Advertisement

Global Epidemiology of Chronic Hepatitis C Virus Infection

  • Resat Ozaras
  • Hakan Leblebicioglu
Chapter

Abstract

Hepatitis C virus (HCV) causes acute and chronic infection and is a global health problem. It leads to cirrhosis and hepatocellular carcinoma and causes several extrahepatic manifestations. Global prevalence of chronic HCV infection is estimated at around 1%. However the epidemiology of HCV infection changes according to the region. The estimated anti-HCV prevalence in Africa and Asia is higher than 2%, the central sub-Saharan Africa having the highest prevalence. Asia, having high prevalence and high population, has 60% of the cases worldwide. In Europe, Americas, and Australia, HCV prevalence is lower than 2%. Although pan-genotypic direct-acting antivirals have been developed, they are not available worldwide. Estimates of HCV genotypes are important for developing strategies for HCV elimination. The most prevalent HCV genotype is genotype 1 in the world (49%), followed by genotype 3 (18%), 4 (17%), and 2 (11%). Genotypes 5 and 6 account for the remaining 5%.

A better estimation of global and regional HCV epidemiology contributes to HCV elimination targets.

Keywords

Hepatitis C virus Genotype Epidemiology 

References

  1. 1.
    Ford N, Kirby C, Singh K, Mills EJ, Cooke G, Kamarulzaman A, duCros P. Chronic hepatitis C treatment outcomes in low- and middle-income countries: a systematic review and meta-analysis. Bull World Health Organ. 2012;90(7):540–50.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    WHO Hepatitis C fact sheet no. 164. Updated July 2015. Available at: http://www.who.int/mediacentre/factsheets/fs164/en/. Accessed 17 Jul 2018.
  3. 3.
    Global hepatitis report, 2017. Geneva: World Health Organization; 2017. http://apps.who.int/iris/bitstream/10665/255016/1/9789241565455-eng.pdf?ua=1. Accessed 20 Jan 2018.
  4. 4.
    Razavi H, Elkhoury AC, Elbasha E, Estes C, Pasini K, Poynard T, Kumar R. Chronic hepatitis C virus (HCV) disease burden and cost in the United States. Hepatology. 2013;57:2164–70.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Petruzziello A, Marigliano S, Loquercio G, Cozzolino A, Cacciapuoti C. Global epidemiology of hepatitis C virus infection: an up-date of the distribution and circulation of hepatitis C virus genotypes. World J Gastroenterol. 2016;22(34):7824–40.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Polaris Observatory HCV Collaborators. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol. 2017;2(3):161–76.CrossRefGoogle Scholar
  7. 7.
    Niebel M, Singer JB, Nickbakhsh S, Gifford RJ, Thomson EC. Hepatitis C and the absence of genomic data in low-income countries: a barrier on the road to elimination? Lancet Gastroenterol Hepatol. 2017;2(10):700–1.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Saraswat V. Historical epidemiology of hepatitis C virus (HCV) in select countries—volume 2. J Viral Hepat. 2015;22(Suppl. 1):6–25.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Bruggmann P, Berg T, Øvrehus AL, et al. Historical epidemiology of hepatitis C virus (HCV) in selected countries. J Viral Hepat. 2014;21(Suppl. 1):5–33.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Liakina V, Hamid S, Tanaka J, et al. Historical epidemiology of hepatitis C virus (HCV) in select countries—volume 3. J Viral Hepat. 2015;22(Suppl. 4):4–20.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Maaroufi A, Vince A, Himatt SM, et al. Historical epidemiology of hepatitis C virus in select countries—volume 4. J Viral Hepat. 2017;24(Suppl. 2):8–24.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Njouom R, Siffert I, Texier G, Lachenal G, Tejiokem MC, Pépin J, Fontanet A. The burden of hepatitis C virus in Cameroon: spatial epidemiology and historical perspective. J Viral Hepat. 2018;25:959–68.  https://doi.org/10.1111/jvh.12894. [Epub ahead of print].CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Alidjinou EK, Moukassa D, Ebatetou-Ataboho E, Mahoungou GH, Pambou J-P, Sané F, et al. Higher levels of hepatitis C virus RNA found in blood donors co-infected with HIV as compared to HCV mono-infected donors. J Infect Dev Ctries. 2014;8:1068–71.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Ntagirabiri R, Baransaka E, Ndayiragije A, Niyongabo T. Prevalence of hepatitis C virus in Burundi: a nationwide survey. J Afr Hépatol Gastroentérol. 2014;8(1):25–8.CrossRefGoogle Scholar
  15. 15.
