Epidemiology and Social
Trends in unsafe sex and influence of viral load among patients followed since primary HIV infection, 2000–2009
Seng, Rémoniea; Rolland, Matthieua; Beck-Wirth, Genevièveb; Souala, Faouzic; Deveau, Christianea; Delfraissy, Jean-Françoisd; Goujard, Cécilea,d; Meyer, Laurencea
aCESP-INSERM U1018, University Paris Sud 11, Epidemiology Service, AP-HP, Bicêtre Hospital, Le Kremlin Bicêtre, France
bMulhouse Hospital, Mulhouse, France
cRennes Hospital, Rennes, France
dDepartment of Internal Medicine, Bicêtre Hospital, Le Kremlin Bicêtre, France.
Received 7 December, 2010
Revised 8 February, 2011
Accepted 18 February, 2011
Correspondence to Rémonie Seng, Service de Santé Publique, Hospital de Bicêtre, 82 rue du Général Leclerc, 94276 Le Kremlin-Bicêtre cedex, France. E-mail: email@example.com
Background: In the current context of increasing unsafe sex, HIV incidence may have evolved, depending on HIV prevalence in sexual networks and, among HIV-infected persons who practice unsafe sex, on their infectivity and partners' HIV serostatus. We examined calendar trends in sexual behaviours at risk of HIV-1 transmission (SBR) among 967 adults followed since primary HIV infection (ANRS PRIMO cohort) and relationship with current treatments and viral load.
Methods: Patients completed since 2000 self-administered questionnaires on sexual practices every 6 months. SBR with HIV-negative/unknown partners were analyzed among 155 heterosexual women, 142 heterosexual men and 670 MSM by using logistic generalized estimating equation models (6656 visits).
Results: During 2000–2009, the frequency of SBR did not increase significantly among women with steady partners; risk factors were a low education level and alcohol/smoking use. Among heterosexual men with steady partners, the frequency of SBR doubled since 2006; during this period, the only associated factor was combined antiretroviral treatment for at least 6 months or viral load less than 400 copies/ml. Among MSM, SBR increased gradually over time; SBR with steady partners was associated with a low education level and alcohol use. SBR was more frequent among MSM with casual partners; no association with viral load was found.
Conclusion: In France, recent trends and risk factors in unprotected sex with HIV-negative/unknown partners differ according to sex/sexual preference. The recent increase in SBR among heterosexual men with low viral load may be related to increasing awareness of the ‘treatment-as-prevention’ concept. The lack of association between SBR and viral load among MSM supports use of treatment-as-prevention as part of diversified prevention strategies.
An increase in unprotected sex and in sexually transmitted infections has been observed in several industrialized countries in the last decade, particularly among MSM [1–5]. The impact of increasing at-risk sexual behaviours among HIV-infected patients on the incidence of HIV infection is influenced by numerous factors, such as the HIV prevalence in sexual networks, antiretroviral treatment of HIV-infected patients , infectivity and sexual partners' HIV serostatus [7–13]. Unprotected sex among HIV-infected patients, and related factors, has mainly been examined in cross-sectional studies [14–30]. However, longitudinal data are crucial to assess the temporal relationship between factors (particularly, between knowledge of viral load and subsequent sexual behaviour) and also to describe behavioural trends over time. Calendar trends in sexual behaviour among HIV-infected patients may be driven both by individual factors (time since infection, viral load and age, for example) and by contextual factors (prevention messages, treatment guidelines, etc.). Evidence has been growing since 2000 that the risk of sexual HIV transmission is markedly reduced by low viral load [7,13,31,32], and it is important to determine whether and how this information has affected the sexual behaviour of HIV-infected homosexual and heterosexual men and women.
We, therefore, examined calendar trends in sexual behaviours at risk of HIV transmission, and their relationship with treatment status and viral load, in the ANRS PRIMO cohort of adults enrolled at diagnosis of primary HIV infection, and followed between 2000 and 2009.
The ANRS PRIMO cohort
The ongoing ANRS PRIMO cohort enrolled 1054 HIV-1-infected adults between June 1996 and December 2009 in 85 French hospitals. The study was approved by the Paris Cochin ethics committee. After giving their written informed consent, patients with primary HIV-1 infection are enrolled, regardless of symptom status. Primary infection is confirmed by an incomplete western blot (absence of antip68 and antip34), or detectable p24 antigenaemia, or detectable plasma viral load with a negative or weakly reactive enzyme-linked immunosorbent assay (ELISA) or an interval of less than 6 months between a negative and a positive ELISA test. Patients have to be antiretroviral-naive at enrolment. They have physical and biological examinations at inclusion, and then at months (M)1, M3 and M6, and every 6 months thereafter. At each scheduled visit from M3 onwards, the patients are asked to state the number of sexual partners (with anal or vaginal penetration) they have had since the last visit, along with the following information on each partner: sex, HIV-1 status (negative, positive or unknown), steady or casual status and condom use (never, seldom, often or always). This sex questionnaire was clinician-administered until 2000, when it started to be self-completed by the patients, with none of the information being passed to their physicians. This led to a sharp increase in the reporting of unprotected sex with casual partners (but, interestingly, not with steady partners), from 6.6% before 2000 to 20.3% in 2000. For this reason, we analysed only the self-completed questionnaires obtained since 2000.
We first studied the frequency of unprotected sex, that is, nonsystematic condom use, since the last scheduled visit, whatever the partners' HIV status. We then focused on sexual behaviours at risk of HIV-1 transmission (SBR). SBR was defined as nonsystematic condom use with a partner of negative or unknown HIV serostatus. The analysis was conducted separately for women, heterosexual men and MSM, and a distinction was made between steady and casual partners. As few casual partners were reported by heterosexual men and women, SBR with a casual partner was only studied among MSM. Sexual preference was recorded as stated by the patient at enrolment.
