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AIDS:
doi: 10.1097/01.aids.0000255087.62223.ff
Editorial

Sexual behaviour of people living with HIV in London: implications for HIV transmission

Elford, Jonathana; Ibrahim, Fowziaa; Bukutu, Ceciliaa; Anderson, Janeb

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Author Information

From the aCity University London, London, UK

bHomerton University Hospital NHS Foundation Trust, London, UK.

Received 4 April, 2006

Revised 10 August, 2006

Accepted 6 November, 2006

Correspondence to Jonathan Elford, City University London, Institute of Health Sciences, St Bartholomew School of Nursing and Midwifery, 24 Chiswell Street, London EC1Y 4TY, UK. Tel: +44 020 7040 5702; fax: +44 020 7040 5717; e-mail: j.elford@city.ac.uk

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Abstract

Objective: To examine the sexual behaviour of gay men as well as black African heterosexual men and women living with diagnosed HIV in London, and to consider the implications for HIV transmission.

Methods: People living with HIV receiving treatment and care in outpatient clinics in north east London were asked to complete a confidential, self-administered questionnaire in 2004–2005. Respondents were asked about unprotected anal or vaginal intercourse in the previous 3 months, and the type (main or casual) and HIV status of their partner(s).

Results: A total of 1687 people with diagnosed HIV returned a completed questionnaire (response rate 73% of eligible clinic attenders) including 480 black African heterosexual women, 224 black African heterosexual men and 758 gay/bisexual men (464 white, 112 ethnic minority). One in five gay men with HIV (20.1%, 144/715) reported unprotected anal intercourse with a partner of unknown or discordant HIV status (usually a casual partner). This presents a risk of HIV transmission. By comparison, one in 20 (5.1%, 32/623) black African heterosexual men and women with HIV reported unprotected vaginal intercourse that presented a risk of HIV transmission; odds ratio (gay men versus black African men and women combined) 5.28, 95% confidence interval 3.52, 7.91, P < 0.001. Neither viral load nor being on HAART were significantly associated with unprotected intercourse among gay men or black African heterosexual men and women (P > 0.05).

Conclusion: Behavioural research among people with diagnosed HIV in London shows that gay men are more likely than black African heterosexual men and women to engage in sexual behaviour that presents a risk of HIV transmission.

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Introduction

In the United Kingdom, the number of heterosexual men and women diagnosed with HIV has risen substantially in recent years. Most of the increase in HIV diagnoses among heterosexuals in the UK has been among people who originate from sub-Saharan Africa. For example, in 2004 more than 3000 black African heterosexual men and women were diagnosed with HIV in the UK. In the same year, just over 2000 gay/bisexual men in the UK also received an HIV diagnosis [1]. The majority of gay men diagnosed with HIV were white, but one in 10 belonged to an ethnic minority [2].

Despite the increase in the number of new diagnoses among black African heterosexual men and women, gay men have remained the group at the greatest risk of acquiring HIV in the United Kingdom to date [1,3]. In 2004, gay men accounted for approximately 80% of all newly diagnosed infections acquired in the UK. This is because the majority of black African heterosexual men and women diagnosed with HIV in the UK acquired their infection abroad.

Because of the recent increase in new diagnoses among heterosexual men and women, an almost equal number of gay men (17 000) and black African heterosexual men and women (13 000) now live with diagnosed HIV in the UK [1]; they are currently the people most affected by HIV in the UK. This raises the question as to whether gay men will continue to account for the majority of new HIV infections acquired in the UK or whether black African heterosexual men and women with HIV will make an increasing contribution to ‘local’ transmission. To answer this question we need detailed information about patterns of sexual behaviour among gay men as well as black African heterosexual men and women living with HIV in the UK, focusing on sexual behaviour that presents a risk of HIV transmission.

In this paper we examine the sexual behaviour of gay men as well as black African heterosexual men and women diagnosed with HIV living in London, examine factors associated with their sexual behaviour, and consider the implications for HIV transmission in the UK.

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Methods

Recruitment

The study population comprised people diagnosed with HIV infection aged 18 years and above receiving treatment and care in six east London public hospitals. In the UK, the majority of people with diagnosed HIV infection seek clinical care in National Health Service (NHS) specialist HIV outpatient clinics [1]. Consequently, an NHS clinic sample is broadly representative of all those living with diagnosed HIV.

In 2004–2005, people diagnosed with HIV infection attending NHS clinics in the six east London hospitals were invited to participate in the study over a 4–6 month period. People with a limited command of English were ineligible as were those who were too ill or too distressed to complete a questionnaire. Clinic attenders were only enrolled after they had given fully informed consent in writing. No financial remuneration was offered to participants. Ethics committees for the participating hospitals approved the research protocol. The methods have been described in detail elsewhere [4].

