The relationship between risk perception and frequency of HIV testing among men who have sex with men and transgender women, Lima, Peru

Abstract

HIV infections in Peru are concentrated among men who have sex with men (MSM) and transgender women (TW). HIV testing rates among them remain low, delaying entrance into care. We assessed the prevalence of frequent HIV testing (at least every 6 months) and associated factors among 310 MSM and TW who attend sexual health clinics in Lima, Peru, and who reported that they were HIV seronegative or unaware of their status. Only 39% of participants tested frequently, and 22% had never tested; 29% reported that they were at low or no risk for acquiring HIV. Reporting low or no risk for acquiring HIV was associated with frequent testing (adjusted prevalence ratio [aPR]=1.53, 95% CI, 1.13–2.08); those reporting unprotected anal sex were less likely to test frequently (aPR=0.66, 95% CI, 0.50–0.87). HIV prevalence was 12% and did not vary by risk perception categories. This at-risk population tests infrequently and may not understand the risk of having unprotected sex.

Introduction

By the first quarter of 2017, the number of HIV and AIDS cases in Peru reached 68,201 and 35,847, respectively, according to official reports of the National Center for Epidemiology, Prevention and Control of Diseases,[1] with more than 50% of cases occurring among men who have sex with men (MSM) and transgender women (TW).[2] Approximately 20% of MSM [3,4] and 30% of TW are HIV infected, with little change in prevalence over the past decade.[5] The incidence of new infection remains about 3 per 100/person-years despite the introduction of antiretroviral therapy (ART).[6,7]

The Peruvian national HIV prevention plan focuses on promotion of HIV testing under the assumption that persons identified as seropositive will be rapidly referred for care and treatment, which are free and government sponsored.[8] However, studies from Peru and the Andean region have shown a low uptake of HIV testing among MSM [9–11]; consequently, many are unaware of their HIV status.[6,12,13] Factors such as poor knowledge of HIV and feelings of being stigmatized and discriminated against have been associated with delayed or infrequent testing.[11,14]

The relationship of risk perception to HIV testing among MSM and TW has been evaluated in multiple settings, and the results have been mixed. Studies from the United States and China have shown that MSM who perceived themselves at higher risk of HIV were less likely to test,[15,16] whereas a study among MSM in Seattle found that those with higher perceived risk were more likely to test.[17] To better understand factors associated with HIV testing in Peru, particularly the perception of risk for HIV acquisition, we evaluated MSM and TW who were attending sexually transmitted infection (STI) clinics in Lima, the capital city.

Methods

Study population

We analyzed data collected from the baseline assessment of participants enrolled in PICASSO, a longitudinal cohort study designed to evaluate the prevalence and acquisition of syphilis among MSM and TW in Lima; study methods have been described in detail elsewhere.[18] In brief, from June 2013 through May 2014, MSM and TW attending two STI clinics in the city were invited to participate. Participants had to be aged ≥18 years and at high risk for syphilis acquisition, defined as having at least 3 of the following risk factors: (1) 5 years of sexual activity, (2) more than 5 sex partners during the preceding 3 months, (3) more than 5 episodes of condomless anal intercourse during the preceding 6 months, (4) a self-reported genital ulcer at recruitment, (5) self-report of a syphilis diagnosis in the preceding 2 years, (6) self-report of an STI diagnosis in the preceding 6 months, and (7) self-report of being HIV seropositive. Subjects willing to participate signed informed-consent forms and received 15 soles ($5) as reimbursement for the cost of transportation.

The PICASSO study recruited a total of 401 MSM and TW. Of these, 310 (77.3%) were included in the current analyses because they reported being HIV seronegative (N=243) or were unaware of their HIV status (N=67). Participants in the PICASSO study who reported that they were HIV seropositive (N=91) were excluded from the current analysis. The ethical review board at Universidad Peruana Cayetano Heredia, Lima, approved the protocol.

