Abstract
Within the MSM population, men who have sex with both men and women (MSMW) are identified as a high-risk group both worldwide and in Europe. In a multi-centred bio-behavioural cross-sectional study, we aimed to assess the relationship(s) between socio-demographic factors, stigma, sexual behavioural patterns, test seeking behaviour and sero-status amongst MSMW. A multi-level analysis was conducted to identify factors associated with being MSMW versus Men who have Sex with Men Only (MSMO). A total of 4901 MSM were enrolled across the 13 study sites. Participants were categorised as MSMW in the 12.64% of the cases. Factors such as educational status, perceived homonegativity, testing facilities knowledge and HIV testing lifetime seem to be relevant factors when characterising the MSMW group. The results highlight the vulnerability of MSMW and the wide spectrum of risky behavioural and psycho-social patterns, particularly in terms of HIV testing, ‘outness’, and perceived stigma.
Resumen
Los Hombres que tienen Sexo con Hombres y Mujeres (HSHM) son un grupo de población de alto riesgo dentro de los HSH. Evaluar la relación entre factores socio-demográficos, estigma, patrones de conducta sexual y de búsqueda de la prueba y el estado serológico de los HSHM. Estudio bio-conductual multicéntrico transversal. Análisis multinivel para identificar factores asociados con ser HSHM respecto a los Hombres que Sólo tienen Sexo con Hombres. Se reclutaron 4.901 HSH en 13 ciudades, siendo un 12,64% HSHM. El nivel educativo, la homonegatividad percibida, el conocimiento de los lugares de realización de la prueba y la prueba del VIH alguna vez son factores relevantes para caracterizar los HSHM. Los resultados subrayan la vulnerabilidad de los HSHM y la diversidad de conductas y patrones psicosociales de riesgo, particularmente en términos de la prueba del VIH, visibilidad de la identidad sexual y estigma percibido.
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References
UNAIDS. Joint United Nations Programme on HIV/AIDS. Global AIDS response progress reporting 2014: construction of core indicators for monitoring the 2011 UN political declaration on HIV/AIDS. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS), WHO Library Cataloguing-in-Publication Data, 2014. ISBN 978 92 4 150.
Beyrer C, Baral SD, Collins C, Richardson ET, Sullivan PS, Sanchez J, Trapence G, Katabira E, Kazatchkine M, Ryan O, Wirtz AL, Mayer KH. The global response to HIV in men who have sex with men. Lancet. 2016;388(10040):198–206.
Mirandola M, Folch C, Krampac I, Nita I, Stanekova D, Stehlikova D, Toskin I, Gios L, Foschia JP, Breveglieri M, Furegato M, Castellani E, Bonavina MG. SIALON network. HIV bio-behavioural survey among men who have sex with men in Barcelona, Bratislava, Bucharest, Ljubljana, Prague and Verona, 2008–2009. Eur Surveill. 2009;14(48):1424–7.
Mirandola M, Gios L, Sherriff N, Toskin I, Marcus U, Schink S, Suligoi B, Folch C, Rosińska M, editors. The Sialon II Project. Report on a Bio-behavioural Survey among MSM in 13 European cities. Cierre Grafica, 2016. ISBN 978-88-98768-55-4.
ECDC, European Centre for Disease Prevention and Control. Thematic Report. Men who have sex with men. Monitoring implementation of the Dublin Declaration on Partnership to Fight HIV/AIDS in Europe and Central Asia: 2014 progress report. Stockholm: ECDC; 2014. p. 2015.
The EMIS Network. EMIS 2010. The European men-who-have-sex-with-men internet survey. Findings from 38 countries. Stockholm: European Centre for Disease Prevention and Control, 2013.
Jeffries WL. Beyond the bisexual bridge: sexual health among U.S. men who have sex with men and women. Am J Prev Med. 2014;47(3):320–9.
Liao M, Wang M, Shen X, Huang P, Yang X, Hao L, et al. Bisexual behaviors, HIV knowledge, and stigmatizing/discriminatory attitudes among men who have sex with men. PLoS ONE. 2015;10(6):e0130866. doi:10.1371/journal.pone.0130866.
