Barriers and facilitators to past six-month HIV testing among men who have sex with men in Belize

Abstract

Prevalence of HIV in Belize is high, and men who have sex with men (MSM) are disproportionately impacted by HIV. HIV testing is critical in curbing the epidemic; however, little is known about factors associated with testing among MSM in Belize. Working with a non-governmental organization in a large, urban city within Belize, snowball sampling was applied to recruit Belizean MSM to complete a self-administered survey. Multivariable logistic regression analysis was employed to understand associations with HIV screening behavior. Access to healthcare, HIV knowledge, and reporting having heard of Section 53 of the Criminal Code of Belize (once outlawing same-sex sexual behavior), but not experiencing any negative impact from Section 53 were significantly positively associated with having received an HIV test in the past six months. Healthcare maltreatment (lifetime), depression symptomology, and shame were significantly negatively associated with having received a HIV test in the past six months. Findings suggest that multiple factors associated with stigma and discrimination negatively affect testing strategies among MSM in Belize.

Keywords

Homosexual men screening human immunodeficiency virus North America

Introduction

With 1.4% of adults living with HIV, the HIV prevalence of Belize exceeds the average prevalence of Latin America and the Caribbean (0.4%).¹ Given this fact, Belize remains an important focus for HIV prevention efforts in Latin America and the Caribbean. In 2012, in order to better understand the HIV epidemic in Belize, the Ministry of Health conducted a study to estimate the prevalence of HIV among groups considered most at risk for HIV, including men who have sex with men (MSM), female sex workers (FSWs) and youth under age 25. According to the results of this study, 13.9% of MSM in Belize were living with HIV compared to 0.91% of FSWs and 0.6% of youth under age 25 sampled, illustrating that MSM may have social vulnerabilities in the context of the HIV epidemic in Belize.² Based on this finding, MSM should be a priority population for research and interventions that address HIV incidence in Belize.² While there are no published annual estimates of HIV incidence of MSM in Belize, the Ministry of Health is considering initiating a population estimation study to provide annual estimates and situational analyses for MSM and transgender women.³

Increasing HIV testing among Belizean MSM could be an effective way to lower new infections in this population. Early HIV diagnosis and initiation of anti-retroviral therapy (ART) among MSM living with HIV are parts of the World Health Organization’s (WHO) recommendations for HIV prevention among MSM globally.⁴ HIV testing is imperative for diagnosing people living with HIV (PLHIV). As diagnosis is the first step of HIV treatment, HIV testing also serves as a way to link PLHIV to treatment, ensuring future retention in HIV care, adherence to ART, and ultimately viral suppression. This method of treatment as prevention (TasP) is widely accepted as an effective way to reduce HIV incidence.⁵ Despite the importance of HIV testing in relation to timely diagnosis and treatment initiation, little is known regarding HIV testing habits as well as factors associated the HIV testing among MSM in Belize. Due to Belize’s anti-LGBT laws,⁶ no research related to HIV has been conducted in this population.⁶

HIV testing in Belize is conducted through HIV voluntary testing and counseling centers in municipal districts throughout the country. HIV testing is offered for free in public health facilities and non-governmental organizations (NGOs) throughout the country.⁷ Though little is known regarding factors associated with HIV testing among Belizean MSM, information regarding HIV testing among MSM in other Latin American and South American countries may point to potential barriers and facilitators to HIV testing among MSM in Belize. In general, barriers to HIV screening in Latin America include fear of discrimination and stigma in healthcare settings.^8,9 In Brazil, younger age, lower socioeconomic status, lower educational achievement as well as a lack of access to health care and poor HIV knowledge were associated with lower testing among MSM¹⁰ while data from El Salvador suggest that HIV testing stigma and healthcare discrimination are associated with lower HIV testing.¹¹ The 2015 National HIV Commission of Belize report identified the need to increase the study of MSM, but noted that existing determinants and factors of HIV infection included inconsistent comprehensive sexuality education throughout the country, lowered condom use from 2010 estimates, poverty, the existence of the criminal code and the exclusion of MSM “in the various domains of life”, discrimination and harassment against MSM and transgender women, including in healthcare settings, and the internalization of stigma.³ The current HIV-TB strategic plan for Belize notes that the country should “expand the network of nurses and physicians who are MSM-friendly”.³

