Secondary Logo

Journal Logo

EPIDEMIOLOGY AND SOCIAL

Undetectable viral load is associated with sexual risk taking in HIV serodiscordant gay couples in Sydney

Ven, Paul Van dea; Mao, Limina; Fogarty, Andreaa; Rawstorne, Patricka; Crawford, Junea; Prestage, Garrettb; Grulich, Andrewb; Kaldor, Johnb; Kippax, Susana

Author Information

Abstract

Introduction

Since the introduction in Western industrialized countries of highly active antiretroviral therapy (HAART), unprotected anal intercourse (UAI) with regular and casual partners has increased among gay men in Sydney [1,2] and elsewhere [3–7], resulting in increasing numbers of new HIV infections and sexually transmitted diseases in such populations [8]. Increases in UAI have been associated with – but not necessarily caused by [7,9] – treatment-related optimism, particularly the success of HAART in reducing viral load [2,10–13]. Evidence supports reduced HIV infectiousness among persons with lower viral load, at both the dyadic [14,15] and population level [16–18]. However, the relationship between viral load and sexual risk taking is unclear.

An Australian qualitative study of gay men's sexual practice and understandings of HIV clinical markers suggested that, in HIV serodiscordant steady relationships in particular, undetectable viral load may provide a sense of confidence about lowered transmission risk, allowing some couples to engage in UAI [19]. A study of HIV-positive men who have sex with men in the United States also linked undetectable viral load with the reduced perception of risk [20].

Viral load status has not been found to be a significant predictor of risk within serodiscordant regular (steady) relationships among HIV-positive men participating in 2002–2003 community-based surveys of gay men in Sydney [21], and findings from the United States were that viral load status was not a significant predictor of risk after controlling for reduced HIV concern [22]. Consistent with these cross-sectional results, a number of longitudinal studies have also found no relationship between viral load and sexual risk behaviour [23–25]. On the other hand, longitudinal studies of gay men in the Netherlands showed not only that more unprotected sex occurred in casual encounters after viral load became undetectable [26], but also that undetectable viral load was a significant predictor of risky sex in steady relationships [27].

Against this background, we examined the relationship between reported viral load and sexual risk taking within HIV serodiscordant gay couples in Sydney, drawing on data from two current cohorts.

Methods

Study population

Health in Men (HIM) is an ongoing prospective cohort of HIV-negative gay men in Sydney. Participants undertake an annual face-to-face structured interview and a blood test for HIV antibodies. From July 2001 to December 2003, 1333 men completed a baseline interview. They were recruited through gay community events (55.3%), word-of-mouth (13.5%), other research studies (7.2%), gay venues (7.2%), gay and AIDS organizations (5.1%), the Internet (4.4%), clinics (3.9%) and gay press (3.4%). Details of recruitment and data collection have been published elsewhere [28].

Complementing the HIM cohort, Positive Health (PH) is an ongoing prospective cohort of HIV-positive gay men, with most participants (77.7%) residing in Sydney. Participants also undertake an annual face-to-face structured interview. From February 2002 to August 2003, 282 men (77.3% of eligible participants) also completed optional questions on sexual practice. The PH men were recruited through gay community events (33.5%), other research studies (26.2%), gay and AIDS organizations (15.7%), clinics (14.9%), word-of-mouth (5.2%) and gay press (4.5%). Details of recruitment and data collection have been published elsewhere [29].

Measures

In both HIM and PH, participants reported numbers of regular and casual partners in the previous 6 months, length of current regular relationship, and HIV serostatus of current regular partner. Questions about sexual practice with regular and casual partners included: condom-protected anal intercourse and UAI; whether insertive or receptive; and whether with ejaculation inside or withdrawal prior to ejaculation. ‘Recreational’ drug use in the previous 6 months was scored from 0 to 4 for any use of the following four categories: speed/crystal/methamphetamine, cocaine, ecstasy and LSD.

PH participants reported the result of their last viral load test in copies/ml or log copies/ml (if known), and as one of the categories: undetectable (<500), low (<10 000), moderate (10 000–50 000) or high (>50 000). Where applicable, HIM participants reported the result of their HIV-positive partner's last viral load test in copies/ml (if known) or as undetectable, and as one of the categories, undetectable (<500), low (<10 000), moderate (10 000–50 000) or high (>50 000). For both PH and HIM participants, viral load <500 copies/ml was categorized as ’undetectable’. Consistent with the Dutch cohort, the measure of viral load was that reported by research participants, not actual viral load [27].