The yearly frequency of SBR with a steady partner was calculated as the ratio of the number of visits at which patients reported SBR with a steady partner during a given year to the number of visits during the same year at which patients reported having a steady partner. The yearly frequency of SBR with a casual partner among MSM was assessed in the same way. Trends over time in the yearly frequency of SBR were plotted for each group (women, heterosexual men and MSM), and temporal trends in SBR were first sought visually. Calendar trends were formally tested after dividing the study into three periods (2000–2002, 2003–2006 and 2007–2009), by using logistic regression fitted by generalized estimating equation (GEE) models that took into account the repeated visits by each patient. A logit link function was used, and an exchangeable correlation structure was assumed. We verified that a different categorization of the study period (2000–2002, 2003–2005 and 2006–2009) provided similar conclusions.
Factors associated with SBR with a steady (casual) partner were studied by comparing visits at which SBR with a steady (casual) partner was reported to other visits at which the patients stated they had a steady (casual) partner. Both fixed and time-dependent variables were included in the GEE models. Fixed variables included the level of education and smoking status (as reported at enrolment). Time-dependent variables included age, plasma viral load, the CD4+ T-cell count, treatment status [ongoing combined antiretroviral treatment (cART) for at least the past 6 months versus no treatment or cART for <6 months] and lipodystrophy (present or absent). For all these time-dependent covariates, the value at the scheduled visit prior to the sexual act was considered; when this visit was missing, variables were treated as missing. As viral load and treatment status were strongly related to each other, we conducted two separate multivariable analyses. Calendar changes in the association between viral load (or treatment status) and SBR were tested by introducing an interaction term between viral load (or treatment status) and the calendar period. The results were stratified for the calendar period when the P value for this interaction term was less than 0.20. As information on alcohol intake was only collected after 2002, analyses including alcohol (as a time-dependent variable) only included follow-up data collected since 2003. For simplicity, the adjusted odds ratios (ORs) for SBR associated with calendar time, educational level, smoking, age, the CD4+ cell count and lipodystrophy are those derived from multivariate models comprising viral load. We checked that similar associations were found in models comprising treatment instead of viral load, and in models comprising alcohol use since 2003.
Data were analysed with Statistical Analysis Software (SAS; SAS Institute Inc., Cary, North Carolina, USA). The cutoff date for this analysis was March 2010.
The 967 patients enrolled in the ANRS PRIMO cohort who completed at least one self-administered questionnaire after January 2000 included 155 women, 142 heterosexual men and 670 MSM (Table 1). Most of the patients (94%) were infected through sexual intercourse. Median age at diagnosis of primary HIV infection was 35 years and median follow-up since January 2000 was 43 months. The proportion of visits at which a sexual partner was reported was lowest among women and highest among MSM, mainly because women and heterosexual men reported casual partners far less frequently (7% and 14% of visits, respectively) than MSM (47%). Steady partners were similarly frequent in the three groups. The steady partner was more often HIV-infected in the female population (41.7% of visits with a steady partner) than in the two male populations (20.6% for heterosexual men and 34% for MSM).
Unprotected sex (i.e. nonsystematic condom use, whatever the partner's HIV status) was more frequent among women (33.7% of visits at which a partner was reported) than among heterosexual men (20.1%) and MSM (29.5%). Taking the partners' HIV status into account, SBR was similarly frequent in the three groups when a steady partner was involved (among women, 12.8% of visits at which a steady partner was reported, compared with 9.3% among heterosexual men, and 10.3% among MSM), but much more frequent among MSM when a casual partner was involved (21.2% of visits).
Few respondents reported that they never used a condom with a partner of negative or unknown HIV status (among women, 4.1% at visits with a steady partner, compared with 2.5% among heterosexual men and 2.1% among MSM, and 1.8% among MSM at visits with casual partners).
The proportion of visits at which the patients reported having been sexually active, that is, having had at least one sexual partner since the last visit, increased slightly from 80.5% in 2000 to 85% in 2009 (P < 0.001), whereas unprotected sex increased far more strongly, from 19.5% in 2000 to 36.3% in 2009 (P < 0.0001; Fig. 1a). During the same period, the frequency of treated patients followed a completely different pattern. The proportion of patients on cART fell from 76.8% of visits in 2000 to 41.4% in 2005, owing both to a high frequency of treatment interruptions and to less frequent treatment initiation during the primary infection, as we have previously observed . The proportion of patients on cART rose again to 66.3% in 2009, mainly because treatment interruptions were no longer recommended in French guidelines. As expected, the percentage of visits at which patients had undetectable viral load followed the same trend.
Trends in SBR over time differed according to sex and sexual preference (Fig. 1b). Among women, there was no significant change in the frequency of SBR with a steady partner: compared to 2000–2002, SBR was not more frequent in 2003–2006 [crude OR = 0.74 (95% confidence interval, CI 0.44–1.23) or 2007–2009, OR = 1.12 (0.56–2.24)]. Different categorization of the study period (2000–2002, 2003–2005 and 2006–2009) revealed no statistically significant trend, and nor did analysis of the calendar years as a continuous variable. Among heterosexual men, the frequency of SBR with a steady partner doubled in the most recent years from 8% in 2006 to 16.7% in 2008 [crude OR = 2.70 (1.32–5.52) for 2007–2009 compared with 2000–2002]. The frequency of SBR with a steady partner also increased among MSM, but the increase occurred earlier and was more gradual [OR = 1.92 (1.12–3.29) in 2003–2006 and 2.59 (1.55–4.30) in 2007–2009 compared with 2000–2002] than among heterosexual men. SBR was more frequent among MSM with casual partners (21.2% of visits overall) and also increased over time [OR = 1.64 (0.62–4.32) in 2003–2006 and 2.63 (1.03–6.69) in 2007–2009].
