After adjustment for socio-demographic and HIV-related factors, compared with MSM on ART with undetectable self-reported viral load, those on ART without undetectable self-reported viral load had significantly lower CLS-D prevalence [adjusted prevalence ratio (95% CI): 0.66 (0.45, 0.95)], whereas those not on ART had similar prevalence [1.08 (0.78, 1.49)] (Table 4a). Attenuation of this latter effect (‘not on ART’ vs. ‘ART with undetectable self-reported viral load’) was primarily because of adjustment for time with diagnosed HIV. The significant difference in CLS-D between the two ‘on ART’ groups persisted after additional adjustment for alcohol and recreational drug use (Table 4a).
Sexual behaviour and association with self-reported antiretroviral treatment/viral load among heterosexual men and women
Table 2 shows sexual behaviour among heterosexual men and women. Of 360 heterosexual men, 226 (62.8%), 83 (23.1%) and 23 (6.4%) reported vaginal/anal sex, CLS and CLS-D respectively in the past 3 months. Among the 629 women, corresponding numbers were: 316 (50.2%), 133 (21.1%) and 67 (10.7%). Inclusion of ‘possible’ CLS-D made little difference to prevalence. Patterns of sexual behaviour among heterosexual participants differed from MSM: the vast majority had sex with a single partner, CLS-D was usually with a long-term partner, recent STI was less common and prevalence of group sex and multiple partners was very low.
Among 351 heterosexual men with information on self-reported ART/viral load, there were no significant differences between those on ART vs. not on ART in prevalence of vaginal/anal sex (63.6% vs. 70.8%), CLS (23.9% vs. 16.7%) and CSL-D (6.4% vs. 4.2%) in the past 3 months. Similarly, among 611 women, ART was not associated with vaginal/anal sex (50.6% vs. 54.4% for on versus not on ART), CLS (21.4% vs. 23.5%) or CLS-D (11.2% vs. 8.8%) (P > 0.3 for all, χ2/Fisher's exact test). Table 3b shows associations for all heterosexual participants combined. Self-reported ART/viral load was not associated with CLS-D. CLS-D was associated with younger age, birth in the United Kingdom, non-black ethnicity, university education, not having a recent HIV diagnosis, higher CD4+ cell count and tended to be associated with greater financial security. CLS-D prevalence was much lower among the majority of individuals who identified with a religion than the minority who did not, and much higher among people with an HIV-negative/unknown status stable partner. CLS-D was associated with recreational drug use, but not with smoking or alcohol use. Patterns of association were broadly similar with all CLS. There remained no significant association of self-reported ART/viral load with CLS-D among heterosexual individuals in adjusted models (Table 4b).
Transmission risk beliefs
Table 2 shows that the vast majority of participants believed in the need for condoms, even with undetectable viral load, and approximately half did not agree that undetectable viral load reduced infectiousness. However, of all 416 participants who reported CLS-D, just over a third (37.7%) gave ‘belief that transmission risk is very low’ as one reason for not using a condom. This percentage was 41.9% among participants on ART with undetectable self-reported viral load, compared with 23.1% among those on ART without undetectable self-reported viral load, and 27.9% among those not on ART (P = 0.008, χ2).
