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Risk Factors for HCV Reinfection or Transmission in HIV-HCV Coinfected MSM (ANRS-VESPA2 French National Survey)

Marcellin, Fabienne MSc*,†,‡; Demoulin, Baptiste MSc*,†,‡; Suzan-Monti, Marie MD*,†,‡; Maradan, Gwenaëlle MSc*,†,‡; Carrieri, Maria P. PhD*,†,‡; Dray-Spira, Rosemary PhD§,‖; Spire, Bruno MD*,†,‡the ANRS-VESPA2 Study Group

JAIDS Journal of Acquired Immune Deficiency Syndromes: December 15th, 2015 - Volume 70 - Issue 5 - p e179–e182
doi: 10.1097/QAI.0000000000000836
Letters to the Editor

*INSERM, UMR912 (SESSTIM), Marseille, France

Aix Marseille Université, UMR_S912, IRD, Marseille, France

ORS PACA, Observatoire Régional de la Santé Provence-Alpes-Côte d'Azur, Marseille, France

§INSERM, UMR_S1136, Pierre Louis Institute of Epidemiology and Public Health, Team Research in Social Epidemiology, Paris, France

Sorbonne Universités, UPMC University of Paris 06, UMR_S1136, Pierre Louis Institute of Epidemiology and Public Health, Team Research in Social Epidemiology, Paris, France

The VESPA2 survey was sponsored and funded by the French National Agency for Research on Aids and Viral Hepatitis (ANRS).

The authors have no funding or conflicts of interest to disclose.

F.M. participated in the data analysis and interpretation of results, wrote the manuscript draft, and revised it after suggestions from the coauthors. B.D. performed the statistical analyses and collaborated in the writing of the manuscript. G.M. was in charge of data management and collaborated in the writing of the manuscript. M.S.M., M.P.C., R.-D.S., and B.S. were involved in the design and conducting of the VESPA2 survey, they also participated in the interpretation of results and revised the manuscript before submission.

The ANRS-VESPA2 Study Group, Methodological and ground support, Data collection, Participating hospitals and investigators, Ethics approval, and Data sharing statement are listed in Appendix 1.

To the Editors:

Apers et al1 analyzed risk factors for hepatitis C virus (HCV) acquisition among HIV-infected men who have sex with men (MSM) in a case-control study conducted between January 2010 and December 2013 in 3 AIDS reference centers in Belgium. In their study, the presence of sexually transmitted infections (STIs) other than HIV, intercourse with other HIV-positive partners, and fisting were all confirmed as risk factors for sexual transmission of HCV in the study population. The risk of reinfection with HCV is high in HIV-infected MSM2–4 2–4 2–4 who clear HCV thanks to successful treatment (hereafter “posttreatment HCV clearers”) and warrants further investigation of associated risk factors.

We used socio-behavioral data from HIV-infected MSM participating in the French national survey ANRS-VESPA25 to compare the rate of posttreatment HCV clearers reporting HCV reinfection at-risk factors with that of HCV-chronically infected individuals reporting transmission at-risk factors.6

The ANRS VESPA2 survey was conducted between April 2011 and January 2012 in 73 HIV services located in 68 French hospitals. Its main objective was to describe the living conditions of adult HIV-infected patients followed up in French hospitals.7 The 3022 participants' socio-demographic, economic, and behavioral characteristics were collected using face-to-face administered questionnaires with trained interviewers. Hospital physicians in charge of participants completed a medical questionnaire. A patient for whom the physician reported a history of successful HCV therapy was considered a “posttreatment HCV clearer.” By contrast, a patient for whom the physician reported chronic HCV infection was considered a “HCV-chronically infected patient.” Men participating in VESPA2 who defined themselves as bisexual, gay, homosexual, or who reported at least one male sexual partner during the previous 12 months were characterized as MSM. Face-to-face questionnaires were used to document the following HCV reinfection/transmission risk factors during the previous 12 months among MSM: presence of STIs (syphilis, lymphogranuloma venereum, gonorrhea, condyloma, other STIs), number of male sexual partners, inconsistent condom use (ICU) during anal intercourse (at the most recent sexual encounter with casual partners), fisting, sex under the influence of drugs (ecstasy, cocaine, GHB, amphetamines, ketamine, mephedrone), and sex partying. Lifetime history of injecting drug use and illicit drug use during the previous 4 weeks were also documented. Data were weighted and calibrated to be representative of all adult HIV-infected patients followed up in French hospitals in 2011.5 The ANRS-VESPA2 survey was approved by the French National Commission for Data Protection and Liberties (CNIL) (approval number DR-2010-368).