Equation (Uncited)Image Tools
Risk factors for sexual behaviour at risk of HIV transmission
Equation (Uncited)Image Tools
Among women reporting a steady partner, a low level of education was associated with a higher frequency of SBR (Table 2). Smoking and alcohol consumption were also linked to SBR. Age of at least 50 years tended to be associated with SBR, but the relation was of borderline significance. No relation between SBR and treatment or viral load was observed, and there was no calendar effect, as stated above.
Among heterosexual men reporting a steady partner (Table 3), SBR increased sharply after 2006. The association between SBR and viral load varied during the study period (interaction term, P = 0.06). In the most recent period (2007–2009), SBR was more likely to be reported by heterosexual men with low viral load (<400 copies/ml) or who had been taking cART for at least 6 months. No such association was found before 2006, when the only factor associated with SBR was a low level of education. The association between SBR with a steady partner and low viral load in the most recent period persisted when the time since diagnosis of HIV infection was taken into account (≤3 versus >3 years, or ≤5 versus >5 years).
Among MSM (Table 4), SBR with a steady partner increased gradually after 2000. This calendar effect remained statistically significant after adjustment for age and viral load. The frequency of SBR in the last period (2007–2009) did not differ according to the time since HIV infection. As observed among women, SBR with a steady partner was more often reported by MSM with a low level of education and also by MSM who reported using alcohol. SBR with a casual partner also increased over time and was more frequent among MSM who had more (≥5) casual partners in the previous 6 months or who had signs of lipodystrophy (as reported by their physician). SBR with steady or casual partners was not associated with low viral load or ongoing cART.
We examined calendar trends in SBR between 2000 and 2009 among 967 HIV-infected men and women followed since diagnosis of primary HIV-1 infection. Trends in SBR, and risk factors for SBR, differed markedly according to the individuals' sex and sexual preference. Among women, no calendar trend in SBR was observed and risk factors were related to social and behavioural factors (low level of education, alcohol use and smoking) and not to clinical factors (viral load or treatment status). Among heterosexual men with a steady partner, the frequency of SBR doubled since 2006, a period during which the only factor associated with SBR was ongoing cART for at least the past 6 months or, which is almost equivalent, current viral load below 400 copies/ml. Among MSM, SBR with both steady and casual partners increased gradually between 2000 and 2009 and no association was found between SBR and viral load or treatment.
We had hypothesized that unprotected sex with a partner of negative or unknown HIV status would be more frequent among patients with low viral load, that is, the least infectious patients. However, our data clearly show that this was the case only for heterosexual men with a regular partner, and only since 2006. No relationship between SBR and viral load was found among women or MSM. In other words, SBR was reported as frequently by individuals with detectable viral load as by those with undetectable viral load. This is of concern, as the participants were not on treatment at half the visits during the period 2000–2009. No relation between unsafe sex and viral load in MSM has been observed in the cART era in other high-income countries [26,27]. Our data underline a persistently high risk of HIV transmission among MSM, not only by individuals with undiagnosed primary infection who are highly contagious, but also by untreated individuals who are aware of their seropositivity as here. MSM reported having a casual partner at almost half their visits and reported SBR at 21% of these visits, a rate twice as high as during visits at which they reported having a steady partner; the frequency of SBR also rose with the number of casual partners. These results may partly explain why the incidence of HIV-1 infection among MSM in France has remained so high since 2003 . It is also conceivable that the incidence will even increase further in coming years. In Australia, an ecological correlation was found between trends in risky behaviour and new HIV diagnoses among MSM at the population level: changes in unprotected anal intercourse predicted changes in HIV diagnoses 2 years later . A survey conducted in eight industrialized countries showed a resurgence of HIV notifications and probably in new infection among MSM in the period 2000–2005 . Together, these findings highlight the need for new prevention messages and support early antiretroviral therapy. Treatment as prevention should be considered, at least for those patients most at risk of transmitting the virus [13,37–43].
Very few studies have simultaneously analysed factors associated with unsafe sex in different exposure groups, and studies of heterosexual men and women are particularly rare [15,22,27,44]. Here we found that trends in SBR and associated risk factors differed markedly according to sex and sexual preference, highlighting the need to diversify prevention strategies. Among women and MSM who had a regular partner with negative or unknown HIV status, SBR was mainly related to social or behavioural factors, such as a low level of education and drinking/smoking. Alcohol is consistently identified as a risk factor for SBR in the literature, whatever the level of consumption (any alcohol consumption/problem drinking/alcohol use in sexual contexts) [44,45]. Here information on occasional excessive consumption was not available. The association with educational level is less consistently reported [15,25,27,46,47]. A difficult household financial situation has been identified as a risk factor for SBR among both heterosexual men and women . We found a borderline significant association between SBR and age of at least 50 years among women, whereas less than 30, 30–39 and 40–49-year-old women had a lower risk. This might reflect difficulties for menopausal women in considering or negotiating condom use for noncontraceptive purposes; age was not a significant risk factor in men. Among heterosexual men with a steady partner, SBR was most frequent when viral load was below 400 copies/ml: this was only noted in the most recent years, possibly resulting from greater awareness of the ‘treatment-as-prevention’ concept among both clinicians and heterosexual patients, which began to spread before 2008. In the Swiss HIV cohort, a trend towards increase in unprotected sex has been also observed before January 2008 . It is also possible that unprotected sex sometimes corresponded to an attempt to conceive. The results for MSM were markedly different: the increase in SBR occurred earlier and risk factors for SBR with casual partners, namely, lipodystrophy and multiple casual partners, were different from those noted among both heterosexual men and MSM with steady partners. Other authors have found that lipodystrophy could be a risk factor for unsafe sex. Dukers et al.  reported that MSM in the Netherlands who experienced lipodystrophy reported a drastic decrease in sexual activity. Suffering from lipodystrophy was associated with sexual difficulties in the large VIH: Enquête sur les Personnes Atteintes (VESPA) study of HIV-infected participants living in France . This could be explained by either a decrease in negotiation skills in case of a perceived decrease in physical capital or by lipodystrophy being a marker for HAART-related sexual dysfunction. It is interesting to note that the calendar increase in SBR among MSM was not explained by individual factors such as treatment, current viral load, age, alcohol use, lipodystrophy, smoking or the time since diagnosis of HIV infection.