Self-reported antiretroviral treatment/viral load and HIV-transmission risk sex
Among 2142 participants on ART who reported undetectable viral load, the vast majority (96.5%; n = 2066) had clinic-recorded viral load 50 copies/ml or less. Conversely, of all 2389 with clinic viral load 50 copies/ml or less, 86.5% had undetectable self-reported viral load. Prevalence of CLS-D-HIV-risk (CLS-D together with either ‘not on ART’ or clinic-recorded viral load >50 copies/ml) was 3.2% (101/3178) overall, 16.1% (61/379) among those not on ART (by definition equivalent to CLS-D), 0.6% (14/2154) among those on ART with undetectable self-reported viral load (the 14 cases because of CLS-D together with clinic viral load >50 copies/ml despite undetectable self-reported viral load), and 4.2% (25/592) among those on ART without undetectable self-reported viral load. Among MSM, these proportions were 3.9% (85/2189) overall, and 18.8% (54/287), 0.8% (12/1569) and 5.9% (18/307) respectively for the three self-reported ART/viral load categories. Among heterosexual individuals, corresponding proportions were 1.6% (16/989) overall; 7.6% (7/92), 0.3% (2/585) and 2.5% (7/285) for the self-reported ART/viral load categories. Therefore, prevalence of CLS-D-HIV-risk was much lower among people on ART, and extremely low (<1%) among those on ART with undetectable self-reported viral load.
Among MSM, when defining CLS-D to include possible CLS-D, adjusted prevalence ratios (95% CI) from model 2 were: 0.74 (0.53, 1.04) for ‘ART without undetectable self-reported viral load’ and 1.06 (0.78, 1.44) for ‘not on ART’, compared with ‘ART with undetectable self-reported viral load’ (global P = 0.11). Including only MSM who had sex in the past 3 months, corresponding adjusted prevalence ratios (95% CI) were 0.68 (0.48, 0.96) and 0.98 (0.72, 1.33) (P = 0.042). Among MSM diagnosed less than 5 years ago, adjusted prevalence ratios (95% CI) were 0.22 (0.08, 0.59) for ‘ART without undetectable self-reported viral load’, and 0.70 (0.46, 1.07) for ‘not on ART’, compared with ‘ART with undetectable self-reported viral load’. Among MSM diagnosed 5 years ago or more, corresponding adjusted prevalence ratios (95% CI) were 0.88 (0.59, 1.31) and 1.60 (1.10, 2.33); this interaction was significant (P = 0.001). Among heterosexual individuals, there was no significant association between self-reported ART/viral load and CLS-D for sensitivity analyses a–c (data not shown).
In this large multicentre study of people attending HIV clinics in the United Kingdom in 2011/12, use of ART was not associated with higher prevalence of CLS-D. Among MSM, those on ART had moderately lower prevalence of CLS-D than those not on ART, although this association was not independent of time since HIV diagnosis. Among MSM on ART, those who reported undetectable viral load had higher levels of CLS-D than those who did not, but CLS-D prevalence in both ‘on ART’ groups was lower than for MSM not on ART. Among heterosexual men and women, self-reported ART/viral load was not significantly associated with CLS-D. Patterns were similar for CLS overall. The prevalence of CLS-D-HIV-risk was low in the study population overall, and extremely low among those on ART with undetectable self-reported viral load.
With few exceptions [18,21,23], previous epidemiological studies [19,20,22–26,28–33] have found either no association of CLS-D with ART use and/or suppressed viral load, or that people on ART had somewhat lower levels of CLS-D. Similarly, a randomized comparison within the SMART trial (2002–2006) found that starting ART led to a reduction in CLS-D in the short term . The most recent observational study used data from 2009, a few years prior to ASTRA. Interview-assessed sexual behaviour was linked to recorded viral load among a large sample of United States’ HIV outpatients (Medical Monitoring Project) . Self-reported viral load was not assessed. Similar to ASTRA results comparing ‘on ART’ with ‘not on ART’, the United States’ study found that individuals with viral load suppression had lower levels of sex, CLS, and CLS-D than those without; the association was significant only for MSM.
For MSM on ART in ASTRA, the prevalence of CLS-D was higher among those who reported undetectable viral load than among those who did not. This modest difference remained after adjustment for other factors, and among the subgroup of MSM who had recent sex (sensitivity analysis b), therefore was not due to those on ART being less likely to be sexually active. The difference was particularly marked among those more recently diagnosed (sensitivity analysis c). Although there may be other differences between the two ‘on ART’ groups, one plausible explanation is that some MSM were choosing not to use a condom with HIV-serodifferent partners because of knowledge of very low infectiousness based on their perceived viral load. Consistent with this, of all participants who reported CLS-D, belief that transmission risk was low was more frequently a reason for not using condoms among those with undetectable self-reported viral load than those without. However, if knowledge of viral load was influencing sexual behaviour among MSM, the effect appeared modest, because levels of CLS-D among those on ART with undetectable self-reported viral load did not exceed those for men not on ART.
