Skip to main content

The change in the nationwide seroprevalence of hepatitis C virus and the status of linkage to care in South Korea from 2009 to 2015

Hepatology International volume 13, pages 599–608 (2019)Cite this article

Abstract

Background

Hepatitis C virus (HCV) requires epidemiological monitoring to estimate its disease burden and to develop countermeasures. This study aimed to investigate the difference between the 2015 and 2009 nationwide anti-HCV seroprevalence and to determine linkage to care estimates in South Korea.

Methods

A total 268,422 examinees ≥ 20 years old were included in 2015 from 33 medical institutions nationwide. Electronically extracted data were retrospectively analyzed to calculate the age-, sex-, and area-adjusted anti-HCV prevalence. Seroprevalence in 2015 was measured using the same method as that in 2009. For anti-HCV-positive subjects, medical records were reviewed to see whether HCV RNA testing or antiviral treatment was performed.

Results

Adjusted anti-HCV prevalence was 0.60% (95% confidence interval, 0.57–0.63) based on general Korean population in 2015. It showed an increasing trend according to age; 0.23% in thirties, 0.38% in forties, 0.63% in fifties, 1.08% in sixties, and 1.65% in those aged ≥ 70 years. From 2009 to 2015, the adjusted anti-HCV prevalence decreased by 30%, with odds ratio of 0.70 (95% CI 0.70–0.71). There was significant intranational regional variation and changing pattern of seroprevalence. Among 1359 anti-HCV-positive subjects, HCV RNA test was performed in 60% and 25.4% had positivity. Treatment-initiated and cured rates in 2015 were 18.5% and 10.9%, respectively.

Conclusions

Anti-HCV prevalence in South Korea was 0.6% in 2015, showing a 30% decrease from that in 2009. Although the HCV RNA testing rate was increased since 2009, this remains suboptimal. Moreover, the treatment uptake rate should be improved in South Korea.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

HCV:

Hepatitis C virus

RNA:

Ribonucleic acid

DAA:

Direct acting antiviral drug

SVR:

Sustained virologic response

AST:

Aspartate aminotransferases

ALT:

Alanine aminotransferases

GGT:

Gamma-glutamyl transferase

CI:

Confidence interval

HLA:

Human leukocyte antigen

IL:

Interleukin

References

  1. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989;244:359–62.

    Article  CAS  PubMed  Google Scholar 

  2. Gower E, Estes C, Blach S, Razavi-Shearer K, Razavi H. Global epidemiology and genotype distribution of the hepatitis C virus infection. J Hepatol. 2014;61:S45–57.

    Article  PubMed  Google Scholar 

  3. Hajarizadeh B, Grebely J, Martinello M, Matthews GV, Lloyd AR, Dore GJ. Hepatitis C treatment as prevention: evidence, feasibility, and challenges. Lancet Gastroenterol Hepatol. 2016;1:317–27.

    Article  PubMed  Google Scholar 

  4. World Health Organization. Global Hepatitis Report 2017, 2017.

  5. World Health Organization. Combating hepatitis B and C to reach elimination by 2030, 2016.

  6. Kim DY, Kim IH, Jeong SH, Cho YK, Lee JH, Jin YJ, Lee D, Suh DJ, Han KH, Park NH, Kang HY, Jung YK, Kim YS, Kim KA, Lee YJ, Lee BS, Yim HJ, Lee HJ, Baik SK, Tak WY, Lee SJ, Chung WJ, Choi SK, Cho EY, Heo J, Kim DJ, Song BC, Kim MW, Lee J, Chae HB, Choi DH, Choi HY, Ki M. A nationwide seroepidemiology of hepatitis C virus infection in South Korea. Liver Int. 2013;33:586–94.

    Article  PubMed  Google Scholar 

  7. Holmberg SD, Spradling PR, Moorman AC, Denniston MM. Hepatitis C in the United States. N Engl J Med. 2013;368:1859–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Yehia BR, Schranz AJ, Umscheid CA, Lo Re V III. The treatment cascade for chronic hepatitis C virus infection in the United States: a systematic review and meta-analysis. PLoS One. 2014;9:e101554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Alter MJ, Kruszon-Moran D, Nainan OV, McQuillan GM, Gao F, Moyer LA, Kaslow RA, Margolis HS. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med. 1999;341:556–62.

