time fluorescence loop-mediated isothermal amplification (LAMP) and colorimetric LAMP combined without DNA extraction in the field
    Eiseul Kim, Seung-Min Yang, Hae-Yeong Kim
    LWT.2023; 182: 114850.     CrossRef
  • Characterization of Salmonella Thompson-specific bacteriophages and their preventive application against Salmonella Thompson biofilm on eggshell as a promising antimicrobial agent in the food industry
    Md. Ashrafudoulla, Hee Jeong Kim, Eun Her, Shanjida Shaila, Si Hong Park, Sang-Do Ha
    Food Control.2023; 154: 110008.     CrossRef
  • Emergence of the fourth mobile sulfonamide resistance gene sul4 in clinical Salmonella enterica
    Kai Peng, Jianping Deng, Nianli Zou, Xinran Sun, Weifeng Huang, Ruichao Li, Xiaorong Yang
    Frontiers in Microbiology.2023;[Epub]     CrossRef
  • Development of rapid on-site detection of Salmonella Enteritidis, S. Typhimurium, and S. Thompson in food samples using an ultrafast PCR system
    Eiseul Kim, Seung-Min Yang, Hae-Yeong Kim
    Food Bioscience.2023; 56: 103242.     CrossRef
  • Whole-Genome Sequencing Analysis of Non-Typhoidal Salmonella Isolated from Breeder Poultry Farm Sources in China, 2020–2021
    Zijing Ju, Lulu Cui, Changwei Lei, Mengze Song, Xuan Chen, Ziwei Liao, Tiejun Zhang, Hongning Wang
    Antibiotics.2023; 12(11): 1642.     CrossRef
  • The Role of Suspension Array Technology in Rapid Detection of Foodborne Pollutants: Applications and Future Challenges
    Xue-Xia Jia, Zi-Yi Yao, Zhi-Xian Gao, Zhen-Chuan Fan
    Critical Reviews in Analytical Chemistry.2022; 52(6): 1408.     CrossRef
  • Efficacy of ficin and peroxyacetic acid against Salmonella enterica serovar Thompson biofilm on plastic, eggshell, and chicken skin
    Shamsun Nahar, Ha Lim Jeong, Ah Jin Cho, Jun-Ha Park, Sangha Han, Younsoo Kim, Si-Hong Park, Sang-Do Ha
    Food Microbiology.2022; 104: 103997.     CrossRef
  • Through the Looking Glass: Genome, Phenome, and Interactome of Salmonella enterica
    Jean Guard
    Pathogens.2022; 11(5): 581.     CrossRef
  • Revisiting the Biological Behavior of Salmonella enterica in Hydric Resources: A Meta-Analysis Study Addressing the Critical Role of Environmental Water on Food Safety and Public Health
    Alan Douglas de Lima Rocha, Rafaela Gomes Ferrari, Walter Esfrain Pereira, Laiorayne Araújo de Lima, Patrícia Emília Naves Givisiez, Andrea Isabel Moreno-Switt, Magaly Toro, Enrique Jesús Delgado-Suárez, Jianghong Meng, Celso José Bruno de Oliveira
    Frontiers in Microbiology.2022;[Epub]     CrossRef
  • Transcriptome analysis revealed the role of capsular polysaccharides in desiccation tolerance of foodborne Staphylococcus aureus
    Hui Wang, Jiawei Shen, Kai Ma, Chengfeng Zhu, Mengcheng Fang, Xue Hou, Shijie Zhang, Wenhui Wang, Ting Xue
    Food Research International.2022; 159: 111602.     CrossRef
  • Resistance and Pathogenicity of Salmonella Thompson Isolated from Incubation End of a Poultry Farm
    Jingju Zhang, Jing Liu, Chen Chen, Yufeng Wang, Xiaojie Chen, Xiubo Li, Fei Xu
    Veterinary Sciences.2022; 9(7): 349.     CrossRef
  • Outbreak of monophasic Salmonella Typhimurium Sequence Type 34 linked to chocolate products
    Sejal Lund, Maliha Tahir, Laiba Imran Vohra, Amatul Hadi Hamdana, Shahzaib Ahmad
    Annals of Medicine & Surgery.2022;[Epub]     CrossRef
  • Characterization of extended-spectrum cephalosporins and fluoroquinolone resistance of a Salmonella enterica serovar Thompson isolate from ready-to-eat pork product in China
    Lili Li, Rikke Heidemann Olsen, Jian Xiao, Meidan Liang, Hecheng Meng, Shifu Peng
    Frontiers in Microbiology.2022;[Epub]     CrossRef
  • Investigation of microbial contamination and use of food additives for pet foods in Gwangju, Korea