Data collection

Participants completed a computer-assisted personal interviewing (CAPI) survey lasting 30 minutes that assessed sociodemographic characteristics, gender or identity, sexual orientation, sexual risk behavior in the preceding 3 months, self-reported current HIV status, and history of syphilis. We also grouped participants who indicated that their sexual identity was “heterosexual” (N=8) with those who were “bisexual” because the number of heterosexuals was small. Participants were asked how often they had undergone HIV testing and their perceived risk of acquiring HIV. Participants who indicated that they had tested at least every 6 months were considered “frequent HIV testers,” regardless of how many times they had tested. Participants reported their perceived risk of acquiring HIV as high, moderate, low, or no risk; we grouped participants who indicated that they had “no risk for HIV” (N=15) with those who reported “low risk” (N=75).

Venous blood samples were obtained for HIV and syphilis testing. At clinic sites, samples were tested for HIV with a third-generation rapid test (Determine HIV 1/2 Alere Determine™, Israel). Syphilis infection was evaluated by using a third-generation treponemal-specific antibody rapid test (Determine syphilis Alere Determine™, Israel) in parallel with a rapid plasma reagin (RPR) test (BD Macro-Vue™ RPR Card Test Kit, Beckton Dickinson, United States). Clients were told that results from rapid testing were preliminary and would be confirmed by further testing of samples at the reference laboratory. Participants also self-collected anal swab samples for Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (GC) testing.

All samples were sent to the Laboratory of Sexual Health, located at Universidad Peruana Cayetano Heredia, Lima, for confirmatory testing. Serum samples were rescreened for HIV using a fourth-generation enzyme immunoassay (EIA) test (Genscreen™ ULTRA HIV Ag-Ab, Bio-Rad, France); samples that were positive in an EIA or rapid test were confirmed using a western blot test (NEW LAV BLOT I, Bio-Rad, France). All samples were evaluated for the presence of syphilis by testing with the Treponema pallidum particle agglutination (TPPA) assay (Fujirebio Diagnostics, Tokyo, Japan). A participant was considered to have a recent syphilis infection if the RPR titer was ≥1:16 and the TPPA test was positive. We used a transcription mediated amplification (TMA) assay (Aptima Combo2 Assay, Gen-probe, United States) on anal swab samples to diagnose CT and GC. The confirmatory results of syphilis, HIV, CT, and GC testing were delivered to participants 2 weeks after sample collection. STIs were treated according to national guidelines [19]; those who were identified as being HIV seropositive were referred for further evaluation and care.

Data analysis

We evaluated the distribution of sociodemographic characteristics, sexual risk behavior in the preceding 3 months, and STIs and HIV infection, as well as the proportion of participants in each category who tested “frequently.” Differences in proportions among the categories were evaluated using the chi-square test. We evaluated the univariate and multivariable association of covariates with frequent HIV testing using prevalence ratios (PRs), as the frequency of the outcome was greater than 10% [20] and all data were cross-sectional. In multivariable models, we included age, monthly income, and presence of a stable sex partner a priori, as well as variables associated with frequent testing and a P value of <0.2 in univariate analysis. We used generalized linear models with a log link and Poisson robust error variance to calculate PRs.[20,21] Our modeling strategy was to group variables into sexual behavior (first subgroup) and sociodemographics (second subgroup). The effect of each significant variable within the sexual behavior subgroup was entered, then the significant variables of the sociodemographics subgroup. Finally, a priori variables were added. The multivariable model was evaluated after the addition of each variable. The selection criteria for inclusion of variables in the final model were based on choosing the regression model with lower values of the Akaike information criterion and the Bayesian information criterion that included a priori variables of importance. We also evaluated the association between sociodemographic and other variables and levels of risk perception using chi-square and Fisher exact tests, as appropriate. The association between self-reported history of syphilis and laboratory-confirmed syphilis infection was determined using chi-square tests.

