Lubricant use among men who have sex with men reporting receptive anal intercourse in Peru: implications for rectal microbicides as an HIV prevention strategy

Abstract

This study assessed lubricant use during receptive anal intercourse (RAI) among Peruvian men who have sex with men (MSM) and willingness to use a hypothetical rectal microbicide (RM) formulated as a lubricant to prevent HIV infection. Data were collected from 843 Peruvian MSM for the 2008 HIV Sentinel Surveillance using a computerized self-interview. Half of the participants reported using a lubricant with their last sex partner during RAI, while 77% were willing to use a lubricant to prevent HIV transmission. Lubricant use with last sex partner was significantly associated with unprotected RAI (odds ratio [OR] 1.59, 95% confidence interval [CI], 1.23, 2.05; P < 0.001) and willingness to use a future lubricant RM (OR 1.56, 95% CI: 1.24, 1.95; P < 0.001). This study provides information on the behaviours associated with lubricant use and non-use among MSM practicing RAI in Peru that should inform future RM studies in Peru and other Latin American countries.

Keywords

lubricant HIV prevention rectal microbicides MSM South America

INTRODUCTION

Microbicides are substances under development that could be used vaginally or rectally to prevent HIV infection. The bulk of research to date has focused on vaginal microbicides; however, rectal microbicides (RM) – products designed specifically for use during anal intercourse (AI) – is a rapidly expanding research field that has grown considerably over the past five years.¹ While AI is not an exclusively homosexual behaviour, globally, men who have sex with men (MSM) are 19 times more likely to be infected with HIV than the general population² and a single act of unprotected receptive anal intercourse (URAI) is 5–80 times riskier for HIV transmission compared with unprotected vaginal intercourse.³ Thus, a safe and effective RM could play an important role in preventing new HIV infections in countries with epidemics concentrated among MSM.

Phase I clinical trials assessing the safety of RM candidates are currently underway in the USA,^4,5 and a number of studies have examined the use and acceptability of potential RM presentations, including lubricants/gels,^6,7 suppositories⁷ and enemas/rectal douches,^8,9 as well as willingness to participate in RM clinical trials among MSM.^6,10 While these studies found that MSM responded positively to hypothetical RM and would be willing to participate in future RM clinical trials, equivalent data in MSM from non-USA populations are virtually non-existent. This need for data on RM acceptability from non-USA populations has already been called for by RM experts who recognize the potential for differences due to cultural, social, economic and other factors.^1,4,11 A key finding in USA-based investigations on lubricant use is that an RM formulated as a sexual lubricant would likely face few barriers to use by MSM since sexual lubricants are already widely used by this population for AI. For example, a household probability study of 879 MSM in San Francisco found that while approximately 50% practiced unprotected AI, lubricant was used by 89% of MSM.¹² Another study among 307 MSM in New York showed that lifetime lubricant use was 94%.⁶

This study explores lubricant use in a sample of non-USA (Peruvian) MSM, focusing specifically on those most likely to use an RM: the receptive partner for AI since these men constitute the primary target population for an RM. Peru was chosen to investigate this issue for multiple reasons. First, it is a country experiencing a concentrated HIV epidemic in MSM (prevalence = 18–22%¹³ versus <1% in the general population¹³) and therefore could benefit from an effective RM. Second, Peru has a highly developed HIV research infrastructure and has conducted or is currently conducting clinical trials on a range of biomedical HIV prevention strategies including pre-exposure prophylaxis and vaccine studies;¹⁴ thus, clinical trials of candidate RM could be feasible in terms of technical capacity and access to research subjects. Finally, beyond RM clinical trials in Peru, information on lubricant use by MSM for AI will inform future scale-up efforts both in Peru and potentially regionally once a safe and effective RM is available for widespread use.

