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Incidence of Sexually Transmitted Diseases and HIV Infection Related to Perceived HIV/AIDS Threat Since Highly Active Antiretroviral Therapy Availability in Men Who Have Sex With Men

van der Snoek, Eric M. MD*; de Wit, John B. F. PhD†; Mulder, Paul G. H. MSc, PhD‡; van der Meijden, Willem I. MD, PhD*

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From the * Department of Dermatology and Venereology, Erasmus MC, Rotterdam, The Netherlands; the † Department of Social and Organizational Psychology, Utrecht University, Utrecht, The Netherlands; and the ‡ Institute of Epidemiology and Biostatistics, Erasmus MC, Rotterdam, The Netherlands

The authors thank Adrie van’t Hof, research nurse, and Edward de Haan, social nurse, Department of Dermatology and Venereology, for their contributions. Dr. B. Tank, Department of Dermatology and Venereology, is thanked for correcting the English.

Correspondence: Eric M. van der Snoek, MD, Erasmus MC, University Medical Center Rotterdam, Department of Dermatology and Venereology, Dr. Molewaterplein 40, 3015 GD Rotterdam, The Netherlands. E-mail: e.vandersnoek@erasmusmc.nl.

Received for publication June 8, 2004, and accepted September 10, 2004.

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Abstract

Objective: Concerns have been expressed regarding increase in risky sex because of the availability of antiretroviral treatments in Western countries.

Goal: The goal of this longitudinal study was to investigate the association between highly active antiretroviral therapy (HAART)- and postexposure prophylaxis-related beliefs and the incidence of sexually transmitted diseases (STDs) and new HIV infections in men who have sex with men (MSM).

Study: Data on the incidence of STDs and new HIV infection, and the level of agreement with different HAART- and PEP-related beliefs from 151 HIV-negative MSM were compiled.

Results: Of all MSM, 65.6% tested negative for any STDs and 7 men HIV seroconverted. Perceiving less HIV/AIDS threat since HAART availability and younger age were significantly associated with a higher incidence of STDs. Perceiving less need for safe sex since HAART availability was significantly associated with an increased likelihood of HIV seroconversion.

Conclusions: The results support the assumption that there is an association between the incidence of STDs and a decreased perception of HIV/AIDS threat resulting from HAART availability. Less perceived need for safe sex since HAART availability was associated with HIV seroconversion.

IN 1995, THE FIRST case–control study showed that treatment with zidovudine after exposure to HIV decreased the risk of infection by 79%.1 Since then, several reports warned for a potential increase in risky sexual behavior because of the widespread availability and use of effective antiretroviral treatments by men who have sex with men (MSM) in Western countries.

Studies in MSM in San Francisco who engaged in high-risk sex reported that some men had less concern of becoming HIV-positive because of the availability of antiretroviral therapy.2,3

Cross-sectional studies on larger samples of respondents also reported that important minorities of MSM changed their perceptions of HIV infection and protective behavior. For instance, in a community sample of 379 MSM who reported awareness of antiretroviral therapy regimens, 10% of the respondents (strongly) agreed with the statement that “AIDS is now very nearly cured” and 13% felt that “the threat of AIDS is less serious now than in the past.” Overall, 8% of all MSM and 18% of HIV-positive MSM on antiretroviral therapy said that they practiced safe sex less often because treatments had advanced.4

In Chicago, 46% of 554 MSM, recruited during the course of a “gay”-oriented street fair, reported unprotected anal sex in the past 6 months. Lowered concern for HIV infection, reflecting the impact of antiretroviral treatment, emerged as an independent predictor of unprotected anal sex. The authors warned that even a small degree of lowered concern may be associated with substantial changes in rates of HIV transmission.5

