Risk of HIV transmission through condomless sex in serodifferent gay couples with the HIV-positive partner taking suppressive antiretroviral therapy (PARTNER): final results of a multicentre, prospective, observational study

Alison J Rodger, Valentina Cambiano, Tina Bruun, Pietro Vernazza, Simon Collins, Olaf Degen, Giulio Maria Corbelli, Vicente Estrada, Anna Maria Geretti, Apostolos Beloukas, Dorthe Raben, Pep Coll, Andrea Antinori, Nneka Nwokolo, Armin Rieger, Jan M Prins, Anders Blaxhult, Rainer Weber, Arne Van Eeden, Norbert H Brockmeyer, Amanda Clarke, Jorge Del Romero Guerrero, Francois Raffi, Johannes R Bogner, Gilles Wandeler, Jan Gerstoft, Felix Gutiérrez, Kees Brinkman, Maria Kitchen, Lars Ostergaard, Agathe Leon, Matti Ristola, Heiko Jessen, Hans-Jürgen Stellbrink, Andrew N Phillips, Jens Lundgren, PARTNER Study Group, Pep Coll, Patricia Cobarsi, Aroa Nieto, Michael Meulbroek, Antonia Carrillo, Jorge Saz, Jorge D R Guerrero, Mar Vera García, Felix Gutiérrez, Mar Masiá, Catalina Robledano, Agathe Leon, Lorna Leal, Eva G Redondo, Vicente P Estrada, Rocio Marquez, Raquel Sandoval, Pompeyo Viciana, Nuria Espinosa, Luis Lopez-Cortes, Daniel Podzamczer, Juan Tiraboschi, Sandra Morenilla, Antonio Antela, Elena Losada, Nneka Nwokolo, Janey Sewell, Amanda Clarke, Sarah Kirk, Alyson Knott, Alison J Rodger, Thomas Fernandez, Mark Gompels, Louise Jennings, Lana Ward, Julie Fox, Julianne Lwanga, Ming Lee, Richard Gilson, Clifford Leen, Sheila Morris, Dan Clutterbuck, Michael Brady, David Asboe, Serge Fedele, Sarah Fidler, Norbert Brockmeyer, Anja Potthoff, Adriane Skaletz-Rorowski, Johannes Bogner, Ulrich Seybold, Julia Roider, Heiko Jessen, Arne Jessen, Slobodan Ruzicic, Hans-Jürgen Stellbrink, Tim Kümmerle, Clara Lehmann, Olaf Degen, Sindy Bartel, Anja Hüfner, Jürgen Rockstroh, Karina Mohrmann, Christoph Boesecke, Ivanka Krznaric, Patrick Ingiliz, Rainer Weber, Christina Grube, Dominique Braun, Huldrych Günthard, Gilles Wandeler, Hansjakob Furrer, Andri Rauch, Pietro Vernazza, Patrick Schmid, Manuela Rasi, Denise Borso, Markus Stratmann, Oliver Caviezel, Marcel Stoeckle, Manuel Battegay, Philip Tarr, Vanessa Christinet, Florent Jouinot, Camille Isambert, Enos Bernasconi, Beatrice Bernasconi, Jan Gerstoft, Lene P Jensen, Anne A Bayer, Lars Ostergaard, Yordanos Yehdego, Ann Bach, Pia Handberg, Gitte Kronborg, Svend S Pedersen, Nete Bülow, Bente Ramskover, Matti Ristola, Outi Debnam, Jussi Sutinen, Anders Blaxhult, Ronnie Ask, Bernt Hildingsson-Lundh, Katarina Westling, Eeva-Maija Frisen, Gráinne Cortney, Siobhan O'Dea, Stephane De Wit, Coca Necsoi, Linos Vandekerckhove, Jean-Christophe Goffard, Sophie Henrard, Jan Prins, Hans-Henrik Nobel, Annouschka Weijsenfeld, Arne Van Eeden, Loek Elsenburg, Kees Brinkman, Danielle Vos, Imke Hoijenga, Elisabeth Gisolf, Petra Van Bentum, Dominique Verhagen, Francois Raffi, Eric Billaud, Michel Ohayon, Daniel Gosset, Alexandre Fior, Gilles Pialoux, Pelagie Thibaut, Julie Chas, Vincent Leclercq, Vincent Pechenot, Vincent Coquelin, Christian Pradier, Sophie Breaud, Veronique Touzeau-Romer, Armin Rieger, Maria Kitchen-Maria Geit, Mario Sarcletti, Martin Gisinger, Angela Oellinger, Andrea Antinori, Samanta Menichetti, Teresa Bini, Cristina Mussini, Marianna Meschiari, Antonio Di Biagio, Lucia Taramasso, Benedetto M Celesia, Maria Gussio, Nuno Janeiro, Alison J Rodger, Valentina Cambiano, Tina Bruun, Pietro Vernazza, Simon Collins, Olaf Degen, Giulio Maria