MATERIALS AND METHODS

Participants

Data for this study were collected from a subsample of Peruvian MSM from three Peruvian cities (Lima, a coastal city, and in the Amazon cities of Iquitos and Pucallpa) participating in the 2008 HIV Sentinel Surveillance. A convenience sample was recruited by peer outreach workers visiting venues frequented by MSM (e.g. bars, clubs, volley-ball courts) and by patient advocates located at sites participating in a larger USA-NIH HIV clinical research study. For this analysis, we examined data from 843 MSM who practiced receptive anal intercourse (RAI) and individuals were included if they were anatomically male, aged 18 years or older and reported RAI with at least one man in the previous three months. Subjects gave voluntary informed consent prior to participation, and the study protocol was approved by the Peruvian National AIDS and STD Control Programme and the Institutional Review Boards of the Asociación Civil Impacta Salud y Educación in Lima and the USA Navy Medical Research Center Detachment.

Procedures

Participants completed a structured interview using a web-based computer-assisted self-interview¹⁵ in a private room at each study site, which collected information on demographics, sexual behaviours, history of HIV/STI, lubricant use during RAI and willingness to use a future ‘commercial lubricant’ (i.e. a lubricant that would be manufactured, marketed and sold specifically for AI) to protect against HIV, i.e. an RM. Following the interview, blood samples were collected and tested for anti-HIV-1 antibodies using Determine HIV-1/2 rapid assay with Western blot confirmation (Biorad Laboratories, Hercules, CA, USA). Participants testing HIV seropositive were referred to the Peruvian Ministry of Health's HIV treatment programme (‘TARGA’, free to all Peruvians) for further evaluation and long-term management. Following the study procedures, participants were offered condoms, water-based lubricant sachets and US$ 3.50 for time and transportation costs.

Measures

Demographics, behavioural characteristics and HIV status

Demographic information collected included city of residence, age, education and sexual orientation. Behavioural characteristics included condom use during RAI with last partner, number of partners in the three months prior to the survey and type of sexual partners in the past three months (stable, casual, one night stand and partners where money was exchanged for sex). HIV status was based on lab reports (Table 1).

Table 1

Demographics, behavioural characteristics and HIV status of MSM who reported receptive anal intercourse in the 2008 Peruvian Sentinel Surveillance survey (total n = 843)*

Characteristics	n (%)
Demographics
City of residence
Lima	376 (44)
Iquitos	225 (27)
Pucallpa	242 (29)
Age (years)
18–24	301 (36)
25–29	207 (25)
30–34	112 (13)
35+	219 (26)
Education
Less than high school	41 (5)
High school	435 (53)
Greater than high school	347 (42)
Self-identified sexual orientation
Heterosexual/straight	15 (2)
Homosexual/gay	628 (82)
Bisexual	125 (16)
Behavioural characteristics
Condom use during intercourse with last partner
No	458 (59)
Yes	316 (41)
Type of sexual partner
Stable	286 (35)
Casual	165 (20)
One night stand	334 (41)
Commercial work	34 (4)
Number of partners in the past three months
1	124 (16)
2–4	251 (31)
5+	423 (53)
HIV status
Negative	730 (90)
Positive	82 (10)

MSM = men who have sex with men

*Due to missing data, not all variables sum to the total n

Lubricant use

Lubricant use was assessed by the question, ‘Did you use a lubricant during RAI with your last sex partner (yes/no)?’ For those who answered ‘yes’, the following list of lubricants was provided to participants who were asked to ‘check all that apply’: ‘gel (e.g. KY)’, ‘Vaseline/oil’, ‘cream (e.g. Ponds)’ and ‘saliva’. For those who answered ‘no’, the following list of reasons was provided to participants who were asked to ‘check all that apply’: ‘used lubricated condoms’, ‘prefer dry sex (without lubricant)’, ‘my partner didn't want to use it’, ‘didn't have money to buy it’, ‘I was in a rush’ and ‘didn't like the brand of lubricant I had’. We also asked participants about the frequency in which lubricant was applied during RAI (1–2 times versus 3 or more), when the lubricant was applied during RAI (prior to sexual contact, after sexual contact, but before penetration, after penetration), who applied the lubricant (self, partner, sometimes self/sometimes partner) and where the lubricant was applied, allowing for multiple responses (‘outside anus’, ‘partner's penis’, ‘outside condom’, ‘inside rectum’ and ‘inside condom’). Finally, participants were asked whether using lubricants interrupted sex (yes/no) (Table 2).

