Development and validation of the HCV-MOSAIC risk score to assist testing for acute hepatitis C virus (HCV) infection in HIV-infected men who have sex with men (MSM)

Astrid M Newsum, Ineke G Stolte, Jan Tm van der Meer, Janke Schinkel, Marc van der Valk, Joost W Vanhommerig, Anne Buvé, Mark Danta, Arjan Hogewoning, Maria Prins, MOSAIC collaborators, J T M van der Meer, R Molenkamp, M Mutschelknauss, H E Nobel, H W Reesink, J Schinkel, M van der Valk, J W Vanhommerig, G E L van den Berk, K Brinkman, D Kwa, N van der Meché, A Toonen, D Vos, M van Broekhuizen, F N Lauw, J W Mulder, J E Arends, A van Kessel, I de Kroon, A Boonstra, M E van der Ende, S Hullegie, B J A Rijnders, T J W van de Laar, L Gras, C Smit, A M Newsum, M Prins, W van der Veldt, Astrid M Newsum, Ineke G Stolte, Jan Tm van der Meer, Janke Schinkel, Marc van der Valk, Joost W Vanhommerig, Anne Buvé, Mark Danta, Arjan Hogewoning, Maria Prins, MOSAIC collaborators, J T M van der Meer, R Molenkamp, M Mutschelknauss, H E Nobel, H W Reesink, J Schinkel, M van der Valk, J W Vanhommerig, G E L van den Berk, K Brinkman, D Kwa, N van der Meché, A Toonen, D Vos, M van Broekhuizen, F N Lauw, J W Mulder, J E Arends, A van Kessel, I de Kroon, A Boonstra, M E van der Ende, S Hullegie, B J A Rijnders, T J W van de Laar, L Gras, C Smit, A M Newsum, M Prins, W van der Veldt

Abstract

Current guidelines recommend hepatitis C virus (HCV) testing for HIV-infected men who have sex with men (MSM) with ongoing risk behaviour, without specifying the type of risk behaviour. We developed and validated the HCV-MOSAIC risk score to assist HCV testing in HIV-infected MSM. The risk score consisted of six self-reported risk factors identified using multivariable logistic regression using data from the Dutch MOSAIC study (n = 213, 2009-2013). Area under the ROC curve (AUC), sensitivity, specificity, post-test-probability-of-disease and diagnostic gain were calculated. The risk score was validated in case-control studies from Belgium (n = 142, 2010-2013) and the United Kingdom (n = 190, 2003-2005) and in cross-sectional surveys at a Dutch sexually transmitted infections clinic (n = 284, 2007-2009). The AUC was 0.82; sensitivity 78.0% and specificity 78.6%. In the validation studies sensitivity ranged from 73.1% to 100% and specificity from 56.2% to 65.6%. The post-test-probability-of-disease ranged from 5.9% to 20.0% given acute HCV prevalence of 1.7% to 6.4%, yielding a diagnostic gain of 4.2% to 13.6%. The HCV-MOSAIC risk score can successfully identify HIV-infected MSM at risk for acute HCV infection. It could be a promising tool to improve HCV testing strategies in various settings.

Keywords: MSM; clinical prediction rule; diagnosis; hepatitis C; risk score; testing.

Conflict of interest statement

Conflict of interest: MV served on a scientific advisory board for AbbVie, Bristol-Myers Squibb, Gilead Sciences, Johnson and Johnson, MSD and a data safety monitoring board for ViiV healthcare. Through his institution he received non-financial support by MSD. The remaining authors (AN, IS, JM, JS, JV, AB, MD, AH, MP) declared no conflict of interest.

This article is copyright of The Authors, 2017.

Figures

Figure 1
Figure 1
Receiver operating characteristic curves for the original and HCV-MOSAIC risk score in the development study (A) and for the HCV-MOSAIC risk score in the three validation studies (B–D)
Figure 2
Figure 2
Fagan’s nomogram for a risk score of ≥ 2.0