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Questionnaire

Study participants were asked to complete (once only) a confidential, self-administered, pen-and-paper questionnaire in the clinic or at home. Respondents were asked to provide information on their age, sex, sexual orientation, ethnicity, education, employment, country of birth, whether they were in a relationship, and if so, the HIV status and ethnicity of their partner and whether their partner knew that the respondent was HIV-positive. They were also asked when they were diagnosed with HIV, whether they were on antiretroviral therapy and their most recent (self-reported) viral load and CD4 cell count. Questions were also included on beliefs and attitudes towards HIV [5], access to and use of the Internet and recreational drug use.

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Sexual behaviour

Respondents were asked whether they had had vaginal or anal intercourse without a condom in the previous 3 months, and if so, the type (main or casual), HIV status and ethnicity of their partner(s). Unprotected intercourse (anal or vaginal) was classified as concordant (only with another HIV-positive partner) or non-concordant (with a partner of unknown or negative HIV status). Non-concordant unprotected anal or vaginal intercourse presents a risk of HIV transmission. Concordant unprotected intercourse does not present a risk of HIV transmission to an uninfected person, but may present a risk of cross-infection and transmission of other sexually transmitted infections (STI). Respondents were asked if they had had an STI in the previous 12 months and whether they had had sex only with men, only with women, or with both men and women.

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Statistical analysis

Data were analysed using STATA version 8.2 (STATA Corp., College Station, Texas, USA). Analyses were conducted separately for gay/bisexual men (referred to here as ‘gay men’), black African heterosexual men and black African heterosexual women. Chi-squared, Fisher's exact and t-tests were used for examining differences in proportions and means between these groups (Table 1 and Table 2). In Table 2, the analysis was restricted to respondents who provided information on unprotected intercourse with main or casual partners. We use the term ‘unprotected intercourse’ to refer to unprotected anal intercourse (gay men) or unprotected vaginal intercourse (black African heterosexual men and women).

Table 1
Table 1
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Table 2
Table 2
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The association between unprotected intercourse and social, demographic and clinical variables (Table 1) was examined in univariate and multivariate logistic models, separately for: (i) gay men; and (ii) black African heterosexual men and women combined. In all models, unprotected intercourse was the dependent variable. Independent variables were age, number of years since diagnosis, CD4 cell count (entered into the models as continuous variables), employment, education, relationship, being on HAART, viral load, recreational drug use, seeking sex through the Internet and HIV optimism (entered as categorical variables). The sexual behaviour of gay men was also compared with that of black African heterosexual men and women combined. Differentials between the two groups were explored in univariate and multivariate logistic models.

Because we conducted multiple statistical tests we set alpha at 0.01 to reduce the risk of a type 1 error. As a consequence, only differences between groups in which the P value was less than 0.01 were considered to be statistically significant.

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Results

Sample

During the study period, 2680 individuals attended the outpatient clinics in the six participating hospitals; 2299 were eligible for the study and 1687 completed and returned a questionnaire (response rate 73% of eligible clinic attenders, 63% of all attenders) [4]. The three main groups of respondents were gay or bisexual men (n = 758), black African heterosexual women (n = 480), and black African heterosexual men (n = 224). These three groups accounted for 87% of the respondents and are included in this analysis. It was not possible to estimate the response rates separately for the three groups because we did not record the ethnicity of non-responders. Of the 758 gay men, 464 were white, whereas 112 were ethnic minority including black Caribbean (26), black African (13), Indian, Pakistani and Bangladeshi (9) and ‘mixed/other’ (57).

The remaining respondents included white heterosexual men (64) and women (39); black Caribbean heterosexual men (13) and women (26); heterosexual men (21) and women (36) of ‘other black’, Asian and ‘mixed/other’ backgrounds; and 26 bisexual women or lesbians of different ethnicities. Because of the small numbers they were not included in the analysis here.

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Background characteristics

There were significant differences between the three groups on a number of sociodemographic, clinical and behavioural variables (Table 1). For example, black African heterosexual men and women were less likely to be employed than gay men (P < 0.001), although there were only small differences between the three groups in their educational attainment.

Between a half and three-quarters of the respondents said they were currently in a relationship; 40–50% of those who were in a relationship said their partner was also HIV-positive. The majority of black African heterosexual men and women (> 80%) said their regular partner (e.g. husband, wife, boyfriend, girlfriend) was also black African.