Table 2

Patterns of lubricant use during receptive anal intercourse among MSM (n = 843)

	n (%)
Lubricant use with last partner
Yes	405 (48)
No	438 (52)
Type of lubricant used with last partner*
Gel (e.g. KY)	240 (59)
Vaseline/oil	37 (9)
Cream (e.g. Ponds)	54 (13)
Saliva	98 (24)
Reasons lubricant not used*
Uses condoms	117 (27)
Prefers dry sex	89 (20)
Partner does not like lubricants	56 (13)
Does not have money for lubricants	46 (11)
Not enough time (in a hurry)	63 (14)
Participant does not like to use lubricants	24 (5)
How often is lubricant applied during anal intercourse? ^†
1–2 times	297 (85)
3+ times	52 (15)
When is lubricant applied? ^†
Prior to sexual contact	328 (82)
After sexual contact, but before penetration	67 (16)
After penetration	7 (2)
Who applies lubricant? ^†
Self	196 (49)
Partner	69 (17)
Sometimes self/sometimes partner	135 (34)
Where is lubricant applied?*^†
Outside anus	216 (53)
Partner's penis	197 (49)
Outside condom	113 (28)
Inside rectum	96 (24)
Inside condom	8 (2)
Does lubricant interrupt sex? ^†
Yes	65 (16)
No	336 (84)
Willingness to use a future commercial lubricant
Yes	563 (77)
No	165 (23)

MSM = men who have sex with men

*Not mutually exclusive categories

^†Based on respondents who reported lubricant use

Willingness to use a future lubricant to protect against HIV

Willingness to use an RM was assessed with the question ‘If there were a commercial lubricant available in the future to protect against HIV, would you use it?’ (yes/no).

Data analysis

First, we examined the univariate distributions of demographics, behavioural characteristics, patterns of lubricant use and willingness to use an RM. Second, we performed bivariate analyses to assess the unadjusted association of lubricant use with last sexual partner during RAI with demographics, behavioural characteristics, HIV status and willingness to use an RM. Third, we used multivariate logistic regression to estimate the adjusted association between willingness to use an RM and lubricant use with last sexual partner during RAI adjusted for demographics and behavioural characteristics. Finally, given that 32% of our sample was recruited from an ongoing clinical research study in Peru (versus 67% from local venues frequented by MSM) and might be more primed to use a lubricant, a future RM and participate in a future clinical trial on RMs, we examined whether there were significant differences between the two sample populations in the bivariate analyses and adjusted multivariate model. Given the lack of significant findings, the results are not presented. All analyses were conducted using STATA 10.0 software (College Station, TX, USA).

RESULTS

Demographics and behavioural characteristics

Participant characteristics are presented in Table 1. Forty-four percent of participants were from Lima, 29% were from Pucallpa and 27% were from Iquitos. Over half of the participants (61%) were between the ages of 18–29 years, and 95% had a high school education or greater. Eighty-two percent identified as homosexual, 16% as bisexual and 2% as heterosexual. Forty-one percent reported not using a condom with their last sex partner, and 53% had five or more partners in the past three months. Type of partners in the past three months included stable partner (35%), casual partner (20%), one night stands (41%) and partners where money was exchanged for sex (4%). Ten percent tested HIV positive.

Lubricant use during RAI with most recent partner

Patterns of lubricant use are presented in Table 2. Approximately half of the participants (48%) reported using a lubricant of any kind with their last sexual partner. The most common formulation of lubricant used was gel (59%). Reasons for not using a lubricant during RAI included ‘uses condoms’ (27%) and ‘prefers dry sex’ (20%). Most participants (85%) reported applying a lubricant 1–2 times during RAI, with 82% applying the lubricant prior to sexual contact. Forty-nine percent reported applying the lubricant themselves, and 34% reported that sometimes they applied the lubricant and sometimes their partner did. Lubricants were most often applied ‘outside the anus’ (53%), ‘on partner's penis’ (49%) and ‘outside the condom’ (28%). Most of the participants (84%) who used lubricants during RAI reported that lubricant did not interrupt sex. Seventy-seven percent of participants reported willingness to use a future RM (Table 2).