The study population included MSM with sustained virological response to HCV treatment (posttreatment HCV clearers) and MSM with chronic HCV coinfection who were not on HCV treatment at the time of the study (characterized as “HCV-chronic individuals”).

We compared the percentage of individuals reporting each HCV risk factor between posttreatment HCV clearers (at risk of HCV reinfection) and HCV-chronic individuals (at risk of HCV transmission) using chi-square tests. Analyses were performed on weighted data. The weighting procedure accounted for both the sampling technique and the heterogeneous rates of nonparticipation in the survey between the subpopulations of HIV-infected patients.5 Stata/SE 12.1 software for Windows (Stata Corp LP) was used for the analyses.

A total of 1337 HIV-infected MSM participated in the ANRS-VESPA2 survey. Among them, 61 individuals (study population) were either posttreatment HCV clearers (n = 17) or HCV-chronic individuals (n = 44). When comparing the first group with the latter, no significant difference was found for age [mean (standard deviation):50.5 (6.6) versus 49.3 (10.6) years, P = 0.63]; time since HIV diagnosis [18.1 (6.0) versus 17.5 (7.3) years, P = 0.76]; time since HCV diagnosis [7.5 (4.8) versus 10.4 (8.8) years, P = 0.18]; history of injecting drug use (80.5% versus 66.2%, P = 0.32); illicit drug use during the previous 4 weeks (1.8% versus 3.5%, P = 0.52); and sexual activity (79.9% versus 78.9%, P = 0.95). Seventeen percent of MSM reported concomitant STIs, the percentage among posttreatment HCV clearers being much higher (39.2% versus 10.5% in HCV-chronic individuals, P = 0.03). Although there were important differences in the weighted prevalence of the other sexual HCV risk factors (such as participating in sex parties and fisting) between posttreatment HCV clearers and HCV-chronic individuals, none was significant (Fig. 1). Among these other factors, ICU during anal intercourse and having had at least 20 male sexual partners during the previous 12 months were most frequently reported in the study population (31.1% versus 29.9%, respectively). Thirteen percent of MSM reported they had participated in sex parties, 11.2% reported fisting, and 6.9% reported drug use during sex.



In this study conducted among 61 HIV-infected MSM, we found similar percentages of individuals reporting HCV reinfection and transmission risk factors among posttreatment HCV clearers and HCV-chronic individuals, respectively. A higher percentage of posttreatment HCV clearers reported STIs. These findings bring valuable information about the risk of both reinfection with HCV and HCV transmission in HIV-HCV coinfected MSMs.8 In the French study HEPAIG,9 in-depth interviews of HIV-infected MSM diagnosed with acute hepatitis C, showed that the moment of HCV diagnosis and the subsequent weeks constitute a prime period for engaging patients in discussion about sexual practices and prevention issues.10 However, the optimism which follows effective HCV treatment and viral clearance may be accompanied by the persistence of at-risk sexual practices unless tailored risk reduction strategies are developed with the support of MSM themselves.10 Because of the cross-sectional design of the ANRS-VESPA2 survey, longitudinal data concerning potential changes over time in individuals' behaviors were not available. In addition, unlike Apers et al,1 we had information about self-reported STIs, but not about medically documented STIs. Our study is also limited by its small sample size and by the lack of data concerning HCV viral load and liver fibrosis stage, the latter being an important criterion for HCV treatment initiation. However, given that the mean time since HCV diagnosis was approximately 10 years in this study, and that being an MSM is not a correlate of delayed access to HCV treatment in France,11 we may hypothesize that, among HCV-chronic patients, many treatment-naive individuals did not meet the criteria for HCV treatment initiation. Nevertheless, our results, based on data collected in a nationally representative sample of HIV-infected patients, complement those from previous multicenter local studies and qualitative research.2,10 2,10