Whereas approximately 40% of gay men had used the Internet to look for sex or had taken recreational drugs, very few black African men and women reported these behaviours (P < 0.001). On the other hand, black African heterosexual men and women were more likely to report HIV optimism than gay men (P < 0.001).

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Sexual behaviour

Of the 224 black African men who described themselves as heterosexual, two reported having sex with another man in the previous 12 months. These two men were included with gay/bisexual men for the purpose of the sexual behaviour analysis. For all other respondents, self-reported sexual orientation and sexual behaviour were congruent.

There were no significant differences between white and ethnic minority gay men on any of the sexual behaviour outcomes (P > 0.2), so the two groups were combined for this analysis. Similarly, no significant differences were found between black African heterosexual men and women on any of the sexual behaviour outcomes (P > 0.3) so they were also combined for the analysis. The majority (≥ 80%) of black African heterosexual men and women said their sexual partners were also black African.

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Gay men

Nearly 40% of gay men reported unprotected intercourse in the previous 3 months; 13.7% only with another man with HIV, 20.2% with a partner of unknown (16.4%) or negative (3.8%) HIV status (Table 2).

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Black African heterosexual men and women

Fourteen per cent (86/623) of black African heterosexual men and women reported unprotected intercourse in the previous 3 months; 6.6% (41/623) only with a partner who was HIV-positive, 5.1% (32/623) with a partner of unknown or negative HIV status (Table 2). Most black African heterosexual men and women reported unprotected intercourse with a main partner rather than with a casual partner.

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Casual partners
Gay men

A quarter of gay men (25.9%) reported unprotected intercourse with a casual partner (Table 2). They were more likely to report unprotected intercourse with a casual partner of unknown or negative HIV status (16.1%) than with a casual partner who was also HIV-positive i.e. ‘serosorting’ (9.2%). Only five men (0.7%) said they had had unprotected intercourse with a casual partner who was HIV-negative. Of the 144 gay men reporting unprotected intercourse with a partner of unknown (117) or discordant (27) HIV status overall, 115 (80%) said this had occurred with a casual partner.

In multivariate analysis, unprotected intercourse with a casual partner of unknown or negative HIV status was associated with seeking sex through the Internet [adjusted odds ratio (AOR) 3.71, 95% confidence interval (CI) 2.26, 6.09, P < 0.001], using recreational drugs (AOR 2.47, 95% CI 1.49, 4.11, P < 0.001) and ‘HIV treatment optimism 1’ (AOR 1.91, 95% CI 1.15, 3.18, P = 0.01). There was no significant association with age, time since diagnosis, being employed, educational attainment, being on HAART, CD4 cell count, viral load or ‘HIV treatment optimism 2’ in the multivariate model (P > 0.1).

Seeking sex through the Internet and recreational drug use were also associated with unprotected intercourse with a casual partner who was HIV-positive i.e. serosorting (seeking sex through the Internet, AOR 7.80, 95% CI 3.76, 16.16, P < 0.001; recreational drug use, AOR 4.87, 95% CI 2.36, 10.02, P < 0.001). No other variables were significantly associated with unprotected sex with a casual partner with HIV in multivariate analysis (P > 0.1).

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Black African heterosexual men and women

Only 3–4% of black African heterosexual men and women reported unprotected intercourse with a casual partner (Table 2); approximately 1% reported unprotected intercourse with a casual partner who was also HIV-positive (serosorting) and 2% with a partner of unknown or negative HIV status. As so few black African heterosexual men and women reported unprotected intercourse with a casual partner, it was not possible to examine this in a multivariate model.

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Main partner
Gay men

Some 19.2% of gay men reported unprotected intercourse with a main partner. They were more likely to report unprotected intercourse with a main partner who was HIV-positive (10.9%) than with a main partner who was HIV-negative or of unknown HIV status (4.3%).

In multivariate analysis, no variables were associated with unprotected intercourse with a main partner of unknown or negative HIV status (P > 0.1). Recreational drug use (but no other variable) was associated with unprotected intercourse with a main partner who was HIV-positive (AOR 4.74, 95% CI 2.50, 8.98, P < 0.001).

All the gay men who reported unprotected intercourse with a main partner of unknown or negative HIV status said their partner knew they were HIV-positive.

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Black African heterosexual men and women

Fifteen per cent of black African heterosexual men and nearly 12% of women reported unprotected intercourse with a main partner (P > 0.05; Table 2). The black African men were more likely to report unprotected intercourse with a main partner who was HIV-positive (9.8%) than with a main partner who was HIV-negative or of unknown HIV status (2.1%). This differential was not so evident for the women (5.3 versus 4.9%).