One strength of our study is its longitudinal design, which allowed us to observe calendar trends in a stable population. The association between viral load and subsequent sexual behaviour can be addressed more accurately in longitudinal studies than in cross-sectional studies . We tried to minimize underreporting of risky behaviour by restricting the analysis to data collected from 2000 onwards, when confidential self-reporting replaced clinician-administered questionnaires. Note that the reported frequency of unsafe sex with casual partners rose sharply after the self-administered questionnaires were introduced, in keeping with the results of a large meta-analysis .
This may explain why we do not observe an association between suppressive ART and unprotected sex in MSM and women, as was observed in a recent study . The ANRS PRIMO cohort consists of patients followed since diagnosis of primary HIV-1 infection, who have relatively preserved health status, either spontaneously or thanks to treatment, as reflected by CD4 cell counts below 350/μl at only 12% of visits. It is conceivable that the frequency of SBR and associated risk factors might differ among individuals with more advanced disease. We analysed the influence of current viral load, a marker of infectivity, and also took into account sexual partners’ HIV status, as known and reported by the patient. However, we did not seek information on disclosure of patients’ HIV-positive serostatus to the sexual partners and on possible risk-reduction strategies, such as perceived viral load, strategic positioning, the number of sexual acts or withdrawal before ejaculation [18,19,50]. Finally, we studied factors associated with unprotected sex with HIV-serodifferent partners, but not factors associated with changes in behaviour, such as a switch from unprotected to protected sex, or the reverse. This question would be better addressed by analysing individual trajectories.
In conclusion, risk factors for sexual behaviour at risk of HIV transmission differed between HIV-infected women, heterosexual men and homosexual men, followed since diagnosis of the primary infection. The recent increase in SBR among heterosexual men with low viral load may be related to increasing awareness of the ‘treatment-as-prevention’ concept among clinicians and patients. In contrast, patients' awareness of their viral load does not seem to have affected the sexual behaviour of women or of MSM. These findings support the use of treatment-as-prevention as part of a diversified prevention strategy [51–54].
The PRIMO cohort study is funded by ANRS (Agence Nationale de Recherches sur le SIDA et les Hépatites Virales), Paris, France.
The authors are grateful to all the participating patients. They also thank Y. Zittoun, A. Talamani, F. Tibaoui and M.O. Wehr for data monitoring; A. Persoz and L. Tran for data management; N. Bajos, R.M. Dray-Spira and J. Warszawski for fruitful discussions; D Young for editing the manuscript and the ANRS PRIMO cohort study group.
R.S., M.R., C.D., C.G. and L.M. contributed to the study design, data interpretation and manuscript preparation. R.S., M.R. and L.M. wrote the paper. R.S. and M.R. conducted the statistical analysis. G. B-W., F. S. and J-F. D. critically revised the manuscript.
The authors have no commercial or other association that might pose a conflict of interest in this study or for this publication.
The ANRS PRIMO cohort study group
Thierry ALLEGRE - Centre hospitalier général d'Aix en Provence – Service d'Hématologie; Jean-Michel LIVROZET, François JEANBLANC, Pierre CHIARELLO - Hôpital Edouard Herriot de Lyon - Immunologie clinique; Christian TREPO, Patrick MIAILHES, Kouadjo KOFFI, Valérie THOIRAIN, Corinne BROCHIER - Hôtel Dieu de Lyon - Service d'Hépato-Gastroentérologie; Antoine CHERET, Julie ALLEMAND, Gisèle PHILIPS, Edith DANIELLI - Hôpital Font-Pré de Toulon - Médecine interne - Hémato-infectiologie; Jean-Gabriel FUZIBET, Jill-Patrice CASSUTO, Michèle QUARANTA - Hôpital L'Archet - Nice - Service de Médecine Interne;Pierre DELLAMONICA, Anne LEPLATOIS - Hôpital de L'Archet - Nice -Maladies Infectieuses et Tropicales; Serge TEMPESTA - Centre Hospitalier d'Antibes - Service de Médecine Interne; Isabelle RAVAUX - Hôpital de la CONCEPTION de Marseille – Service des Maladies Infectieuses; Isabelle POIZOT MARTIN - Hôpital Sainte Marguerite de Marseille - Unité d'Hématologie; Hélène CHAMPAGNE - Centre Hospitalier de Valence - Maladies Infectieuses et Tropicales; Gilles PICHANCOURT - Centre Hospitalier Henri Duffaut d'Avignon - Service Hématologie Maladies Infectieuse
