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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e318231cf2d
Original Study

Unsafe Sexual Behaviors Among HIV-Positive Men and Women in Honduras: The Role of Discrimination, Condom Access, and Gender

Paz-Bailey, Gabriela MD, MSc, PhD*†; Isern Fernandez, Virginia MD, MSc‡; Morales Miranda, Sonia MSc*; Jacobson, Jerry O. PhD§; Mendoza, Suyapa MPH¶; Paredes, Mayte A. MD¶; Danaval, Damien C. PhD∥; Mabey, David MD‡; Monterroso, Edgar MD, MPH**

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Author Information

From the *Center for Health Studies, Del Valle University, Guatemala City, Guatemala; †Tephinet, Inc, Atlanta, GA; ‡London School of Hygiene and Tropical Medicine, London, United Kingdom; §Pan American Health Organization, Bogota, Colombia; ¶Ministry of Health, Tegucigalpa, Honduras; ∥Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, GA; and **Global AIDS Program, Centers for Disease Control and Prevention, Atlanta, GA

The authors thank the Department of Health of Honduras for leading this study and providing permission to use government health facilities. The authors also thank the staff at the participating hospitals; the study participants who made this survey possible; Ron Ballard, Celine Taboy, and Lisa Steele for processing the specimens at the Centers for Disease Control and Prevention STD Laboratory and providing technical advice; the United States Agency for International Development office in Honduras and the Centers for Disease Control and Prevention for funding the study; Kelly Stewart from United States Agency for International Development for her advice and support; and Dr. Armando Medina and Sandra Nuñez for sharing data from the national information system on HIV-positive in care.

Supported by funds from the United States Agency for International Development office in Honduras and the Centers for Disease Control and Prevention and the Network for Research and Training in Tropical Diseases in Central America (NeTropica) under the project No. 06-R-2010.

The findings and conclusions in this paper are those of the authors and do not necessarily represent those of the Centers for Disease Control and Prevention.

G.P.B. conceived and designed the study protocol, supervised data collection, drafted the manuscript and participated in data analysis. V.I.F. conducted data analysis, participated in the preparation of the manuscript and interpretation of findings. S.M.M., S.M., M.P. participated in the study design and conducted data collection. J.J. helped conceptualize the analysis and participated in manuscript preparation and review. D.D. participated in preparing the study flow and conducted all laboratory testing. D.M. and E.M. supervised different aspects of the study. All authors helped to conceptualize ideas, interpret findings, and review drafts of the manuscript. All authors have read and approved the final version of the manuscript.

Correspondence: Gabriela Paz-Bailey, MD, MSc, PhD, 1600 Clifton Road, Atlanta GA, 30333, MS E46. E-mail: gmb5@cdc.gov.

Received for publication March 9, 2011, and accepted August 8, 2011.

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Abstract

Background: We conducted a study among HIV-positive men and women in Honduras to describe demographics, HIV risk behaviors and sexually transmitted infection prevalence, and identify correlates of unsafe sex.

Methods: Participants were recruited from HIV clinics and nongovernmental organizations in Tegucigalpa and San Pedro Sula, Honduras in a cross-sectional study in 2006. We used audio-assisted computer interviews on demographics; behaviors in the past 12 months, 6 months, and 30 days; and access to care. Assays performed included herpes (HSV-2 Herpes Select), syphilis (rapid plasma reagin [RPR] and Treponema pallidum particle agglutination assay [TPPA]) serology, and other sexually transmitted infections by polymerase chain reaction (PCR). Bivariate and multivariate analyses were conducted to assess variables associated with unprotected sex across all partner types in the past 12 months.

Results: Of 810 participants, 400 were from Tegucigalpa and 410 from San Pedro Sula; 367 (45%) were men. Mean age was 37 years (interquartile range: 31–43). Consistent condom use for men and women was below 60% for all partner types. In multivariate analysis, unprotected sex was more likely among women (odds ratio [OR]: 1.9, 95% confidence interval [CI]: 1.2–3.1, P = 0.007), those with HIV diagnoses within the past year (OR: 2.0, 95% CI: 1.1–3.7, P = 0.016), those reporting difficulty accessing condoms (OR: 2.6, 95% CI: 1.4–4.7, P = 0.003), and those reporting discrimination (OR: 1.8, 95% CI: 1.1–3.0, P = 0.016).