The HIV Treatments Optimism–Scepticism Scale [30] assesses both reduced concern about HIV and confidence associated with the success of treatments in reducing HIV infectiousness. Eleven items of the scale were included in both HIM and PH. For the short-form (11-item) HIV Optimism Scale used in this analysis, the Cronbach's α was 0.83 for HIM and 0.77 for PH.

Statistical analysis

Age differences between HIM (HIV-negative) and PH (HIV-positive) respondents were assessed using ANOVA. Bivariate associations between viral load and sexual practice within the relationship were assessed using χ2. Univariate analyses were undertaken to examine other covariates of UAI, and possible confounders of viral load. (Use of HAART was not included as a confounder because it was unavailable in HIM.) Independent predictors of UAI within HIV serodiscordant relationships were examined using multivariate logistic regression.

Results

Of the 1333 HIM participants (all confirmed HIV-negative through serological testing), 83 reported having an HIV-positive regular partner. Since sexual practice questions were asked regarding the period of 6 months prior to interview, only relationships of at least 6 months were included in subsequent analyses. As a result, 22 men were excluded. A further 16 men were excluded because they did not know the viral load of their HIV-positive regular partner. Of the 45 HIV-negative men included in the analyses, the mean age was 37.7 years (range, 22–53 years; SD, 7.67 years).

Of the 282 PH (HIV-positive) participants, 87 reported having an HIV-negative regular partner. Excluded were 10 men whose relationships were of less than 6 months duration and a further three men who reported not knowing their own viral load. Of the 74 HIV-positive men included in the analyses, the mean age was 42.7 years (range, 23–60 years; SD, 7.61 years), significantly older than their HIM counterparts (P < 0.001).

Overall, then, data were available from 119 HIV serodiscordant regular relationships. Table 1 shows sexual practice within these relationships according to the HIV-positive partner's reported viral load. In 21.0% (25 of 119) of these relationships anal intercourse was not practised, with little difference according to viral load. In a further 47.9% (57 of 119) of relationships, only condom-protected anal intercourse was reported. UAI was reported in the remaining 31.1% (37 of 119) of relationships.

Table 1
Table 1:
Sexual practice in HIV serodiscordant regular gay relationships by reported viral load (n = 119).

UAI was significantly more likely where viral load was undetectable (39.4 versus 20.8%; P = 0.04), that is, undetectable viral load is a significant predictor of UAI in serodiscordant relationships.

In univariate analyses, UAI was also significantly associated with younger age (P = 0.008), shorter relationship (P = 0.05), greater HIV Optimism (P = 0.03) and more ‘recreational’ drug use (P = 0.03). None of these variables was a confounder of reported viral load.

To verify that reported viral load remains a significant predictor of UAI after adjustment for other variables, a multivariate logistic regression (any UAI versus no UAI) was undertaken (Table 2). Variables controlled for were age, length of relationship, HIV Optimism, ‘recreational’ drug use, cohort membership (HIM HIV-negative versus PH HIV-positive respondents), and potential interactions between the independent variables.

Table 2
Table 2:
Predictors of unprotected anal intercourse in HIV serodiscordant regular gay relationships (n = 119).

The results of the multivariate analysis (Table 2) confirmed that reported undetectable viral load remained a significant predictor of UAI [odds ratio (OR), 2.88; P = 0.03]. Younger age (OR, 0.94; P = 0.05) and greater HIV Optimism (OR, 4.98; P = 0.02) were also significantly related to UAI. Length of relationship and ‘recreational’ drug use were not independently associated with UAI. Importantly, UAI was independent of study source (HIM versus PH) indicating consistency in reporting across the two cohorts.

Risk management

There were 26 men in HIV serodiscordant relationships in which the HIV-positive partner was reported to have undetectable viral load and in which UAI was practised (Table 1). Fifteen of these men were HIV-negative, 11 HIV-positive. Among the HIV-negative men, 11 (73.3% of the 15 men) reported never engaging in receptive UAI in which their HIV-positive partner ejaculated inside. Among the HIV-positive men, eight (72.7% of the 11 men) reported never engaging in insertive UAI in which they ejaculated inside their HIV-negative partner. The similarity of these proportions corroborates consistency of reporting by HIV-negative and HIV-positive men in HIV serodiscordant relationships.