In recent years, a large increase in gonorrhea and early syphilis was reported in MSM in several cities such as San Francisco, London, Sydney, and Amsterdam.6–10 These trends indicate a change in sexual behavior, possibly as a result of the introduction of highly active antiretroviral therapy (HAART).10,11 Data from a cohort study in Amsterdam showed that HIV-positive and HIV-negative MSM practiced anal sex more often in the period after the introduction of improved antiretroviral therapies. The proportion of men who had unprotected anal sex increased among HIV-negative men.10–12

Elford et al. recently suggested that optimism resulting from the availability of HAART is unlikely to explain the increased high-risk sexual behavior in MSM over time.13 It was stated that most studies report cross-sectional associations between optimism and self-reported anal sex rather than longitudinal data. In their longitudinal study among almost 3000 MSM using London gyms, Elford et al. suggested that the upward trend in self-reported high-risk behavior might be explained by increased sex-seeking on the Internet, an increased opportunity for meeting sexual partners in saunas and backrooms, and the possibility that MSM have become accustomed to the risk of HIV infection after 2 decades of AIDS.

A recent prospective study from Amsterdam of MSM showed that a tendency toward agreement with “perceiving less HIV/AIDS threat” predicted individuals’ change to unprotected receptive anal intercourse over time.14 The authors concluded that the data supported the hypothesis of a causal relation between decreased HIV/AIDS threat and a change to unsafe receptive anal intercourse at an individual level.

A relation between HIV optimistic MSM and self-reported unprotected anal intercourse with casual partners was also found by Williamson et al. However, after multivariable logistic regression, controlling for confounding factors as survey year, the authors concluded “our results strongly suggest that HIV optimism can not explain recent high-risk sexual behavior among Scottish MSM.”15

Concerns have equally been expressed regarding the possibility that the availability of postexposure prophylaxis (PEP) may lead people to have unsafe sexual intercourse in the belief that they were protected from infection if they used PEP.16,17

In a study in the gay community of San Francisco, Waldo et al. reported a small percentage of MSM who self-reported that availability of PEP increased their risky sexual behavior.17

Very recently, a study among almost 400 mostly MSM (92%) who used PEP after sexual exposure (95%) or injection drug exposure showed, after 5 sessions of risk-reduction behavioral counseling, an increase in high-risk sexual intercourse in 14% of the men after a 12 months of follow up.18

The aim of this study was to prospectively investigate the association between HAART- and PEP-related beliefs and cumulative new STD and HIV infections among HIV-negative MSM participating in the ongoing Rotterdam cohort study. In this study, we focused on STD/HIV diagnoses rather than data on self-reported unprotected sexual contacts. Data on the prospective relation between optimism resulting from HAART and PEP and new STD and HIV infections among HIV-negative MSM provide an important insight into this extensively debated and investigated issue.

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Materials and Methods

Study Population and Study Design

The study was conducted at the STD clinic of the Department of Dermatology and Venerology, Erasmus MC, University Medical Center, Rotterdam, The Netherlands.

From February 1999 onward, we recruited 286 MSM to participate in the Rotterdam MSM-cohort study. Both HIV-positive and HIV-negative MSM were recruited by trained volunteers at gay meeting places like bars and saunas and with the use of advertisements in newspapers and gay periodicals. The way participants were recruited has been described in more detail elsewhere.19 At enrollment all participants provided written informed consent. The ethics committee of our hospital approved the protocol. Cohort participants were tested for STD and HIV every 6 months. In case of STD symptoms in between 2 biannual cohort visits, participants were urged to visit the STD clinic on short notice.

Inclusion criteria for the current study were having had sex with at least 1 male partner in the preceding 12 months, being HIV-negative at enrollment, and participating in 5 successive cohort visits, starting with visit number 3, which took place between January 2000 and September 2001.

The questionnaire measuring beliefs concerning PEP and HAART was first introduced at the third cohort visit.

A total of 151 HIV-negative MSM who participated in all 5 successive biannual cohort visits (visit nos. 3–7), between January 2000 and April 2003, were included in this study.