Corbelli, Vicente Estrada, Anna Maria Geretti, Apostolos Beloukas, Dorthe Raben, Pep Coll, Andrea Antinori, Nneka Nwokolo, Armin Rieger, Jan M Prins, Anders Blaxhult, Rainer Weber, Arne Van Eeden, Norbert H Brockmeyer, Amanda Clarke, Jorge Del Romero Guerrero, Francois Raffi, Johannes R Bogner, Gilles Wandeler, Jan Gerstoft, Felix Gutiérrez, Kees Brinkman, Maria Kitchen, Lars Ostergaard, Agathe Leon, Matti Ristola, Heiko Jessen, Hans-Jürgen Stellbrink, Andrew N Phillips, Jens Lundgren, PARTNER Study Group, Pep Coll, Patricia Cobarsi, Aroa Nieto, Michael Meulbroek, Antonia Carrillo, Jorge Saz, Jorge D R Guerrero, Mar Vera García, Felix Gutiérrez, Mar Masiá, Catalina Robledano, Agathe Leon, Lorna Leal, Eva G Redondo, Vicente P Estrada, Rocio Marquez, Raquel Sandoval, Pompeyo Viciana, Nuria Espinosa, Luis Lopez-Cortes, Daniel Podzamczer, Juan Tiraboschi, Sandra Morenilla, Antonio Antela, Elena Losada, Nneka Nwokolo, Janey Sewell, Amanda Clarke, Sarah Kirk, Alyson Knott, Alison J Rodger, Thomas Fernandez, Mark Gompels, Louise Jennings, Lana Ward, Julie Fox, Julianne Lwanga, Ming Lee, Richard Gilson, Clifford Leen, Sheila Morris, Dan Clutterbuck, Michael Brady, David Asboe, Serge Fedele, Sarah Fidler, Norbert Brockmeyer, Anja Potthoff, Adriane Skaletz-Rorowski, Johannes Bogner, Ulrich Seybold, Julia Roider, Heiko Jessen, Arne Jessen, Slobodan Ruzicic, Hans-Jürgen Stellbrink, Tim Kümmerle, Clara Lehmann, Olaf Degen, Sindy Bartel, Anja Hüfner, Jürgen Rockstroh, Karina Mohrmann, Christoph Boesecke, Ivanka Krznaric, Patrick Ingiliz, Rainer Weber, Christina Grube, Dominique Braun, Huldrych Günthard, Gilles Wandeler, Hansjakob Furrer, Andri Rauch, Pietro Vernazza, Patrick Schmid, Manuela Rasi, Denise Borso, Markus Stratmann, Oliver Caviezel, Marcel Stoeckle, Manuel Battegay, Philip Tarr, Vanessa Christinet, Florent Jouinot, Camille Isambert, Enos Bernasconi, Beatrice Bernasconi, Jan Gerstoft, Lene P Jensen, Anne A Bayer, Lars Ostergaard, Yordanos Yehdego, Ann Bach, Pia Handberg, Gitte Kronborg, Svend S Pedersen, Nete Bülow, Bente Ramskover, Matti Ristola, Outi Debnam, Jussi Sutinen, Anders Blaxhult, Ronnie Ask, Bernt Hildingsson-Lundh, Katarina Westling, Eeva-Maija Frisen, Gráinne Cortney, Siobhan O'Dea, Stephane De Wit, Coca Necsoi, Linos Vandekerckhove, Jean-Christophe Goffard, Sophie Henrard, Jan Prins, Hans-Henrik Nobel, Annouschka Weijsenfeld, Arne Van Eeden, Loek Elsenburg, Kees Brinkman, Danielle Vos, Imke Hoijenga, Elisabeth Gisolf, Petra Van Bentum, Dominique Verhagen, Francois Raffi, Eric Billaud, Michel Ohayon, Daniel Gosset, Alexandre Fior, Gilles Pialoux, Pelagie Thibaut, Julie Chas, Vincent Leclercq, Vincent Pechenot, Vincent Coquelin, Christian Pradier, Sophie Breaud, Veronique Touzeau-Romer, Armin Rieger, Maria Kitchen-Maria Geit, Mario Sarcletti, Martin Gisinger, Angela Oellinger, Andrea Antinori, Samanta Menichetti, Teresa Bini, Cristina Mussini, Marianna Meschiari, Antonio Di Biagio, Lucia Taramasso, Benedetto M Celesia, Maria Gussio, Nuno Janeiro

Abstract

Background: The level of evidence for HIV transmission risk through condomless sex in serodifferent gay couples with the HIV-positive partner taking virally suppressive antiretroviral therapy (ART) is limited compared with the evidence available for transmission risk in heterosexual couples. The aim of the second phase of the PARTNER study (PARTNER2) was to provide precise estimates of transmission risk in gay serodifferent partnerships.