References

    1. van de Laar TJ, Matthews GV, Prins M, Danta M. Acute hepatitis C in HIV-infected men who have sex with men: an emerging sexually transmitted infection. AIDS. 2010;24(12):1799-812. 10.1097/QAD.0b013e32833c11a5
    1. Kaplan-Lewis E, Fierer DS. Acute HCV in HIV-infected MSM: modes of acquisition, liver fibrosis, and treatment. Curr HIV/AIDS Rep. 2015;12(3):317-25. 10.1007/s11904-015-0279-3
    1. Hagan H, Jordan AE, Neurer J, Cleland CM. Incidence of sexually transmitted hepatitis C virus infection in HIV-positive men who have sex with men. AIDS. 2015;29(17):2335-45. 10.1097/QAD.0000000000000834
    1. van Santen DK. on behalf of the CASCADE Collaboration in EuroCoord. No Decline in Hepatitis C Virus (HCV) Incidence among HIV-positive Men who Have Sex with Men (MSM) within CASCADE: 1990-2014. European AIDS Conference. Barcelona. 21-24 Oct 2015. Abstract. BPD2/7.
    1. American Association for the Study of Liver Disease (AASLD) / Infectious Diseases Society of America (IDSA) / International AIDS Society (IAS)–USA. HCV testing and linkage to care. [Accessed 4 Apr 2016]. Available from:
    1. Nederlandse Vereniging van Hiv-behandelaren. [Dutch Association of HIV treating physicians]. Richtlijn HIV. [HIV guidelines]. [Accessed 4 Apr 2016]. Dutch. Available from:
    1. 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.
    1. Thomson EC, Nastouli E, Main J, Karayiannis P, Eliahoo J, Muir D, et al. Delayed anti-HCV antibody response in HIV-positive men acutely infected with HCV. AIDS. 2009;23(1):89-93. 10.1097/QAD.0b013e32831940a3
    1. Vanhommerig JW, Thomas XV, van der Meer JT, Geskus RB, Bruisten SM, Molenkamp R, et al. Hepatitis C virus (HCV) antibody dynamics following acute HCV infection and reinfection among HIV-infected men who have sex with men. Clin Infect Dis. 2014;59(12):1678-85. 10.1093/cid/ciu695
    1. Martin NK, Vickerman P, Dore GJ, Hickman M. The hepatitis C virus epidemics in key populations (including people who inject drugs, prisoners and MSM): the use of direct-acting antivirals as treatment for prevention. Curr Opin HIV AIDS. 2015;10(5):374-80. 10.1097/COH.0000000000000179
    1. Wand H, Iversen J, Wilson D, Topp L, Maher L. Developing and validating a scoring tool for identifying people who inject drugs at increased risk of hepatitis C virus infection. BMJ Open. 2012;2(1):e000387. 10.1136/bmjopen-2011-000387
    1. Bharti AR, Letendre SL, Wolfson T, Clifford D, Collier AC, Gelman B, et al. Clinical variables identify seronegative HCV co-infection in HIV-infected individuals. J Clin Virol. 2011;52(4):328-32. 10.1016/j.jcv.2011.08.021
    1. Nguyen MT, Herrine SK, Laine CA, Ruth K, Weinberg DS. Description of a new hepatitis C risk assessment tool. Arch Intern Med. 2005;165(17):2013-8. 10.1001/archinte.165.17.2013
    1. Zuure F, Davidovich U, Kok G, Depla AC, Hoebe C, van den Hoek A, et al. Evaluation of a risk assessment questionnaire to assist hepatitis C screening in the general population. Euro Surveill. 2010;15(15):19539.
    1. McGinn T, O’Connor-Moore N, Alfandre D, Gardenier D, Wisnivesky J. Validation of a hepatitis C screening tool in primary care. Arch Intern Med. 2008;168(18):2009-13. 10.1001/archinte.168.18.2009
    1. Lapane KL, Jakiche AF, Sugano D, Weng CS, Carey WD. Hepatitis C infection risk analysis: who should be screened? Comparison of multiple screening strategies based on the National Hepatitis Surveillance Program. Am J Gastroenterol. 1998;93(4):591-6. 10.1111/j.1572-0241.1998.170_b.x
    1. Lambers FA, Brinkman K, Schinkel J, Spijkerman IJ, Molenkamp R, Coutinho RA, et al. Treatment of acute hepatitis C virus infection in HIV-infected MSM: the effect of treatment duration. AIDS. 2011;25(10):1333-6. 10.1097/QAD.0b013e3283480144
    1. Vanhommerig JW, Lambers FA, Schinkel J, Geskus RB, Arends JE, van de Laar TJ, et al. Risk Factors for Sexual Transmission of Hepatitis C Virus Among Human Immunodeficiency Virus-Infected Men Who Have Sex With Men: A Case-Control Study. Open Forum Infect Dis. 2015;2(3):ofv115.
    1. Apers L, Vanden Berghe W, De Wit S, Kabeya K, Callens S, Buyze J, et al. Risk factors for HCV acquisition among HIV-positive MSM in Belgium. J Acquir Immune Defic Syndr. 2015;68(5):585-93. 10.1097/QAI.0000000000000528
    1. Danta M, Brown D, Bhagani S, Pybus OG, Sabin CA, Nelson M, et al. Recent epidemic of acute hepatitis C virus in HIV-positive men who have sex with men linked to high-risk sexual behaviours. AIDS. 2007;21(8):983-91. 10.1097/QAD.0b013e3281053a0c