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Data Collection and Questionnaires

At each visit, medical history was taken, including self-reported information on STDs in the past 6 months. Also, demographic and sexual behavior information was collected, including ethnic background, age, educational level (defined as “low” with school attendance up to the age of approximately 16 years, “middle” with school attendance up to the age of approximately 18 years, and “high” with a college degree or equivalent), sexual orientation, and number of sexual partners during the previous 6 months. Participants further completed self-administered questionnaires on behavioral and psychologic issues related to STDs, HIV, and AIDS during the 5 consecutive visits. During the third visit, participants were asked to complete a standardized behavioral questionnaire that included a total of 24 statements concerning PEP and HAART. Statements were selected from other studies.7,17,20

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Highly Active Antiretroviral Therapy-Related Beliefs

Seventeen items, measured with a 5-point rating scale ranging from 1 (“strongly disagree”) to 5 (“strongly agree”) assessed participants’ HAART-related perceptions.

Using principal components analysis (PCA) with varimax rotation (assuming no correlation between the factors), we distinguished 4 principal components (Table 1), each consisting of several related statements. The cumulative variance explained by the 4 components was 62.4%.

Table 1
Table 1
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Reliability analysis was used to confirm internal consistency of scales constructed on the basis of identified principal components. Scores on each principal component were calculated as the average scores of the statements involved and ranged from 1 to 5. Odds ratios were calculated per unit increase of the average scores.

The first principal component, perceiving less HIV/AIDS threat since HAART availability, explained 19.7% of the variance and consisted of 5 related statements with a reliability of 0.84 (Cronbach’s α). The second principal component, perceiving less need for safe sex since HAART availability, explained 16.4% of the variance and consisted of 3 related statements with a reliability of 0.93. The third principal component, general beliefs concerning the start of HAART, explained 13.8% of the variance and consisted of 4 related statements with a reliability of 0.73. The fourth principal component, perceiving high effectiveness of HAART in curing HIV/AIDS, explained 12.5% of the variance and consisted of 2 related statements with a reliability of 0.80.

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Postexposure Prophylaxis-Related Beliefs

To examine the association between knowledge of postexposure prophylaxis and perceptions on AIDS and safe sex, it was first necessary to determine whether respondents were aware of these prophylactic therapies. A “gatekeeper” item was used for this purpose that described “PEP” as “the opportunity for an HIV-negative individual to use antiretroviral therapy for a short period immediately after an unsafe sexual contact or condom failure in order to reduce the risk of HIV infection.” Respondents who answered “no” to the question if they were aware of this opportunity did not complete 6 items measuring PEP-related perceptions.

Again, we used PCA with varimax rotation (assuming no correlation between the factors) to reduce the amount of data, to distinguish 2 principal components (Table 2), each consisting of several related statements. The cumulative variance explained by the 2 components was 76.3%.

Table 2
Table 2
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Reliability analysis was used to confirm internal consistency of scales constructed on the basis of identified principal components. The first principal component, perceiving less HIV/AIDS threat since PEP availability, explained 50.2% of the variance and consisted of 4 related statements with a reliability of 0.89. The second principal component, perceiving high effectiveness of PEP in preventing HIV/AIDS, explained 26.1% of the variance and consisted of 2 related statements with a reliability of 0.65.

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Diagnostic Methods

At each biannual visit, all participants underwent a routine STD examination using standardized procedures.19 Blood samples were analyzed for HIV antibodies (microparticle enzyme immunoassay AxSym HIV-1/2 reagins; Abbott, Santa Clara, CA), syphilis (Treponema pallidum particle agglutination (TPPA)-test; Serodia-TPPA, Fujirebio Inc., Tokyo, Japan), and hepatitis B (anti-HBc and HBsAg, microparticle enzyme immunoassay IMX; Abbott). Microbiologic investigation included testing on gonorrhea (GC-Lect agar plates; Becton & Dickson Europe, Meylan, France) and Chlamydia trachomatis infection (Cobas Amplicor PCR; Roche Diagnostic Systems, Branchburg, NJ).