Prevalence estimates of CLS-D among MSM (15%) and heterosexual men (6%) and women (11%) with HIV in ASTRA are similar to those from two clinic-based studies in the United Kingdom in 2004–2005 using an identical definition (20 and 15% among 758  and 451  MSM, respectively; less than 10% among heterosexual men and women [22,29]), and from the European START trial participants at baseline: 15, 3 and 10% in the past 2 months for 1518 MSM, 207 heterosexual men and 138 women with HIV not taking ART (recently diagnosed participants were included) . The START analysis found no significant trend in baseline CLS-D prevalence over the recruitment period (2009–2013). Taken together these results suggest levels of CLS-D among people with HIV have remained fairly stable in the past decade, emphasising further that any change related to new messages about ‘safe sex’ has not been significant. Comparison with other studies is complicated by different recall periods and sampling frames: internet and venue-based studies tend to yield higher CLS-D estimates among HIV-positive MSM [42,43], which may be because of selection bias. Consistent with other studies [41,44–46], ASTRA suggests that perceived risk-reduction strategies (withdrawal before ejaculation and being the receptive partner) are commonly used among HIV-positive MSM having CLS-D.
Among MSM in ASTRA, CLS-D prevalence was lower with longer time since diagnosis, and higher among younger men, those without an HIV-positive stable partner, and those with higher alcohol and drug use, but CLS-D was not linked to socio-economic status. Similarly, among MSM in START, CLS-D was not associated with education level . We have previously described the strong link between polydrug use and CLS/CLS-D among MSM , in part reflecting use of ‘chemsex’ . Among heterosexual individuals in ASTRA, factors associated with CLS-D included white ethnicity, and higher socio-economic status in unadjusted analysis. In contrast, among heterosexual individuals in START, CLS-D tended to be associated with non-white ethnicity and lower education in unadjusted analysis . START had a diverse international population; socio-demographic effects on sexual behaviour may vary across cultural settings. Among heterosexuals in ASTRA, female sex, not having a recent HIV diagnosis, not identifying with a religion and recreational drug use were independent correlates of CLS-D, but the dominant association was with having an HIV-negative stable partner – this was the context of CLS-D for most heterosexual men and women who reported it. There may be specific issues relating to CLS-D in this context, such as desire for conception, or mutuality of decision making about condom use.
ASTRA is the largest questionnaire study of sexual behaviour among people living with HIV in the United Kingdom; although power to assess associations among heterosexual men and women separately was limited. Participants were reassured that questionnaire responses were confidential and would not be seen by clinic staff. Nevertheless, self-reported behaviour and attitudes may be subject to errors and social desirability bias.
What are the implications of these results for HIV- transmission? The prevalence of ‘HIV-transmission risk sex’ was much lower among those on ART vs. not on ART (1.4% vs 16.1%), and less than 1% among those on ART with undetectable self-reported viral load. Even if the ASTRA results do indicate the start of a trend of increasingly higher levels of CLS-D with perceived undetectable viral load (among MSM or the HIV-diagnosed population overall), prevalence of CLS-D-HIV-risk will likely continue to remain far lower among those on ART with undetectable self-reported viral load than among those not on ART. This is because of the effectiveness of ART and the apparent high accuracy of self-reported undetectable viral load status in this population. These results highlight the importance, as ART use expands, of promoting sustained high adherence, regular viral load testing, and on-going awareness of personal viral load level. It is also important to note that the definition of CLS-D-HIV-risk used here is based on the single clinic viral load measurement collected for all ASTRA participants, assumes elimination of risk with viral suppression on ART (as assumed with condom use), and does not incorporate factors such as self-reported ART non-adherence or presence of other STIs, the additional impact of which are uncertain [13,48].