    1. Urbanus AT, Van De Laar TJ, Geskus R, Vanhommerig JW, Van Rooijen MS, Schinkel J, et al. Trends in hepatitis C virus infections among MSM attending a sexually transmitted infection clinic; 1995-2010. AIDS. 2014;28(5):781-90. 10.1097/QAD.0000000000000126
    1. Newcombe RG. Interval estimation for the difference between independent proportions: comparison of eleven methods. Stat Med. 1998;17(8):873-90. 10.1002/(SICI)1097-0258(19980430)17:8<873::AID-SIM779>;2-I
    1. Akobeng AK. Understanding diagnostic tests 2: likelihood ratios, pre- and post-test probabilities and their use in clinical practice. Acta Paediatr. 2007;96(4):487-91. 10.1111/j.1651-2227.2006.00179.x
    1. Fagan TJ. Letter: Nomogram for Bayes theorem. N Engl J Med. 1975;293(5):257. 10.1056/NEJM197507312930513
    1. De Vries HJC, Van Doornum GJJ, Bax CJ, Van Bergen JEAM, De Bes J, Van Dam AP, et al. Multidisciplinaire Richtlijn Seksueel Overdraagbare Aandoeningen voor de 2e Lijn. [Multidisciplinary guideline Sexually Transmitted Infections for the second line]. Utrecht: Nederlandse Vereniging voor Dermatologie en Venereologie [Dutch Society for Dermatology and Venereology]; 2012. Dutch. Available from:
    1. Sharghi N, Bosch RJ, Mayer K, Essex M, Seage GR., 3rd The development and utility of a clinical algorithm to predict early HIV-1 infection. J Acquir Immune Defic Syndr. 2005;40(4):472-8. 10.1097/01.qai.0000164246.49098.47
    1. Hoenigl M, Weibel N, Mehta SR, Anderson CM, Jenks J, Green N, et al. Development and validation of the San Diego Early Test Score to predict acute and early HIV infection risk in men who have sex with men. Clin Infect Dis. 2015;61(3):468-75. 10.1093/cid/civ335
    1. Powers KA, Miller WC, Pilcher CD, Mapanje C, Martinson FE, Fiscus SA, et al. Improved detection of acute HIV-1 infection in sub-Saharan Africa: development of a risk score algorithm. AIDS. 2007;21(16):2237-42. 10.1097/QAD.0b013e3282f08b4d
    1. Jordan AE, Perlman DC, Neurer J, Smith DJ, Des Jarlais DC, Hagan H. Prevalence of hepatitis C virus infection among HIV+ men who have sex with men: a systematic review and meta-analysis. Int J STD AIDS. 2017;28(2):145-59. 10.1177/0956462416630910
    1. Lambers FA, Prins M, Thomas X, Molenkamp R, Kwa D, Brinkman K, et al. Alarming incidence of hepatitis C virus re-infection after treatment of sexually acquired acute hepatitis C virus infection in HIV-infected MSM. AIDS. 2011;25(17):F21-7. 10.1097/QAD.0b013e32834bac44
    1. Vanhommerig JW, van de Laar TJ, Koot M, van Rooijen MS, Schinkel J, Speksnijder AG, et al. Evaluation of a hepatitis C virus (HCV) antigen assay for routine HCV screening among men who have sex with men infected with HIV. J Virol Methods. 2015;213:147-50. 10.1016/j.jviromet.2014.11.026
    1. van de Laar TJ, Paxton WA, Zorgdrager F, Cornelissen M, de Vries HJ. Sexual transmission of hepatitis C virus in human immunodeficiency virus-negative men who have sex with men: a series of case reports. Sex Transm Dis. 2011;38(2):102-4. 10.1097/OLQ.0b013e3181ec9de5
    1. Volk JE, Marcus JL, Phengrasamy T, Hare CB. Incident Hepatitis C Virus Infections Among Users of HIV Preexposure Prophylaxis in a Clinical Practice Setting. Clin Infect Dis. 2015;60(11):1728-9. 10.1093/cid/civ129
    1. Molina JM, Capitant C, Spire B, Pialoux G, Cotte L, Charreau I, et al. On-Demand Preexposure Prophylaxis in Men at High Risk for HIV-1 Infection. N Engl J Med. 2015;373(23):2237-46. 10.1056/NEJMoa1506273
    1. McCormack S, Dunn DT, Desai M, Dolling DI, Gafos M, Gilson R, et al. Pre-exposure prophylaxis to prevent the acquisition of HIV-1 infection (PROUD): effectiveness results from the pilot phase of a pragmatic open-label randomised trial. Lancet. 2016;387(10013):53-60. 10.1016/S0140-6736(15)00056-2
    1. Ingiliz P, Martin TC, Rodger A, Stellbrink HJ, Mauss S, Boesecke C, et al. HCV reinfection incidence and spontaneous clearance rates in HIV-positive men who have sex with men in Western Europe. J Hepatol. 2017;66(2):282-7. 10.1016/j.jhep.2016.09.004
    1. Martin TC, Martin NK, Hickman M, Vickerman P, Page EE, Everett R, et al. Hepatitis C virus reinfection incidence and treatment outcome among HIV-positive MSM. AIDS. 2013;27(16):2551-7. 10.1097/QAD.0b013e32836381cc

Source: PubMed

3
Předplatit