In contrast, there were only 11 men in HIV serodiscordant relationships in which the HIV-positive partner was reported to have detectable viral load and in which UAI was practised (Table 1). Three of these men were HIV-negative and eight were HIV-positive (small numbers which require cautious interpretation). All three of the HIV-negative men reported never engaging in receptive UAI in which their HIV-positive partner ejaculated inside. Among the HIV-positive men, five (62.5% of the eight men) reported never engaging in insertive UAI in which they ejaculated inside their HIV-negative partner.

Discussion

Most HIV serodiscordant gay couples in Sydney (68.9% based on our research participants) do not engage in UAI within their relationship. Where they do, UAI in HIV serodiscordant gay relationships is associated with reporting that the HIV-positive partner has undetectable viral load rather than detectable viral load. The association between UAI and reported undetectable viral load found in the current analysis corroborates gay men's own discursive accounts of what informs their sexual practice: that for some gay men in HIV serodiscordant steady relationships, undetectable viral load provides a sense of confidence which allows for UAI [19]. It also supports data from the United States regarding low viral load being related to reduced HIV infectiousness [20].

Our finding also resonates with results from gay men in the Netherlands of undetectable viral load associated with a higher level of UAI with regular partners [27]. As more HIM and PH cohort data become available, it will be possible in the next year or so to undertake longitudinal analyses of changes in sexual practice in order to assess how couples respond to changes in viral load.

The cross-sectional data of the two cohorts presented here are not consistent with earlier results from community-based surveys of gay men in Sydney [21]. Whereas in both datasets most HIV-positive men in serodiscordant regular relationships did not engage in sexual practice which risked HIV transmission within the relationship, in the community-based surveys there was no significant association between UAI within the relationship and viral load. Possible explanations for this disparity are that the earlier data were based on short self-complete rather than lengthy face-to-face questionnaires and drawn from community-based convenience samples rather than two cohorts in which participants invest a considerable amount of time.

The finding that UAI is more likely among younger men needs to be read with caution. This is a small select group of men who are in a relationship with an HIV serodiscordant partner. The same may be said about the association of HIV Optimism with UAI, but here the relationship confirms previous research findings [2,10–13]. HIV Optimism is also conceptually related to beliefs about undetectable viral load. What is new about these results is that reporting that a partner's viral load is undetectable predicts UAI over and above such optimism. This contrasts with the finding from the United States where reduced HIV concern acted as a suppressor variable of viral load status [22].

We also found that despite reported viral load and optimism, strategic positioning [31] also appears to enter into the risk calculus. In HIV serodiscordant relationships where the HIV-positive partner is reported to have undetectable viral load and where UAI is practised, approximately three-quarters of the HIV-negative partners avoid receptive UAI with ejaculation inside and a similar proportion of HIV-positive partners avoid insertive UAI with ejaculation inside. There is some evidence that strategic positioning may also be adopted where the HIV-positive partner is reported to have detectable viral load although this requires cautious interpretation because of small numbers. In all probability, avoiding specific high-risk practices is a deliberate risk reduction strategy [21].

Our data show that approximately 40% of HIV serodiscordant gay couples in Sydney are engaging in some UAI when the HIV-positive partner's reported viral load is undetectable. This relatively high percentage is of concern even though the research evidence suggests that lower viral load corresponds with reduced infectiousness of HIV [14,15]. Of perhaps greater concern is that approximately 20% of HIV serodiscordant gay couples are engaging in some UAI when the HIV-positive partner's reported viral load is detectable. A long-term cohort study of HIV serodiscordant gay couples is a priority to determine the likelihood of HIV transmission within serodiscordant relationships in the time of HAART, and to further clarify use of HAART in relation to viral load and sexual practice.

The relationship between viral load and infectiousness of HIV – at both the individual and community level – is problematic for other reasons. The success of HAART in reducing viral load depends on high levels of adherence that are not easy to maintain over extended periods. This renders viral load quite variable and frequently more so by treatment breaks, be they structured treatment interruptions or otherwise [32,33]. Microbial resistance is inevitable as demonstrated by the ready detection of resistant isolates of HIV in both men and women [34,35], and in people with newly diagnosed infections [36]. Given that gay men in HIV serodiscordant relationships are incorporating clinical information in their sexual practice, it is important that they be made aware of how transmission risks, viral load variability and drug-resistant strains of HIV may relate to their specific situation.