    Article  CAS  PubMed  Google Scholar 

  10. Kwon GY, Lee H, Gwack J, Lee SW, Ki M, Youn SK. Regional distribution of hepatitis C virus infection in the Republic of Korea, 2007-2011. Gut Liver. 2014;8:428–32.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Jeong SH, Jang ES, Choi HY, Kim KA, Chung W, Ki M. Current status of hepatitis C virus infection and countermeasures in South Korea. Epidemiol Health. 2017;39:e2017017.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sohn HS, Kim JR, Ryu SY, Lee YJ, Lee MJ, Min HJ, Lee J, Choi HY, Song YJ, Ki M. Risk factors for hepatitis C virus (HCV) infection in areas with a high prevalence of HCV in the Republic of Korea in 2013. Gut Liver. 2016;10:126–32.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kim JY, Cho J, Hwang SH, Kil H, Bae SH, Kim YS, Lee HC, Jeong SH. Behavioral and healthcare-associated risk factors for chronic hepatitis C virus infection in Korea. J Korean Med Sci. 2012;27:1371–7.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Seong MH, Kil H, Kim YS, Bae SH, Lee YJ, Lee HC, Kang BH, Jeong SH. Clinical and epidemiological features of hepatitis C virus infection in South Korea: a prospective, multicenter cohort study. J Med Virol. 2013;85:1724–33.

    Article  PubMed  Google Scholar 

  15. Shin A, Cho ER, Kim J, Sung J, Park KW, Lim MK, Shin HR. Factors associated with awareness of infection status among chronic hepatitis B and C carriers in Korea. Cancer Epidemiol Biomark Prev. 2009;18:1894–8.

    Article  Google Scholar 

  16. Zuckerman A, Douglas A, Nwosu S, Choi L, Chastain C. Increasing success and evolving barriers in the hepatitis C cascade of care during the direct acting antiviral era. PLoS One. 2018;13:e0199174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chirikov VV, Marx SE, Manthena SR, Strezewski JP, Saab S. Development of a comprehensive dataset of hepatitis C patients and examination of disease epidemiology in the United States, 2013–2016. Adv Ther. 2018;35:1087–102.

    Article  PubMed  Google Scholar 

  18. Viejo LG, Herola AG, Lloret IS, Ruano FS, Paulino IC, Ivorra CQ, Saavedra IA, Perez DM, de la Osa JV. Screening of hepatitis C virus infection in adult general population in Spain. Eur J Gastroenterol Hepatol. 2018;30:1077–81.

    Article  Google Scholar 

  19. Huang P, Dong L, Lu X, Zhang Y, Chen H, Wang J, Zhang Y, Su J, Yu R. Genetic variants in antigen presentation-related genes influence susceptibility to hepatitis C virus and viral clearance: a case control study. BMC Infect Dis. 2014;14:716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jeong SH, Jung YK, Yang JW, Park SJ, Kim JW, Kwon OS, Kim YS, Choi DJ, Kim JH. Efficacy of peginterferon and ribavirin is associated with the IL28B gene in Korean patients with chronic hepatitis C. Clin Mol Hepatol. 2012;18:360–7.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Jimenez-Sousa MA, Fernandez-Rodriguez A, Guzman-Fulgencio M, Garcia-Alvarez M, Resino S. Meta-analysis: implications of interleukin-28B polymorphisms in spontaneous and treatment-related clearance for patients with hepatitis C. BMC Med. 2013;11:6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Huang J, Huang K, Xu R, Wang M, Liao Q, Xiong H, Li C, Tang X, Shan Z, Zhang M, Rong X, Nelson K, Fu Y. The associations of HLA-A*02:01 and DRB1*11:01 with hepatitis C virus spontaneous clearance are independent of IL28B in the Chinese population. Sci Rep. 2016;6:31485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lee SS, Jeong SH, Jang ES, Kim YS, Lee YJ, Jung EU, Kim IH, Bae SH, Lee HC. Treatment rate and factors related to interferon-based treatment initiation for chronic hepatitis C in South Korea. J Med Virol. 2016;88:275–81.