In multivariate analysis, there was no significant association between any of the social, demographic or clinical variables and unprotected intercourse with a main partner who was HIV-positive or with a partner of unknown or negative HIV status (P > 0.05) for both the men and women.

Three of the four men, and nine of the 20 women (data missing for one woman) who reported unprotected intercourse with a main partner of unknown or negative HIV status said their partner knew they were HIV-positive.

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Comparison of gay men and black African heterosexual men and women

Overall, one in five gay men (20.1%, 117 + 27 = 144/715) reported unprotected intercourse with a partner of unknown or negative HIV status compared with one in 20 black African heterosexual men and women (5.1%, 6 + 26 = 32/623; odds ratio 5.28, 95% CI 3.52, 7.91, P < 0.001; Table 2).

This difference was seen largely with casual partners of unknown HIV status (gay men 15.4%, black African heterosexual men and women, 1.4%; 9/623, P < 0.001). Gay men were also more likely to report unprotected intercourse with a casual partner who was HIV-positive than black African heterosexual men and women i.e. serosorting (9.2 versus 1.0%, P < 0.001).

In multivariate analysis these differentials remained significant. However, as so few black African men and women reported unprotected sex with a casual partner, the standard errors in the multivariate models were large. Consequently, the adjusted odds ratios were imprecise and are not presented here.

No significant differences were seen between gay men and black African heterosexual men and women in their sexual behaviour with a main partner. For example, 4.3% of gay men reported unprotected intercourse with a main partner of unknown or discordant HIV status compared with 4.0% (25/623) of black African heterosexual men and women (P = 0.3; Table 2). In a multivariate model, there was no significant difference between gay men and black African heterosexual men and women in the percentage reporting unprotected intercourse with a main partner who was HIV-positive (P = 0.3). When we restricted the analysis to those who said they were in a relationship, we found that respondents were significantly more likely to report unprotected sex if their main partner was HIV-positive than if their main partner was of unknown or discordant HIV status (gay men, 57%, [78/138] versus 14%, [31/221]; black African heterosexual men 30%, [19/64] versus 7%, [4/61]; black African heterosexual women 28%, [23/83] versus 14%, [21/153]; all P < 0.001).

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Sexually transmitted infections

Just over a quarter of gay men reported having an STI in the previous 12 months compared with 7% of black African heterosexual men women (P < 0.001; Table 2).

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Discussion

Among people diagnosed with HIV surveyed in London clinics in 2004–2005, gay men were significantly more likely to report unprotected intercourse than black African heterosexual men and women. This difference was seen for unprotected intercourse with both HIV-positive partners (serosorting) as well as with partners of unknown or negative HIV status. The differential was explained by the fact that gay men were more likely to report unprotected intercourse with a casual partner than black African heterosexual men and women. No significant differences were seen between gay men and black African men and women in their sexual behaviour with a main partner, in multivariate analysis.

Overall, one in five gay men living with HIV reported unprotected intercourse with a partner of unknown or negative HIV status in the previous 3 months (usually with a partner of unknown status), compared with just over one in 20 black African heterosexual men and women living with HIV. Unprotected intercourse (anal or vaginal) with a partner of unknown or discordant HIV status presents a risk of HIV transmission to an uninfected person. In our study of people living with diagnosed HIV, it appeared that gay men were more likely than black African heterosexual men and women to engage in sexual behaviour that presents a risk of HIV transmission. It seems likely, therefore, that gay men will continue to account for the majority of new HIV infections acquired in the UK for the foreseeable future.

Most gay men living with HIV who reported unprotected anal intercourse with a partner of unknown or negative HIV status said that this had occurred with a casual partner, highlighting the continuing risk of HIV transmission in casual sexual encounters for gay men [6]. Among gay men, unprotected intercourse with a casual partner of unknown or negative HIV status was associated with seeking sex through the Internet, using recreational drugs and HIV optimism; there was no association with viral load or being on HAART. The association with the Internet probably reflects the fact that high-risk men selectively use the Internet to seek sexual partners rather than the Internet itself amplifying the risk of HIV [7,8].

Unprotected intercourse with a casual partner who was HIV-positive (i.e. serosorting) was also associated with seeking sex through the Internet. The Internet appears to facilitate serosorting because gay men with HIV find it easier to disclose their HIV status to people they meet online rather than offline [9]. Serosorting among gay men with HIV is an HIV risk reduction strategy, because there is no risk of HIV transmission to an uninfected person. However, there is a risk of HIV cross-infection and transmission of other STI such as syphilis, hepatitis C or lymphogranuloma venereum.