Acknowledgements

Sponsorship: The Health in Men cohort study (for the Australian Thai HIV Vaccine Consortium) was supported by the Commonwealth Department of Health and Ageing (Canberra), the New South Wales Health Department (Sydney) and the National Institutes of Health, a component of the US Department of Health and Human Services (NIH/NIAID/DAIDS: HVDDT Award N01-AI-05395). The Positive Health cohort study was supported by the New South Wales Health Department (Sydney). The National Centre in HIV Social Research and the National Centre in HIV Epidemiology and Clinical Research are funded by the Commonwealth Department of Health and Ageing, Canberra.

References

1 Van de Ven P, Prestage G, French J, Knox S, Kippax S. Increase in unprotected anal intercourse with casual partners among Sydney gay men in 1996-98. Aust N Z J Public Health 1998; 22:814–818.
2 Van de Ven P, Prestage G, Crawford J, Grulich A, Kippax S. Sexual risk behaviour increases and is associated with HIV optimism among HIV-negative and HIV-positive gay men in Sydney over the four-year period to February 2000. AIDS 2000; 14:2952–2953.
3 Dodds JP, Nardone A, Mercey DE, Johnson AM. Increase in high risk sexual behaviour among homosexual men, London 1996–8: cross sectional, questionnaire study. BMJ 2000; 320:1510–1511.
4 Dodds JP, Mercey DE, Parry JV, Johnson AM. Increasing risk behaviour and high levels of undiagnosed HIV infection in a community sample of homosexual men. Sex Transm Infect 2004; 80:236–240.
5 Dukers NHTM, Goudsmit J, de Wit JBF, Prins M, Weverling GJ, Coutinho RA. Sexual risk behaviour relates to the virological and immunological improvements during highly active antiretroviral therapy in HIV-1 infection. AIDS 2001; 15:369–378.
6 Chen SY, Gibson S, Katz MH, Klausner JD, Dilley J, Schwarcz SK, et al. Continuing increases in sexual risk behaviour and sexually transmitted diseases among men who have sex with men, San Francisco 1999–2001. Am J Public Health 2002; 92:1387–1388.
7 Elford J, Bolding G, Sherr L. High-risk sexual behaviour increases among London gay men between 1998 and 2001: What is the role of HIV optimism? AIDS 2002; 16:1537–1544.
8 UNAIDS. 2004 Report on the Global AIDS Epidemic. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS); 2004.
9 Williamson LM, Hart GJ. HIV optimism does not explain increases in high-risk sexual behaviour among gay men in Scotland. AIDS 2004; 18:834–835.
10 Van de Ven P, Kippax S, Knox S, Prestage G, Crawford J. HIV treatments optimism and sexual behaviour among gay men in Sydney and Melbourne. AIDS 1999; 13:2289–2294.
11 Kelly J, Hoffman R, Rompa DJ, Gray M. Protease inhibitor combination therapies and perceptions of gay men regarding AIDS severity and the need to maintain safer sex. AIDS 1998; 12:F91–F95.
12 Vanable PA, Ostrow DG, McKirnan DJ, Taywaditep KJ, Hope BA. Impact of combination therapies on HIV risk perceptions and sexual risk among HIV-positive and HIV-negative gay and bisexual men. Health Psychol 2000; 19:134–135.
13 International Collaboration on HIV Optimism. HIV treatments optimism among gay men: an international perspective.J Acquired Immune Defic Syndr 2003; 32:545–550.
14 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 Study Group. N Engl J Med 2000; 342:921–929.
15 Chakraborty H, Sen PK, Helms RW, Vernazza PL, Fiscus SA, Eron JJ, et al. Viral burden in genital secretions determines male-to-female sexual transmission of HIV-1: a probabilistic empiric model. AIDS 2001; 15:621–627.
16 Law MG, Prestage G, Grulich A, Van de Ven P, Kippax S. Modelling the effect of combination antiretroviral treatments on HIV incidence. AIDS 2001; 15:1287–1294.
17 Blower SM, Gershengorn HB, Grant RM. A tale of two futures: HIV and antiretroviral therapy in San Francisco. Science 2000; 287:650–654.
18 Porco TC, Martin JN, Page-Shafer KA, Cheng A, Charlebois E, Grant RM, et al. Decline in HIV infectivity following the introduction of highly active antiretroviral therapy. AIDS 2004; 18:81–88.
