Epidemiologic Investigation
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An outbreak of hepatitis A associated with salted clams in Busan, Korea
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Hyunjin Son
, Miyoung Lee
, Youngduck Eun
, Wonseo Park
, Kyounghee Park
, Sora Kwon
, Seungjin Kim
, Changhoon Kim
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Epidemiol Health. 2022;44:e2022003. Published online December 29, 2021
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DOI: https://doi.org/10.4178/epih.e2022003
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7,229
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Abstract
OBJECTIVES
In July 2019, there were multiple reports on patients with hepatitis A among the visitors of a restaurant in Busan. The current study presents the results of an epidemiological investigation and outlines the supplementary measures that would help with hepatitis A control.
METHODS
A cohort study was conducted for all 2,865 customers who visited restaurant A from June to July. Using a standardized questionnaire, participants reported the presence of hepatitis A symptoms and whether they had consumed any of 19 food items. As for participants who had visited public health centers, their specimens were collected.
RESULTS
From the study cohort, 155 participants (5.4%) had confirmed hepatitis A. The epidemic curve was unimodal, and the median number of days from the restaurant visit to symptom onset was 31 days. A genotype analysis indicated that 89 of 90 tested patients had hepatitis A virus (HAV) genotype 1A. The results of a multivariate logistic regression analysis indicated that the ingestion of salted clams increased the risk of hepatitis A by 68.12 times (95% confidence interval [CI], 9.22 to 510.87). In an unopened package of salted clams found and secured through traceback investigation, HAV genotype 1A was detected.
CONCLUSIONS
To prevent people from ingesting uncooked clams, there needs to be more efforts to publicize the dangers of uncooked clams; the food sampling test standards for salted clams should also be expanded. Furthermore, a laboratory surveillance system based on molecular genetics should be established to detect outbreaks earlier.
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Summary
Korean summary
2019년 7월, 부산시의 한 식당을 방문한 사람에서 다수의 A형간염 환자가 신고되었다. 2019년 6월 1일부터 7월 28일까지 해당 식당을 방문하여 카드 결제를 한 사람과 동반자 2,865명 전체를 대상으로 코호트 조사를 수행하였다. A형간염에 확진 된 사람은 총 155명으로 발병률은 5.4%였다. 다변량 로지스틱 회귀분석 결과 조개젓 섭취는 A형간염 발병 위험을 68.62배(95% CI, 9.22 to 510.87) 증가시키는 것으로 나타났다. 익히지 않은 조개류를 섭취하지 않도록 더욱 홍보를 강화해야 한다.
Key Message
In July 2019, there were multiple reports on patients with hepatitis A among the visitors of a restaurant in Bu¬san. A cohort study was conducted for all 2,865 customers who visited the restaurant from June to July. From the study cohort, 155 participants (5.4%) had confirmed hepatitis A. The results of a multivariate logistic regression analysis indicated that the ingestion of salted clams increased the risk of hepatitis A by 68.12 times. To prevent people from ingesting uncooked clams, there needs to be more efforts to publicize the dangers of uncooked clams.
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Citations
Citations to this article as recorded by

- Investigating the spatio-temporal variation of hepatitis A in Korea using a Bayesian model
Jaehong Jeong, Mijeong Kim, Jungsoon Choi
Frontiers in Public Health.2023;[Epub] CrossRef - Influence of temperature and precipitation on the incidence of hepatitis A in Seoul, Republic of Korea: a time series analysis using distributed lag linear and non-linear model
Kiook Baek, Jonghyuk Choi, Jong-Tae Park, Kyeongmin Kwak
International Journal of Biometeorology.2022; 66(9): 1725. CrossRef
Special Article
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Causes and countermeasures for repeated outbreaks of hepatitis A among adults in Korea
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Moran Ki
, Hyunjin Son
, Bo Youl Choi
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Epidemiol Health. 2019;41:e2019038. Published online September 22, 2019
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DOI: https://doi.org/10.4178/epih.e2019038
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8,828
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219
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8
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Supplementary Material
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Abstract
The 2019 hepatitis A outbreak has become increasingly prevalent among adults in Korea and is the largest outbreak since that in 2009-2010. The incidence in the current outbreak is highest among adults aged 35-44 years, corresponding to the peak incidence among those aged 25-34 years 10 years ago. This may indicate a cohort effect in the corresponding age group. Causes of these repeated outbreaks of hepatitis A in Korea are low level of immunity among adults, Korean food culture that consumes raw seafood such as salted clam and inadequate public health system. Among countermeasures, along with general infectious disease control measures including control of the infectious agent, infection spread, and host, urgent actions are needed to review the vaccination policy and establish an adequate public health system.