Dyer TP, Regan R, Pacek LR, Acheampong A, Khan MR. Psychosocial vulnerability and HIV-related sexual risk among men who have sex with men and women in the United States. Arch Sex Behav. 2015;44(2):429–41.
ECDC, European Centre for Disease Prevention and Control. A comprehensive approach to HIV/STI prevention in the context of sexual health in the EU/EEA. Stockholm: ECDC, 2013.
Yun K, Xu JJ, Reilly KH, Zhang J, Jiang YJ, Wang N, Shang H. Prevalence of bisexual behaviour among bridge population of men who have sex with men in China: a meta-analysis of observational studies. Sex Transm Infect. 2011;87(7):563–70.
Gorbach PM, Murphy R, Weiss RE, Hucks-Ortiz C, Shoptaw S. Bridging sexual boundaries: men who have sex with men and women in a street-based sample in Los Angeles. J Urban Health. 2009;86(Suppl 1):63–76.
Godbole S, Sane S, Kamble P, Raj Y, Dulhani N. Predictors of bisexual behaviour among MSM attending Intervention sites may help in prevention interventions for the bridge to the heterosexual epidemic in India: data from HIV sentinel surveillance. PLoS ONE. 2014;9(9):e107439.
Beyrer C, Baral SD, van Griensven F, et al. Global epidemiology of HIV infection in men who have sex with men. Lancet. 2012;380(9839):367–77.
Sanders EJ, Graham SM, Okuku HS, van der Elst EM, Muhaari A, Davies A, Peshu N, Price M, McClelland RS, Smith AD. HIV-1 infection in high risk men who have sex with men in Mombasa, Kenya. AIDS. 2007;21(18):2513–20.
Cáceres CF, Konda K, Segura ER, Lyerla R. Epidemiology of male same-sex behaviour and associated sexual health indicators in low- and middle-income countries: 2003–2007 estimates. Sex Transm Infect. 2008;84(Suppl 1):i49–56.
Friedman MR, Wei C, Klem ML, Silvestre AJ, Markovic N, Stall R. HIV infection and sexual risk among men who have sex with men and women (MSMW): a systematic review and meta-analysis. PLoS ONE. 2014;9(1):e87139.
Maulsby C, Sifakis F, German D, Flynn CP, Holtgrave D. HIV risk among men who have sex with men only (MSMO) and men who have sex with men and women (MSMW) in Baltimore. J Homosex. 2013;60(1):51–68.
Mirandola M, Gios L, Davis RJ, Furegato M, Breveglieri M, Folch C, Stanekova D, Nita I, Stehlíková D. Socio-demographic factors predicting HIV test seeking behaviour among MSM in 6 EU cities. Eur J Pub Health. 2016. doi:10.1093/eurpub/ckw144.
Phillips AN, et al. Potential impact on HIV incidence of higher HIV testing rates and earlier antiretroviral therapy initiation in MSM. AIDS. 2015;29:1855–62.
WHO, World Health Organisation, Department of Reproductive Health and Research. Emergence of multi-drug resistant Neisseria gonorrhoeae—threat of global rise in untreatable sexually transmitted infections. World Health Organisation, 2011.
Schrimshaw EW, Downing MJ, Cohn DJ. Reasons for non-disclosure of sexual orientation among behaviorally bisexual men: non-disclosure as stigma management. Arch Sex Behav. 2016. doi:10.1007/s10508-016-0762-y.
Pachankis JE, Hatzenbuehler ML, Hickson F, Weatherburn P, Berg RC, Marcus U, Schmidt AJ. hidden from health: structural stigma, sexual orientation concealment, and hiv across 38 countries in the european msm internet survey. AIDS. 2015;29(10):1239–46.
Pachankis JE, Hatzenbuehler ML, Mirandola M, Weatherburn P, Berg RC, Marcus U, Schmidt AJ. The geography of sexual orientation: structural stigma and sexual attraction, behavior, and identity among men who have sex with men across 38 European countries. Arch Sex Behav. 2016. doi:10.1007/s10508-016-0819-y.