    Article  CAS  PubMed  Google Scholar 

  24. Jang ES, Kim YS, Kim KA, Lee YJ, Chung WJ, Kim IH, Lee BS, Jeong SH. Final report of unmet needs of interferon-based therapy for chronic hepatitis C in Korea: basis for moving into the direct-acting antiviral era. Gut Liver. 2017;11:543–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Janjua NZ, Kuo M, Yu A, Alvarez M, Wong S, Cook D, Wong J, Grebely J, Butt ZA, Samji H, Ramji A, Tyndall M, Krajden M. The population level cascade of care for hepatitis C in British Columbia, Canada: the BC hepatitis testers cohort (BC-HTC). EBioMedicine. 2016;12:189–95.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Simmons R, Ireland G, Irving W, Hickman M, Sabin C, Ijaz S, Ramsay M, Lattimore S, Mandal S. Establishing the cascade of care for hepatitis C in England-benchmarking to monitor impact of direct acting antivirals. J Viral Hepat. 2018;25:482–90.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare (Grant number: HC15C1193) and by a grant of the Chronic Infectious Disease Cohort Study (Korea HCV Cohort Study, 4800-4859-304) from the Korea Centers for Disease Control, Republic of Korea. The Korean hepatitis epidemiology study group included: Eun Sun Jang: Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Gyeonggi, Moran Ki: Department of Cancer Control and Population Health, Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, Gyeonggi, Geum-Youn Gwak: Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Kyung-Ah Kim: Department of Internal Medicine, Inje University Ilsan Paik Hospital, Goyang, Gyeonggi, Gi-Ae Kim: Health Screening and Promotion Center, Asan Medical Center, University of Ulsan College of Medicine, Seoul. Do Young Kim: Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Dong Joon Kim: Department of Internal Medicine, Hallym University College of Medicine, Chuncheon, Gangwon, Man Woo Kim: Department of Internal Medicine, Chosun University School of Medicine, Gwangju, Sung Eun Kim: Department of Internal Medicine, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Gyeonggi, Yun Soo Kim: Department of Internal Medicine, Gachon College of Medicine, Incheon, Young Seok Kim: Department of Internal Medicine, Soonchunhyang University Bucheon Hospital, Soonchunhyang University College of Medicine, Bucheon, Gyeonggi, In Hee Kim: Department of Internal Medicine, Chonbuk National University Hopital, Chonbuk National University College of Medicine, Chonju, Republic of Korea, Chang Wook Kim: Department of Internal Medicine, Uijeongbu St.Mary’s Hospital, Catholic University College of Medicine, Uijeongbu, Gyeonggi, Ho Dong Kim: Department of Internal Medicine, St.Carollo General Hospital, Suncheon, Jeonnam, Hyung Joon Kim: Department of Internal Medicine, Chung-Ang University Hospital, Chungang University College of Medicine, Seoul, Neung Hwa Park: Department of Internal Medicine, University of Ulsan College of Medicine, Ulsan, Soon Koo Baik: Department of Internal Medicine, Yonsei University Wonju College of Medicine, Wonju, Gangwon, Jeong Ill Suh: Department of Internal Medicine, Dongguk University Gyeongju Hospital, Dongguk University College of Medicine, Gyeongju, Gyeongbuk, Byung-Cheol Song: Department of Internal Medicine, Jeju National University College of Medicine, Jeju, Il Han Song: Department of Internal Medicine, Dankook University Hospital, Cheonan, Chungnam, Jong Eun Yeon: Department of Internal Medicine, Korea University Guro Hospital, Korea University College of Medicine, Byung Seok Lee: Department of Internal Medicine, Chungnam National University College of Medicine, Daejeon, Republic of Korea, Youn Jae Lee: Department of Internal Medicine, Inje University Busan Paik Hospital, Inje University College of Medicine, Busan, Republic of Korea, Young Kul Jung: Department of Internal Medicine, Korea University Ansan Hospital, Korea University College of Medicine, Ansan, Gyeonggi, Woo Jin Chung: Department of Internal Medicine, Keimyung University School of Medicine, Daegu, Sung Bum Cho: Department of Internal Medicine, Chonnam National University Hwasun Hospital, Jeonnam, Eun-Young Cho: Department of Internal Medicine, Wonkwang University College of Medicine, Iksan, Jeonbuk, Hyun Chin Cho: Department of Internal Medicine, Gyeongsang National University Hospital, Gyeongsang National University College of Medicine, Jinju, Gyeongnam, Gab Jin Cheon: Department of Internal Medicine, GangNeung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Gangwon, Hee Bok Chae: Department of Internal Medicine, Chungbuk National University College of Medicine, Cheongju, Chungbuk, Dae Hee Choi: Department of Internal Medicine, Kangwon National University School of Medicine, Chuncheon, Gangwon, Sung-Kyu Choi: Department of Internal Medicine, Chonnam National University Medical School, Gwangju, Hwa Young Choi: Department of Cancer Control and Population Health, Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, Gyeonggi, Won Young Tak: Department of Internal Medicine, Kyungpook National University College of Medicine, Daegu, Jeong Heo: Department of Internal Medicine, Pusan National University School of Medicine, Busan, Sook-Hyang Jeong: Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, Gyeonggi.