Results

Approximately two thirds (68.1%) of recruited participants were aged 35 years or younger (Table 1). More than half (53.8%) self-identified as gay or homosexual, 24.2% as bisexual, and 22.0% as TW. Nearly two thirds (63.4%) earned more than the Peruvian monthly minimum wage of about 250 USD; 51.0% reported having had at least some postsecondary education. Eighty percent reported having more than 1 sex partner during the preceding three months, and almost the same proportion reported unprotected anal intercourse. About one third (31.9%) reported having had syphilis in the past; 28.4% had a laboratory-confirmed diagnosis of an STI, including anal chlamydia (14%), anal gonorrhea (9%), and recent syphilis infection (12%). Twenty-three percent of the entire sample considered themselves at high risk for HIV, 47.7% at moderate risk, and 29.0% at low or no risk. A total of 37 participants (12%) were found to be HIV infected. In subanalyses for which data are not shown, 11% (26 of 243) of those who reported themselves as HIV negative at enrollment were found to be HIV seropositive, and 16% (11 of 67) of those who did not know their HIV status were identified as being infected (P value <0.1). The proportion of MSM and TW who reported testing frequently was 39.3%. Participants reporting low or no HIV risk had a higher prevalence of frequent testing (55.6%) when compared with those who perceived themselves at moderate (29.7%) or high (38.9%) HIV risk. Variables related to testing frequently included being a TW, reporting 2 or more recent sex partners, being engaged primarily in receptive anal intercourse, having engaged in sex work, or reporting a previous syphilis infection.

Table 1.

Characteristics of MSM and TW attending STI clinics and the proportion who reported testing frequently^a for HIV, Lima, Peru, 2014.

Variable	All	Tested frequently	Test statistic	P value
	N(%)	n(%)
All	310(100)	122(39.3)
Sexual orientation/gender identityb			X2=14.1, df=2	.001
Gay/homosexual	164(53.8)	66(40.2)
Bisexual/heterosexual	74(24.2)	18(24.3)
Transgender woman	67(22.0)	37(55.2)
Age (years)			X2=1.1, df=2	.565
18–25	102(32.9)	36(35.3)
26–35	109(35.2)	44(40.4)
≥36	99(31.9)	42(42.4)
Monthly income (USD)b			X2=6.9, df=2	.031
≤250	109(36.6)	54(49.5)
251–500	147(49.3)	49(33.3)
≥501	42(14.1)	18(42.9)
Education			X2=2.5, df=1	.113
≤ High school	152(49.0)	53(34.9)
> High school	158(51.0)	69(43.7)
Perceived risk for HIV			X2=15.8, df=3	<.001
High	72(23.3)	28(38.9)
Moderate	148(47.7)	44(29.7)
Low/none	90(29.0)	50(55.6)
Number of sex partners, last 3 months			X2=7.2, df=2	.028
0–1	62(20.0)	16(25.8)
2–4	82(26.5)	39(47.6)
≥5	166(53.5)	67(40.4)
Condomless anal intercourse, last 3 monthsb			X2=13.1, df=1	<.001
Yes	239(79.7)	84(35.1)
No	61(20.3)	37(60.7)
Sex role during intercourse, last 3 months			X2=6.8, df=2	.034
Insertive	77(24.8)	22(28.6)
Receptive	98(31.6)	47(48.0)
Insertive and receptive	135(43.6)	53(39.3)
Had male/TW stable sex partner, last 3 months			X2=2.6, df=1	.152
Yes	147(47.4)	64(43.5)
No	163(52.6)	58(35.6)
Had male/TW casual sex partner, last 3 months			X2=0.1, df=1	.740
Yes	159(51.3)	64(40.3)
No	151(48.7)	58(38.4)
Performed sex work, last 3 months			X2=3.7, df=1	.055
Yes	62(20.0)	31(50.0)
No	248(80.0)	91(36.7)
Self-reported history of syphilis, ever			X2=14.1, df=1	<.001
Yes	99(31.9)	54(54.5)
No	211(68.1)	68(32.2)
Laboratory diagnosis of STIc			X2=0.5, df=1	.497
Yes	88(28.4)	32(36.4)
No	222(71.6)	90(40.5)
Laboratory diagnosis of HIV			X2= 0.3, df=1	.432
Positive	37(11.9)	13(35.1)
Negative	273(88.1)	109(39.9)

^aTesting frequently was defined as having tested at least every 6 months.

^bSmall discrepancies in subtotals and totals are due to rounding and/or missing values.