Lubricant use, demographics, sexual risk behaviours, HIV status and willingness to use a future lubricant to protect against HIV

In bivariate analyses, lubricant use with last sexual partner was significantly associated with living in Lima (odds ratio [OR] 1.84, 95% confidence interval [CI], 1.32, 2.55; P < 0.001), being 25–29 years of age (OR 1.51, 95% CI: 1.06, 2.16; P < 0.05), not using a condom during intercourse with last partner (OR 1.70, 95% CI: 1.27, 2.027; P < 0.001) and willingness to use an RM (OR 1.86, 95% CI: 1.230, 2.66; P < 0.01). Participants having ‘one night stands’ and exchanging money for sex (as either receiving money or paying money) were significantly less likely to use lubricants than participants with a stable partner (OR 0.44, 95% CI: 0.32, 0.61; P < 0.001 and OR 0.46, 95% CI: 0.22, 0.96; P < 0.01, respectively) (Table 3).

Table 3

Bivariate logistic regression analysis of the association of lubricant use with last sexual partner during receptive anal intercourse with demographics, behavioural characteristics, and HIV status

Variable (reference group)	n	Lubricant use (yes) odds ratio (95% CI)
City of residence (Pucallpa)	843
Lima		1.84 (1.32 to 2.55)^‡
Iquitos		1.00 (0.69–1.45)
Age (18–24 years)	839
25–29		1.51 (1.06–2.16)*
30–34		1.38 (0.89–2.14)
35+		1.30 (0.91–1.84)
Education (less than high school)	823
High school		0.63 (0.33–1.19)
Greater than high school		1.04 (0.55–2.00)
Sexual orientation (heterosexual)	768
Homosexual/gay		2.00 (0.68–5.92)
Bisexual		1.52 (0.49–4.71)
Type of partner (stable)	819
Casual		0.98 (0.67–1.48)
One night stand		0.44 (0.32–0.61)^‡
Commercial sex work		0.46 (0.22–0.96)*
Condom use with last partner (yes)	774
No		1.70 (1.27–2.27)^§
Number of partners, past three months (1)	798
2–4		0.79 (0.52–1.22)
5+		0.97 (0.65–1.44)
HIV status (negative)	812
Positive		1.33 (0.84–2.10)
Willingness to use a lubricant in the future (no)	728
Yes		1.86 (1.30–2.66)^‡

CI = confidence interval

*P < 0.05; ^† P < 0.01; ^‡ P < 0.001

In multivariate analyses, lubricant use with last sexual partner was significantly associated with willingness to use an RM (OR 1.96, 95% CI: 1.26, 3.05; P < 0.01). Multivariate analyses also showed that individuals aged 35 or older were more willing to use an RM than those between the ages of 18 and 24 (OR 2.62, 95% CI: 1.49, 4.61; P < 0.01), and individuals not using a condom during RAI with their last sexual partner were less willing to use an RM compared with those who used a condom during RAI with their last sexual partner (OR 0.63, 95% CI: 0.40, 0.97; P < 0.05).

DISCUSSION

In this convenience sample of Peruvian MSM where unprotected RAI (URAI) was common and 10% were HIV positive, we found that lubricants were used during RAI by approximately half of the participants, while 77% reported they would use a future lubricant (i.e. an RM) that protected against HIV. These findings are an indicator that an RM formulated as a sexual lubricant may be acceptable to Peruvian MSM.