Section 53 of the Belize Criminal Code previously banned “carnal intercourse against the order of nature”—essentially banning intercourse between lesbian, gay, bisexual, and transgender (LGBT) individuals. Previous research on LGBT criminalization from 115 countries and its relation to HIV services has found MSM living under these laws have lower access to HIV testing and greater perceived stigma and shame when compared to MSM where there is no LGBT criminalization.¹² Though overturned in 2016,¹³ the impact of the policy may have lasting effects.¹⁴ Because of this, depression, internalized homophobia (IHP), and experiences of shame should also be evaluated in addition to knowledge and negative impact from the law itself. Additionally, because of the social-political climate of Belize, social support should also be evaluated as peer-driven approaches to HIV testing referral have been effective in communities with high prevalence of undiagnosed HIV.¹⁵

The present analysis aims to fill the aforementioned gaps by (1) identifying prevalence of past six-month HIV testing among HIV-negative MSM in Belize; and (2) exploring whether the following items are associated with past six-month HIV testing among MSM in Belize: healthcare access, healthcare maltreatment, depression, IHP, HIV knowledge, experiences of shame, social support, and impact of Section 53.

Methods

Sample

From July 2016 through December 2016, MSM in Belize were recruited to the study in the setting of a local NGO in Belize City. The overall study included individuals who (1) were 18-years of age or older; (2) were citizens or permanent residents of Belize; (3) had sex with a male partner in the past year; and (4) identified as male. While the larger study included MSM who identified as HIV-negative and MSM living with HIV, the current analysis includes only those who self-identified as HIV-negative.

Design

This pilot study used a social network-based approach to recruitment. Similar to previous studies^15–17 the use of recruitment seeds allowed this pilot study to contact MSM in Belize. A local NGO with a history of serving MSM in Belize identified individuals using their services to assist as recruitment seeds. The National HIV Commission acknowledged in their 2015 report that MSM in Belize are “likely an aggregation of a number of diverse sub-populations”; therefore, researchers worked with the local NGO to develop a recruitment strategy for MSM using terms known to the community. In order to ensure diversity of study participants, three individuals from each of the following six subpopulations of MSM in Belize were recruited to serve as recruitment seeds: 1) open (i.e., public about sexual orientation and identifies as gay); 2) closeted (i.e., identifies as gay but is not public about this identity); 3) effeminate (i.e., appears feminine, may include transgender individuals); 4) sex worker (i.e., identifies as heterosexual but have sex with men in exchange for goods or money); 5) straight (i.e., identifies as straight but has sex with men as a top only); 6) bisexual (i.e., may or may not identify as gay, but has sex with both male and female partners). Seeds were informed of the objectives and methods of the study and provided verbal informed consent. Additionally, seeds were required to sign a confidentiality agreement in order to ensure participant anonymity, and therefore safety. Seeds were given five vouchers to provide to members of their social networks in order to refer individuals to participate in the study. Seeds were compensated $5 on a pre-paid phone card for successfully recruiting one or more participants.

Potential participants were referred to the local NGO where they presented their voucher to study staff. They were provided an overview of the study goals, procedures and potential uses for study data and asked to provide verbal informed consent in order to mitigate the risk that any questionnaire or form could be linked to an individual. Participants had the option of completing a self-administered paper survey in English or having a member of the study team assist them in survey completion. Upon completion of the survey, participants were compensated $10 and invited to serve as recruitment seeds in the same manner described above. All study procedures were approved by the University of Pittsburgh Institutional Review Board.