Dodge B, Schnarrs PW, Reece M, Martinez O, Goncalves G, Malebranche D, Fortenberry JD. Sexual behaviors and experiences among behaviorally bisexual men in the midwestern United States. Arch Sex Behav. 2013;42(2):247–56.
Gios L, Mirandola M, Toskin I, Marcus U, et al. Bio-behavioural HIV and STI surveillance among men who have sex with men in Europe: the Sialon II protocols. BMC Public Health. 2016;16(1):212.
Grov C, Rendina HJ, Moody RL, Ventuneac A, Parsons JT. HIV serosorting, status disclosure, and strategic positioning among highly sexually active gay and bisexual men. AIDS Patient Care STDS. 2015;29(10):559–68.
Martos AJ, Nezhad S, Meyer IH. Variations in sexual identity milestones among lesbians, gay men, and bisexuals. Sex Res Soc Policy. 2014;12(1):24–33.
Bowring AL, Veronese V, Doyle JS, Stoove M, Hellard M. HIV and sexual risk among men who have sex with men and women in Asia: a systematic review and meta-analysis. AIDS Behav. 2016;20:2243–5.
Guo Y, Li X, Song Y, Liu Y. Bisexual behavior among Chinese young migrant men who have sex with men: implications for HIV prevention and intervention. AIDS Care. 2012;24:451–8.
Guadamuz TE, Cheung DH, Wei C, Koe S, Lim SH. Young, online and in the dark: scaling up HIV testing among MSM in ASEAN. PLoS ONE. 2015;10(5):e0126658.
MacKellar D, Gallagher K, Sanchez T, Lansky A, Sullivan P. Surveillance of HIV risk and prevention behaviors of men who have sex with men—a national application of venue-based, time-space sampling. Public Health Rep. 2007;122(Suppl 1):39–47.
Johnston LG, Whitehead S, Simic-Lawson M, Kendall C. Formative research to optimize respondent-driven sampling surveys among hard-to-reach populations in HIV behavioral and biological surveillance: lessons learned from four case studies. AIDS Care. 2010;22(6):784–92.
Rabe-Hesketh S, Skrondal A. Multilevel and longitudinal modeling using Stata. College Station: Stata Press; 2008.
Benoit E, Koken JA. Perspectives on substance use and disclosure among behaviorally bisexual Black men with female primary partners. J Ethn Subst Abuse. 2012;11(4):294–317.
Friedman MR, Stall R, Silvestre AJ, et al. Stuck in the middle: longitudinal HIV-related health disparities among men who have sex with men and women (MSMW). J Acquir Immune Defic Syndr. 2014;66(2):213–20.
Maulsby C, Sifakis F, German D, Flynn CP, Holtgrave D. Differences and similarities in HIV testing among men who have sex with men and women (MSMW) and men who have sex with men only (MSMO). Open AIDS J. 2012;6:53–9.
CDC, Centers for Disease Control and Prevention. HIV testing and risk behaviors among gay, bisexual, and other men who have sex with men—United States. MMWR. 2013;62(47):958–62.
Zule WA, Bobashev GV, Wechsberg WM, Costenbader EC, Coomes CM. Behaviorally bisexual men and their risk behaviors with men and women. J Urban Health. 2009;86(Suppl 1):48–62.
Toskin I, Cooper B, Troussier T, Klugman B, Kulier R, Chandra-Mouli V, Temmerman M. WHO guideline for brief sexuality-related communication: implications for STI/HIV policy and practice. Reprod Health Matters. 2015;23(46):177–84.
Cooper B, Toskin I, Kulier R, Allen T, Hawkes S. Brief sexuality communication–a behavioural intervention to advance sexually transmitted infection/HIV prevention: a systematic review. BJOG. 2014;121(Suppl 5):92–103.
World Health Organization. Brief sexuality-related communication: recommendations for a public health approach. World Health Organization, 2015. ISBN 978 92 4 154900 4.