The examination included testing for urethral, rectal, and oropharyngeal gonorrhea and urethral and rectal C. trachomatis infection.

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Statistical Methods

Univariable and multivariable logistic regression analyses were used to investigate the association between HAART- and PEP-related beliefs and the incidence of STDs. A multivariable logistic regression model was built by including variables with a univariable P value of less than 0.05. P values were calculated using the likelihood ratio test. To investigate the association between HAART- and PEP-related beliefs and new HIV infection, only univariable and exact logistic regression were done because of the small numbers of new HIV cases.

All statistical analyses mentioned in this manuscript were done using SPSS for Windows, version 11.0 (SPSS Inc., Chicago, IL). For exact logistic regression analysis, LogXact-4 for Windows, version 4.1 (Cytel Software Corp., Cambridge, MA) was used.

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Results

Of the originally recruited 286 cohort participants, a total of 247 (86.4%) MSM completed the behavioral questionnaire with the statements concerning PEP and HAART at their third visit. The median age of these 247 MSM was 41 years (interquartile range 34–49), 93.2% were of native Dutch descent, and 45.4% had a high educational level. Ninety-one percent identified themselves as “gay,” and 9% described their sexual orientation as bisexual. The median number of sexual partners during the previous 6 months was 8 (interquartile range 3–20). Regarding HIV serostatus, 14 MSM (5.7%) were HIV-positive and 5 (35.7%) of these men were on antiretroviral therapy at their third visit. Of the 247 MSM, 80 (32.4%) indicated that they knew of PEP.

In total, 151 HIV-negative MSM (52.8% of the original 286 cohort recruits), who participated in all 5 successive cohort visits, were included in this study. These MSM were comparable with all other MSM completing the self-administered questionnaire at the third visit with regard to median age, ethnicity, sexual orientation, number of sexual partners in the previous 6 months, and educational level as well as incidence of STDs and HIV.

Of the 151 HIV-negative MSM, 99 (65.6%) tested negative for any STDs, including HIV infection, at all subsequent visits. Nine (6.0%) MSM had an STD twice or more often, and a total of 7 (4.6%) MSM HIV seroconverted during the study period.

Number and type of prevalent and incident STD and HIV infection detected at the consecutive cohort visits are summarized in Table 3.

Table 3
Table 3
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Highly Active Antiretroviral Therapy-Related Beliefs

Of all MSM, between 4.0 and 32.7% (strongly) agreed with statements in principal component 1 of the HAART-related beliefs. Between 9.0% and 17.3% (strongly) disagreed with statements in principal component 3. These proportions for agreement with statements in principal component 4 were between 4.6% and 5.8%. A rather small minority of men (strongly) agreed with statements in principal component 2 (between 0.6% and 0.7%).

In univariable analyses (Table 4), only 1 treatment-related belief component (perceiving less HIV/AIDS threat since HAART availability) and age were associated with the incidence of STDs. Men who reported less perceived HIV/AIDS threat were more likely to have an STD. Furthermore, older men were less likely to present with an STD. In multivariable analysis, both variables remained independently associated with the incidence of STDs. Extending the model with the nonsignificant variables educational level, ethnicity, and number of sex partners in the previous 6 months, neither had any significant influence nor did it change the already estimated coefficient and its significance.

Table 4
Table 4
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With regard to new HIV infections (Table 5), univariable analysis showed that the treatment belief factor perceiving less need for safe sex since HAART availability was associated with HIV seroconversion. Men who perceived less need for safe sex since HAART availability were more likely to HIV seroconvert.

Table 5
Table 5
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Postexposure Prophylaxis-Related Beliefs

Of all MSM, between 1.6% and 1.7% (strongly) agreed with statements in principal component 1 and between 9.4% and 30.8% (strongly) agreed with statements in principal component 2 of the PEP-related beliefs.

