Observational Study

. 2019 Jun 15;393(10189):2428-2438.

doi: 10.1016/S0140-6736(19)30418-0. Epub 2019 May 2.

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 Rodger¹, Valentina Cambiano², Tina Bruun³, Pietro Vernazza⁴, Simon Collins⁵, Olaf Degen⁶, Giulio Maria Corbelli⁷, Vicente Estrada⁸, Anna Maria Geretti⁹, Apostolos Beloukas¹⁰, Dorthe Raben³, Pep Coll¹¹, Andrea Antinori¹², Nneka Nwokolo¹³, Armin Rieger¹⁴, Jan M Prins¹⁵, Anders Blaxhult¹⁶, Rainer Weber¹⁷, Arne Van Eeden¹⁸, Norbert H Brockmeyer¹⁹, Amanda Clarke²⁰, Jorge Del Romero Guerrero²¹, Francois Raffi²², Johannes R Bogner²³, Gilles Wandeler²⁴, Jan Gerstoft²⁵, Felix Gutiérrez²⁶, Kees Brinkman²⁷, Maria Kitchen²⁸, Lars Ostergaard²⁹, Agathe Leon³⁰, Matti Ristola³¹, Heiko Jessen³², Hans-Jürgen Stellbrink³³, Andrew N Phillips², Jens Lundgren³; PARTNER Study Group

Collaborators, Affiliations

Collaborators

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

Affiliations

¹ Institute for Global Health, University College London, London, UK. Electronic address: alison.rodger@ucl.ac.uk.
² Institute for Global Health, University College London, London, UK.
³ Department of Infectious Diseases (CHIP), Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
⁴ Division of Infectious Diseases and Hospital Epidemiology, Cantonal Hospital, St Gallen, Switzerland.
⁵ HIV i-Base, London, UK.
⁶ University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
⁷ European AIDS Treatment Group, Brussels, Belgium.
⁸ Hospital Clinico San Carlos and Universidad Complutense, Madrid, Spain.
⁹ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
¹⁰ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK; Department of Biomedical Sciences, University of West Attica, Athens, Greece.
¹¹ AIDS Research Institute-IrsiCaixa, Hospital Universitari Germans Trias i Pujol and BCN Checkpoint, Badalona and Barcelona, Spain.
¹² Istituto Nazionale per le Malattie Infettive Lazzaro Spallanzani IRCCS, Rome, Italy.
¹³ Chelsea and Westminster NHS Foundation Trust, London, UK.
¹⁴ Medical University of Vienna, Vienna, Austria.
¹⁵ Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
¹⁶ Venhälsan, Södersjukhuset, Stockholm, Sweden.
¹⁷ Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
¹⁸ DC Klinieken, Amsterdam, Netherlands.
¹⁹ Centre for Sexual Health and Medicine, Walk in Ruhr, Ruhr University Bochum, Bochum, Germany.
²⁰ Brighton and Sussex University Hospitals NHS Trust, and Brighton and Sussex Medical School, Brighton, UK.
²¹ Centro Sanitario Sandoval, Madrid, Spain.
²² Infectious Diseases Department, University Hospital (Centre Hospitalier Universitaire de Nantes) Hotel-Dieu, and INSERM UIC 1413 Nantes University, Nantes, France.
²³ Medizinische Klinik und Poliklinik IV, University Hospital Munich, Munich, Germany.
²⁴ Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.
²⁵ Rigshospitalet, Copenhagen, Denmark.
²⁶ Hospital General de Elche and Universidad Miguel Hernández, Alicante, Spain.
²⁷ Onze Lieve Vrouwe Gasthuis (OLVG), Amsterdam, Netherlands.
²⁸ Medical University Innsbruck, Innsbruck, Austria.
²⁹ Aarhus University Hospital, Skejby, Denmark.
³⁰ Hospital Clinic - IDIBAPS, University of Barcelona, Barcelona, Spain.
³¹ Helsinki University Hospital and University of Helsinki, Helsinki, Finland.
³² Praxis Jessen(2) + Kollegen, Berlin, Germany.
³³ ICH Study Centre, Hamburg, Germany.

PMID: 31056293
PMCID: PMC6584382
DOI: 10.1016/S0140-6736(19)30418-0

Observational Study

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 et al. Lancet. 2019.

. 2019 Jun 15;393(10189):2428-2438.

doi: 10.1016/S0140-6736(19)30418-0. Epub 2019 May 2.