    Delaporte E, Thiers V, Dazza MC, Romeo R, Mlika-Cabanne N, Aptel I, Schrijvers D, Bréchot C, Larouzé B. High level of hepatitis C endemicity in Gabon, equatorial Africa. Trans R Soc Trop Med Hyg. 1993;87(6):636–7.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Ndong-Atome GR, Makuwa M, Ouwe-Missi-Oukem-Boyer O, Pybus OG, Branger M, Le Hello S, Boye-Cheik SB, Brun-Vezinet F, Kazanji M, Roques P, Bisser S. High prevalence of hepatitis C virus infection and predominance of genotype 4 in rural Gabon. J Med Virol. 2008;80(9):1581–7.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Riou J, Aït Ahmed M, Blake A, Vozlinsky S, Brichler S, Eholié S, Boëlle PY, Fontanet A, HCV Epidemiology in Africa Group. Hepatitis C virus seroprevalence in adults in Africa: a systematic review and meta-analysis. J Viral Hepat. 2016;23(4):244–55.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Biggar RJ, Ortiz-Conde BA, Bagni RK, Bakaki PM, Wang CD, Engels EA, Mbulaiteye SM, Ndugwa CM. Hepatitis C virus genotype 4 in Ugandan children and their mothers. Emerg Infect Dis. 2006;12(9):1440–3.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Karoney MJ, Siika AM. Hepatitis C virus (HCV) infection in Africa: a review. Pan Afr Med J. 2013;14:44.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Chaabna K, Kouyoumjian SP, Abu-Raddad LJ. Hepatitis C virus epidemiology in Djibouti, Somalia, Sudan, and Yemen: systematic review and meta-analysis. PLoS One. 2016;11(2):e0149966.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Xie DD, Li J, Chen JT, Eyi UM, Matesa RA, Obono MM, Ehapo CS, Yang LY, Yang H, Yang HT, Lin M. Seroprevalence of human immunodeficiency virus, hepatitis B virus, hepatitis C virus, and Treponema pallidum infections among blood donors on Bioko Island, Equatorial Guinea. PLoS One. 2015;10(10):e0139947.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Chaabna K, Cheema S, Abraham A, Alrouh H, Lowenfels AB, Maisonneuve P, Mamtani R. Systematic overview of hepatitis C infection in the Middle East and North Africa. World J Gastroenterol. 2018;24(27):3038–54.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Ayele W, Nokes DJ, Abebe A, et al. Higher prevalence of anti-HCV antibodies among HIV-positive compared to HIV-negative inhabitants of Addis Ababa, Ethiopia. J Med Virol. 2002;68:12–7.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Ramarokoto CE, Rakotomanana F, Ratsitorahina M, Raharimanga V, Razafindratsimandresy R, Randremanana R, Rakoto-Andrianarivelo M, Rousset D, Andrianaja V, Richard V, Soares JL, Rabarijaona LP. Seroprevalence of hepatitis C and associated risk factors in urban areas of Antananarivo, Madagascar. BMC Infect Dis. 2008;8:25.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Razafindratsimandresy R, Dubot A, Ramarokoto CE, Iehlé C, Soares JL, Rousset D. Hepatitis C virus infection and genotypes in Antananarivo, Madagascar. J Med Virol. 2007;79(8):1082–8.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Fessehaye N, Naik D, Fessehaye T. Transfusion transmitted infections—a retrospective analysis from the National Blood Transfusion Service in Eritrea. Pan Afr Med J. 2011;9:40.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Siraj N, Achila OO, Issac J, Menghisteab E, Hailemariam M, Hagos S, Gebremeskel Y, Tesfamichael D. Seroprevalence of transfusion-transmissible infections among blood donors at National Blood Transfusion Service, Eritrea: a seven-year retrospective study. BMC Infect Dis. 2018;18(1):264.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Maida MJ, Daly CC, Hoffman I, Cohen MS, Kumwenda M, Vernazza PL. Prevalence of hepatitis C infection in Malawi and lack of association with sexually transmitted diseases. Eur J Epidemiol. 2000;16(12):1183–4.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Sonderup MW, Afihene M, Ally R, et al., Gastroenterology and Hepatology Association of Sub-Saharan Africa (GHASSA). Hepatitis C in sub-Saharan Africa: the current status and recommendations for achieving elimination by 2030. Lancet Gastroenterol Hepatol. 2017;2(12):910–9.CrossRefGoogle Scholar
  30. 30.
