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With regards to the global strategy towards eliminating viral hepatitis, reliable surveillance systems are essential to assess the national response for eliminating hepatitis C virus (HCV).


We aimed to assess the completeness of the two national registries with data on acute HCV infection in people with HIV, and estimated the number of acute HCV infections among adults (aged ≥ 18 years) with HIV in the Netherlands.


In this observational study, cases of HCV infection and reinfection among adults with a positive or unknown HIV-serostatus were identified from 2003 to 2016 in two national registries: the ATHENA cohort and the National Registry for Notifiable Diseases. For 2013–2016, cases were linked, and two-way capture–recapture analysis was carried out.


During 2013–2016, there were an estimated 282 (95% confidence interval (CI): 264–301) acute HCV infections among adults with HIV. The addition of cases with an unknown HIV-serostatus increased the matches (from n = 107 to n = 129), and subsequently increased the estimated total: 330 (95%CI: 309–351). Under-reporting was estimated at 14–20%.


Under-reporting of acute HCV infection among people with HIV could partially be explained by an unknown HIV-serostatus, or by differences in HCV stage (acute or chronic) at first diagnosis. Surveillance data should ideally include both acute and chronic HCV infections, and enable to distinguish these as well as initial- and re-infections. National surveillance of acute HCV can be improved by increased notification of infections.


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  1. World Health Organization (WHO). Global health sector strategy on viral hepatitis 2016-2021: Towards ending viral hepatitis. Geneva: WHO; 2016. Available from: https://apps.who.int/iris/bitstream/handle/10665/246177/WHO-HIV-2016.06-eng.pdf;jsessionid=FB9C9C5560E13229A9093ED20742C384?sequence=1
  2. Action plan for the health sector response to viral hepatitis in the WHO European Region (2017). Geneva: WHO (World Health Organization); 2017. Available from: http://www.euro.who.int/en/health-topics/communicable-diseases/hepatitis/publications/2017/action-plan-for-the-health-sector-response-to-viral-hepatitis-in-the-who-european-region-2017
  3. Hogenbirk R, David S. van Steenbergen J, Urbanus A. Meer dan opsporen. Nationaal hepatitisplan: een strategie voor actie. [More than tracing. National hepatitis plan: a strategy for action] Bilthoven: Rijksinstituut voor Volksgezondheid en Milieu (RIVM); 2016. RIVM Rapport 2016-0166. Dutch. Available from: https://www.rivm.nl/bibliotheek/rapporten/2016-0166.pdf
  4. Koopsen J, van Steenbergen JE, Richardus JH, Prins M, Op de Coul ELM, Croes EA, et al. Chronic hepatitis B and C infections in the Netherlands: estimated prevalence in risk groups and the general population. Epidemiol Infect. 2019;147:e147.  https://doi.org/10.1017/S0950268819000359  PMID: 30869044 
  5. van Sighem AI, Boender TS, Wit FWNM, Smit C, Matser A, Reiss P. Monitoring Report 2017. Human Immunodeficiency Virus (HIV) Infection in the Netherlands. Amsterdam: Stichting HIV Monitoring; 2017. Available from: https://www.hiv-monitoring.nl/application/files/2015/3312/7799/2017_HIV_Monitoring_Report_updated_version.pdf
  6. van de Laar TJ, Richel O. Emerging viral STIs among HIV-positive men who have sex with men: the era of hepatitis C virus and human papillomavirus. Sex Transm Infect. 2017;93(5):368-73.  https://doi.org/10.1136/sextrans-2016-052677  PMID: 27789574 