The associations seen here among gay men between unprotected intercourse and both recreational drug use and HIV treatment optimism have been reported elsewhere [7,10–14]. As our study was cross-sectional we were not able to establish cause-and-effect. It is possible that some men are drawn to recreational drugs and high-risk sex rather than the drugs per se, leading to greater sexual risk-taking [15]. Equally, HIV optimism may have triggered high-risk behaviour or may have been used as a post-hoc justification [16,17].

In marked contrast to the gay men, in multivariate analysis we found no variables that were significantly associated with unprotected intercourse among black African heterosexual men and women. Interestingly, for both gay men and black African men and women, we found no association between unprotected intercourse and being treated with HAART or having an undetectable viral load, reflecting findings from a recent meta-analysis [12].

Between 40 and 50% of respondents who were in a relationship said their partner was also HIV-positive, throwing into sharp focus the substantial number of people with HIV who are in seroconcordant relationships. The majority of black African heterosexual men and women said their partner was also black African. People in a relationship were more likely to report unprotected sex if their main partner was HIV-positive than if their partner was of unknown or negative HIV status. Nonetheless, between 2 and 5% of respondents reported unprotected intercourse with a main partner who was HIV-negative or of unknown status, highlighting the risk of HIV transmission within these relationships. All the gay men, but only half the black African women reporting this behaviour said their main partner knew they had HIV. This striking differential highlights the difficulties African women face in disclosing their HIV status to their regular partners [18].

As is the case with much behavioural research, our analysis was based on self-reported risk [19]. It is possible that high-risk sexual behaviours may be underreported because of social desirability bias or because of the associated stigma. To minimize this bias, all questionnaires were confidential and anonymized for the analysis, which protected individual respondents from being identified. Social and cultural factors may impact on the reliability of self-reported sexual behaviour [19]; this could have contributed to the differences seen here between (mostly white) gay men and black African heterosexual men and women. However, we saw similar differences in the reporting of STI, which are less likely to be selectively underreported in our study because all patients were recruited in HIV clinics within STI services.

The study was restricted to people with diagnosed HIV. As a consequence, we may have underestimated the absolute level of risk. A recent meta-analysis found that the prevalence of unprotected anal or vaginal intercourse was lower in people with HIV who were aware of their status compared with those who were unaware [20]. Respondents were all recruited in HIV outpatient clinics in one part of London – east London. However, the social, demographic and behavioural characteristics of the gay men in this study are broadly similar to those of gay men with HIV surveyed in other outpatient clinics elsewhere in London [7,21,22]. We were not able to make a similar comparison for black African heterosexual men and women with HIV as ours is the first large-scale survey of this population in outpatient clinics.

Our findings are consistent with those from a national probability survey of sexual behaviour in Britain (Natsal, 2000). In Natsal (a survey of the general population, not just people diagnosed with HIV), men who have sex with men reported more sexual partners than black African heterosexual men and women; men who have sex with men were also more likely to report an STI diagnosis [23–25]. Although our study was conducted only in London, it is likely that the differentials reported here (between gay men and black African heterosexual men and women) will be seen in patients diagnosed with HIV living outside the capital.

One of the strengths of the analysis is that it is based on a broad cross-section of people diagnosed with HIV all coming from a common source (NHS clinics). Furthermore, an NHS clinic sample is broadly representative of people living with an HIV diagnosis [1]. Previous studies in the UK among black African heterosexual men and women with HIV have relied on convenience samples recruited through community groups and social networks [26–30].

In conclusion, an almost equal number of gay men and black African heterosexual men and women now live with diagnosed HIV in the UK [1]. In our study of people living with diagnosed HIV, the majority of respondents reported safer sexual practices. However, some gay men as well as black African heterosexual men and women reported sexual behaviour that presents a risk of HIV transmission, gay men moreso than black African heterosexual men and women. Differences between gay men and black African heterosexual men and women in their sexual behaviour with casual partners must be taken into account as part of any comprehensive HIV prevention strategy. There remains a need for targeted HIV prevention among people with HIV in the UK, which must be given high priority [31].

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Acknowledgements

The authors would like to thank all the patients who took part in the study and gave their time to complete the questionnaire. They would also like to thank the staff in all the participating clinics for their support throughout the project, the people who distributed questionnaires in the clinics and those who conducted data entry.

Sponsorship: The study was funded by St Bartholomew's and the Royal London Charitable Foundation, Research Advisory Board (grant JRB XMNS) with additional support from City University London, Institute of Health Sciences, St Bartholomew School of Nursing and Midwifery.

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Keywords:

Black African; gay men; heterosexual men and women; HIV transmission; London; sexual behaviour

© 2007 Lippincott Williams & Wilkins, Inc.

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