    Smuts HE, Kannemeyer J. Genotyping of hepatitis C virus in South Africa. J Clin Microbiol. 1995;33(6):1679–81.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Harfouche M, Chemaitelly H, Kouyoumjian SP, Mahmud S, Chaabna K, Al-Kanaani Z, Abu-Raddad LJ. Hepatitis C virus viremic rate in the Middle East and North Africa: systematic synthesis, meta-analyses, and meta-regressions. PLoS One. 2017;12(10):e0187177.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Kouyoumjian SP, Chemaitelly H, Abu-Raddad LJ. Characterizing hepatitis C virus epidemiology in Egypt: systematic reviews, meta-analyses, and meta-regressions. Sci Rep. 2018;8(1):1661.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Mahmud S, Akbarzadeh V, Abu-Raddad LJ. The epidemiology of hepatitis C virus in Iran: systematic review and meta-analyses. Sci Rep. 2018;8(1):150.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Cornberg M, Razavi HA, Alberti A, et al. A systematic review of hepatitis C virus epidemiology in Europe, Canada and Israel. Liver Int. 2011;31(Suppl. 2):30–60.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Abro AH, Al-Dabal L, Younis NJ. Distribution of hepatitis C virus genotypes in Dubai, United Arab Emirates. J Pak Med Assoc. 2010;60(12):987–90.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Tanaka J, Koyama T, Mizui M, et al. Total numbers of undiagnosed carriers of hepatitis C and B viruses in Japan estimated by age- and area-specific prevalence on the national scale. Intervirology. 2011;54:185–95.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Chung H, Ueda T, Kudo M. Changing trends in hepatitis C infection over the past 50 years in Japan. Intervirology. 2010;53(1):39–43.PubMedCrossRefGoogle Scholar
  38. 38.
    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(10):1724–33.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    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(1 Suppl):S45–57.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Baatarkhuu O, Gerelchimeg T, Munkh-Orshikh D, Batsukh B, Sarangua G, Amarsanaa J. Epidemiology, genotype distribution, prognosis, control, and management of viral hepatitis B, C, D, and hepatocellular carcinoma in Mongolia. Euroasian J Hepatogastroenterol. 2018;8(1):57–62.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Bennett H, Waser N, Johnston K, Kao JH, Lim YS, Duan ZP, Lee YJ, Wei L, Chen CJ, Sievert W, Yuan Y, Li H. A review of the burden of hepatitis C virus infection in China, Japan, South Korea and Taiwan. Hepatol Int. 2015;9(3):378–90.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Lu W-P, Lin G-X, Shi S, Dong J-H. Simultaneously high prevalences of hepatitis B and C virus infections in a population in Putian County, China. J Clin Microbiol. 2012;50:2142–4.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Yu ML, Yeh ML, Tsai PC, et al. Huge gap between clinical efficacy and community effectiveness in the treatment of chronic hepatitis C: a nationwide survey in Taiwan. Medicine (Baltimore). 2015;94:e690.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Chen CH, Yang PM, Huang GT, Lee HS, Sung JL, Sheu JC. Estimation of seroprevalence of hepatitis B virus and hepatitis C virus in Taiwan from a large-scale survey of free hepatitis screening participants. J Formos Med Assoc. 2007;106:148–55.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Zhang Y, Chen LM, He M. Hepatitis C virus in mainland China with an emphasis on genotype and subtype distribution. Virol J. 2017;14(1):41.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Al Kanaani Z, Mahmud S, Kouyoumjian SP, Abu-Raddad LJ. The epidemiology of hepatitis C virus in Pakistan: systematic review and meta-analyses. R Soc Open Sci. 2018;5(4):180257.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Mamun-Al-Mahtab. Past, present, and future of viral hepatitis in Bangladesh. Euroasian J Hepatogastroenterol. 2016;6(1):43–4.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Mahajan R, Midha V, Goyal O, Mehta V, Narang V, Kaur K, Singh A, Singh D, Bhanot R, Sood A. Clinical profile of hepatitis C virus infection in a developing country: India. J Gastroenterol Hepatol. 2018;33(4):926–33.