Conclusions: Programs targeting HIV-positive patients need to address gender-based disparities, improve condom access and use, and help establish a protective legal and policy environment free of stigma and discrimination.

Worldwide there have been dramatic gains achieved in increasing access to highly-active antiretroviral therapy (HAART) for people with HIV in low- and middle-income countries—from 0.3 million individuals on treatment in 2002 to 5.3 million people in 2009.1–4 Based on recent findings on the impact of antiretroviral treatment to prevent HIV transmission,5 broadening treatment access continues to be a public health priority, which will have the potential to bring more individuals with HIV within the reach of additional health care, support, and prevention services. Antiretroviral treatment for prevention will have to be complemented with other successful strategies.6 The World Health Organization released new guidelines for integrating prevention as a routine part of HIV management in resource-limited settings which reaffirms prevention for people with HIV as an international priority for HIV control.4

Little is known about the profiles of people with HIV in most areas where HAART has become available. Information is scarce outside the context of controlled trials or from regions other than Africa.7–9 Relatively high levels of sexual activity (84%) and recent unprotected sex (25%–39%) have been reported in studies among men in Brazil and men and women at selected HIV treatment centers in urban areas of Brazil and Argentina.10,11

Although two-thirds of the estimated 1.7 million people with HIV in Latin America live in the largest countries (Argentina, Brazil, Colombia, and Mexico), the smaller Central American countries present the highest HIV prevalence. Honduras, with just 18.0% of the Central American population, accounted for 38.5% of the 45,621 cases of AIDS reported regionally during 2005.12 Public provision of antiretroviral treatment for HIV began with 200 patients in Honduras in 2002, scaling up rapidly to 4072 patients at 22 comprehensive HIV treatment centers by 2006, equivalent to 42% coverage of those eligible for HIV treatment.12,13 To date, HIV surveillance to build understanding of transmission risk behaviors in Honduras and other Central American countries has primarily monitored groups vulnerable to HIV infection as opposed to people currently infected with HIV.

In Central America as elsewhere, many people living with HIV suffer from stigma and discrimination, especially those already marginalized by gender, race and socioeconomic status, or sexual identity.14 Stigma amplifies the complexities of living with HIV.14 Moreover, there is some empirical evidence that stigma, discrimination, and fear of both may contribute to an increase in HIV-related risk behaviors among the HIV-positive and HIV-negative populations.15–17 Policy recommendations by international organizations have advocated for a human rights approach to treatment, prevention, support, and care, that stresses the need for interventions aimed at reducing stigma against people living with HIV.18

This article describes findings from the first survey of people with HIV in Central America. We describe transmission risk behaviors, knowledge of HIV transmission and prevention, experiences of stigma and discrimination, and infection with other sexually transmitted infection (STI). We explore correlates of unprotected sex, including self-reported discrimination and other factors.

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METHODS

Study Population and Enrollment

The study was conducted in 2006 in the two principal cities of Honduras—Tegucigalpa, the political capital; and San Pedro Sula, the nation's industrial and business capital and considered the epicenter of the HIV epidemic. Together, these cities account for 70% of HIV-positive persons on care and treatment in the country.12 Participants were HIV-positive men and women living or receiving care or treatment in the two cities, that is, those aged 18 years or older with a documented positive HIV test result and willing and able to provide written informed consent. In each city, clinical, public-sector HIV service providers and nongovernment organizations (NGOs) working with people with HIV were identified by the Honduran Ministry of Health's National HIV/AIDS Program and by iterative consultations with known sites to identify additional sites. The number of people with HIV selected into the study from each HIV service provider and NGO was determined proportional to size based on the current patient register. Participant selection at each site was carried out using consecutive sampling. All clients arriving for HIV care or treatment services received an envelope that determined if they would participate or not in the study based on a list of random numbers, designed to achieve the predetermined sampling fraction during similar data collection periods across sites. Clients selected were offered referral to the HIV reference hospital in each city, Hospital del Torax in Tegucigalpa and Hospital Mario Catarino Rivas in San Pedro Sula, for eligibility determination, informed consent, and enrollment.

We planned for a sample size of 200 men and 200 women in each city, 400 per city, for a total of 800 participants, based on feasibility of recruitment, ability to detect differences between cities, and by sex, provided 80% power, a level of significance (α) of 5%, and a design effect of two.