Author information

Author notes

  1. Eun Sun Jang and Moran Ki contributed equally to this work as first authors.

Authors and Affiliations

  1. Department of Internal Medicine, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 82 Gumi-ro, 173 Beon-gil, Bundang-gu, Seongnam-si, Gyeonggi-do, South Korea

    Eun Sun Jang & Sook-Hyang Jeong

  2. Department of Cancer Control and Population Health, Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, Gyeonggi, South Korea

    Moran Ki & Hwa Young Choi

  3. Department of Internal Medicine, Inje University Ilsan Paik Hospital, Goyang, Gyeonggi, South Korea

    Kyung-Ah Kim

Authors
  1. Eun Sun Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Moran Ki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hwa Young Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kyung-Ah Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sook-Hyang Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The Korean hepatitis epidemiology study group

  • Eun Sun Jang
  • , Moran Ki
  • , Geum-Youn Gwak
  • , Kyung-Ah Kim
  • , Gi-Ae Kim
  • , Do Young Kim
  • , Dong Joon Kim
  • , Man Woo Kim
  • , Sung Eun Kim
  • , Yun Soo Kim
  • , Young Seok Kim
  • , In Hee Kim
  • , Chang Wook Kim
  • , Ho Dong Kim
  • , Hyung Joon Kim
  • , Neung Hwa Park
  • , Soon Koo Baik
  • , Jeong Ill Suh
  • , Byung-Cheol Song
  • , Il Han Song
  • , Jong Eun Yeon
  • , Byung Seok Lee
  • , Youn Jae Lee
  • , Young Kul Jung
  • , Woo Jin Chung
  • , Sung Bum Cho
  • , Eun-Young Cho
  • , Hyun Chin Cho
  • , Gab Jin Cheon
  • , Hee Bok Chae
  • , Dae Hee Choi
  • , Sung-Kyu Choi
  • , Hwa Young Choi
  • , Won Young Tak
  • , Jeong Heo
  •  & Sook-Hyang Jeong

Corresponding author

Correspondence to Sook-Hyang Jeong.

Ethics declarations

Conflict of interest

Eun Sun Jang, Moran Ki, Hwa Young Choi, Kyung-Ah Kim and Sook-Hyang Jeong have nothing to declare.

Ethical approval

The study protocol was reviewed and approved by the institutional review board of each hospital.

Informed consent

Requirement for informed consent was waived due to the retrospective nature of this study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The members of the Korean hepatitis epidemiology study group are listed in the Acknowledgements section.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 59 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jang, E.S., Ki, M., Choi, H.Y. et al. The change in the nationwide seroprevalence of hepatitis C virus and the status of linkage to care in South Korea from 2009 to 2015. Hepatol Int 13, 599–608 (2019). https://doi.org/10.1007/s12072-019-09975-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12072-019-09975-y

Keywords

  • Hepatitis C virus
  • Epidemiology
  • Prevalence
  • Anti-HCV
  • HCV RNA
  • Antiviral treatment