Approximately half of MSM (48%) reported using lubricants of any kind during RAI with their last sexual partner. The majority of MSM reported using a commercial (water-based) lubricant, such as KY Jelly. Other substances used as a lubricant included saliva, cream and Vaseline/cooking oil. This result is simultaneously promising and concerning. On the one hand, it suggests that non-commercial lubricant users do in fact use something for lubrication during RAI and may serve as a proxy for the future use of RM formulated as a sexual lubricant as the application behaviour would share similarities. Nevertheless, with the exception of saliva, the other products that are currently being used are oil-based, a known contributor to latex condom failure. Even in the absence of commercial lubricants or future RM, current users of oil-based substances for lubricants should be educated on the risks of and alternatives to such products. The rate of lubricant use found in our study contrasts with studies conducted among MSM in the USA where lifetime lubricant use ranges from 89% to 94%;^6,10 however, given that we restricted the sample to MSM reporting RAI with their last partner during the past three months, lifetime prevalence of lubricant use may be underestimated.

Equally important to assess are the reasons for non-lubricant use, as such reasons could be barriers to both conducting future clinical trials of RM or the uptake of actual RM once they become available. Indeed, successful product development may not equate to ready adoption by the targeted population; the decade-long challenges faced in the scale up of the female condom illustrate the need to carefully understand and prospectively address potential barriers to the use of an HIV prevention product prior to its introduction.^16–18 The most frequent reason for lack of lubricant use was ‘uses condoms’ (27%); therefore, it is possible that participants found the condom's lubricant sufficient, rendering additional lubricant application unnecessary. The second most common reason for lack of lubricant use was the preference for dry sex, reported by one-fifth of non-lubricant users. While heterosexual dry sex has been documented in a number of sub-Saharan African countries and Caribbean countries (Dominican Republic and Haiti), equivalent data for Peruvian MSM practicing AI are non-existent.^19–21 The reasons for engaging in this behaviour are complex and vary by country, gender (male versus female) and type of sex (e.g. anal versus vaginal). This finding warrants further investigation to understand the specific aspects of dry sex desired by Peruvian MSM that pre-empt lubricant use. Issues such as a dislike of lubricants by the participant or his partner and lack of money or time were less commonly reported. Taken together, these data offer an important initial understanding of the reasons for non-lubricant use, but point to the need for expanded research.

Patterns of lubricant use shed light on important factors to be considered in the context of a future RM in this population. For example, in current RM development it is assumed that the product would need to be introduced inside the rectum and in sufficient volume to infer protection.^4,22 Experts estimate that up to 50 mL of the product may be necessary in order to provide sufficient coverage and HIV protection in the rectum.²² In this study, only approximately one-fourth of participants applied lubricant inside the rectum, and while data on the amount of lubricant used were not collected, the volume was most likely insufficient to achieve the rectal mucosa coating necessary for HIV prevention by RM. A study assessing various volumes of a placebo microbicidal gel among USA MSM found that up to 35 mL of the gel was acceptable to the majority of participants;²² similar research is needed on non-USA MSM populations. Most of the participants in this study applied lubricant prior to sexual contact, and reported that lubricant did not interrupt sex. These are promising findings for the acceptability of a future RM.

Bivariate analyses revealed that lubricant use during RAI with last sexual partner was significantly associated with having URAI. Given the elevated risk of HIV infection during URAI, this finding is promising for the successful introduction of a future RM into this population. We also found that participants from Lima were more likely than participants from Pucallpa to use a lubricant. This is not surprising as Lima is the capital and lubricants are likely more accessible than in the Amazon cities (e.g. greater number of pharmacies in Lima, with a population of over eight million compared with Pucallpa with a population of approximately 200,000). Participants having ‘one night stands’ and exchanging money for sex were significantly less likely to use lubricants than participants with a stable partner. This finding may be related to the portability of lubricants, making them less available in sexual venues (i.e. bath houses, saunas, cinemas) common in ‘one night stands’, where a tube or bottle of lubricant could not be conveniently transported or it may be that sex with non-stable partners is more spontaneous such that use of lubrication was not planned. Further related research should explore packaging preferences for RM so that they can be transported easily for use in a variety of places where sexual intercourse could take place, both planned and spontaneous.