^cSyphilis, rectal chlamydia, and/or rectal gonorrhea.

Factors independently associated with frequent HIV testing included having postsecondary education (aPR=1.38, 95% CI, 1.03–1.84); believing oneself to have little or no risk for HIV (aPR=1.53, 95% CI, 1.13–2.08), compared with feeling at moderate risk; reporting a history of syphilis (aPR=1.59, 95% CI, 1.23–2.06); and having 2 to 4 recent sex partners (aPR=1.73, 95% CI, 1.09–2.72) (Table 2). Having condomless anal intercourse was associated with being less likely to test frequently (aPR=0.66, 95% CI, 0.50–0.87).

Table 2.

Factors associated with frequent HIV testing^a among MSM and TW, Lima, Peru, 2014.

Variables		PR(b)	95% CI	z score	P value	aPRb	95% CI	z score	P value
Sexual orientation/gender identity
Gay/homosexual		Ref.	-	-		Ref.	-	-
Bisexual/heterosexual		0.60	0.39–0.94	–2.22	.026	0.77	0.48–1.24	–1.06	.291
Transgender woman		1.37	1.03–1.83	2.17	.030	1.28	0.91–1.79	1.43	.152
Age (years)
18–25		Ref.	-	-		Ref.	-	-
26–35		1.14	0.81–1.62	0.76	.450	1.04	0.73–1.46	0.20	.839
≥36		1.20	0.85–1.70	1.03	.302	0.96	0.69–1.33	–0.24	.809
Monthly income (USD)
≤250		Ref.	-	-		Ref.	-	-
251–500		0.67	0.50–0.91	–2.61	.009	0.76	0.57–1.01	–1.92	.055
≥501		0.87	0.58–1.29	–0.71	.475	0.81	0.53–1.23	–0.98	.325
Education
≤ High school		Ref.	-	-		Ref.	-	-
> High school		1.25	0.95–1.66	1.57	.116	1.38	1.03–1.84	2.20	.028
Perceived risk for HIV
High		1.31	0.89–1.92	1.38	.168	1.02	0.71–1.46	0.11	.913
Moderate		Ref.	-	-		Ref.	-	-
Low/none		1.87	1.37–2.55	3.96	<.001	1.53	1.13–2.08	2.77	.006
Number of sex partners, last 3 months
0–1		Ref.	-	-		Ref.	-	-
2–4		1.84	1.14–2.98	2.50	.013	1.73	1.09–2.72	2.36	.018
≥5		1.56	0.99–2.48	1.90	.058	1.49	0.94–2.36	1.71	.086
Condomless anal intercourse, last 3 months
Yes		0.58	0.44–0.76	–4.02	<.001	0.66	0.49–0.87	–3.01	.003
No		Ref.	-	-		Ref.	-	-
Sex role during anal intercourse, last 3 months
Insertive		Ref.	-	-		Ref.	-	-
Receptive		1.68	1.11–2.53	2.48	.013	1.04	0.66–1.62	0.17	.865
Insertive and receptive		1.37	0.91–2.07	1.51	.130	0.97	0.63–1.51	–0.11	.915
Had male/TW stable sex partner, last 3 months
Yes		1.22	0.93–1.61	1.43	.154	1.2	0.93–1.56	1.43	.152
No		Ref.	-	-		Ref.	-	-
Performed sex work, last 3 months
Yes		1.36	1.01–1.83	2.03	.042	1.21	0.89–1.65	1.20	.229
No		Ref.	-	-		Ref.	-	-
Self-reported history of syphilis, ever
Yes		1.69	1.29–2.21	3.87	<.001	1.59	1.23–2.06	3.60	<.001
No		Ref.	-	-		Ref.	-	-
Laboratory diagnosis of STIc
Yes		0.89	0.65–1.23	–0.67	.505	-	-	-
No		Ref.	-	-		-	-	-
Laboratory diagnosis of HIV
Positive		0.88	0.55–1.39	–0.54	.588	-	-	-
Negative		Ref.	-	-		-	-	-

^aTesting frequently was defined as having tested at least every 6 months.