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Study Procedures

Written informed consent was obtained from all participants. Each interview included an audio computer-assisted interview (ACASI) and collection of specimens for testing of STI. Interviewers were trained peer outreach workers. Using ACASI, participants viewed the survey questions on a computer screen while listening to audio recordings of the questions using headphones and entered their answers using the computer keyboard. The study questionnaires elicited information on demographics, sexual behavior in the past 12 months, 6 months, and 30 days; knowledge about HIV; health-seeking behaviors; lifetime and past-year use of alcohol and drugs, including injected drugs; as well as perceptions of experienced stigma and discrimination related to HIV status. Questionnaires for most at-risk populations used in previous studies in Honduras and those used in research supported by the US Centers for Disease Control and Prevention were used as a basis for the Honduras instrument. The questionnaire was standardized for the different survey populations and with instruments used by similar studies in other countries in the region.

Following the consent process and computer interview, study staff provided STI counseling and collected biologic specimens. A nurse or doctor conducted a physical examination to evaluate signs and symptoms of STI. Female participants received a pelvic examination during which vaginal swabs were collected. Male participants provided a urine specimen. Blood specimens were collected by a trained phlebotomist. First-catch urine (for men) and vaginal samples were screened using an in-house real-time PCR for STIs. Detection of Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium and Trichomonas vaginalis in urine (for men) and vaginal swabs (for women) was done using a multiplex real-time PCR. STI PCR testing was done at the STI Laboratory of the Centers for Disease Control and Prevention. Blood samples were tested for syphilis and HSV-2. Syphilis seropositivity was based on reactive RPR confirmed with a positive TPPA result. Active syphilis was defined as an RPR titer ≥1:8 and a reactive TPPA result. HSV-2 serology was performed with the HerpeSelect (Focus Technologies, Cypress, CA). Serology testing was done at the National Laboratory in Honduras. STI test results were provided within 4 weeks through the participating hospitals. Free treatment was provided to participants with STI symptoms or a laboratory-diagnosed STI. The study protocol was reviewed by the CDC Associate Director for Science who deferred approval to the Ethics Review Committee of the Autonomous National Honduras University.

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Measures

To assess knowledge of HIV transmission, the Joint United Nations Programme on HIV/AIDS (UNAIDS) indicator was used,19 which included the following questions: (1) Can having sex with only one faithful, uninfected partner reduce the risk of HIV transmission? (2) Can using condoms reduce the risk of HIV transmission? (3) Can a healthy-looking person have HIV? (4) Can a person get HIV from mosquito bites? (5) Can a person get HIV by sharing a meal with someone who is infected? Having correct knowledge was defined as providing the correct answer to all 5 questions among respondents who gave answers. To assess if patients had unprotected sex in the past 12 months, we considered variables on consistent condom use and condom use during past sexual encounter for all partner types. The study outcome was unprotected sex with any partner in the past year, measured as self-report of less than consistent condom use in the past 12 months with either regular, casual, or commercial partners.

The self-stigma variable was a dichotomous variable constructed based on 4 questions. If answering yes to any of the following, the participant was classified as experiencing self-stigma: avoiding friends, avoiding family, not presenting a work or school application, and/or avoiding medical care because of HIV serostatus. Regarding HIV-related discrimination, participants were asked whether they have ever felt discriminated against because of their serostatus. We further inquired what type of discrimination they had suffered and by whom (relatives, friends, or colleagues, community members, and health care providers). A series of questions also inquired about discrimination experiences in health care facilities. For the bivariate and multivariate analysis, we used the binary indicator of reported discrimination.

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Data Analysis

Data are presented pooled across cities as no major differences were detected across study sites. Descriptive analysis was performed separately by sex. χ2 tests were used to test for differences between men and women for categorical variables and t tests were used to test differences on continuous variables following Shapiro–Wilk tests to assess normality. Ninety-five percent confidence intervals (95% CI) were estimated for percentages in univariate analysis.

We developed a logistic regression model predicting the dichotomous outcome, unsafe sex in the past year, among participants reporting past-year sexual activity. Models were built using a backward selection procedure. A variable was retained in each model if the P-value obtained from a likelihood ratio test was less than 0.05. Variables considered potential confounders, as well as city and sex, were also included. Associations are reported as odds ratios (ORs) with 2-sided P-values and 95% CI. Interactions of all variables with sex and city were also evaluated given the possibility of varying effects by sex and location. Data were analyzed using the statistical software program Stata, version 7 (Stata Corporation, College Station, TX).