Lubricant use with last sexual partner was significantly associated with willingness to use an RM, even after controlling for demographics, behavioural characteristics and HIV status (Table 4). However, the percentage of MSM who would actually use an RM formulated as a lubricant may be lower, especially given the multiple other attributes that will affect the acceptability of an RM, including efficacy, side-effects, duration of protection, accessibility issues, volume needed, cost, etc. Multivariate analyses also showed that MSM aged 35 or older were more willing to use a future RM than men aged 18–24 years. Finally, men who practiced URAI were less willing to use a future RM than men who had protected RAI. This could be related to a general perception of lack of risk or lack of personal concern with regard to HIV in general. These findings warrant larger studies focusing specifically on factors influencing RM willingness before conclusions can be made.

Table 4

Multivariate logistic regression analysis of willingness to use a future commercial lubricant to protect against HIV by lubricant use with last sexual partner adjusted for demographics and behavioral characteristics (total N = 564)

Variable (reference group)	Willingness to use a future commercial lubricant to protect against HIV Odds ratio (95% CI)
Lubricant use with last partner (no)
Yes	1.95 (1.26–3.03)^†
City of residence (Pucallpa)
Lima	1.20 (0.73–2.05)
Iquitos	1.01 (0.57–1.78)
Age (18–24 years)
25–29	1.40 (0.81–2.43)
30–34	1.57 (0.81–3.07)
35+	2.55 (1.44–4.50)^†
Education (less than high school)
High school	1.29 (0.44–3.76)
Greater than high school	1.43 (0.48–4.24)
Sexual orientation (heterosexual)
Homosexual/gay	0.36 (0.04–3.04)
Bisexual	0.31 (0.04–2.77)
Type of partner (stable)
Casual	1.23 (0.68–2.24)
One night stand	1.36 (0.81–2.29)
Commercial sex work	2.68 (0.73–9.90)
Condom use with last partner (yes)
No	0.62 (0.40–0.96)*
Number of partners, past three months (1)
2–4	1.07 (0.55–2.10)
5+	1.43 (0.73–2.80)
HIV status (negative)
Positive	0.88 (0.43–1.78)

CI = confidence interval

*P < 0.05; ^† P < 0.01

There were study limitations. First, the sample was restricted to a relatively educated high-risk MSM population practicing RAI from three Peruvian cities who were recruited from venues participating in a larger USA-NIH HIV clinical research study where they received HIV education, testing and counselling, and may not be generalizable to all MSM in Peru or in other Latin American countries. Second, condom use was self-reported, leaving the potential for reporting bias, although it is hoped that the use of computerized self-interviewing mitigated this error. Third, despite rigorous attempts to identify and adjust for differential non-response, such bias may have affected the results; missing data may have been the result of recall bias, questionnaire fatigue or technical problems with the computerized questionnaire. Finally, the expressed attitudes about willingness to use hypothetical products may not be maintained when the actual product is presented.

This is the first study to examine patterns of lubricant use in a non-USA, Latin American setting focusing specifically on Peruvian MSM practicing RAI, a behaviour that constitutes one of the greatest risks for HIV transmission. Despite the limitations, this study provides important and novel information on the behaviours associated with lubricant use and non-use among MSM practicing RAI in Peru that could prove useful for future RM acceptability and feasibility studies in Peru and other Latin American countries.

Footnotes

ACKNOWLEDGEMENTS

This work was partially funded by US HIV Research Programme, Walter Reed Army Institute of Research, Work Unit No. 62787A S17 H B0002. The views expressed in this paper are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense nor the US Government. Dr Silvia Montano is an employee of the US Government. This work was prepared as part of her official duties. Title 17 USC § 105 provides that ‘Copyright protection under this title is not available for any work of the United States Government’. Title 17 USC § 101 defines a US Government work as a work prepared by a military service member or employee of the US Government as part of that person's official duties.