Philippe MORLAT, Fabrice BONNET, Isabelle LOUIS, Caroline ASLAN - Hôpital Saint André de Bordeaux - Médecine Interne; Jean-Marie RAGNAUD, Michel DUPONT - Hôpital Pellegrin de Bordeaux - Maladies Infectieuses; Jean-Luc PELLEGRIN, Isabelle RAYMOND – Hôpital Haut Lévèque de Bordeaux – Médecine Interne et Maladies Infectieuses; Jacques REYNES, Vincent BAILLAT, Corinne MERLE, Vincent LEMOING, Christine TRAMONI - Hôpital Gui de Chauliac de Montpellier - Service des Maladies Infectieuses et Tropicales; Hugues AUMAITRE, Mathieu SAADA, Marie MEDUS, Martine MALET - Hôpital Saint Jean de Perpignan - Service des Maladies Infectieuses; Martine OBADIA, Marie CHAUVEAU, Florence BALZARIN - Hôpital Purpan de Toulouse - SMIT-CISIH; Francis SAINT DIZIER, Daniel GARIPUY - Hôpital Joseph Ducuing de Toulouse - Médecine Interne
François RAFFI, Bénédicte BONNET, Clotilde ALLAVENA, Jean-Philippe TALARMIN, Olivier MOUNOURY, Véronique RELIQIET, Hervé HUE, Delphine BROSSEAU - Hôtel-Dieu de Nantes - CISIH Médecine Interne; Faouzi SOUALA, Maja RATAJCZAK - CHRU Pontchaillou de Rennes - Clinique des Maladies Infectieuses; Louis BERNARD, François BASTIDES, Pascale NAU - Hôpital Bretonneau de Tours - Service des maladies Infectieuses; Renault VERDON, Arnaud de la BLANCHARDIERE, Philippe FERRET - CH régional Côte de Nacre de Caen - Service de Maladies Infectieuses; Loïk GEFFRAY - Hôpital Robert Bisson de Lisieux - Service de Médecine Interne; Claude BEUSCART, Corinne DANIEL - Centre Hospitalier La Beauchée de Saint-Brieuc - Médecine Interne et Maladies infectieuses; Pascale FIALAIRE, Jocelyne LOISON - Centre hospitalier régional d'Angers - Service des Maladies Infectieuses; Odile VAILLANT, Matilde NIAULT - Centre Hospitalier Bretagne Sud de Lorient - Service d'Hématologie; Yves POINSIGNON - Centre Hospitalier Bretagne Atlantique de Vannes - Service de Medecine Interne et Maladies Infectieuses; Dominique HOULBERT - Centre Hospitalier d'Alençon - Médecine 2; Philippe PERRE, Isabelle SUAUD - Centre Hospitalier Départemental de La Roche sur Yon - Service de Médecine; Jean-Jacques GIRARD - Hôpital de Lôches - Service de Médecine Interne; Yasmine DEBAB - CHU Charles Nicolle de Rouen - Maladies infectieuses et Tropicales
Geneviève BECK-WIRTH, Catherine MICHEL, Meryem BENOMAR - Hôpital Emile Muller de Mulhouse - Hématologie Clinique; Bruno HOEN, Christine DROBACHEFF, Catherine BOURDEAUX - Hôpital St Jacques de Besançon - Service des Maladies Infectieuses et de Dermatologie; Lionel PIROTH, Marielle BUISSON, Sandrine TREUVELOT - Hôpital du Bocage de Dijon - Service des Maladies Infectieuses; Thierry MAY, Laurence BOYER, Simone WASSOUMBOU - CHU de Vandoeuvre-lès-Nancy - Hôpital de Brabois – Service des Maladies Infectieuses et Tropicales; Bruno AUDHUY, Masha MOHSENI ZADEH, Anne SCHIEBER - Hôpital Louis PASTEUR de Colmar – Service d'Immunologie Clinique; Benoît MARTHA - Centre Hospitalier William Morey de Chalon Sur Saône - Service de médecine interne
Christine JACOMET, Florence GOURDON - Hôpital Gabriel MONTPIED de Clermont Ferrand - Service des Maladies Infectieuses et Tropicales; Claire GENET - Hôpital DUPUYTREN de Limoges - Maladies Infectieuses et Tropicales; Bruno ABRAHAM, Claire PERINO - Centre Hospitalier de Brive - Departement de maladies infectieuses; Alain REGNIER - Centre Hospitalier de Vichy - Service de Médecine Interne; Odile ANTONIOTTI - Centre Hospitalier de Montluçon - Dermatologie
Hospitalier DRON de Tourcoing – Service de Maladies Infectieuses; Dominique MERRIEN - Centre Hospitalier de Compiègne - Service de Médecine Interne; Georges DIAB - C H de la Haute Vallée de l'Oise de Noyon - Service de Médecine
Jean-Michel MOLINA, Bénédicte LOZE - Hôpital Saint Louis de Paris - Service des Maladies Infectieuses et Tropicales; Caroline LASCOUX-COMBE, Claire PINTADO, Jeannine DELGADO - Hôpital Saint Louis de Paris - Service de Médecine Interne; Julie TIMSIT, Patrice MOREL - Hôpital Saint Louis de Paris - Clinique MST; Laurence GERARD - Hôpital Saint Louis de Paris - Service d'Immunologie Clinique; Pierre-Marie GIRARD, Odile PICARD, Gürgen TREDUP, Diane BOLLENS, Nadia VALIN, Pauline CAMPA, Nelly DESPLANQUE - Hôpital Saint Antoine de Paris - Service des Maladies Infectieuses et Tropicales; Patrick YENI, Bao PHUNG, François LOUNI - Gr. hospitalier Bichat-Claude Bernard de Paris - Service de Maladies Infectieuses et Tropicales; Catherine LEPORT, Corinne JADAND - Gr. hospitalier Bichat-Claude Bernard de Paris - Service des Maladies Infectieuses et Tropicales; Gilles PIALOUX, Thomas LYAVANC - Hopital Tenon de Paris - Service des Maladies Infectieuses; Esma BADSI, Agathe RAMI, Maguy PARRINELLO - Hôpital Lariboisière de Paris - Service de Médecine Interne A; Loïc GUILLEVIN, Dominique SALMON, Tassadit TAHI - G. H. Cochin de Paris – Département de Médecine Interne; Anne SIMON COUTELLIER - G. H. Pitié-Salpétrière de Paris - Service de Médecine Interne; Christine KATLAMA, Houcine AIT MOHAND, Saadia BEN ABDALLAH - G. H. Pitié-Salpétrière de Paris - Service des Maladies Infectieuses; Laurence WEISS, Martin BUISSON - Hôpital Européen Georges Pompidou de Paris - Service d'Immunologie Clinique; Jean-Paul VIARD, Aline MAIGNAN - Hôtel Dieu de Paris - Centre de Diagnostic et Thérapeutique; Paul Henri CONSIGNY, Claudine DUVIVIER - Centre Médical de l'Institut Pasteur de Paris - Service des Maladies Infectieuses; Loïc BODARD, Sylvie GIBERT - Institut Mutualiste Montsouris de Paris - Département de Médecine Interne