Measures

Demographics

Participants were asked about their age, sexual orientation, education status, and ethnicity. Age was measured in years. Sexual orientation was assessed with two categories: gay and other. Two levels were used to measure education: high school degree or less and more than a high school degree. Three categories were used to assess ethnicity: Creole, Mestizo, and other.

Past six-month HIV testing

Past six-month HIV testing was assessed with two questions: “Have you ever been tested for HIV?” with responses “yes/no;” and “How often do you test for HIV?” with the following response options “every month,” “every three months,” “every six months,” “yearly,” “every two years,” and “more than two years.” Participants were assigned as having had received an HIV test in the past six months if they responded (1) every month; (2) every three months; or (3) every six months to this question. Participants were assigned as having not received an HIV test in the past six months if they responded (1) yearly; (2) every two years; or (3) more than two years to this question, or if they indicated they had never received an HIV test.

Health care access, past year

Past-year health care access was assessed with one question, “In the last 12 months have you accessed any health services, public or private for any reason?” with response options “yes/no.”

Healthcare maltreatment, lifetime

Lifetime healthcare maltreatment was assessed with one question: “Have you ever been maltreated in a health center or by a health professional?” with response options “yes/no.”

Depression symptomology

The PHQ-9 measured depression symptoms using a 9-item scale that ranged from 0 to 27.¹⁸ Consistent with the literature, individuals were assigned a depression score, and were subsequently coded as having any depression (i.e., mild, moderate, major) if they scored five or more on the PHQ-9 scale (alpha = 0.846).

Internalized homophobia

Herek’s internalized homophobia (IHP) scale was used to evaluate IHP.¹⁹ Consistent with existing literature, individuals were assigned a continuous IHP score from the sum of their responses to scale questions.^20,21 Scores ranged from zero to 34 (alpha = 0.954).

HIV knowledge

A 25-item adapted version of the HIV Knowledge Questionnaire was used to assess HIV knowledge.²² A continuous HIV knowledge score was assigned to each participant based on their responses to the 25 questionnaire items.²² Scores ranged from 10 to 25 (alpha = 0.683).

Shame

Participants were assigned a shame score based on their responses to the 25-item Experiences of Shame Scale.²³ Scores ranged from 18 to 91 (alpha = 0.963).

Friend support

Friend support was measured with the Multidimensional Scale of Perceived Social Support Friend Subscale.²⁴ Scores ranged from four to 28 (alpha = 0.903).

Family support

Family support was measured with the Multidimensional Scale of Perceived Social Support Family Subscale.²⁴ Scores ranged from four to 28 (alpha = 0.860).

Impact of Section 53 of the criminal code of Belize

The impact of Section 53 of the Criminal Code of Belize on the lives of participants was evaluated with four questions developed by a resident researcher with the local NGO: (1) “Do you know what Section 53 of the criminal code of Belize states?” with response options “yes/no;” and (2) “How often do you think that Section 53 negatively affects your professional life?” (3) “How often do you think that Section 53 negatively affects your capacity to date/find a partner?” and (4) “How often do you think that Section 53 negatively affects your daily life?” with response options: “never;” “almost never;” “sometimes;” “fairly often;” “very often.” Participants were assigned to three different groups: 1) No knowledge of Section 53 if they answered “no” to the question “Do you know what section 53 of the criminal code of Belize states?”); 2) No negative impact from Section 53 if they answered “yes” to this question and answered “no” to the next three questions; and 3) Negative impact from Section 53 if they answered “yes” to any of the next three questions.

Analysis

Basic frequencies were used to assess the prevalence of MSM who had received an HIV test in the past six months. Bivariate analysis using chi-square tests for categorical variables and t-tests for continuous variables were used to determine what differentiates MSM who had received an HIV test in the past six months to those who had not on the following items: healthcare access, healthcare maltreatment, depression, internalized homophobia, HIV knowledge, experiences of shame, social support, and impact of Section 53. Multivariable logistic regression analyses further explored the relationship of items found to be significant in bivariate analysis with past six-month HIV testing. The first model was designed to understand differences in sociodemographic factors (e.g. sexual orientation, education) on HIV screening in the past six months. Subsequent models were used to understand the significance of variables (e.g. healthcare access, HIV knowledge) on past six-month HIV screening while controlling for sexual orientation identity, education, ethnicity, and age. Significance was set to alpha ≤0.05. We conducted analyses in SAS version 9.4 (SAS Institute, Inc., Cary, NC).