Kurth AE, Celum C, Baeten JM, Vermund SH, Wasserheit JN. Combination HIV prevention: significance, challenges, and opportunities. Curr HIV/AIDS Rep. 2011;8(1):62–72.
Muñoz-Laboy M, Severson N, Bannan S. Occupations, social vulnerability and HIV/STI risk: the case of bisexual Latino men in the New York City metropolitan area. Global Public Health. 2014;9(10):1167–83.
Chen JP, Han MM, Liao ZJ, Dai ZZ. HIV-related behaviors, social support and health-related quality of life among men who have sex with men and women (MSMW): a cross-sectional study in Chongqing, China. PLoS ONE. 2015;10(2):e0118651. doi:10.1371/journal.pone.0118651.
Callis AS. Playing with butler and foucault: bisexuality and queer theory. J Bisexuality. 2009;9(3–4):213–33.
Ramakrishnan L, Ramanathan S, Chakrapani V, Goswami P, Deshpande S, Yadav D, Sen S, George B, Paranjape R. Comparison of sexual risk, HIV/STI prevalence and intervention exposure among men who have sex with men and women (MSMW) and men who have sex with men only (MSMO) in India: implications for HIV prevention. AIDS Behav. 2015;19(12):2255–69.
Funding
This manuscript is based on data from the Sialon II project, co-funded under the Second Programme of Community Action in the field of Health (2008–2013) (Work Plan 2010) (Grant Agreement Number: 2010 12 11). The sole responsibility lies with the authors of this manuscript and the Commission is not responsible for any use that may be made of the information contained therein.
The Sialon II Network (extended list)
Massimo Mirandola, Lorenzo Gios, Stefano Benvenuti, Ruth Joanna Davis, Massimo Lunardi, Silvana Menichelli, Michele Breveglieri (Coordinamento Regionale per il Management e la Progettazione Europea, Azienda Ospedaliera Universitaria Integrata, Verona, Italy); Wim Vanden Berghe, Peter de Groot, Christiana Nöstlinger, Veronica van Wijk, Katrien Fransen, Tine Vermoesen, Michiel Vanackere (Institute of Tropical Medicine, Antwerp, Belgium); Fourat Benchikha, Sandra Van den Eynde, Boris Cruyssaert, Mark Sergeant, Karel Blondeel, Pieter Damen (Sensoa, Antwerp, Belgium); François Massoz, Erwin Carlier (Rainbowhouse Brussels, Belgium); Michael François, Stephen Karon (Ex Aequo, Belgium); Safia Soltani, Thierry Martin (Belgium); Alan De Bruyne (The Belgian Pride, Belgium); Françoise Bocken (Alias, Belgium); Myriam Dieleman (Observatoire du sida et des sexualités, Belgium); Ivailo Alexiev, Reneta Dimitrova, Anna Gancheva, Dobromira Bogeva, Maria Nikolova, Mariya Muhtarova, Todor Kantarjiev (National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria); Viara Georgieva (National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria; Ministry of Health, Sofia, Bulgaria); Emilia Naseva, Petar Tsintsarski, Hristo Taskov, Tonka Varleva (Program “Prevention and Control of HIV/AIDS”, Ministry of Health, Sofia, Bulgaria); Elena Birindjieva, Aneliya Angelova, Manol Antonov (Association “Health without borders”, Bulgaria); Ulrich Marcus, Susanne Barbara Schink, Sandra Dudareva-Vizule, Matthias an der Heiden, Sami Marzougui, Viviane Bremer, Andrea Kühne, Kerstin Schönerstedt-Zastrau, Ruth Zimmermann (Robert Koch Institute, Berlin, Germany); Andreas Wille (Institut für Hygiene und Umwelt, Hamburg, Germany); Kai Eckstein, Norman Buch, Philipp Moskophidis, Marc Grenz, Danilo Schmogro (Hein & Fiete, Hamburg, Germany); Giuseppe Cornaglia, Antonella Zorzi, Elisabetta Tonolli, Giuliana