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Summary
Korean summary
2019년 한국 성인의 A형 간염 유행은 10년전 대규모 유행 이후 가장 큰 규모로발생하고 있다. 주 발생 연령이 10년전 유행보다 10세가 증가한 35-44세로 나타나 연령 코호트 효과라 볼 수 있다. 우리나라의 A형 간염 반복 유행의 원인은 성인의 낮은 집단면역수준, 어패류 생식문화, 공중보건의료체계 미비 등으로 보인다. 이에 대한 대책은 일반적인 감염관리대책인 감염원관리, 전파관리, 숙주관리와 함께 효율적인 백신접종정책, 공고한 공중보건관리체계 마련 등의 근본적 대책이 시급하다.
Key Message
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Citations
Citations to this article as recorded by

- Investigating the spatio-temporal variation of hepatitis A in Korea using a Bayesian model
Jaehong Jeong, Mijeong Kim, Jungsoon Choi
Frontiers in Public Health.2023;[Epub] CrossRef - Influence of temperature and precipitation on the incidence of hepatitis A in Seoul, Republic of Korea: a time series analysis using distributed lag linear and non-linear model
Kiook Baek, Jonghyuk Choi, Jong-Tae Park, Kyeongmin Kwak
International Journal of Biometeorology.2022; 66(9): 1725. CrossRef - A case-control study of acute hepatitis A in South Korea, 2019
Jung Hee Hyun, Ju Young Yoon, Sang Hyuk Lee
Osong Public Health and Research Perspectives.2022; 13(5): 352. CrossRef - An outbreak of hepatitis A associated with salted clams in Busan, Korea
Hyunjin Son, Miyoung Lee, Youngduck Eun, Wonseo Park, Kyounghee Park, Sora Kwon, Seungjin Kim, Changhoon Kim
Epidemiology and Health.2021; 44: e2022003. CrossRef - Hepatitis A vaccination
Li Zhang
Human Vaccines & Immunotherapeutics.2020; 16(7): 1565. CrossRef - A Study on Seroprevalence of Hepatitis A Virus among Healthcare Workers at a University-Affiliated Hospital in Deajeon, Korea
Seul Ki Ji, So Hee Jang, Min Hee Park, Ji Eun Lee, Hye Sook Jeong, Joonhong Park, Seung Beom Han, Yunmi Yi, Sun Hee Park
The Korean Journal of Healthcare-Associated Infection Control and Prevention.2020; 25(1): 54. CrossRef - Epidemiology of viral disease outbreaks in Odisha, India (2010–2019)
J.S. Kshatri, J. Turuk, J. Sabat, S. Subhadra, L.M. Ho, S. Rath, S.K. Palo, D. Bhattacharya, B. Dwibedi, S. Pati
Epidemiology and Infection.2020;[Epub] CrossRef - Current State and Problems of Hepatitis A and E in Japan
Jun Inoue, Atsushi Masamune
Nihon Naika Gakkai Zasshi.2020; 109(7): 1439. CrossRef
Original Articles
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Age-period-cohort analysis of hepatitis A incidence rates in Korea from 2002 to 2012
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Joo Yeon Seo
, Sungyong Choi
, BoYoul Choi
, Moran Ki
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Epidemiol Health. 2016;38:e2016040. Published online September 30, 2016
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DOI: https://doi.org/10.4178/epih.e2016040
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11,866
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Abstract
OBJECTIVES
This study aimed to evaluate the epidemiology of hepatitis A in Korea from 2002 to 2012 using age-period-cohort analyses.
METHODS
We used claims data from the Korean National Health Insurance Corporation for the entire population. Census data from 2010 were used as the standard population. The incidence of hepatitis A was assumed to have a Poisson distribution, and the models and effects were evaluated using the intrinsic estimator method, the likelihood ratio, and the Akaike information criterion.
RESULTS
The incidence of hepatitis A gradually increased until 2007 (from 17.55 to 35.72 per 100,000 population) and peaked in 2009 (177.47 per 100,000 population). The highest incidence was observed among 27-29-year-old individuals when we omitted data from 2005 to 2007. From 2005 to 2007, the peak incidence was observed among 24-26-year-old individuals, followed by 27-29-year-olds. The best model fits were observed when the age-period-cohort variables were all considered at the same time for males, females, and the whole population.
CONCLUSIONS
The incidence of hepatitis A exhibited significant age-period-cohort effects; its incidence peaked in 2009 and was especially high among Koreans 20-39 years of age. These epidemiological patterns may help predict when high incidence rates of hepatitis A may occur in developing countries during their socioeconomic development.