In terms of transmission of other STIs, CLS overall is the most relevant measure. Similar to CLS-D, CLS prevalence among MSM was highest for those not on ART with no significant difference by ART use among heterosexual individuals. Therefore these data give little suggestion that expansion of ART use will have a negative impact on STI transmission. Nevertheless, the high prevalence of CLS compared with CLS-D-HIV risk, and the possibility that levels of CLS among those with undetectable self-reported viral load may continue to increase, emphasise the importance of ongoing promotion of condom use, STI prevention and testing among people with HIV.
The ASTRA study was planned in the period following the Swiss statement, which was then hugely controversial . During recruitment, results were released from HPTN 052 ; PARTNER results were first presented after completion of ASTRA . During this period United Kingdom  and other [50,51] treatment guidelines were changed to recommend discussing with HIV-positive people the beneficial effect of ART on infectiousness. The extent to which, and the rapidity with which, these findings and recommendations may influence the sexual behaviour of people with HIV , or change the long-standing culture of condom use , is unclear. With increasing use of early ART, it will be important to continue monitoring the association between ART and CLS, not only to understand the impact on HIV transmission, but also to assess implications for transmission of hepatitis C and other STIs.
In conclusion, among people with HIV in the United Kingdom, use of ART was not associated with increased prevalence of CLS or CLS-D, and was associated with greatly reduced prevalence of HIV-transmission risk sex. Although there was evidence that perceived undetectable viral load may influence condom use among MSM, any such effect was modest at the time of the study, and would not undermine the effect of early ART on HIV/STI transmission. These results support the prevention role of ART offered to all people with HIV, and emphasise the need to focus on HIV/STI prevention among those not on ART.
Funding: The ASTRA study presents independent research funded by the National Institute for Health Research (NIHR) under its Programme Grants for Applied Research funding scheme (RP-PG-0608–10142). The views expressed in this presentation are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. The ASTRA Study Group acknowledges the support of the NIHR, through the Comprehensive Clinical Research Network.
We thank all study participants for their time and effort, and gratefully acknowledge the contributions of all the ASTRA clinic teams in recruitment and data collection.
ASTRA clinic teams: Royal Free Hospital: Alison Rodger; Margaret Johnson; Jeffrey McDonnell; Aderonke Adebiyi, Mortimer Market Centre: Richard Gilson; Simon Edwards; Lewis Haddow; Simon Gilson; Christina Broussard; Robert Pralat; Sonali Wayal. Brighton and Sussex University Hospital: Martin Fisher; Nicky Perry; Alex Pollard; Serge Fedele; Louise Kerr; Lisa Heald; Wendy Hadley; Kerry Hobbs; Julia Williams; Elaney Youssef; Celia Richardson; Sean Groth. North Manchester General Hospital: Ed Wilkins; Yvonne Clowes; Jennifer Cullie; Cynthia Murphy; Christina Martin; Valerie George; Andrew Thompson. Homerton University Hospital: Jane Anderson; Sifiso Mguni; Damilola Awosika; Rosalind Scourse. East Sussex Sexual Health Clinic: Kazeem Aderogba; Caron Osborne; Sue Cross; Jacqueline Whinney; Martin Jones. Newham University Hospital: Rebecca O’Connell; Cheryl Tawana. Whipps Cross University Hospital: Monica Lascar; Zandile Maseko; Gemma Townsend; Vera Theodore; Jas Sagoo. ASTRA core team: Fiona Lampe; Alison Rodger; Andrew Speakman; Andrew Phillips. ASTRA data management: Andrew Speakman; Marina Daskalopoulou; Fiona Lampe. ASTRA advisory group: Lorraine Sherr; Simon Collins; Jonathan Elford; Alec Miners; Anne Johnson; Graham Hart; Anna-Maria Geretti; Bill Burman. CAPRA grant Advisory Board: Nick Partridge; Kay Orton; Anthony Nardone; Ann Sullivan.