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RESULTS

A total of 810 HIV-positive individuals were enrolled in the study, 400 from Tegucigalpa and 410 from San Pedro Sula. Among all participants, 367 (45.3%) were men and 443 (54.7%) were women, and the mean age was 37 years (interquartile range: 31–43). Nearly half of the participants (45.4%) had little formal education and less than half (43.3%) were employed at the time of the interview. The majority of participants (77.8%) had been diagnosed with HIV for a year or longer, and 84.0% were receiving antiretroviral treatment. Any drug use in the past year was reported by 24.0%, primarily involving marijuana (37.4%), cocaine (28.6%), and crack (11.8%). Only 2.8% (23/810) of participants reported ever injecting drugs; yet 30.4% (7/23) of these reported sharing injecting equipment during last injection (Table 1).

Table 1
Table 1
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Most participants also reported being sexually active in the past 12 months (62.9%), and this was higher for men (69.5%) than women (57.7%) (P = 0.001). Past-year risk behaviors and conditions influencing vulnerability among those sexually active also varied by sex. Nearly 1 in 5 men (17.7%) reported paying for sex in the past year compared with 3.8% of women (P < 0.001); close to 5% of men and women had ever sold sex and just 1.6% to 1.7% were currently involved in sex work. A high proportion reported being forced to have sex in the past 12 months (9.5% of men and 17.4% of women, P = 0.014). Men in the sample were more likely to report past-year casual, noncommercial partners (61.2%) than women (37.0%) (P < 0.001). Twenty percent of men reported having sex with another man in the past year. Among men who reported sex with another man, 23.3% reported forced sex ever.

Participants reported relatively low levels of consistent condom use, which, among men, was similar across all partner types. With regular partners, 58.8% of men and 38.1% of women reported consistent condom use (P < 0.001); with casual partners these percentages were 60.3% and 42.4% (P = 0.095), respectively; for commercial partners they were 59.5% and 54.6% (P = 0.702), respectively. Regarding reasons for not using condoms, men reported being drunk (23.6%), having sex with regular partners (23.6%), having oral sex (14.7%), and relatively few cited having a partner known to be infected with HIV (9.0%). Among women, the principal reasons were having sex with regular partner (43.4%), a partner known to be infected with HIV (19.6%) and being drunk (10.3%). When asked specifically about regular partners, 51.0% of women reported not using condoms because their partners refused to use them. Overall, nearly 1 in 5 participants (19.8%) reported that condoms were difficult to obtain; reasons included embarrassment when purchasing condoms (69.8%), cost (18.8%), or unavailability at the health center where the participant received HIV monitoring (17.0%), indicating problems with access to condoms.

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STI Prevalence

HSV-2 seroprevalence was considerably high among study participants, with 84.8% of females and 71.2% of males infected (P < 0.001). Prevalence of most bacterial STI, however, was relatively low (Table 2). Overall, 1.4% had chlamydial infection, 1.2% had syphilis, and 0.2% had gonorrhea. Mycoplasma genitalium was higher among women (16.1%) than among men (6.9%) (P < 0.001), as was trichomoniasis at 8.1% and 1.4%, respectively (P < 0.001).

Table 2
Table 2
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Discrimination

Most participants reported having experienced discrimination because of their HIV infection. More than 1 in 5 said their employment was terminated following disclosure of their HIV status (22.5%). About 13.2% reported being abandoned by their family as a result of their HIV status, 11.8% were forced to eat alone and 8% to use different cutlery. Some also said they had been denied renting a house (10.8%) or removed from their residence (10.2%). In relation to health services, 10.3% reported feeling discriminated against at public health facilities and 4.8% reported denial of treatment or other health care because of their HIV status. Self-stigma was reported by more than one-third of participants (36.3%) with no difference by sex.

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Factors Associated With Unprotected Sexual Intercourse

We evaluated variables associated with unprotected sex among 457 sexually active individuals (Table 3). In bivariate analysis, female sex, being unemployed, having been diagnosed with HIV less than 12 months ago, having only regular partners in the past 12 months, reporting difficulty accessing condoms, having suffered discrimination, and self-stigma, were associated with increased unprotected sex. In multivariate analysis (Table 4, n = 324), unprotected sex was more likely among women (OR:1.9, 1.2–3.1, P = 0.007), those with HIV diagnoses within the past year (OR: 2.0, 95% CI: 1.1–3.7, P = 0.016), those reporting difficulty accessing condoms (OR: 2.6, 95% CI: 1.4–4.7, P = 0.003), and those reporting discrimination (OR: 1.8, 95% CI: 1.1–3.0, P = 0.016).