  7. Visser M, van Aar F, Op de Coul ELM, Slurink IAL, van Wees DA, Hoenderboom BM, et al. Sexually transmitted infections in the Netherlands in 2017. Bilthoven: Rijksinstituut voor Volksgezondheid en Milieu (RIVM); 2018. Available from: https://www.rivm.nl/bibliotheek/rapporten/2018-0012.pdf
  8. Boerekamps A, van den Berk GE, Lauw FN, Leyten EM, van Kasteren ME, van Eeden A, et al. Declining Hepatitis C Virus (HCV) Incidence in Dutch Human Immunodeficiency Virus-Positive Men Who Have Sex With Men After Unrestricted Access to HCV Therapy. Clin Infect Dis. 2018;66(9):1360-5.  https://doi.org/10.1093/cid/cix1007  PMID: 29186320 
  9. Popping S, Hullegie SJ, Boerekamps A, Rijnders BJA, de Knegt RJ, Rockstroh JK, et al. Early treatment of acute hepatitis C infection is cost-effective in HIV-infected men-who-have-sex-with-men. PLoS One. 2019;14(1):e0210179.  https://doi.org/10.1371/journal.pone.0210179  PMID: 30629662 
  10. Boerekamps A, Newsum AM, Smit C, Arends JE, Richter C, Reiss P, et al. , NVHB-SHM Hepatitis Working Group and the Netherlands ATHENA HIV Observational Cohort. High Treatment Uptake in Human Immunodeficiency Virus/Hepatitis C Virus-Coinfected Patients After Unrestricted Access to Direct-Acting Antivirals in the Netherlands. Clin Infect Dis. 2018;66(9):1352-9.  https://doi.org/10.1093/cid/cix1004  PMID: 29186365 
  11. Boender TS, Smit C, Sighem AV, Bezemer D, Ester CJ, Zaheri S, et al. , ATHENA national observational HIV cohort. AIDS Therapy Evaluation in the Netherlands (ATHENA) national observational HIV cohort: cohort profile. BMJ Open. 2018;8(9):e022516.  https://doi.org/10.1136/bmjopen-2018-022516  PMID: 30249631 
  12. van Sighem AI, Smit C, Wit FWNM, Boender TS, Matser A, Reiss P. Monitoring Report 2016. Human Immunodeficiency Virus (HIV) Infection in the Netherlands. Amsterdam: Stichting HIV Monitoring; 2016. Available from: https://www.hiv-monitoring.nl/application/files/3415/3312/9474/HIV_Monitoring_Report_2016_24_Nov.pdf
  13. European Centre for Disease Prevention and Control (ECDC). Annual Epidemiological Report 2015 – Hepatitis C. 2017;23-26. Available from: https://www.ecdc.europa.eu/en/publications-data/hepatitis-c-annual-epidemiological-report-2017
  14. European AIDS Treatment Network (NEAT) Acute Hepatitis C Infection Consensus Panel. Acute hepatitis C in HIV-infected individuals: recommendations from the European AIDS Treatment Network (NEAT) consensus conference. AIDS. 2011;25(4):399-409. PMID: 21139491 
  15. Arends JE, Lambers FA, van der Meer JT, Schreij G, Richter C, Brinkman K, et al. , The Netherlands Society for AIDS Physicians-NVAB. Treatment of acute hepatitis C virus infection in HIV+ patients: Dutch recommendations for management. Neth J Med. 2011;69(1):43-9. PMID: 21325703 
  16. Raad van State, Ministerie van Volksgezondheid Welzijn en Sport. Wet publieke gezondheid. 2008: BWBR0024705. [Accessed 14 Nov 2016]. Available from: http://wetten.overheid.nl/BWBR0024705/2016-08-01
  17. Rijksinstituut voor Volksgezondheid en Milieu (RIVM). Hepatitis C Richtlijn. 2013. Bilthoven: RIVM. Available from: https://lci.rivm.nl/richtlijnen/hepatitis-c
  18. Chao A, Tsay PK, Lin SH, Shau WY, Chao DY. The applications of capture-recapture models to epidemiological data. Stat Med. 2001;20(20):3123-57.  https://doi.org/10.1002/sim.996  PMID: 11590637 
  19. Chao A, Pan HY, Chiang SC. The Petersen-Lincoln estimator and its extension to estimate the size of a shared population. Biom J. 2008;50(6):957-70.  https://doi.org/10.1002/bimj.200810482  PMID: 19067330 