Writing committee: Fiona C. Lampe1, Marina Daskalopoulou1, Andrew N. Phillips1, Andrew Speakman1, Margaret A. Johnson2, Richard Gilson1, Martin Fisher3†, Ed Wilkins4, Jane Anderson5, Rebecca O’Connell6, Monica Lascar6, Kazeem Aderogba7, Jeffrey McDonnell1, Jonathan Elford8, Simon Collins9, Simon Edwards10, Nicky Perry3, Lorraine Sherr1, Anna Maria Geretti11, Graham Hart1, Anne M. Johnson1, Alec Miners12, William J. Burman13, Alison J. Rodger1.
1. Research Department of Infection and Population Health, University College London, London, UK.
2. Royal Free London NHS Foundation Trust, London, UK.
3. Brighton and Sussex University Hospitals NHS Trust, Brighton, UK.
4. Pennine Acute Hospitals NHS Trust, Manchester, UK.
5. Centre for the study of Sexual Health and HIV, Homerton University Hospital NHS Foundation Trust London, UK.
6. Barts Health NHS Trust, London, UK.
7. East Sussex Healthcare NHS Trust, Eastbourne, UK.
8. School of Health Sciences, City University London, London, UK.
9. HIV i-Base, London, UK.
10. Mortimer Market Centre, Central and North West London NHS Foundation Trust, London, UK.
11. Institute of Infection and Global Health, University of Liverpool, Liverpool, UK.
12. London School of Hygiene and Tropical Medicine, London, UK.
13. Denver Public Health, Denver, Colorado, USA; †Professor Martin Fisher died in April 2015.
Contribution of authors: F.C.L., A.N.P., A.R., A.S., M.A.J., R.G., M.F., E.W., J.A., J.E., S.C., N.P., L.S., A.M.G., G.H., A.J., A.M. and W.J.B. conceived and designed the study. A.S., A.R., M.A.J., R.G., M.F., E.W., J.A., R.O., M.L., K.A., J.M., S.E. and N.P. collected the data. F.C.L., A.S. and M.D. managed the data. F.C.L. performed the analysis and drafted the manuscript. All authors contributed to data interpretation and writing and revision of the article. F.C.L. had full access to all the data in the study and takes responsibility for the integrity of the data and accuracy of the data analysis.
Conflicts of interest
The authors declare the following conflicts of interest: AP - consultancy with GSK Biologicals; advisory board for Abbvie, Gilead Sciences; speaker's fees (Gilead Sciences). EW- travel bursaries, honoraria for lectures and advisory boards from Gilead, Janssen, Merck-Sharpe-Dohme, Bristol-Myers-Squibb, AbbVie, Abbott, and ViiV over the last 24 months. JA - grants and personal fees from Gilead Sciences, personal fees from ViiV, MSD, Bristol Myers Squibb, Jansen, Abbvie, outside the submitted work. AMG - consultancy and speaker's fees from Abbvie, Bristol Meyers Squibb (BMS), Gilead, GlaxoSmithKline (GSK), Janssen, Pfizer, and ViiV; the University of Liverpool receives grant funding from BMS, Gilead, Janssen and ViiV for research studies of which AMG is the principal investigator, and fees from Abbott Molecular and Pfizer for consultancy work provided by AMG. FCL, MD, AS, MAJ, RG, RO, ML, KA, JM, JE, SC, SE, NP, LS, GH, AMJ, AM, WJB, AJR declared no conflicts of interest.
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Keywords:Copyright © 2016 Wolters Kluwer Health, Inc.
antiretroviral treatment; condomless sex; self-report; sexual behaviour; viral load