Results

Of the 306 MSM who completed the survey, 251 met the inclusion criteria for this analysis of self-reported, HIV-negative men. Fourteen (5.6%) were missing information for one or more of our measures of interest, and these cases were deleted using listwise deletion yielding an analytic sample of 237 MSM. As shown in Table 1, 81.9% of MSM reported having received an HIV test in the past six months. The majority of participants identified as gay (83.1%), reported past-year healthcare access (70.5%), and had received a high school degree or less (50.6%). When asked about Section 53, 33.8% reported having never heard of it; 40.5% reported having heard of it but experienced no negative impact from it; and 25.7% reported some negative impact from Section 53.

Table 1.

Characteristics of men who have sex with men in Belize, 2016.

	Total sample, n = 237% (n)
Sexual orientation identity
Gay	83.1 (197)
Other	16.9 (40)
Education
High school degree or less	50.6 (120)
More than a high school degree	49.4 (117)
Ethnicity
Creole	36.7 (87)
Mestizo	52.7 (125)
Other	10.6 (25)
Age in years, mean (sd)	26.7 (6.5)
Health Care
Healthcare access, past-year	70.5 (167)
Maltreatment when accessing care, lifetime	9.3 (22)
Depression symptomology	36.3 (86)
Internalized homophobia, mean (sd)	6.3 (6.4)
HIV knowledge, mean (sd)	20.3 (2.8)
Shame, mean (sd)	33.4 (12.1)
Social support
Friend, mean (sd)	13.6 (5.8)
Family, mean (sd)	13.5 (5.2)
Section 53
Never heard of Section 53	33.8 (80)
No negative impact from Section 53	40.5 (96)
Any negative impact from Section 53	25.7 (61)
Past six-month HIV testing	81.9 (194)

Note: sd = standard deviation.

Table 2 shows results from bivariate analysis. Younger age was significantly associated with past six-month HIV testing (p = 0.006). MSM who reported past-year healthcare access were significantly more likely to have received an HIV test in the past six months (p = 0.007). MSM who reported lifetime healthcare maltreatment (p < 0.001) and depression symptomology consistent with minor, moderate, and major depression (p < 0.001) were less likely to have received an HIV test in the past six months. MSM reporting higher levels of social support from friends (p = 0.044) and greater HIV knowledge (p < 0.001) were significantly more likely to have received an HIV test in the past six months, while MSM reporting higher levels of shame (p < 0.001) were significantly less likely to have received an HIV test in the past six months. MSM who had never heard of Section 53 were significantly less likely to have received an HIV test in the past six months (p < 0.001).

Table 2.

Correlates of past six-month HIV testing among men who have sex with men in Belize, 2016.

	Tested in past six months, n = 196 % (n)	No test in the past six months, n = 43 % (n)	p
Sexual orientation identity
Gay	82.0 (159)	88.4 (38)	0.310
Other	18.0 (35)	11.6 (5)
Education
High school degree or less	52.0 (101)	44.2 (19)	0.350
More than a high school degree	48.0 (93)	55.8 (24)
Ethnicity
Creole	35.6 (69)	41.9 (18)	0.662
Mestizo	54.1 (105)	46.5 (20)
Other	10.3 (20)	11.6 (5)
Age in years, mean (sd)	26.2 (6.2)	29.2 (7.5)	0.006
Healthcare
Healthcare access, past-year	74.2 (149)	53.5 (23)	0.007
Maltreatment when accessing care, lifetime	6.2 (12)	23.3 (10)	<0.001
Depression symptomology	31.4 (61)	58.1 (25)	0.001
Internalized homophobia, mean (sd)	6.1 (6.4)	7.1 (6.1)	0.357
HIV knowledge, mean (sd)	20.8 (2.4)	18.4 (3.1)	<0.001
Shame, mean (sd)	31.9 (11.8)	40.0 (11.5)	<0.001
Social support
Friend, mean (sd)	13.8 (5.3)	12.0 (4.5)	0.044
Family, mean (sd)	13.5 (5.6)	14.3 (6.8)	0.376
Section 53
Never heard of Section 53	29.9 (58)	51.2 (22)	<0.001
No negative impact from Section 53	46.4 (90)	14.0 (6)
Any negative impact from Section 53	23.7 (46)	34.9 (15)