Methods: The PARTNER study was a prospective observational study done at 75 sites in 14 European countries. The first phase of the study (PARTNER1; Sept 15, 2010, to May 31, 2014) recruited and followed up both heterosexual and gay serodifferent couples (HIV-positive partner taking suppressive ART) who reported condomless sex, whereas the PARTNER2 extension (to April 30, 2018) recruited and followed up gay couples only. At study visits, data collection included sexual behaviour questionnaires, HIV testing (HIV-negative partner), and HIV-1 viral load testing (HIV-positive partner). If a seroconversion occurred in the HIV-negative partner, anonymised phylogenetic analysis was done to compare HIV-1 pol and env sequences in both partners to identify linked transmissions. Couple-years of follow-up were eligible for inclusion if condomless sex was reported, use of pre-exposure prophylaxis or post-exposure prophylaxis was not reported by the HIV-negative partner, and the HIV-positive partner was virally suppressed (plasma HIV-1 RNA <200 copies per mL) at the most recent visit (within the past year). Incidence rate of HIV transmission was calculated as the number of phylogenetically linked HIV infections that occurred during eligible couple-years of follow-up divided by eligible couple-years of follow-up. Two-sided 95% CIs for the incidence rate of transmission were calculated using exact Poisson methods.

Findings: Between Sept 15, 2010, and July 31, 2017, 972 gay couples were enrolled, of which 782 provided 1593 eligible couple-years of follow-up with a median follow-up of 2·0 years (IQR 1·1-3·5). At baseline, median age for HIV-positive partners was 40 years (IQR 33-46) and couples reported condomless sex for a median of 1·0 years (IQR 0·4-2·9). During eligible couple-years of follow-up, couples reported condomless anal sex a total of 76 088 times. 288 (37%) of 777 HIV-negative men reported condomless sex with other partners. 15 new HIV infections occurred during eligible couple-years of follow-up, but none were phylogenetically linked within-couple transmissions, resulting in an HIV transmission rate of zero (upper 95% CI 0·23 per 100 couple-years of follow-up).

Interpretation: Our results provide a similar level of evidence on viral suppression and HIV transmission risk for gay men to that previously generated for heterosexual couples and suggest that the risk of HIV transmission in gay couples through condomless sex when HIV viral load is suppressed is effectively zero. Our findings support the message of the U=U (undetectable equals untransmittable) campaign, and the benefits of early testing and treatment for HIV.

Funding: National Institute for Health Research.

Copyright © 2019 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY-NC-ND 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Figures

Figure 1
Figure 1
Rate of within-couple HIV transmission through condomless sex according to sexual behaviour reported by the HIV-negative partner STI=sexually transmitted infection. NA=not applicable. *Estimated using the exact Poisson method. †Numerator is the number of HIV-negative men within the eligible couples ever reporting that specific sexual act and denominator is the group-specific number of HIV-negative participants who contributed eligible couple-years of follow-up. ‡Refers to STIs (excluding HIV) self-reported by the HIV-negative partner.
Figure 2
Figure 2
Phylogenetic tree of pol and env sequences from nine couples with subtype B infection Bayesian Markov Chain Monte-Carlo inference (012313+I+G+F). Branch length is proportional to the genetic distance and line weight is proportional to the posterior probability. (A) Partners' (initially HIV-positive partners and seroconverters) sequences are in blue and found phylogenetically unlinked to viruses recovered from their putative transmitters, with a median pairwise genetic distance of 0·069 (IQR 0·057–0·076) and pairwise genetic distances consistently greater than 0·040. Positive control sequences comprised replicate sequences from study partners and sequences from confirmed transmission pairs obtained in a separate study. The positive control sequences show pairwise genetic distance 0·004 (IQR

Figure 3

Upper 95% CI limit around…

Figure 3

Upper 95% CI limit around estimated rate of zero HIV transmissions through penetrative…

Figure 3
Upper 95% CI limit around estimated rate of zero HIV transmissions through penetrative sex (vaginal or anal) at the end of PARTNER1 and PARTNER2
Figure 3
Figure 3
Upper 95% CI limit around estimated rate of zero HIV transmissions through penetrative sex (vaginal or anal) at the end of PARTNER1 and PARTNER2

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