Now that direct-acting antiviral based therapies are becoming increasingly available, and that more individuals are being cured of HCV, further social science studies are needed to better understand the dynamics of sexual and injection-related HCV risk behaviors in HIV-infected MSM,8 and to identify the innovative interventions needed to make the maintenance of HCV clearance a public health goal.

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The authors thank all the HIV-infected patients who agreed to participate in the survey, the medical staff from the participating hospitals, and the community-based organizations AIDES and Act-Up Paris who supported the survey. Finally, the authors thank Jude Sweeney for the English revision and editing of the manuscript.

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1. Apers L, Vanden Berghe W, De Wit S, et al.. Risk factors for HCV acquisition among HIV-positive MSM in Belgium. J Acquir Immune Defic Syndr. 2015;68:585–593.
2. Martin TCS, Martin NK, Hickman M, et al.. Hepatitis C virus reinfection incidence and treatment outcome among HIV-positive MSM. AIDS. 2013;27:2551–2557.
3. Lambers FAE, Prins M, Thomas X, 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:F21–F27.
4. Ingiliz P, Krznaric I, Stellbrink HJ, et al.. Multiple hepatitis C virus (HCV) reinfections in HIV-positive men who have sex with men: no influence of HCV genotype switch or interleukin-28B genotype on spontaneous clearance. HIV Med. 2014;15:355–361.
5. Dray-Spira R, Spire B, Lert F, et al.; le groupe Vespa2. General method of the ANRS-VESPA2 Study [in French]. Bull Epidémiologique Hebd. 2013;26:321–324.
6. Marcellin F, Lorente N, Demoulin B, et al.. Comparison of risk factors in HIV-infected men who have sex with men, coinfected or not with hepatitis C virus (ANRS VESPA2 French cross-sectional national survey). Sex Transm Infect. 2015;91:21–23.
7. Douab T, Marcellin F, Vilotitch A, et al.. Health-related quality of life of people living with HIV followed up in hospitals in France: comparing trends and correlates between 2003 and 2011 (ANRS-VESPA and VESPA2 national surveys). AIDS Care. 2014;26(suppl 1):S29–S40.
8. Young B, Martin NK, Martin TCS. Reinfection: Does it Limit HCV Treatment as Prevention? Medscape; International Conference on Viral Hepatitis (ICVH) 2014. Available at:
9. Larsen C, Chaix M-L, Le Strat Y, et al.. Gaining greater insight into HCV emergence in HIV-infected men who have sex with men: the HEPAIG Study. PLoS One. 2011;6:e29322.
10. Le Talec JY. When “raw sex” turns to a “raw deal” … taking the opportunity to think about sex? Interviews with HIV-positive gay men diagnosed with acute hepatitis C. Cult Health Sex. 2013;15:1133–1147.
11. Salmon-Ceron D, Cohen J, Winnock M, et al.. Engaging HIV-HCV co-infected patients in HCV treatment: the roles played by the prescribing physician and patients' beliefs (ANRS CO13 HEPAVIH cohort, France). BMC Health Serv Res. 2012;12:59.

The ANRS-VESPA2 Study Group: France Lert and Bruno Spire (scientific coordinators), Maria Patrizia Carrieri, Rosemary Dray-Spira, Christine Hamelin, Nicolas Lorente, Marie Préau, Marie Suzan-Monti, Fabienne Marcellin, and Martin Duracinsky, with the collaboration of Marion Mora.