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Puri P, Anand AC, Saraswat VA, et al. Consensus Statement of HCV Task Force of the Indian National Association for Study of the Liver (INASL). Part I: status report of HCV infection in India. J Clin Exp Hepatol. 2014;4(2):106–16.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Sanders-Buell E, Rutvisuttinunt W, Todd CS, Nasir A, Bradfield A, Lei E, Poltavee K, Savadsuk H, Kim JH, Scott PT, de Souza M, Tovanabutra S. Hepatitis C genotype distribution and homology among geographically disparate injecting drug users in Afghanistan. J Med Virol. 2013;85(7):1170–9.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Yamada H, Fujimoto M, Svay S, Lim O, Hok S, Goto N, Ohisa M, Akita T, Matsuo J, Do SH, Katayama K, Miyakawa Y, Tanaka J. Seroprevalence, genotypic distribution and potential risk factors of hepatitis B and C virus infections among adults in Siem Reap, Cambodia. Hepatol Res. 2015;45(4):480–7.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    McDonald SA, Mohamed R, Dahlui M, Naning H, Kamarulzaman A. Bridging the data gaps in the epidemiology of hepatitis C virus infection in Malaysia using multi-parameter evidence synthesis. BMC Infect Dis. 2014;14:564.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Senevirathna D, Amuduwage S, Weerasingam S, Jayasinghe S, Fernandopulle N. Hepatitis C virus in healthy blood donors in Sri Lanka. Asian J Transfus Sci. 2011;5(1):23–5.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Ishizaki A, Tran VT, Nguyen CH, Tanimoto T, Hoang HTT, Pham HV, Phan CTT, Bi X, Pham TV, Ichimura H. Discrepancies in prevalence trends for HIV, hepatitis B virus, and hepatitis C virus in Haiphong, Vietnam from 2007 to 2012. PLoS One. 2017;12(6):e0179616.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Nguyen VT, McLaws ML, Dore GJ. Prevalence and risk factors for hepatitis C infection in rural north Vietnam. Hepatol Int. 2007;1:387–93.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Do SH, Yamada H, Fujimoto M, Ohisa M, Matsuo J, Akita T, Katayama K, Van Nguyen N, Miyakawa Y, Tanaka J. High prevalences of hepatitis B and C virus infections among adults living in Binh Thuan province, Vietnam. Hepatol Res. 2015;45:259–68.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Jutavijittum P, Yousukh A, Samountry B, Samountry K, Ounavong A, Thammavong T, Keokhamphue J, Toriyama K. Seroprevalence of hepatitis B and C virus infections among Lao blood donors. Southeast Asian J Trop Med Public Health. 2007;38(4):674–9.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Yanase Y, Ohida T, Kaneita Y, Agdamag DM, Leaño PS, Gill CJ. The prevalence of HIV, HBV and HCV among Filipino blood donors and overseas work visa applicants. Bull World Health Organ. 2007;85(2):131–7.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Leblebicioglu H, Arends JE, Ozaras R, et al., ESGHV (Part of ESCMID). Availability of hepatitis C diagnostics and therapeutics in European and Eurasia countries. Antiviral Res. 2018;150:9–14.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Tahan V, Ozaras R, Karaca C, Uraz S, Eren F, Danalioglu A, Avsar E, Turkoglu S, Midilli K, Tabak F, Ozturk R, Mert A, Senturk H, Tozun N. Is HCV genotyping cost-effective even when the prevalences of genotypes 2 and 3 are low? Hepatogastroenterology. 2009;56(94–95):1425–8.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Al Naamani K, Al Sinani S, Deschênes M. Epidemiology and treatment of hepatitis C genotypes 5 and 6. Can J Gastroenterol. 2013;27(1):e8–12.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Denniston MM, Jiles RB, Drobeniuc J, Klevens RM, Ward JW, McQuillan GM, Holmberg SD. Chronic hepatitis C virus infection in the United States, National Health and Nutrition Examination Survey 2003 to 2010. Ann Intern Med. 2014;160:293–300.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Smith BD, Morgan RL, Beckett GA, et al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945–1965. MMWR Recomm Rep. 2012;61:1–32.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Centers for Disease Control and Prevention (CDC). Viral hepatitis statistics and surveillance—United States; 2016.Google Scholar
  65. 65.