There were no associations between any PEP-related beliefs and the incidence of STDs or new HIV infection.

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Discussion

To our knowledge, this is the first study in which the relationship between the incidence of STDs and HIV infection and HAART- and PEP-related beliefs in MSM was investigated. In this study, we focused on the incidence of STD and HIV diagnoses rather than on self-reported unprotected anal intercourse. Longitudinal data that relate new STD and HIV infections to HAART- and PEP-related perceptions contributes to our understanding of the extensively debated issue regarding the existence of any association between so-called “HIV optimism” and risky sexual behavior in HIV-negative MSM.

In general, MSM in this Rotterdam cohort study were quite realistic about the effectiveness and consequences of HAART and PEP. This has also been reported in other studies.7,8,17 The majority (86.2%) of MSM (strongly) disagreed with belief statements measuring less perceived threat of HIV/AIDS and (strongly) disagreed with the idea that safe sex was less necessary because of the availability of HAART (97.3%) or PEP (90.2%). Only a minority (4.2%) of MSM in our study (strongly) held the belief that new HIV/AIDS treatments can eradicate the virus from a person’s body.

Nonetheless, the results of this study are consistent with the hypothesis that perceiving less HIV/AIDS threat since HAART is associated with more risky sexual behavior, which in turn might lead to a higher incidence of STDs in MSM. Perceived less need for safe sex was associated with HIV seroconversion. Although an association between “perceiving less HIV/AIDS threat since HAART availability” and the incidence of STD was seen, no such an association could be found between “perceiving less need for safe sex since HAART availability” and the incidence of STDs. Possibly as a result of social desirability, some MSM were unwilling to report a tendency toward unsafe sex when participating in our cohort study.

Alternatively, one could assume that “HIV-optimistic” men predominantly participate in sexual networks with a high prevalence of STDs and HIV infection. This seems, however, highly unlikely.

In their Chicago study, Vanable et al. noted a substantial minority of men who reported reduced HIV concern related to treatment advances. Despite the low prevalence of reduced concern, these authors warned that even slightly reduced concern could be associated with a considerable increase in the rate of HIV transmission.8 It is hard to comment on a possible association between PEP-related beliefs and the incidence of STDs and HIV infection, because there was only limited awareness on the availability of PEP in our study.

It is important to be aware that our cohort consisted of MSM from the Rotterdam region who were invited to participate in the study and therefore possibly were not representative of the MSM population at large, either in Rotterdam or in The Netherlands. The cohort of MSM primarily consisted of native Dutch, HIV-negative men in their 40s with a high educational level. Extrapolation of our findings to the total population of MSM should therefore be done with caution.

Despite these limitations, the results of this study have implications for preventive interventions. Even a small minority of HIV-positive MSM who practice unsafe sex may increase the incidence of HIV infection. Reduction in risky sexual behavior therefore needs continued emphasis. The advice on the use of condoms during anal sex is important in the light of (long-term) side effects of HAART and PEP, recent increase in the incidence of HIV infection worldwide, and increasing transmission of drug-resistant HIV-1 strains.17,21,22 Such advice should also include the fact that, whereas treatment progress has been made, there is still no cure for HIV and that some patients are nonresponsive to antiretroviral therapies. Finally, it is necessary to stress the fact that an undetectable viral load does not eliminate the risk of infection.8 Discussing these issues including participants perceptions on HAART is necessary in consultations with either medical specialist or paramedical staff in contact with the patient.

In conclusion, the results of this study showed that, in general, MSM participating in our cohort were realistic on their beliefs on the effectiveness of HAART and PEP. The large majority of participants did not find safe sex less necessary because of the availability of HAART and PEP. Nevertheless, the reported findings are consistent with the hypothesis that a decreased perception of HIV/AIDS threat because of HAART availability might lead to increasing incidence of STD and HIV infections. Therefore, ongoing prevention emphasis on reducing risky sexual behavior by using condoms during anal sex is essential.

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