Jean-François DELFRAISSY, Cécile GOUJARD, Jade GHOSN, Yann QUERTAINMONT, Arnaud BECHARA, Marie-Thérèse RANNOU, Martine MOLE - Hôpital de Bicêtre - Médecine Interne; Yves LEVY, Alain SOBEL, Anne Sophie LASCAUX, Jean Daniel LELIEVRE, Cécile DUMONT - Hôpital Henri Mondor de Créteil - Immunologie clinique; François BOUE, Dominique BORNAREL - Hôpital Antoine Béclère de Clamart - Médecine Interne et Immunologie Clinique; Pierre DE TRUCHIS, Huguette BERTHE - Hôpital Raymond Poincaré de Garches - Service des Maladies Infectieuses et Tropicales; Pierre CHEVOJON, Alain DEVIDAS, Yvon LEMERCIER, Isabelle TURPAULT - Hôpital de Corbeil-Essonnes - Service d'Hématologie; Olivier BOUCHAUD, François ROUGES, Sophie ABGRALL, Asmaa BOUDRIBILA - Hôpital Avicenne de Bobigny – Maladies Infectieuses et Tropicales; Elisabeth ROUVEIX, Evelyne REIMANN - Hôpital Ambroise Paré de Boulogne - Médecine Interne; Alix GREDER BELAN, Audrey THERBY, Maria RUQUET - Hôpital du Chesnay CH Andre Mignot du Chesnay - Maladies Infectieuses et Tropicales; Martine BLOCH, Emmanuel MORTIER, Ai-feng ZENG - Hôpital Louis Mourier de Colombes – Médecine Interne; David ZUCMAN, Cécile LECOMTE - Hôpital Foch de Suresnes - Médecine Interne; Agnès ULUDAG, Justine GELLEN-DAUTREMER - Hôpital Beaujon de Clichy – Médecine Interne; Vincent DANELUZZI, Juliette GERBE - Centre Hospitalier de Nanterre - Service de Médecine Interne; Virginie PRENDKI – Hôpital Jean Verdier de Bondy - Service de Médecine Interne - Unité de Maladies Infectieuses; Olivier PATEY - Centre Hospitalier Inter-Communal de Villeneuve St Georges – Médecine Interne; Valérie GARRAIT, Laurent RICHIER - Centre Hospitalier Intercommunal de Créteil - Médecine Interne - Hépato-Gastroentérologie; Daniel VITTECOQ, Claudine BOLLIOT - Hôpital Paul Brousse de Villejuif - Service de Médecine Interne; Annie LEPRETRE - Hôpital Simone Veil d'Eaubonne - Médecine 2 - Consultation ESCALE; Philippe GENET, Juliette GERBE - Consultation d'Immuno/Hématologie d'Argenteuil; Véronique PERRONE - Centre Hospitalier François Quesnay de Mantes La Jolie - Service des Maladies Infectieuses; Jean-Luc BOUSSARD - Centre hospitalier Marc Jacquet de Melun - Service de Médecine; Eric FROGUEL - Hôpital de Lagny – Service de Médecine Interne
André CABIE, Sylvie ABEL, Sandrine PIERRE-FRANCOIS, Véronique BEAUJOLAIS - CHU Fort de France - Hôpital de Jour; Isabelle LAMAURY - CHU de Pointe à Pitre/ABYMES - Service de Dermatologie/Maladies Infectieuses.
Part of the data was presented at XVIII International AIDS Conference (2010, Vienna, Austria) [abstract TUPE0273].
1. van Kesteren NM, Hospers HJ, Kok G. Sexual risk behavior among HIV-positive men who have sex with men: a literature review. Patient Educ Couns 2007; 65:5–20.
2. Lattimore S, Delpech V, Elford J. Trends in sexual behaviour among London gay men between 1988 and 2008
. In: Proceedings of the International Society for Sexually Transmitted Diseases Research (ISSTDR) Conference
; June 2009; London.
4. Zablotska IB, Crawford J, Imrie J, Prestage G, Jin F, Grulich A, et al
. Increases in unprotected anal intercourse with serodiscordant casual partners among HIV-negative gay men in Sydney. AIDS Behav 2009; 13:638–644.
6. Montaner JS, Lima VD, Barrios R, Yip B, Wood E, Kerr T, et al
. Association of highly active antiretroviral therapy coverage, population viral load, and yearly new HIV diagnoses in British Columbia, Canada: a population-based study. Lancet 2010; 376:532–539.
7. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al
. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000; 342:921–929.
8. Wawer MJ, Gray RH, Sewankambo NK, Serwadda D, Li X, Laeyendecker O, et al
. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191:1403–1409.
9. Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F, et al
. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001; 357:1149–1153.
10. Wilson DP, Law MG, Grulich AE, Cooper DA, Kaldor JM. Relation between HIV viral load and infectiousness: a model-based analysis. Lancet 2008; 372:314–320.