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Summary
Korean summary
A형 간염 발생률은 서서히 증가하는 추세였으나 2009년 가파르게 증가하여 최고조에 이르렀으며, (177 명 100,000 명당) 1978–1986 년 생 (발생 당시25–35세) 사이에서 가장 높았다. 남성, 여성, 전체 인구를 통틀어 가장 적합한 모형은 연령, 기간, 코호트 변수를 모두 고려한 모형이었다. 한국의 A형 간염 발생은 고위험 양상에서 중등도 위험양상으로 변해가고 있으며, 이는 역학적 변화를 겪는 여러 나라의 향후 양상을 예측하는데 도움이 될 것이다.
Key Message
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Citations
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- Hepatitis A vaccination
Li Zhang
Human Vaccines & Immunotherapeutics.2020; 16(7): 1565. CrossRef - Causes and countermeasures for repeated outbreaks of hepatitis A among adults in Korea
Moran Ki, Hyunjin Son, Bo Youl Choi
Epidemiology and Health.2019; 41: e2019038. CrossRef - The unrealized potential: cohort effects and age-period-cohort analysis
Jongho Heo, Sun-Young Jeon, Chang-Mo Oh, Jongnam Hwang, Juhwan Oh, Youngtae Cho
Epidemiology and Health.2017; 39: e2017056. CrossRef - Viral Hepatitis in South Korea
Stella C Pak, Yaseen Alastal, Zubair Khan, Umar Darr
Euroasian Journal of Hepato-Gastroenterology.2017; 7(2): 163. CrossRef
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The costs of hepatitis A infections in South Korea
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Kyohyun Kim
, Baek-Geun Jeong
, Moran Ki
, Mira Park
, Jin Kyung Park
, Bo Youl Choi
, Weon-Seob Yoo
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Epidemiol Health. 2014;36:e2014011. Published online August 18, 2014
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DOI: https://doi.org/10.4178/epih/e2014011
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16,629
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6
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Supplementary Material
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Abstract
OBJECTIVES
The incidence of hepatitis A infections among young adults has recently increased in South Korea. Although universal vaccination has often been suggested to mitigate the problem, its rationale has not been well-understood. Estimating the societal costs of hepatitis A infections might support the development of intervention strategies.
METHODS
We classified hepatitis A infections into eight clinical pathways and estimated the number of occurrences and cost per case for each clinical pathway using claim data from National Health Insurance and several national surveys as well as assumptions based on previous studies. To determine the total costs of a hepatitis A infection, both direct and indirect costs were estimated. Indirect costs were estimated using the human-capital approach. All costs are adjusted to the year 2008.
RESULTS
There were 30,240 identified cases of hepatitis A infections in 2008 for a total cost of 80,873 million won (2.7 million won per case). Direct and indirect costs constituted 56.2% and 43.8% of the total costs, respectively. People aged 20-39 accounted for 71.3% of total cases and 74.6% of total costs. Medical costs per capita were the lowest in the 0-4 age group and highest in the 20-29 age group.
CONCLUSIONS
This study could provide evidence for development of cost-effective interventions to control hepatitis A infections. But the true costs including uncaptured and intangible costs of hepatitis A infections might be higher than our results indicate.