Lo Cascio, Teresa Todeschini, Manuela Recchia, Lorella Pattini, Maria Rocca, Alessandra Bighignoli, Anita Galardi, Loredana Martini, Francesco Cobello, Chiara Bovo (Azienda Ospedaliera Universitaria Integrata, Verona, Italy); Oscar Bortolami, Laura Crestani (Unità Supporto alla Ricerca e Biostatistica, Azienda Ospedaliera Universitaria Integrata, Verona, Italy); Fabiano Comperini (Italy); Ercole Concia, Emanuela Lattuada, Massimiliano Lanzafame, Paola Del Bravo (Infectious Diseases Section, Department of Pathology, Verona University Hospital, Veneto Region, Verona, Italy); Maddalena Cordioli, Fabio Rigo, Emanuele Guardalben, Ivan Marchesoni (Università degli studi di Verona, Verona, Italy); Barbara Suligoi, Vincenza Regine, Lucia Pugliese (Centro Operativo AIDS, Istituto Superiore di Sanità, Rome, Italy); Saulius Caplinskas, Irma Caplinskiene, Rima Krupenkaite (Centre for Communicable Diseases and AIDS, Vilnius, Lithuania); Gediminas Sargelis, Arturas Rudomanskis (“Tolerant Youth Association”, Vilnius, Lithuania); Sónia Dias, Ana Gama, Oriana Brás (Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Portugal); João Piedade (Medical Microbiology Unit, Instituto de Higiene e Medicina Tropical, Lisbon, Portugal); Ricardo Fuertes, Nuno Pinto, João Brito, Júlio Esteves, Jesus Rojas, Fernando Ferreira, Miguel Rocha, Hugo Machado, Maria José Campos (CheckpointLX, Portugal); Luís Mendão (Grupo Português de Ativistas sobre Tratamentos de VIH/SIDA—Pedro Santos, Portugal); Magdalena Rosińska, Bożena Kucharczyk, Marta Niedźwiedzka-Stadnik, Łukasz Henszel, Andrzej Zieliński, Michał Czerwiński (National Institute of Public Health—National Institute of Hygiene, NIPH-NIH, Warsaw, Poland); Michał Pawlęga, Ewelina Burdon, Małgorzata Gajdemska, Agnieszka Guściora, Nikodem Klasik, Katarzyna Rżanek, Michał Sawicki, Michał Tęcza (Lambda Warszawa, Warsaw, Poland); Mateusz Dębski, Anna Maciejewska, Izabela Pazdan (SKA Warsaw, Poland); Alexandru Rafila, Daniela Pitigoi, Adrian Abagiu (National Institute for Infectious Diseases Prof. Dr. Matei Bals, Bucharest, Romania); Carolina Marin, Ioana Panzariu, Alexandru Miroiu (ACCEPT Association, Bucharest, Romania); Madalina Popa, Monica Likker (National Institute for Infectious Diseases Prof. Dr. Matei Bals, Bucharest, Romania); Maria Georgescu, Galina Musat, Dan Cojocaru, Mihai Lixandru, Raluca Teodorescu (Romanian Anti-AIDS Association—ARAS, Bucharest, Romania); Danica Staneková, Monika Hábeková, Tatiana Drobková, Zuzana Chabadová, Soňa Wimmerova, Maria Mojzesová (Slovak Medical University, NRC for HIV/AIDS Prevention, Bratislava, Slovakia); Filip Kunč, Michal Skurák, Peter Bodnar, Katarína Horniaková, Mária Krahulcová, Jarmila Präsensová (Slovakia); Martin Smoleň, Peter Záhradník, Pavol Tibaj (NGO Dúhové srdce, Bratislava, Slovakia); Irena Klavs, Tanja Kustec, Claudia Adamič (National Institute of Public Health, Ljubljana, Slovenia); Mario Poljak, Robert Krošelj, Jana Mlakar (Institute of Microbiology and Immunology, Medical Faculty, University of Ljubljana, Ljubljana, Slovenia); Miran Šolinc (Association SKUC, Ljubljana, Slovenia); Cinta Folch, Laia Ferrer, Alexandra Montoliu, Jordi Casabona, Anna Esteve, Montserrat Galdon (Centre for Epidemiological Studies on HIV/STI in Catalonia CEEISCAT, Dept Salut, Generalitat de Catalunya, Barcelona, Spain); Victoria Gonzalez (Microbiology Service, Hospital Universitari