Note: N = 237; sd = standard deviation.

When controlling for sexual orientation identity, education, ethnicity, and age in multivariable models (Table 3), access to healthcare (adjusted odds ratio [aOR] = 2.23, 95% confidence interval [CI]: 1.08, 4.60), higher levels of HIV knowledge (aOR = 1.32, 95% CI: 1.16, 1.49), and reporting having heard of Section 53 but experiencing no negative impact from Section 53 (aOR = 6.13, 95% CI: 2.27, 16.54) were significantly positively associated with having received an HIV test in the past six months. Lifetime healthcare maltreatment (aOR = 0.22, 95% CI: 0.08, 0.57), depression symptomology (aOR = 0.27, 95% CI: 0.13, 0.55), and shame (aOR = 0.94, 95% CI: 0.91, 0.96) were significantly negatively associated with having received an HIV test in the past six months.

Table 3.

Multivariable logistic regression comparison of MSM who had received an HIV test in the past six months to those who had not received an HIV test in the past six months: Belize, 2016.

	Received an HIV test in the past six months, aOR (95% CI)
Model 1
Sexual orientation identity
Gay	Referent
Other	2.44 (0.83, 7.15)
Education
High school degree or less	Referent
More than a high school degree	0.83 (0.41, 1.66)
Ethnicity
Creole	Referent
Mestizo	1.19 (0.57, 2.46)
Other	0.93 (0.29, 2.95)
Age	0.93 (0.89, 0.98)*
Model 2
Accessed health care	2.23 (1.08, 4.60)*
Model 3
Health care maltreatment	0.22 (0.08, 0.57)*
Model 4
Depression symptomology	0.27 (0.13, 0.55)*
Model 5
HIV knowledge	1.32 (1.16, 1.49)*
Model 6
Shame	0.94 (0.91, 0.96)*
Model 8
Friend support	1.07 (0.99, 1.15)
Model 9
Section 53
No knowledge	Referent
No negative impact	6.13 (2.27, 16.54)*
Negative impact	1.25 (0.55, 2.83)

Note: N=237; aOR = adjusted odds ratio; CI = confidence interval; Models 2-9 controlled for sexual orientation, education, ethnicity, and age.

*p<0.05.

Discussion

The findings of this study of Belizean MSM suggest consistency with other Latin American countries that healthcare access and HIV knowledge were associated with HIV screening in the previous six months.^10,25 Younger MSM in Belize were more likely to report being screened, perhaps indicating a lessening effect of Section 53, given that a 2014 study of MSM in the Caribbean noted greater stigma and less testing among younger MSM.²⁶ This result may also be due to the localized strategy that is being used by the Ministry of Health. According to the 2016 annual HIV report, data from 2010–2015 indicated that while women were twice as likely to test for HIV, nearly two-thirds of new diagnoses were in men; thus shifting the HIV testing focus to men in Belize.²⁷ The same report also noted that the Ministry of Health wanted to focus on early intervention by testing likely groups through targeted radio and television advertisements.²⁷ Further, awareness of Section 53 with no negative impact from Section 53 was associated with HIV screening in the previous six months. Depression symptomology, lifetime healthcare discrimination and perceptions of shame appeared to deter MSM from screening as suggested in previous literature.²⁸