Methodological and ground support: Yann Le Strat (InVS, Saint-Maurice), Lise Cuzin (Hôpital Purpan, Toulouse), Laurence Meyer (Cesp, Inserm, Le Kremlin Bicêtre), Daniela Rojas-Castro (Aides, Pantin), and Hugues Fischer (Act-Up Paris).

Data collection: The ClinSearch firm and the social research institute Ipsos.

Participating hospitals and investigators: Aix-en-Provence, CH Pays d'Aix (T. Allègre, P. Mours, J. M. Riou, M. Sordage); Angers, CHU Hôtel-Dieu (J. M. Chennebault, P. Fialaire, V. Rabier); Annemasse, CH Alpes-Léman (M. Froidure, D. Huguet, D. Leduc); Avignon, Hôpital Henri Duffaut (G. Pichancourt, A. Wajsbrot); Besançon, Hôpital Saint-Jacques (C. Bourdeaux, A. Foltzer, B. Hoen, L. Hustache-Mathieu); Bobigny, Hôpital Avicenne (S. Abgrall, R. Barruet, O. Bouchaud, A. Chabrol, S. Mattioni, F. Mechai); Bondy, Hôpital Jean Verdier (V. Jeantils); Bordeaux, Hôpital Saint-André (N. Bernard, F. Bonnet, M. Hessamfar, D. Lacoste, D. Malvy, P. Mercié, P. Morlat, F. Paccalin, M. C. Pertusa, T. Pistone, M. C. Receveur, M. A. Vandenhende); Boulogne-Billancourt, Hôpital Ambroise Paré (C. Dupont, A. Freire Maresca, J. Leporrier, E. Rouveix); Caen, Hôpital Clémenceau (S. Dargere, A. de la Blanchardière, A. Martin, V. Noyon, R. Verdon); CH de Chambéry (O. Rogeaux); Clermont-Ferrand, CHU Gabriel Montpied (J. Beytout, F. Gourdon, H. Laurichesse); Colombes, Hôpital Louis-Mourier (F. Meier, E. Mortier, A. M. Simonpoli); Creil, CH Laennec (F. Cordier); Créteil, CHIC (I. Delacroix, V. Garrait, B. Elharrar); Hôpital Henri Mondor (S. Dominguez, A. S. Lascaux, J. D. Lelièvre, Y. Levy, G. Melica); Dijon, Hôpital du Bocage (M. Buisson, L. Piroth, A. Waldner); Eaubonne, Hôpital Simone Veil (N. Gruat, A. Leprêtre); Garches, Hôpital Raymond-Poincaré (P. de Truchis, D. Le Du, J. Cl. Melchior); CH de Gonesse (R. Sehouane, D. Troisvallets); CHU de Grenoble (M. Blanc, I. Boccon-Gibod, A. Bosseray, J. P. Brion, F. Durand, P. Leclercq, F. Marion, P. Pavese); La Rochelle, Hôpital Saint-Louis (E. Brottier-Mancini, L. Faba, M. Roncato-Saberan); La Roche-sur-Yon, CHD Les Oudairies (O. Bollengier-Stragier, J. L. Esnault, S. Leautez-Nainville, P. Perré); CH de Lagny Marne-la-Vallée (E. Froguel, M. Nguessan, P. Simon); Le Chesnay, CH de Versailles (P. Colardelle, J. Doll, C. Godin-Collet, S. Roussin-Bretagne); Le Kremlin-Bicêtre, Hôpital de Bicêtre (J. F. Delfraissy, M. Duracinsky, C. Goujard, D. Peretti, Y. Quertainmont); CH du Mans (J. Marionneau); Lens, CH Dr. Schaffner (E. Aissi, N. Van Grunderbeeck); Limoges, CHU Dupuytren (E. Denes, S. Ducroix-Roubertou, C. Genet, P. Weinbreck); Lyon, Hôpital de la Croix-Rousse (C. Augustin-Normand, A. Boibieux, L. Cotte, T. Ferry, J. Koffi, P. Miailhes, T. Perpoint, D. Peyramond, I. Schlienger); Hôpital Édouard-Herriot (J. M. Brunel, E. Carbonnel, P. Chiarello, J. M. Livrozet, D. Makhloufi); Marseille, Hôpital de la Conception (C. Dhiver, H. Husson, A. Madrid, I. Ravaux, M. L. de Severac, M. Thierry Mieg, C. Tomei); Hôpital Nord (S. Hakoun, J. Moreau, S. Mokhtari, M. J. Soavi); Hôpital Sainte Marguerite (O. Faucher, A. Ménard, M. Orticoni, I. Poizot-Martin, M. J. Soavi); Montpellier, Hôpital Gui de Chauliac (N. Atoui, V. Baillat, V. Faucherre, C. Favier, J. M. Jacquet, V. Le Moing, A. Makinson, R. Mansouri, C. Merle); Montivilliers, Hôpital Jacques Monod (N. Elforzli); Nantes, Hôtel-Dieu (C. Allavena, O. Aubry, M. Besnier, E. Billaud, B. Bonnet, S. Bouchez, D. Boutoille, C. Brunet, N. Feuillebois, M. Lefebvre, P. Morineau-Le Houssine, O. Mounoury, P. Point, F. Raffi, V. Reliquet, J. P. Talarmin); Nice, Hôpital l'Archet (C. Ceppi, E. Cua, P. Dellamonica, F. De Salvador-Guillouet, J. Durant, S. Ferrando, V. Mondain-Miton, I. Perbost, S. Pillet, B. Prouvost-Keller, C. Pradier, P. Pugliese, V. Rahelinirina, P. M. Roger, E. Rosenthal, F. Sanderson); Orléans, Hôpital de La Source (L. Hocqueloux, M. Niang, T. Prazuck); Hôpital Porte Madeleine (P. Arsac, M. F. Barrault-Anstett); Paris, Hôpital Bichat—Claude-Bernard (M. Ahouanto, E. Bouvet, G. Castanedo, C. Charlois-Ou, A. Dia Kotuba, Z. Eid-Antoun, C. Jestin, K. Jidar, V. Joly, M. A. Khuong-Josses, N. Landgraf, R. Landman, S. Lariven, A. Leprêtre, F. L'hériteau, M. Machado, S. Matheron, F. Michard, G. Morau, G. Pahlavan, B. C. Phung, M. H. Prévot, C. Rioux, P. Yéni); Hôpital Cochin-Tarnier (F. Bani-Sadr, A. Calboreanu, E. Chakvetadze, D. Salmon, B. Silbermann); Hôpital européen Georges-Pompidou (D. Batisse, M. Beumont, M. Buisson, P. Castiel, J. Derouineau, M. Eliaszewicz, G. Gonzalez, D. Jayle, M. Karmochkine, P. Kousignian, J. Pavie, I. Pierre, L. Weiss); Hôpital Lariboisière (E. Badsi, M. Bendenoun, J. Cervoni, M. Diemer, A. Durel, A. Rami, P. Sellier); Hôpital Pitié-Salpêtrière (H. Ait-Mohand, N. Amirat, M. Bonmarchand, F. Bourdillon, G. Breton, F. Caby, J. P. Grivois, C. Katlama, M. Kirstetter, L. Paris, F. Pichon, L. Roudière, L. Schneider, M. C. Samba, S. Seang, A. Simon, H. Stitou, R. Tubiana, M. A. Valantin); Hôpital Saint-Antoine (D. Bollens, J. Bottero, E. Bui, P. Campa, L. Fonquernie, S. Fournier, P. M. Girard, A. Goetschel, H. F. Guyon, K. Lacombe, F. Lallemand, B. Lefebvre, J. L. Maynard, M. C. Meyohas, Z. Ouazene, J. Pacanowski, O. Picard, G. Raguin, P. Roussard, M. Tourneur, J. Tredup, N. Valin); Hôpital