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- The chronological changes in the seroprevalence of anti-hepatitis A virus IgG from 2005 to 2019: Experience at four centers in the capital area of South Korea
Dae Hyun Lim, Won Sohn, Jae Yoon Jeong, Hyunwoo Oh, Jae Gon Lee, Eileen L. Yoon, Tae Yeob Kim, Seungwoo Nam, Joo Hyun Sohn
Medicine.2022; 101(48): e31639. CrossRef - Perspectives on Acute Hepatitis A Control in Korea
Seong Hee Kang, Moon Young Kim, Soon Koo Baik
Journal of Korean Medical Science.2019;[Epub] CrossRef - Seropositive rate of the anti-hepatitis A immunoglobulin G antibody in maintenance hemodialysis subjects from two hospitals in Korea
Hyunsuk Kim, Jiwon Ryu, Young-Ki Lee, Myung Jin Choi, Ajin Cho, Ja-Ryong Koo, Sae Yun Baik, Eun Hee Lee, Jong-Woo Yoon, Jung-Woo Noh
The Korean Journal of Internal Medicine.2019; 34(6): 1297. CrossRef - Causes and countermeasures for repeated outbreaks of hepatitis A among adults in Korea
Moran Ki, Hyunjin Son, Bo Youl Choi
Epidemiology and Health.2019; 41: e2019038. CrossRef - Estimating the Incidence of Cases and Deaths Resulting from Hand, Foot and Mouth Disease and Its Related Socioeconomic Disease Burden in Republic of Korea (2010 – 2014)
Donghee Seo
Osong Public Health and Research Perspectives.2018; 9(3): 112. CrossRef - Viral Hepatitis in South Korea
Stella C Pak, Yaseen Alastal, Zubair Khan, Umar Darr
Euroasian Journal of Hepato-Gastroenterology.2017; 7(2): 163. CrossRef
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Hepatitis A Vaccination Rates and Related Factors in a 2005 Population-based Study in Nonsan, Korea
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Eun Young Kim, Baeg Ju Na, Moo Sik Lee, Keon Yeop Kim, Moran Ki
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Epidemiol Health. 2009;31:e2009003. Published online October 12, 2009
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DOI: https://doi.org/10.4178/epih/e2009003
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13,156
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100
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Abstract
OBJECTIVESThe incidence of clinical hepatitis A has increased in young Korean adults since the mid-1990s. Although hepatitis A vaccinations have been administered in private clinics over the past 10 yr, no data exist on the vaccination rate and relating factors.
METHODSIn 2005, a population-based survey of 12-35-month-old children was carried out in Nonsan, Korea. An interview survey was completed for 71.3% of the children. All data came from a vaccination card or confirmation from a provider.
RESULTSThe hepatitis A vaccination rate was 42.3% for ≥1 dose and 24.7% for 2-dose. The results of the multivariate regression analysis for the hepatitis A vaccination showed that the second (OR=1.6) and third and successive children (OR=3.3) were less often immunized than the first child. Low economic status (OR=1.6), rural area (OR=1.5) and employed mother (OR=1.5) were also correlated with a lower vaccination rate. The hepatitis A vaccination rate was significantly lower in children who had no other vaccinations: measlesmumps-rubella (OR=2.8 for ≥1 dose and 7.3 for 2-dose), varicella (OR=20.2 and 22.0, respectively) and Haemophilus influenza type b (OR=14.3 and 13.3, respectively).
CONCLUSIONTo prevent outbreaks of clinical hepatitis A by enough herd immunity, a vaccination should be included in the National Immunization Program and a vaccination policy developed and implemented that can overcome the barriers to immunization such as late birth order and a mother's employment.
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- Very low prevalence of anti-HAV in Japan: high potential for future outbreak
Chikako Yamamoto, Ko Ko, Shintaro Nagashima, Takayuki Harakawa, Toshiko Fujii, Masayuki Ohisa, Keiko Katayama, Kazuaki Takahashi, Hiroaki Okamoto, Junko Tanaka
Scientific Reports.2019;[Epub] CrossRef - Changing sero-epidemiology of hepatitis A in Asia Pacific countries: A systematic review
Marissa Gripenberg, Naveena Aloysia D’Cor, Maïna L’Azou, Grenville Marsh, Sophie Druelles, Joshua Nealon
International Journal of Infectious Diseases.2018; 68: 13. CrossRef - Hepatitis A Virus Vaccination Status and Related Factors among College Students
Jae Seong Baek, Mi Ah Han, Jong Park, Na-Ra Yun
Korean Journal of Health Promotion.2014; 14(3): 103. CrossRef - Vaccination rates and related factors among health care workers in South Korea, 2009
Hee Jung Yoon, Jiseun Lim, BoYoul Choi, Jungsoo Kim, Jeonguk Kim, Changhwi Kim, Joon Soo Park, Sang-Bum Hong, Jooyoun Seo, Geun-Ryang Bae, Moran Ki
American Journal of Infection Control.2013; 41(8): 753. CrossRef - Factors Related to Completed Status and Seropositivity of Hepatitis A Immunization Among Children Aged 1–3 Years and 6–8 Years in South Korea
Jee-Young Hong, Mo Ran Ki, Hye-Jung Hwang, Delacroix Sinny, Young-Joon Park, Geun-Ryang Bae, Moo-Sik Lee
Osong Public Health and Research Perspectives.2013; 4(2): 93. CrossRef - Evaluation on the Accuracy of Vaccination Card for National Immunization Program in a 2005 Population-Based Survey in Nonsan, Korea
Moo-Sik Lee, Jee-Hee Kim, Kwang-Hwan Kim, Jee-Young Hong, Jin-Yong Lee, Keon-Yeop Kim
Journal of agricultural medicine and community health.2011; 36(2): 113. CrossRef