References

International Rectal Microbicide Advocates (IRMA). Less Silence More Science: advocacy to Make Rectal Microbicides a Reality. Chicago: IRMA/AIDS Foundation of Chicago, 2008

Baral

, Sifakis

, Cleghorn

, Elevated risk for HIV infection among men who have sex with men in low- and middle income countries 2000–2006: a systematic review. PLoS Med 2007;4:e339

Gray

, Wawer

, Brookmeyer

, Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001;357:1149–53

McGowen

. Rectal microbicides: a new focus for HIV prevention. Sex Transm Infect 2008;84:413–17

Ventuneac

, Carballo-Diéguez

, McGowen

, Acceptability of UC781 gel as a rectal microbicide among HIV-uninfected women and men. AIDS Behav 2009; DOI: 10.1007/s10461-009-9611-5

Carballo-Diéguez

, Stein

, Saez

, Frequent use of lubricants for anal sex among men who have sex with men: the HIV prevention potential of a microbicidal gel. Am J Public Health 2000;90:1117–21

Carballo-Diéguez

, Dolezal

, Bauermeister

, Preference for gel over suppository as delivery vehicle for a rectal microbicide: results of a randomised, crossover acceptability trial among men who have sex with men. Sex Transm Infect 2008;84:483–7

Carballo-Diéguez

, Bauermeister

, Ventuneac

, The use of rectal douches among HIV-uninfected and infected men who have unprotected receptive anal intercourse: implications for rectal microbicides. AIDS Behav 2008;12:860–6

Balan

, Carballo-Diéguez

, Ventuneac

, Intentional condomless anal intercourse among Latino MSM who meet sexual partners on the internet. AIDS Educ Prev 2009;21:4–24

10.

Gross

, Buchbinder

, Celum

, Rectal microbicides for U.S. gay men. Are clinical trials needed? Are they feasible? HIVNET Vaccine Preparedness Study Protocol Team. Sex Transm Dis 1998;25:296–302

11.

Mantell

, Myer

, Carballo-Diéguez

, Microbicide acceptability research: current approaches and future directions. Soc Sci Med 2005;60:319–30

12.

Carballo-Diéguez

, O'Sullivan

, Lin

, Awareness and attitudes regarding microbicides and nonoxynol-9 use in a probability sample of gay men. AIDS Behav 2007;11:271–6

13.

UNAIDS. Report on the Global AIDS Epidemic. Geneva, Switzerland: UNIAIDS, 2008

14.

AVAC-Global Advocacy for HIV prevention. Current Research: HIV Prevention around the Globe. See http://www.avac.org/ht/d/sp/i/189/pid/189PrEPwatch.org/pdf/Trials/PrEP_trials_table.pdf (last accessed 3 March 2010)

15.

Peinado

, Lama

, Sánchez

. Web based interviewing system for HIV-behavior research in the settings of vaccine and non vaccine prevention trials. AIDS Vaccine 2009 Conference

16.

Mantell

, Dworkin

, Exner

, The promise and limitations of female-initiated methods of HIV/STI protection. Soc Sci Med 2006;63:1998–2009

17.

Moore

, Rogers

. Female controlled prevention technologies. In: O'Leary

, ed. Beyond Condoms: Alternative Approaches to HIV Prevention,. New York: Kluwer Academic Publishers/Plenum Press, 2002

18.

Rotheram-Borus

, Swendeman

, Chovnick

. The past, present, and future of HIV prevention: integrating behavioral, biomedical, and structural intervention strategies for the next generation of HIV prevention. Annu Rev Clin Psychol 2009;5:143–67

19.

Halperin

. Dry sex practices and HIV infection in the Dominican Republic and Haiti. Sex Transm Infect 1999;75:445–6

20.

Civic

, Wilson

. Dry sex in Zimbabwe and implications for condom use. Soc Sci Med 1996;42:91–8

21.

Beksinska

, Rees

, Kleinschmidt

The practice and prevalence of dry sex among men and women in South Africa: a risk factor for sexually transmitted infections?

Sex Transm Infect 1999;5: 178–80

22.

Carballo-Diéguez

, Exner

, Dolezal

, Rectal microbicide acceptability: results of a volume escalation trial. Sex Transm Dis 2007;34:224–9