    Williams IT, Bell BP, Kuhnert W, Alter MJ. Incidence and transmission patterns of acute hepatitis C in the United States, 1982–2006. Arch Intern Med. 2011;171:242–8.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Trubnikov M, Yan P, Archibald C. Estimated prevalence of hepatitis C virus infection in Canada, 2011. Canada communicable disease report: volume 40-19; 18 Dec 2014. Available at: http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/14vol40/dr-rm40-19/surveillance-b-eng.php.
  67. 67.
    Castells M, Bello G, Ifrán S, Pereyra S, Boschi S, Uriarte R, Cristina J, Colina R. Epidemic history of major genotypes of hepatitis C virus in Uruguay. Infect Genet Evol. 2015;32:231–8.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Sibley A, Han KH, Abourached A. The present and future disease burden of hepatitis C virus infections with today’s treatment paradigm—volume 3. J Viral Hepat. 2015;22(Suppl. 4):21–41.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Hatzakis A, Chulanov V, Gadano AC, et al. The present and future disease burden of hepatitis C virus (HCV) infections with today’s treatment paradigm—volume 2. J Viral Hepat. 2015;22(Suppl. 1):26–45.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Chan HLY, Chen CJ, Omede O, et al. The present and future disease burden of hepatitis C virus infections with today’s treatment paradigm: volume 4. J Viral Hepat. 2017;24(Suppl. 2):25–43.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Ghaderi-Zefrehi H, Gholami-Fesharaki M, Sharafi H, Sadeghi F, Alavian SM. The distribution of hepatitis C virus genotypes in Middle Eastern countries: a systematic review and meta-analysis. Hepat Mon. 2016;16(9):e40357.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    World Bank Country and Lending Groups. Available at: https://datahelpdesk.worldbank.org/knowledgebase/articles/906519-world-bank-country-and-lending-groups. Accessed 14 Aug 2018.
  73. 73.
    Center for Disease Control and Prevention, Infectious diseases related to travel, hepatitis C. Available at: https://wwwnc.cdc.gov/travel/yellowbook/2018/infectious-diseases-related-to-travel/hepatitis-c. Accessed 14 Aug 2018.
  74. 74.
    Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology. 2015;61(1):77–87.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Tanaka Y, Hanada K, Mizokami M, et al. A comparison of the molecular clock of hepatitis C virus in the United States and Japan predicts that hepatocellular carcinoma incidence in the United States will increase over the next two decades. Proc Natl Acad Sci U S A. 2002;99(24):15584–9.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Chiaramonte M, Stroffolini T, Lorenzoni U, et al. Risk factors in community-acquired chronic hepatitis C virus infection: a case-control study in Italy. J Hepatol. 1996;24:129–34.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Mariano A, Scalia Tomba G, Tosti ME, Spada E, Mele A. Estimating the incidence, prevalence and clinical burden of hepatitis C over time in Italy. Scand J Infect Dis. 2009;41(9):689–99.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    World Health Organization (WHO). Guidelines for the screening, care and treatment of persons with hepatitis C infection; 2014. Available: http://apps.who.int/iris/bitstream/10665/111747/1/9789241548755_eng.pdf. Accessed 14 July 2018.
  79. 79.
    Moyer VA, Preventive Services Task Force US. Screening for hepatitis C virus infection in adults: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2013;159(5):349–57.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Mukomolov S, Trifonova G, Levakova I, Bolsun D, Krivanogova E. Hepatitis C in the Russian Federation: challenges and future directions. Hepat Med. 2016;8:51–60.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Manns MP, Buti M, Gane E, Pawlotsky JM, Razavi H, Terrault N, Younossi Z. Hepatitis C virus infection. Nat Rev Dis Primers. 2017;3:17006.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Forbi JC, Layden JE, Phillips RO, Mora N, Xia GL, Campo DS, Purdy MA, Dimitrova ZE, Owusu DO, Punkova LT, Skums P, Owusu-Ofori S, Sarfo FS, Vaughan G, Roh H, Opare-Sem OK, Cooper RS, Khudyakov YE. Next-generation sequencing reveals frequent opportunities for exposure to hepatitis C virus in Ghana. PLoS One. 2015;10(12):e0145530.  https://doi.org/10.1371/journal.pone.0145530. eCollection 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    CDC healthcare-associated hepatitis B and C outbreaks reported to the Centers for Disease Control and Prevention (CDC) 2008–2014. Available at: http://www.cdc.gov/hepatitis/outbreaks/healthcarehepoutbreaktable.htm. Accessed 11 Aug 2018.