Table 3
Table 3
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Table 4
Table 4
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DISCUSSION

This is the first study among HIV-infected people in Central America to evaluate HIV knowledge, risk behaviors, and STI prevalence, providing essential information to inform prevention initiatives. The study demonstrated that it was feasible to collect biologic specimens and to administer interviews through ACASI in this population.

We confirmed our hypothesis that discrimination was associated with unprotected intercourse. Stigma and discrimination may contribute to the spread of HIV through various pathways.20 In generalized epidemics, stigma and discrimination may lead some HIV-infected mothers to opt for breast-feeding instead of formula feeding because the latter would raise suspicion about their serostatus.21 Second, stigma induces delays in HIV testing and nondisclosure of seropositivity to sexual partners that could both result in further transmission of HIV.16 Third, perceived stigma is also correlated to poor adherence to HAART,22 and poor adherence results in the development and transmission of drug-resistant strains of HIV.23 In addition to prevention efforts to reduce high-risk behaviors such as unprotected sex, buying and selling of sex, and injecting drug use, it is imperative to address vulnerability and risk related to discrimination against HIV-positive individuals.

Importantly, we found high rates of unprotected sex among sexually active HIV-positive men and women with relatively few individuals citing a relationship with a partner of known HIV status as a reason for not using condoms. Furthermore, among sexually active participants, two-thirds of men and nearly 40% of women reported having a recent casual sex partner. There was no evidence that safe sex was practiced more often with casual or commercial sex partners. Condom access was the most important predictor of unprotected sexual intercourse and often cited as a reason for not using condoms. Honduras could learn from successful experiences with structural-level condom distribution interventions elsewhere. These interventions have been shown to be efficacious in increasing condom use, increasing condom acquisition, or condom carrying among a wide range of populations including youth, female sex workers, adult males, STD clinic patient attendants, and others.24 Interventions that combine with additional individual-, group-, or community-level activities have shown the greatest efficacy. These activities will also need to address different behavioral determinants as well as other prevention needs, including the reduction in casual partners.

People who were aware they were HIV infected for more than 1 year had safer practices, which may indicate that changes in behavior with knowledge of HIV status might be improved over time, as in other settings.8 Women differed from men in our study in many aspects. They had less formal education, were less likely to be employed, and more likely to report sexual abuse and discrimination. They were less likely to report risk behaviors such as drug use and casual sex, but more likely to report unprotected sex. These gender differences should be considered when designing interventions for people with HIV in Honduras. Importantly, there are likely gender power imbalances that affect the ability of women to effectively negotiate condom use.25–27

Our study may not be representative of all HIV-positive individuals in Honduras, as recruitment was from public HIV service providers and NGOs in two cities and may not represent patients in private care and other regions. The randomization procedure, which involved opening sequential envelopes, may have been vulnerable to staff bias. However, we found that the study population was similar to the clinic population based on 2009 information available from an electronic system in terms of age, education, employment, and marital status (Sandra Nunez, HIV AIDS Program, Honduras Ministry of Health, personal communication). Moreover, some participants with STI-positive test results reported that they were not sexually experienced, suggesting either misclassification caused by social desirability bias, imperfect specificity of laboratory test results, or contamination of specimens. Misclassification by study participants has been reported frequently in population-based surveys and other behavioral surveys among specific groups and is a common limitation of research that relies on self-report.28,29 The use of ACASI may lead to an increased, but not necessarily complete, reporting of stigmatized behaviors. The misclassification of participants' sexual activity may lead to underestimation of high-risk behaviors and a decreased ability to detect significant associations with condom use and STI.

Together, our findings suggest a pressing need to strengthen positive prevention interventions in Honduras. Interventions should address the specific needs of the different subgroups such as newly diagnosed persons, MSM, and women, and should be based on a comprehensive framework of meeting individuals' health, social, and prevention needs in a context of empowerment and dignity.18 There is global consensus on the importance of tackling AIDS-related stigma and discrimination.30 Not only is HIV-related discrimination a human rights violation, but it is also necessary to address such discrimination and stigma in order to achieve public health goals and overcome the epidemic.14 Confronting stigma and discrimination is a prerequisite for effective prevention and care.

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