11. Vernazza PL, Troiani L, Flepp MJ, Cone RW, Schock J, Roth F, et al
. Potent antiretroviral treatment of HIV-infection results in suppression of the seminal shedding of HIV. The Swiss HIV Cohort Study. AIDS 2000; 14:117–121.
12. Brenner BG, Roger M, Routy JP, Moisi D, Ntemgwa M, Matte C, et al
. High rates of forward transmission events after acute/early HIV-1 infection. J Infect Dis 2007; 195:951–959.
13. Attia S, Egger M, Muller M, Zwahlen M, Low N. Sexual transmission of HIV according to viral load and antiretroviral therapy: systematic review and meta-analysis. AIDS 2009; 23:1397–1404.
14. Marcellin F, Bonono CR, Blanche J, Carrieri MP, Spire B, Koulla-Shiro S, EVAL study group. Higher risk of unsafe sex and impaired quality of life among patients not receiving antiretroviral therapy in Cameroon: results from the EVAL survey (ANRS 12-116). AIDS 2010; 24(Suppl 1):S17–S25.
15. Morin SF, Myers JJ, Shade SB, Koester K, Maiorana A, Rose CD. Predicting HIV transmission risk among HIV-infected patients seen in clinical settings. AIDS Behav 2007; 11:S6–S16.
16. Drumright LN, Little SJ, Strathdee SA, Slymen DJ, Araneta MR, Malcarne VL, et al
. Unprotected anal intercourse and substance use among men who have sex with men with recent HIV infection. J Acquir Immune Defic Syndr 2006; 43:344–350.
17. Mayer KH, O'Cleirigh C, Skeer M, Covahey C, Leidolf E, Vanderwarker R, et al
. Which HIV-infected men who have sex with men in care are engaging in risky sex and acquiring sexually transmitted infections: findings from a Boston community health centre. Sex Transm Infect 2010; 86:66–70.
18. Begley K, Chan DJ, Jeganathan S, Batterham M, Smith DE. Factors associated with unprotected anal intercourse between HIV-positive men and regular male partners in a Sydney cohort. Int J STD AIDS 2009; 20:704–707.
19. Stolte IG, de Wit JB, van Eeden A, Coutinho RA, Dukers NH. Perceived viral load, but not actual HIV-1-RNA load, is associated with sexual risk behaviour among HIV-infected homosexual men. AIDS 2004; 18:1943–1949.
20. Schwarcz S, Scheer S, McFarland W, Katz M, Valleroy L, Chen S, et al
. Prevalence of HIV infection and predictors of high-transmission sexual risk behaviors among men who have sex with men. Am J Public Health 2007; 97:1067–1075.
21. Bouhnik AD, Preau M, Schiltz MA, Lert F, Obadia Y, Spire B, VESPA study group. Unprotected sex in regular partnerships among homosexual men living with HIV: a comparison between sero-nonconcordant and seroconcordant couples (ANRS-EN12-VESPA study). AIDS 2007; 21(Suppl 1):S43–S48.
22. Bouhnik AD, Preau M, Lert F, Peretti-Watel P, Schiltz MA, Obadia Y, et al
. Unsafe sex in regular partnerships among heterosexual persons living with HIV: evidence from a large representative sample of individuals attending outpatients services in France (ANRS-EN12-VESPA Study). AIDS 2007; 21(Suppl 1):S57–S62.
23. Bouhnik AD, Preau M, Schiltz MA, Peretti-Watel P, Obadia Y, Lert F, et al
. Unsafe sex with casual partners and quality of life among HIV-infected gay men: evidence from a large representative sample of outpatients attending French hospitals (ANRS-EN12-VESPA). J Acquir Immune Defic Syndr 2006; 42:597–603.
24. Peretti-Watel P, Spire B, Schiltz MA, Bouhnik AD, Heard I, Lert F, et al
. Vulnerability, unsafe sex and nonadherence to HAART: evidence from a large sample of French HIV/AIDS outpatients. Soc Sci Med 2006; 62:2420–2433.
25. Wolf K, Young J, Rickenbach M, Vernazza P, Flepp M, Furrer H, et al
. Prevalence of unsafe sexual behavior among HIV-infected individuals: the Swiss HIV Cohort Study. J Acquir Immune Defic Syndr 2003; 33:494–499.
26. Crepaz N, Marks G, Liau A, Mullins MM, Aupont LW, Marshall KJ, et al
. Prevalence of unprotected anal intercourse among HIV-diagnosed MSM in the United States: a meta-analysis. AIDS 2009; 23:1617–1629.
27. Elford J, Ibrahim F, Bukutu C, Anderson J. Sexual behaviour of people living with HIV in London: implications for HIV transmission. AIDS 2007; 21(Suppl 1):S63–S70.
28. Dia A, Marcellin F, Bonono RC, Boyer S, Bouhnik AD, Protopopescu C, et al
. Prevalence of unsafe sex with one's steady partner either HIV-negative or of unknown HIV status and associated determinants in Cameroon (EVAL ANRS12-116 survey). Sex Transm Infect 2010; 86:148–154.
29. Protopopescu C, Marcellin F, Preau M, Gabillard D, Moh R, Minga A, et al
. Psychosocial correlates of inconsistent condom use among HIV-infected patients enrolled in a structured ART interruptions trial in Cote d'Ivoire: results from the TRIVACAN trial (ANRS 1269). Trop Med Int Health 2010; 15:706–712.
30. Henry E, Marcellin F, Yomb Y, Fugon L, Nemande S, Gueboguo C, et al
. Factors associated with unprotected anal intercourse among men who have sex with men in Douala, Cameroon. Sex Transm Infect 2010; 86:136–140.