19 Rosengarten M, Race K, Kippax S. ‘Touch wood, everything will be OK’: Gay Men's Understandings of Clinical Markers in Sexual Practice. Sydney: National Centre in HIV Social Research, The University of New South Wales; 2000.
20 Suarez TP, Kelly JA, Pinkerton SD, Stevenson YL, Hayat M, Smith MD, et al. Influence of a partner's HIV serostatus, use of highly active antiretroviral therapy, and viral load on perceptions of sexual risk behavior in a community sample of men who have sex with men. J Acquired Immune Defic Syndr 2001; 28:471–477.
21 Van de Ven P, Murphy D, Hull P, Prestage G, Batrouney C, Kippax S. Risk management and harm reduction among gay men in Sydney.Critical Public Health (in press).
22 Vanable PA, Ostrow DG, McKirnan DJ. Viral load and HIV treatment attitudes as correlates of sexual risk behavior among HIV-positive gay men. J Psychosom Res 2003; 54:263–269.
23 Miller M, Meyer L, Boufassa F, Persoz A, Sarr A, Robain M, et al. Sexual behavior changes and protease inhibitor therapy. SEROCO Study Group. AIDS 2000; 14:F33–F39.
24 van der Straten A, Gomez CA, Saul J, Quan J, Padian N. Sexual risk behaviors among heterosexual HIV serodiscordant couples in the era of post-exposure prevention and viral suppressive therapy. AIDS 2000; 14:F47–F54.
25 Desquilbet L, Deveau C, Goujard C, Hubert JB, Derouineau J, Meyer L. PRIMO Cohort Study Group. Increase in at-risk sexual behaviour among HIV-1-infected patients followed in the French PRIMO cohort. AIDS 2002; 16:2329–2333.
26 Dukers NHTM, Goudsmit J, de Wit JBF, Prins M, Weverling GJ, Coutinho RA. Sexual risk behaviour relates to the virological and immunological improvements during highly active antiretroviral therapy in HIV-1 infection. AIDS 2001; 15:369–378.
27 Stolte IG, de Wit JBF, van Eeden A, Coutinho RA, Dukers NHT. The perceived viral load level, and not the actual viral load, is a predictor for risky sex with steady partners among HIV-infected homosexual men. In: XV International AIDS Conference. Bangkok, July 2004 [WeOrC1334].
28 Mao L, Van de Ven P, Prestage G, Jin F, Grulich A, Crawford J, et al. Health in Men: Baseline Data. Sydney: National Centre in HIV Social Research, The University of New South Wales; 2002.
29 Prestage G, Race K, Grierson J, Grulich A, Kippax S. Positive Health: Method and Sample. Sydney: National Centre in HIV Social Research, The University of New South Wales; 2000.
30 Van de Ven P, Crawford J, Kippax S, Knox S, Prestage G. A scale of optimism-scepticism in the context of HIV treatments. AIDS Care 2000; 12:171–176 (2000).
31 Van de Ven P, Kippax S, Crawford J, Rawstorne P, Prestage G, Grulich A, et al. In a minority of gay men, sexual risk practice indicates strategic positioning for perceived risk reduction rather than unbridled sex. AIDS Care 2002; 14:471–480.
32 Miller V, Sabin C, Hertogs K, Bloor S, Martinez-Picado J, D’Aquila R, et al. Virological and immunological effects of treatment interruptions in HIV-1 infected patients with treatment failure. AIDS 2000; 14:2857–2867.
33 Fagard C, Oxenius A, Gunthard H, Garcia F, Le Braz M, Mestre G, et al. A prospective trial of structured treatment interruptions in human immunodeficiency virus infection. Arch Intern Med 2003; 163:1220–1226.
34 Eron JJ, Vernazza PL, Johnston DM, Seillier-Moiseiwitsch F, Alcorn TM, Fiscus SA, et al. Resistance of HIV-1 to antiretroviral agents in blood and seminal plasma: implications for transmission. AIDS 1998; 12:F181–F189.
35 Coombs RW, Reichelderfer PS, Landay AL. Recent observations of HIV type-1 infection in the genital tract of men and women. AIDS 2003; 17:455–480.
36 Little SJ, Holte S, Routy JP, Daar ES, Markowitz M, Collier AC, et al. Antiretroviral drug resistance among patients recently infected with HIV. N Engl J Med 2002; 347:385–394.
Keywords:

HIV; homosexual men; sexual behaviour; viral load

© 2005 Lippincott Williams & Wilkins, Inc.