    Daewoong Lim, Ji Yeon Kim, Ahjin An, Jiyeong Park, Hajin Jeong, Jinju Gwak, Doori Seo, Jae Gi Lee, Miseon Jang, Taekyeong Ji, Yonghwan Kim
    Korean Journal of Veterinary Service.2022; 45(3): 155.     CrossRef
  • Genomic characteristics and comparative genomics analysis of Salmonella enterica subsp. enterica serovar Thompson isolated from an outbreak in South Korea
    Woojung Lee, Eiseul Kim, Hyunwoo Zin, Soohyun Sung, Jungha Woo, Min Jung Lee, Seung-Min Yang, Seung Hwan Kim, Soon Han Kim, Hae-Yeong Kim
    Scientific Reports.2022;[Epub]     CrossRef
  • Comparative Analysis of Salmonella enterica subsp. enterica Serovar Thompson Isolates associated with Outbreaks Using PFGE and wgMLST
    Youngho Koh, Yunyoung Bae, Min-Jung Lee, Yu-Si Lee, Dong-Hyun Kang, Soon Han Kim
    Journal of Microbiology and Biotechnology.2022; 32(12): 1605.     CrossRef
  • A Comparison of Salmonella Survival and Detection Using an Enrichment Technique in Dry- and Wet-Inoculated Rendered Chicken Fat Treated with Sodium Bisulfate
    Janak Dhakal, Charles G. Aldrich
    Journal of Food Protection.2021; 84(2): 249.     CrossRef
  • Predictive Modeling for the Growth of Salmonella spp. in Liquid Egg White and Application of Scenario-Based Risk Estimation
    Mi Seon Kang, Jin Hwa Park, Hyun Jung Kim
    Microorganisms.2021; 9(3): 486.     CrossRef
  • Mathematical Modeling for the Growth of Salmonella spp. and Staphylococcus aureus in Cake at Fluctuating Temperatures
    Heeyoung Lee, Jin Hwa Park, Yu Kyoung Park, Hyun Jung Kim
    Applied Sciences.2021; 11(6): 2475.     CrossRef
  • Rapid Detection of Salmonella Enteritidis, Typhimurium, and Thompson by Specific Peak Analysis Using Matrix-Assisted Laser Desorption Ionization Time-of-Flight Mass Spectrometry
    Seung-Min Yang, Eiseul Kim, Dayoung Kim, Jiwon Baek, Hyunjin Yoon, Hae-Yeong Kim
    Foods.2021; 10(5): 933.     CrossRef
  • Parvoviral enteritis and salmonellosis in raccoons with sudden death
    Chun-Ming Lin, Benjamin Hause, Deanna Gualtieri, Nicholas Robinson
    Journal of Veterinary Diagnostic Investigation.2021; 33(6): 1172.     CrossRef
  • Assessment of the Microbial Quality of Industrial Ready-to-Eat Salads Containing Meat Products
    Mohammadreza Koushki, Paliz Koohy-Kamaly, Sara Sohrabvandi
    Current Research in Nutrition and Food Science Journal.2021; 9(2): 662.     CrossRef
  • A dynamic predictive model for the growth of Salmonella spp. and Staphylococcus aureus in fresh egg yolk and scenario-based risk estimation
    Jin Hwa Park, Mi Seon Kang, Kyung Min Park, Hee Young Lee, Gyeong Sik Ok, Min Seon Koo, Seok In Hong, Hyun Jung Kim
    Food Control.2020; 118: 107421.     CrossRef
  • Nationwide surveillance on serotype distribution and antimicrobial resistance profiles of non-typhoidal Salmonella serovars isolated from food-producing animals in South Korea
    Abraham Fikru Mechesso, Dong Chan Moon, Su-Jeong Kim, Hyun-Ju Song, Hee Young Kang, Seok Hyeon Na, Ji-Hyun Choi, Ha-Young Kim, Soon-Seek Yoon, Suk-Kyung Lim
    International Journal of Food Microbiology.2020; 335: 108893.     CrossRef
  • Survival of Salmonella and Enterococcus faecium in High Fructose Corn Syrup and Honey at Room Temperature (22 °C)
    Jaza Alshammari, Nitin Dhowlaghar, Yucen Xie, Jie Xu, Juming Tang, Shyam Sablani, Mei-Jun Zhu
    Food Control.2020; : 107765.     CrossRef
  • A quantitative risk assessment model for salmonellosis due to milk chocolate consumption in Brazil
    Fernanda B. Campagnollo, Marianna M. Furtado, Beatriz S. Silva, Larissa P. Margalho, Joyce A. Carminati, Anderson S. Sant’Ana, Maristela S. Nascimento
    Food Control.2019; : 106804.     CrossRef

Epidemiol Health : Epidemiology and Health