Saint-Louis (S. Balkan, F. Clavel, N. Colin de Verdière, N. De Castro, V. de Lastours, S. Ferret, S. Gallien, V. Garrait, L. Gérard, J. Goguel, M. Lafaurie, C. Lascoux-Combe, J. M. Molina, E. Oksenhendler, J. Pavie, C. Pintado, D. Ponscarme, W. Rozenbaum, A. Scemla); Hôpital Tenon (P. Bonnard, L. Lassel, M. G. Lebrette, T. Lyavanc, P. Mariot, R. Missonnier, M. Ohayon, G. Pialoux, M. P. Treilhou, J. P. Vincensini); Hôtel-Dieu (J. Gilquin, B. Hadacek, L. Nait-Ighil, T. H. Nguyen, C. Pintado, A. Sobel, J. P. Viard, O. Zak Dit Zbar); Perpignan, Hôpital Saint-Jean (H. Aumaître, A. Eden, M. Ferreyra, F. Lopez, M. Medus, S. Neuville, M. Saada); Pontoise, CH René Dubos (L. Blum); Quimper, Hôpital Laennec (P. Perfezou); Rennes, Hôpital de Pontchaillou (C. Arvieux, J. M. Chapplain, M. Revest, F. Souala, P. Tattevin); Rouen, Hôpital Charles-Nicolle (S. Bord, F. Borsa-Lebas, F. Caron, C. Chapuzet, Y. Debab, I. Gueit, M. Etienne, C. Fartoukh, K. Feltgen, C. Joly, S. Robaday-Voisin, P. Suel); Saint-Denis, CH Delafontaine (M. A. Khuong, J. Krausse, M. Poupard, G. Tran Van); Saint-Étienne, CHU Nord (C. Cazorla, F. Daoud, P. Fascia, A. Frésard, C. Guglielminotti, F. Lucht); Strasbourg, Nouvel hôpital civil (C. Bernard-Henry, C. Cheneau, J. M. Lang, E. de Mautort, M. P artisani, M. Priester, D. Rey); Suresnes, Hôpital Foch (C. Majerholc, D. Zucman); Toulon, CHI Chalucet (A. Assi, A. Lafeuillade); Hôpital Sainte-Anne (J. P. de Jaureguiberry, O. Gisserot); Toulouse, Hôpital de La Grave (C. Aquilina, F. Prevoteau du Clary); Hôpital Purpan (M. Alvarez, M. Chauveau, L. Cuzin, P. Delobel, D. Garipuy, E. Labau, B. Marchou, P. Massip, M. Mularczyk, M. Obadia); Tourcoing, CH Gustave Dron (F. Ajana, C. Allienne, V. Baclet, X. de la Tribonnière, T. Huleux, H. Melliez, A. Meybeck, B. Riff, M. Valette, N. Viget); Tours, CHRU Bretonneau (F. Bastides, L. Bernard, G. Gras, P. Guadagnin); Vandoeuvre-lès-Nancy, CHU Brabois (T. May, C. Rabaud); Vannes, CH Bretagne Atlantique (A. Dos Santos, Y. P oinsignon); Villejuif, Hôpital Paul-Brousse, (O. Derradji, L. Escaut, E. Teicher, D. Vittecoq); CHI de Villeneuve-Saint-Georges, (J. Bantsima, P. Caraux-Paz, O. Patey).

Ethics approval: The ANRS-VESPA2 survey was approved by the French National Commission for Data Protection and Liberties (CNIL) (approval number DR-2010-368).

Data sharing statement: No additional data available.

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