  20. van der Heijden PGM, Hirasing RA. Dwalingen in de methodologie. XXX. De vangst-hervangstmethode. [Roaming through methodology. XXX. The capture-recapture method]. Ned Tijdschr Geneeskd. 2001;145(4):161-3. PMID: 11213559 
  21. Bijkerk P, Fanoy EB, Kardamanidis K, van der Plas SM, Te Wierik MJ, Kretzschmar ME, et al. To notify or not to notify: decision aid for policy makers on whether to make an infectious disease mandatorily notifiable. Euro Surveill. 2015;20(34):30003.  https://doi.org/10.2807/1560-7917.ES.2015.20.34.30003  PMID: 26530302 
  22. World Health Organisation (WHO). International Health Regulations. Geneva: WHO; 2005;84. Available from: http://www.who.int/ihr/publications/9789241580496/en/
  23. European Commission. Regulation (EU) 2016/679 of the European Parliament and of the Council of 27 April 2016 on the protection of natural persons with regard to the processing of personal data and on the free movement of such data, and repealing Directive 95/46/EC (General Data Protection Regulation). Luxembourg: Official Journal of the European Union. 2016; 4.5.2016:L119/1-88. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32016R0679&rid=1
  24. World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-4.  https://doi.org/10.1001/jama.2013.281053  PMID: 24141714 
  25. Vanhommerig JW, Stolte IG, Lambers FA, Geskus RB, van de Laar TJ, Bruisten SM, et al. Stabilizing incidence of hepatitis C virus infection among men who have sex with men in Amsterdam. J Acquir Immune Defic Syndr. 2014;66(5):e111-5.  https://doi.org/10.1097/QAI.0000000000000208  PMID: 24853305 
  26. van Santen DK, van der Helm JJ, Del Amo J, Meyer L, D’Arminio Monforte A, Price M, et al. . Lack of decline in hepatitis C virus incidence among HIV-positive men who have sex with men during 1990-2014. J Hepatol. 2017;67(2):255-62.  https://doi.org/10.1016/j.jhep.2017.03.038  PMID: 28412290 
  27. Vickerman P, Grebely J, Dore GJ, Sacks-Davis R, Page K, Thomas DL, et al. , International Collaboration of Incident HIV and Hepatitis C in Injecting Cohorts (InC3). The more you look, the more you find: effects of hepatitis C virus testing interval on reinfection incidence and clearance and implications for future vaccine study design. J Infect Dis. 2012;205(9):1342-50.  https://doi.org/10.1093/infdis/jis213  PMID: 22457292 
  28. Slurink I, van Aar F, Coul E. Op de, et al. Sexually transmitted infections in the Netherlands in 2018. Bilthoven, the Netherlands: 2019. Available from: https://www.rivm.nl/publicaties/sexually-transmitted-infections-in-netherlands-in-2018
  29. Bezemer D, Cori A, Ratmann O, van Sighem A, Hermanides HS, Dutilh BE, et al. Dispersion of the HIV-1 Epidemic in Men Who Have Sex with Men in the Netherlands: A Combined Mathematical Model and Phylogenetic Analysis. PLoS Med. 2015;12(11):e1001898, discussion e1001898.  https://doi.org/10.1371/journal.pmed.1001898  PMID: 26529093 
  30. Toxopeus DCM, Pell CL, Westrhenen NB, Smit C, Wit FWNM, Ondoa P, et al. Compliance with laboratory monitoring guidelines in outpatient HIV care: a qualitative study in the Netherlands. AIDS Care. 2019;31(7):840-7.  https://doi.org/10.1080/09540121.2018.1563280  PMID: 30602294 
  31. Ramière C, Charre C, Miailhes P, Bailly F, Radenne S, Uhres AC, et al. Patterns of hepatitis C virus transmission in human immunodeficiency virus (HIV)-infected and HIV-negative men who have sex with men. Clin Infect Dis. 2019;69(12):2127-35.  https://doi.org/10.1093/cid/ciz160  PMID: 30810158 