  84. 84.
    de Lédinghen V, Trimoulet P, Mannant PR, Dumas F, Champbenoît P, Baldit C, Foucher J, Faure M, Vergniol J, Castéra L, Bertet J, Fleury H, Couzigou P, Bernard PH. Outbreak of hepatitis C virus infection during sclerotherapy of varicose veins: long-term follow-up of 196 patients (4535 patient-years). J Hepatol. 2007;46(1):19–25.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Ross RS, Viazov S, Khudyakov YE, Xia GL, Lin Y, Holzmann H, Sebesta C, Roggendorf M, Janata O. Transmission of hepatitis C virus in an orthopedic hospital ward. J Med Virol. 2009;81(2):249–57.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Judd A, Hickman M, Jones S, McDonald T, Parry JV, Stimson GV, Hall AJ. Incidence of hepatitis C virus and HIV among new injecting drug users in London: prospective cohort study. BMJ. 2005;330(7481):24–5.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Zibbell JE, Asher AK, Patel RC, Kupronis B, Iqbal K, Ward JW, Holtzman D. Increases in acute hepatitis C virus infection related to a growing opioid epidemic and associated injection drug use, United States, 2004 to 2014. Am J Public Health. 2018;108(2):175–81.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Rossi C, Butt Z, Wong S, Buxton J, Islam N, Yu A, Darvishian M, Gilbert M, Wong J, Chapinal N, Binka M, Alvarez M, Tyndall M, Krajden M, Janjua N, BC Hepatitis Testers Cohort Team. Hepatitis C virus reinfection after successful treatment with direct-acting antiviral therapy in a large population-based cohort. J Hepatol. 2018. pii: S0168-8278(18)32288-8;  https://doi.org/10.1016/j.jhep.2018.07.025. [Epub ahead of print].PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Tahan V, Karaca C, Yildirim B, Bozbas A, Ozaras R, Demir K, Avsar E, Mert A, Besisik F, Kaymakoglu S, Senturk H, Cakaloglu Y, Kalayci C, Okten A, Tozun N. Sexual transmission of HCV between spouses. Am J Gastroenterol. 2005;100(4):821–4.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Gogela NA, Sonderup MW, Rebe K, Chivese T, Spearman CW. Hepatitis C prevalence in HIV-infected heterosexual men and men who have sex with men. S Afr Med J. 2018;108(7):568–72.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Cuomo G, Digaetano M, Menozzi M, Tagliazucchi S, Guaraldi G, Borghi V, Mussini C. Incidence of HCV infection amongst HIV positive men who had sex with men and prevalence data from patients followed at the Infectious Diseases Clinic of Modena, Italy. Dig Liver Dis. 2018. pii: S1590-8658(18)30765-5.Google Scholar
  92. 92.
    Nwaohiri A, Schillie S, Bulterys M, Kourtis AP. Hepatitis C virus infection in children: how do we prevent it and how do we treat it? Expert Rev Anti Infect Ther. 2018;16:1–6.CrossRefGoogle Scholar
  93. 93.
    Tovo PA, Calitri C, Scolfaro C, Gabiano C, Garazzino S. Vertically acquired hepatitis C virus infection: correlates of transmission and disease progression. World J Gastroenterol. 2016;22(4):1382–92.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Cottrell EB, Chou R, Wasson N, Rahman B, Guise JM. Reducing risk for mother-to-infant transmission of hepatitis C virus: a systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2013;158(2):109–13.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Ozaras R, Leblebicioglu H, Sunbul M, Tabak F, Balkan II, Yemisen M, Sencan I, Ozturk R. The Syrian conflict and infectious diseases. Expert Rev Anti Infect Ther. 2016;14(6):547–55.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Falla AM, Ahmad AA, Duffell E, Noori T, Veldhuijzen IK. Estimating the scale of chronic hepatitis C virus infection in the EU/EEA: a focus on migrants from anti-HCV endemic countries. BMC Infect Dis. 2018;18:42.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Resat Ozaras
    • 1
  • Hakan Leblebicioglu
    • 2
  1. 1.ESCMID Study Group for Viral Hepatitis (ESGVH)IstanbulTurkey
  2. 2.ESCMID Study Group for Infections in Travelers and Migrants (ESGITM)SamsunTurkey

Personalised recommendations