Germans Trias i Pujol, Barcelona, Spain); Rafael Muñoz (StopSida, Barcelona, Spain); Maria Axelsson, Torsten Berglund, Sharon Kuhlmann-Berenzon, Achilleas Tsoumanis, Inga Velicko, Christer Janson, Bartek Lindh, Kajsa Aperia (Public Health Agency of Sweden, Stockholm, Sweden); Buddha Babulanam, Hans Carlberg, Malte Davidsson, Nedo Entenza Gutierrez, Viktor Hildingsson, Henrik Klasson, Moises Peña Ramos, Cristian Quintero Rojas, Sven-Olof Sandberg, Andreas Samuelson,Eric Sjöberg, Tommy Sjölund,Simon Svensson, Iván Valencia (Sweden); Filip Garcia, Olov Lindblad (RFSL Stockholm, Sweden); Jon Voss (Stockholm Gay Life, Sweden); Ronnie Ask, Anders Blaxhult, Maarit Maliniemi (Venhälsan, Stockholm South General Hospital, Stockholm, Sweden); Monica Ideström, Nils Blom (Public Health Agency of Sweden, Stockholm, Sweden); Nigel Sherriff, Christina Panton, Glynis Flood (Centre for Health Research, University of Brighton, Brighton, UK); Katrien Fransen, Tine Vermoesen (Aids Reference Laboratory, Institute of Tropical Medicine, Antwerp, Belgium); Ross Boseley, Marc Tweed (Terrence Higgins Trust, South, UK); Jonathon Roberts (Claude Nicol Centre, Royal Sussex County Hospital, Brighton, UK); Cinthia Menel Lemos (Executive Agency for Health and Consumers); Paolo Guglielmetti, Wolfgang Philipp (DG SANTE); Andrew Amato, Irina Dinca, Karin Haar, Anastasia Pharris, Teymur Noori (European Centre for Disease Prevention and Control ECDC); Igor Toskin, Natalie Maurer (Department of Reproductive Health & Research of the World Health Organization, WHO); Lev Zohrabyan, Alexandrina Iovita, Maddalena Campioni, Patrick Noack (Joint United Nations Programme on HIV/AIDS UNAIDS); Rosanna Peeling (London School of Hygiene and Tropical Medicine); Lisa Johnston (USA).
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MMI, LGI, NSH, ITO, LFE, SDI, IVE, DST, SCA, ENA participated in the design of the survey questionnaire and the organisation and implementation of the survey in the survey cities. This analysis was conceived by MMI and LGI. Data were analysed by MMI and LGI. The first manuscript draft was jointly written by MMI and LGI. All authors (MMI, LGI, NSH, JPA, ITO, LFE, SDI, IVE, DST, SCA, MNI, ENA) contributed writing to the following drafts. All authors read and approved the final manuscript.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Prior to data collection, research protocols were submitted to, and approved by, an appropriate institutional ethical review board in each participating city, as well as by the WHO Research Project Review Panel (RP2) and the WHO Research Ethics Review Committee (ERC) during 2012–2013.
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According to the study protocol procedures, informed consent was obtained from all individual participants included in the study.
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Collaborators of the Sialon II Network are listed in “Acknowledgements”.
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Mirandola, M., Gios, L., Sherriff, N. et al. Socio-demographic Characteristics, Sexual and Test-Seeking Behaviours Amongst Men Who have Sex with Both Men and Women: Results from a Bio-behavioural Survey in 13 European Cities. AIDS Behav 21, 3013–3025 (2017). https://doi.org/10.1007/s10461-017-1831-5
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DOI: https://doi.org/10.1007/s10461-017-1831-5