Interventions aimed at increasing past six-month HIV testing among MSM in Belize could focus on reducing shame, depression, and healthcare maltreatment. While Section 53 banning gay, lesbian, bisexual, and transgender relationships was overturned in 2016, the stigma and discrimination this law fueled has not vanished. A study published in 2017 sampling populations from seven Caribbean countries found that people in Belize were less likely to hate homosexuals than in comparative counties such as St. Lucia and Guyana, although gender differences did occur. Men were not only more likely to express hate toward homosexuals, but also were less likely to socialize with homosexuals, even when they tolerated or accepted homosexuals.²⁹ Because such discrimination and stigma can in turn lead to depression and shame,³⁰ interventions designed to address homophobia and normalize the lives and relationships of MSM in Belize are likely needed to increase the prevalence of past six-month HIV testing.³¹ Along these lines, given the negative association of healthcare maltreatment with past six-month HIV testing, providing cultural competency trainings designed to increase understanding of the lived experiences of MSM in Belize could possibly increase the prevalence of past six-month HIV testing. Finally, efforts to increase HIV knowledge as well as access to medical care could increase past six-month HIV testing.

Limitations

Though our study has several strengths, it is not without weaknesses. First, while the utilization of social networks and recruitment seeds produced one of the largest samples of Belizean MSM ever assembled, it is not representative of all MSM in Belize. Though great effort was taken to ensure diversity of recruitment seeds, most seeds had a previous relationship with the local NGO conducting the study. Because of this, it is likely the social network they recruited from also had some kind of previous relationship with the local NGO. This could have skewed the results, particularly since data regarding reasons for non-participation were not collected. Second, HIV-negative status was not biologically confirmed. Recent studies in the United States have shown a discrepancy between self-report and clinical evaluation of HIV negativity.³² Therefore, there may be social desirability bias related to self-reported HIV-negative status and retention in care, indicating that biological confirmation screening alongside survey data collection may be important in future studies of MSM.

Notably, surveys were both self-administered and facilitator administered. Because of the sensitive nature of survey questions, responses to facilitator-administered surveys may suffer from social desirability bias. However, when the study was implemented in Belize, no differentiation between self-administered and facilitator-administered surveys was made. Because of this, we could not control for possible differences in responses in our multivariable models. An additional concern of the study was that while the outcome of interest of this analysis was past six-month HIV testing, the survey instrument asked men how often they screened for HIV and did not assess the date of the last screening; therefore if men were tested outside of their self-identified screening window, it cannot be assessed here and our results are limited by this measurement. Studies that advance this work will benefit from asking more specific information (e.g. date of last test) to assess testing timing more precisely. Finally, preexposure prophylaxis was not available in Belize at the time of the survey; therefore, future research may benefit from including this important variable.

Conclusions

The heightened HIV prevalence among MSM in Belize indicates that while healthcare access and HIV knowledge are important when predicting screening behavior, healthcare providers must be aware of the impact of discrimination on MSM and others who may be at risk for HIV. While this study found that younger MSM were more likely to report being tested for HIV, there were many other MSM who were impacted by Section 53. Most likely, given that bans on same sex behavior were imposed during British colonial rule, and codified in 1888,³³ there may be a generational or cohort effect regarding the removal of the law which will require additional study. Lastly, building on social support and cultural nuances as a way to assuage shame and depression remain promising opportunities for intervention.

Footnotes

Acknowledgements

The authors would like to thank the participants of this research study, who without their participation, this information would not have been possible. We would also like to thank the staff and volunteers of C-NET for participating in this important research.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial sup- port for the research, authorship, and/or publication of this article: All study procedures were approved by the University of Pittsburgh Institutional Review Board. This study was partially supported by the amfAR GMT Initiative Grants #109555 and 109334. Support for mentorship and training was partially supported by NIMH training grant 5-T32MH094174-09.

ORCID iD

Cristian J Chandler

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