31. Lingappa JR, Hughes JP, Wang RS, Baeten JM, Celum C, Gray GE, et al
. Estimating the impact of plasma HIV-1 RNA reductions on heterosexual HIV-1 transmission risk. PLoS One 2010; 5:e12598.
32. Vernazza P, Hirschel B, Bernasconi E, Flepp M. HIV-positive individuals who have no other sexually transmitted infection and are on effective antiretroviral therapy will not transmit the virus by sexual contact. Bull Med Suisses 2008; 89:156–169.
33. Schiffer V, Deveau C, Meyer L, Iraqui I, Nguyen-Wartel A, Chaix ML, et al
. Recent changes in the management of primary HIV-1 infection: results from the French PRIMO cohort. HIV Med 2004; 5:326–333.
34. Le Vu S, Le Strat Y, Barin F, Pillonel J, Cazein F, Bousquet V, et al
. Population-based HIV-1 incidence in France, 2003-08: a modelling analysis. Lancet Infect Dis 2010; 10:682–687.
35. Zablotska IB, Prestage G, Middleton M, Wilson D, Grulich AE. Contemporary HIV diagnoses trends in Australia can be predicted by trends in unprotected anal intercourse among gay men. AIDS 2010; 24:1955–1958.
36. Sullivan PS, Hamouda O, Delpech V, Geduld JE, Prejean J, Semaille C, et al
. Reemergence of the HIV epidemic among men who have sex with men in North America, Western Europe, and Australia, 1996-2005. Ann Epidemiol 2009; 19:423–431.
37. Del Romero J, Castilla J, Hernando V, Rodriguez C, Garcia S. Combined antiretroviral treatment and heterosexual transmission of HIV-1: cross sectional and prospective cohort study. BMJ 2010; 340:c2205.
38. Bunnell R, Ekwaru JP, Solberg P, Wamai N, Bikaako-Kajura W, Were W, et al
. Changes in sexual behavior and risk of HIV transmission after antiretroviral therapy and prevention interventions in rural Uganda. AIDS 2006; 20:85–92.
39. Donnell D, Baeten JM, Kiarie J, Thomas KK, Stevens W, Cohen CR, et al
. Heterosexual HIV-1 transmission after initiation of antiretroviral therapy: a prospective cohort analysis. Lancet 2010; 375:2092–2098.
40. Fang CT, Hsu HM, Twu SJ, Chen MY, Chang YY, Hwang JS, et al
. Decreased HIV transmission after a policy of providing free access to highly active antiretroviral therapy in Taiwan. J Infect Dis 2004; 190:879–885.
41. Das M, Chu PL, Santos GM, Scheer S, Vittinghoff E, McFarland W, et al
. Decreases in community viral load are accompanied by reductions in new HIV infections in San Francisco. PLoS One 2010; 5:e11068.
42. Cohen MS, Gay CL. Treatment to prevent transmission of HIV-1. Clin Infect Dis 2010; 50(Suppl 3):S85–S95.
43. McDaid LM, Hart GJ. Sexual risk behaviour for transmission of HIV in men who have sex with men: recent findings and potential interventions
. Curr Opin HIV AIDS
44. Hasse B, Ledergerber B, Hirschel B, Vernazza P, Glass TR, Jeannin A, et al
. Frequency and determinants of unprotected sex among HIV-infected persons: the Swiss HIV cohort study. Clin Infect Dis 2010; 51:1314–1322.
45. Shuper PA, Joharchi N, Irving H, Rehm J. Alcohol as a correlate of unprotected sexual behavior among people living with HIV/AIDS: review and meta-analysis. AIDS Behav 2009; 13:1021–1036.
46. Reilly T, Woodruff SI, Smith L, Clapp JD, Cade J. Unsafe sex among HIV positive individuals: cross-sectional and prospective predictors. J Commun Health 2010; 35:115–123.
47. Peretti-Watel P, Spire B, Obadia Y, Moatti JP, VESPA study group. Discrimination against HIV-infected people and the spread of HIV: some evidence from France. PLoS One 2007; 2:e411.
48. Dukers NH, Stolte IG, Albrecht N, Coutinho RA, de Wit JB. The impact of experiencing lipodystrophy on the sexual behaviour and well being among HIV-infected homosexual men. AIDS 2001; 15:812–813.
49. Bouhnik AD, Preau M, Schiltz MA, Obadia Y, Spire B, VESPA study group. Sexual difficulties in people living with HIV in France: results from a large representative sample of outpatients attending French hospitals (ANRS-EN12-VESPA). AIDS Behav 2008; 12:670–676.
50. Sullivan PS, Salazar L, Buchbinder S, Sanchez TH. Estimating the proportion of HIV transmissions from main sex partners among men who have sex with men in five US cities. AIDS 2009; 23:1153–1162.
51. Hart GJ, Elford J. Sexual risk behaviour of men who have sex with men: emerging patterns and new challenges. Curr Opin Infect Dis 2010; 23:39–44.
52. Coates TJ, Richter L, Caceres C. Behavioural strategies to reduce HIV transmission: how to make them work better. Lancet 2008; 372:669–684.
53. van Griensven F, de Lind van Wijngaarden JW, Baral S, Grulich A. The global epidemic of HIV infection among men who have sex with men. Curr Opin HIV AIDS 2009; 4:300–307.
54. Beyrer C. Global prevention of HIV infection for neglected populations: men who have sex with men. Clin Infect Dis 2010; 50(Suppl 3):S108–S113.
calendar trends; heterosexual men; MSM; primary HIV infection; unsafe sex; viral load; women
© 2011 Lippincott Williams & Wilkins, Inc.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Highlight selected keywords in the article text.
Data is temporarily unavailable. Please try again soon.