Authors

Collaborators

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

Affiliations

¹ Institute for Global Health, University College London, London, UK. Electronic address: alison.rodger@ucl.ac.uk.
² Institute for Global Health, University College London, London, UK.
³ Department of Infectious Diseases (CHIP), Rigshospitalet, University of Copenhagen, Copenhagen, Denmark.
⁴ Division of Infectious Diseases and Hospital Epidemiology, Cantonal Hospital, St Gallen, Switzerland.
⁵ HIV i-Base, London, UK.
⁶ University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
⁷ European AIDS Treatment Group, Brussels, Belgium.
⁸ Hospital Clinico San Carlos and Universidad Complutense, Madrid, Spain.
⁹ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
¹⁰ Institute of Infection and Global Health, University of Liverpool, Liverpool, UK; Department of Biomedical Sciences, University of West Attica, Athens, Greece.
¹¹ AIDS Research Institute-IrsiCaixa, Hospital Universitari Germans Trias i Pujol and BCN Checkpoint, Badalona and Barcelona, Spain.
¹² Istituto Nazionale per le Malattie Infettive Lazzaro Spallanzani IRCCS, Rome, Italy.
¹³ Chelsea and Westminster NHS Foundation Trust, London, UK.
¹⁴ Medical University of Vienna, Vienna, Austria.
¹⁵ Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands.
¹⁶ Venhälsan, Södersjukhuset, Stockholm, Sweden.
¹⁷ Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
¹⁸ DC Klinieken, Amsterdam, Netherlands.
¹⁹ Centre for Sexual Health and Medicine, Walk in Ruhr, Ruhr University Bochum, Bochum, Germany.
²⁰ Brighton and Sussex University Hospitals NHS Trust, and Brighton and Sussex Medical School, Brighton, UK.
²¹ Centro Sanitario Sandoval, Madrid, Spain.
²² Infectious Diseases Department, University Hospital (Centre Hospitalier Universitaire de Nantes) Hotel-Dieu, and INSERM UIC 1413 Nantes University, Nantes, France.
²³ Medizinische Klinik und Poliklinik IV, University Hospital Munich, Munich, Germany.
²⁴ Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland.
²⁵ Rigshospitalet, Copenhagen, Denmark.
²⁶ Hospital General de Elche and Universidad Miguel Hernández, Alicante, Spain.
²⁷ Onze Lieve Vrouwe Gasthuis (OLVG), Amsterdam, Netherlands.
²⁸ Medical University Innsbruck, Innsbruck, Austria.
²⁹ Aarhus University Hospital, Skejby, Denmark.
³⁰ Hospital Clinic - IDIBAPS, University of Barcelona, Barcelona, Spain.
³¹ Helsinki University Hospital and University of Helsinki, Helsinki, Finland.
³² Praxis Jessen(2) + Kollegen, Berlin, Germany.
³³ ICH Study Centre, Hamburg, Germany.

PMID: 31056293
PMCID: PMC6584382
DOI: 10.1016/S0140-6736(19)30418-0

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.

PubMed Disclaimer

Figures

**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**
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 <0·000 to 0·007) and always closely linked on monophyletic clusters with posterior probabilities more than 0·98 (red and orange clusters in the phylogenetic tree). Control sequences comprised the ten closest sequences identified through BLAST searches of GenBank. (B) 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 0·14 (IQR 0·125–0·169). Positive control sequences comprised replicate sequences from study partners (in red). The positive control sequences show pairwise genetic distance 0·001 (IQR <0·001 to 0·014) and always linked on monophyletic clusters with posterior probabilities equal to 1·00 (red clusters in the phylogenetic tree). Control sequences comprised the ten closest sequences identified through BLAST searches of GenBank.

**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

See this image and copyright information in PMC

Comment in

Providers should discuss U=U with all patients living with HIV.
Calabrese SK, Mayer KH. Calabrese SK, et al. Lancet HIV. 2019 Apr;6(4):e211-e213. doi: 10.1016/S2352-3018(19)30030-X. Epub 2019 Feb 13. Lancet HIV. 2019. PMID: 30772420 No abstract available.
Successful treatment of HIV eliminates sexual transmission.
Cohen MS. Cohen MS. Lancet. 2019 Jun 15;393(10189):2366-2367. doi: 10.1016/S0140-6736(19)30701-9. Epub 2019 May 2. Lancet. 2019. PMID: 31056290 No abstract available.
The perfect PARTNER: no HIV transmission with ART.
Stone L. Stone L. Nat Rev Urol. 2019 Jul;16(7):387. doi: 10.1038/s41585-019-0205-3. Nat Rev Urol. 2019. PMID: 31165784 No abstract available.
Preventing HIV transmission.
Stower H. Stower H. Nat Med. 2019 Jun;25(6):877. doi: 10.1038/s41591-019-0490-7. Nat Med. 2019. PMID: 31171873 No abstract available.
Antiretroviral treatment can reduce the risk of HIV transmission between male partners to 'zero'.
Cook R, Davidson P; clinical adviser,; Martin R; NIHR Dissemination Centre. Cook R, et al. BMJ. 2019 Aug 27;366:l4915. doi: 10.1136/bmj.l4915. BMJ. 2019. PMID: 31455630

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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

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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

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