  32. Hoornenborg E, Achterbergh RCA, Schim van der Loeff MF, Davidovich U, Hogewoning A, de Vries HJC, et al. , Amsterdam PrEP Project team in the HIV Transmission Elimination AMsterdam Initiative, MOSAIC study group. MSM starting preexposure prophylaxis are at risk of hepatitis C virus infection. AIDS. 2017;31(11):1603-10.  https://doi.org/10.1097/QAD.0000000000001522  PMID: 28657964 
  33. Ingiliz P, Wehmeyer MH, Boesecke C, Schulze Zur Wiesch J, Schewe K, Lutz T, et al. , NEAT study group, GECCO study group. Reinfection with the hepatitis C virus in men who have sex with men after successful treatment with direct-acting antivirals in Germany: Current incidence rates compared with rates during the interferon era. Clin Infect Dis. 2019;•••:ciz949.  https://doi.org/10.1093/cid/ciz949  PMID: 31562816 
  34. Berenguer J, Gil-Martin Á, Jarrin I, Montes ML, Domínguez L, Aldámiz-Echevarría T, et al. , Madrid-CoRe Study Group. Reinfection by hepatitis C virus following effective all-oral direct-acting antiviral drug therapy in HIV/hepatitis C virus coinfected individuals. AIDS. 2019;33(4):685-9.  https://doi.org/10.1097/QAD.0000000000002103  PMID: 30829744 
  35. van Leth F, Evenblij K, Wit F, Kiers A, Sprenger H, Verhagen M, et al. TB-HIV co-infection in the Netherlands: estimating prevalence and under-reporting in national registration databases using a capture-recapture analysis. J Epidemiol Community Health. 2016;70(6):556-60.  https://doi.org/10.1136/jech-2015-206680  PMID: 26700301 
  36. Hansen N, Hay G, Cowan S, Jepsen P, Bygum Krarup H, Obel N, et al. Hepatitis B prevalence in Denmark - an estimate based on nationwide registers and a national screening programme, as on 31 December 2007. Euro Surveill. 2013;18(47):20637.  https://doi.org/10.2807/1560-7917.ES2013.18.47.20637  PMID: 24300884 
  37. Christensen PB, Hay G, Jepsen P, Omland LH, Just SA, Krarup HB, et al. Hepatitis C prevalence in Denmark -an estimate based on multiple national registers. BMC Infect Dis. 2012;12(1):178.  https://doi.org/10.1186/1471-2334-12-178  PMID: 22866925 
  38. Thomas XV, Grady BPX, Van Der Meer JTM, Ho CK, Vanhommerig JW, Rebers SP, et al. Genetic characterization of multiple hepatitis C virus infections following acute infection in HIV-infected men who have sex with men. AIDS. 2015;29(17):2287-95.  https://doi.org/10.1097/QAD.0000000000000838  PMID: 26258527 
  39. van Rooijen M, Heijman T, de Vrieze N, Urbanus A, Speksnijder A, van Leeuwen P, et al. Earlier Detection of Hepatitis C Virus Infection Through Routine Hepatitis C Virus Antibody Screening of Human Immunodeficiency Virus-Positive Men Who Have Sex With Men Attending A Sexually Transmitted Infection Outpatient Clinic: A Longitudinal Study. Sex Transm Dis. 2016;43(9):560-5.  https://doi.org/10.1097/OLQ.0000000000000497  PMID: 27513382 
  40. Screening van risicogroepen op hepatitis B en C. Den Haag: De Gezondheidsraad; 2016.
  41. Falade-Nwulia O, Sulkowski MS, Merkow A, Latkin C, Mehta SH. Understanding and addressing hepatitis C reinfection in the oral direct-acting antiviral era. J Viral Hepat. 2018;25(3):220-7.  https://doi.org/10.1111/jvh.12859  PMID: 29316030 
  42. Martin NK, Boerekamps A, Hill AM, Rijnders BJA. Is hepatitis C virus elimination possible among people living with HIV and what will it take to achieve it? J Int AIDS Soc. 2018;21(Suppl 2):e25062.  https://doi.org/10.1002/jia2.25062  PMID: 29633560 
  43. Martin NK, Jansen K, An der Heiden M, Boesecke C, Boyd A, Schewe K, et al. Eliminating Hepatitis C Virus Among Human Immunodeficiency Virus-Infected Men Who Have Sex With Men in Berlin: A Modeling Analysis. J Infect Dis. 2019;220(10):1635-44.  https://doi.org/10.1093/infdis/jiz367  PMID: 31301142 

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