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Original Investigation |

Sexual Activity Without Condoms and Risk of HIV Transmission in Serodifferent Couples When the HIV-Positive Partner Is Using Suppressive Antiretroviral Therapy

Alison J. Rodger, MD1; Valentina Cambiano, PhD1; Tina Bruun, RN2; Pietro Vernazza, MD3; Simon Collins4; Jan van Lunzen, PhD5; Giulio Maria Corbelli6; Vicente Estrada, MD7; Anna Maria Geretti, MD8; Apostolos Beloukas, PhD8; David Asboe, FRCP9; Pompeyo Viciana, MD10; Félix Gutiérrez, MD11; Bonaventura Clotet, PhD12; Christian Pradier, MD13; Jan Gerstoft, MD14; Rainer Weber, MD15; Katarina Westling, MD16; Gilles Wandeler, MD17; Jan M. Prins, PhD18; Armin Rieger, MD19; Marcel Stoeckle, MD20; Tim Kümmerle, PhD21; Teresa Bini, MD22; Adriana Ammassari, MD23; Richard Gilson, MD1; Ivanka Krznaric, PhD24; Matti Ristola, PhD25; Robert Zangerle, MD26; Pia Handberg, RN27; Antonio Antela, PhD28; Sris Allan, FRCP29; Andrew N. Phillips, PhD1; Jens Lundgren, MD2 ; for the PARTNER Study Group
[+] Author Affiliations
1Research Department of Infection and Population Health, University College London, London, United Kingdom
2Department of Infectious Diseases/CHIP, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
3Division of Infectious Diseases and Hospital Epidemiology, Cantonal Hospital, St Gallen, Switzerland
4HIV i-Base, London, United Kingdom
5University Medical Center Hamburg-Eppendorf, Hamburg-Eppendorf, Germany
6European AIDS Treatment Group, Bruxelles, Belgium
7Hospital Clinico San Carlos and Universidad Complutense, Madrid, Spain
8Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom
9Chelsea and Westminster NHS Foundation Trust, London, United Kingdom
10Hospital Virgen del Rocío, Sevilla, Spain
11Hospital General de Elche & Universidad Miguel Hernández, Alicante, Spain
12IrsiCaixa Foundation, UAB, UVIC-UCC, Hospital Universitari “Germans Trias i Pujol,” Badalona, Catalonia, Spain
13Department of Public Health, Nice University Hospital and EA 6312, University Nice Sophia-Antipolis, France
14Rigshospitalet, Copenhagen, Denmark
15Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, University of Zurich, Zurich, Switzerland
16Unit of Infectious Diseases and Dermatology, Department of Medicine, Karolinska Institutet, and Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden
17Department of Infectious Diseases, Bern University Hospital, University of Bern, Bern, Switzerland
18Academic Medical Center, Amsterdam, the Netherlands
19Medical University of Vienna, Vienna, Austria
20Division of Infectious Diseases and Hospital Epidemiology, University Hospital Basel, Basel, Switzerland
21Department of Internal Medicine 1, University Hospital of Cologne, Cologne, Germany
22Ospedal San Paolo, Milan, Italy
23Ospedale L. Spallanzani, Roma, Italy
24Praxis Driesener Straße, Berlin, Germany
25Helsinki University Central Hospital, Helsinki, Finland
26Medical University Innsbruck, Innsbruck, Austria
27Hvidovre Universitets Hospital, Hvidovre, Denamrk
28Hospital Clínico Universitario de Santiago de Compostela, Santiago de Compostela, Spain
29Coventry and Warwickshire Hospital, Coventry, United Kingdom
JAMA. 2016;316(2):171-181. doi:10.1001/jama.2016.5148.
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Importance  A key factor in assessing the effectiveness and cost-effectiveness of antiretroviral therapy (ART) as a prevention strategy is the absolute risk of HIV transmission through condomless sex with suppressed HIV-1 RNA viral load for both anal and vaginal sex.

Objective  To evaluate the rate of within-couple HIV transmission (heterosexual and men who have sex with men [MSM]) during periods of sex without condoms and when the HIV-positive partner had HIV-1 RNA load less than 200 copies/mL.

Design, Setting, and Participants  The prospective, observational PARTNER (Partners of People on ART—A New Evaluation of the Risks) study was conducted at 75 clinical sites in 14 European countries and enrolled 1166 HIV serodifferent couples (HIV-positive partner taking suppressive ART) who reported condomless sex (September 2010 to May 2014). Eligibility criteria for inclusion of couple-years of follow-up were condomless sex and HIV-1 RNA load less than 200 copies/mL. Anonymized phylogenetic analysis compared couples’ HIV-1 polymerase and envelope sequences if an HIV-negative partner became infected to determine phylogenetically linked transmissions.

Exposures  Condomless sexual activity with an HIV-positive partner taking virally suppressive ART.

Main Outcomes and Measures  Risk of within-couple HIV transmission to the HIV-negative partner

Results  Among 1166 enrolled couples, 888 (mean age, 42 years [IQR, 35-48]; 548 heterosexual [61.7%] and 340 MSM [38.3%]) provided 1238 eligible couple-years of follow-up (median follow-up, 1.3 years [IQR, 0.8-2.0]). At baseline, couples reported condomless sex for a median of 2 years (IQR, 0.5-6.3). Condomless sex with other partners was reported by 108 HIV-negative MSM (33%) and 21 heterosexuals (4%). During follow-up, couples reported condomless sex a median of 37 times per year (IQR, 15-71), with MSM couples reporting approximately 22 000 condomless sex acts and heterosexuals approximately 36 000. Although 11 HIV-negative partners became HIV-positive (10 MSM; 1 heterosexual; 8 reported condomless sex with other partners), no phylogenetically linked transmissions occurred over eligible couple-years of follow-up, giving a rate of within-couple HIV transmission of zero, with an upper 95% confidence limit of 0.30/100 couple-years of follow-up. The upper 95% confidence limit for condomless anal sex was 0.71 per 100 couple-years of follow-up.

Conclusions and Relevance  Among serodifferent heterosexual and MSM couples in which the HIV-positive partner was using suppressive ART and who reported condomless sex, during median follow-up of 1.3 years per couple, there were no documented cases of within-couple HIV transmission (upper 95% confidence limit, 0.30/100 couple-years of follow-up). Additional longer-term follow-up is necessary to provide more precise estimates of risk.

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Figure 1.
Rate of HIV Transmission According to Sexual Behavior Reported by the HIV-Negative Partner

Denominators are the group-specific number of HIV-negative participants who contributed eligible couple-years of follow-up. The upper limit of the 95% confidence interval was estimated using the exact Poisson method.

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Figure 2.
Phylogenetic Tree of Pol Sequences From 9 Couples With Subtype B Infection

Bayesian Markov Chain Monte-Carlo (MCMC) inference (012212+I+G+F model). Branch length is proportional to the genetic distance and line weight is proportional to the posterior probability. Partners’ sequences are in blue; N indicates the initially HIV-negative partner, whereas P indicates the initially HIV-positive partner. Control sequences comprised the 10 closest sequences identified through BLAST searches of GenBank. Positive control sequences comprised replicate sequences from study partners (in red) and sequences from confirmed transmission pairs obtained in a separate study (in orange).19

aSequences 9N2 and 9N3 were obtained from the same sample in 2 separate experiments.

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