^bPR = prevalence ratio, (a)PR = adjusted prevalence ratio.

^cSyphilis, rectal chlamydia, and/or rectal gonorrhea.

We analyzed the association of sociodemographic characteristics and sexual behavior with HIV risk perception (Table 3). Among those with less education, 27.0% reported being at high risk for HIV, compared with 19.6% of those who had postsecondary education. Among those reporting more than 4 recent sex partners, 30.7% felt at high risk for HIV, compared with 18.3% of those who had 2 to 4 sex partners and 17.7% of those with 1 or no recent sex partners. The proportion of MSM and TW who perceived themselves at high risk for HIV was higher among those who engaged in sex work compared with those who did not (32.3% vs 11.2%). There was no association between recently identified HIV infection and risk perception. A subanalysis among those who reported having had a syphilis infection showed that 65% had a positive TPPA test (data not shown).

Table 3.

Factors associated with perceived risk for HIV among MSM and TW attending STI clinics, Lima, Peru, 2014.

Variable	N (%)	Perceived risk			Test statistic	P value
		High	Moderate	Low/None
All	310 (100)	72 (23.3)	148 (47.7)	90 (29.0)		-
Sexual orientation/gender identitya					X2=8.5, df=4	.075
Gay/homosexual	164 (53.8)	33 (20.1)	75 (45.7)	56 (34.2)
Bisexual/heterosexual	74 (24.2)	16 (21.6)	43 (58.1)	15 (20.3)
Transgender woman	67 (22.0)	21 (31.3)	29 (43.2)	17 (25.4)
Age (years)					X2=2.4, df=4	.658
18–25	102 (32.9)	22 (21.6)	50 (49.0)	30 (29.4)
26–35	109 (35.2)	26 (23.9)	56 (51.4)	27 (24.7)
≥36	99 (31.9)	24 (24.2)	42 (42.4)	33 (33.4)
Monthly income (USD)a					X2=4.5, df=4	.346
≤250	109 (36.6)	27 (24.8)	45 (41.3)	37 (33.9)
251–500	147 (49.3)	36 (24.5)	73 (49.7)	38 (25.8)
≥501	42 (14.1)	6 (14.3)	22 (52.4)	14 (33.3)
Education					X2=6.9, df=2	.032
≤ High school	152 (49.0)	41 (27.0)	77 (50.7)	34 (22.3)
> High school	158 (51.0)	31 (19.6)	71 (44.9)	56 (35.4)
Number of sex partners, last 3 months					X2=17.6, df=4	.002
0–1	62 (20.0)	11 (17.7)	28 (45.2)	23 (37.1)
2–4	82 (26.5)	15 (18.3)	32 (39.0)	35 (42.7)
≥5	166 (53.5)	46 (27.7)	88 (53.0)	32 (19.3)
Condomless anal intercoursea, last 3 months					X2=2.4, df=2	.299
Yes	239 (79.7)	57 (23.9)	119 (49.8)	63 (26.4)
No	61 (20.3)	14 (23.0)	25 (41.0)	22 (36.1)
Sex role during anal intercourse, last 3 months					X2=6.2, df=4	.182
Insertive	77 (24.8)	22 (28.6)	38 (49.4)	17 (22.0)
Receptive	98 (31.6)	22 (22.5)	40 (40.8)	36 (36.7)
Insertive and receptive	135 (43.6)	28 (20.7)	70 (51.9)	37 (27.4)
Had male/TW stable sex partner, last 3 months					X2=5.4, df=2	.067
Yes	147 (47.4)	38 (25.8)	60 (40.8)	49 (33.3)
No	163 (52.6)	34 (20.9)	88 (54.0)	41 (25.1)
Performed sex work, last 3 months					X2=5.2, df=2	.073
Yes	62 (20.0)	20 (32.3)	30 (48.4)	12 (19.3)
No	248 (80.0)	52 (21.0)	118 (47.6)	78 (31.4)
Self-reported history of syphilis					X2=1.2, df=2	.542
Yes	99 (31.9)	26 (26.3)	43 (43.4)	30 (30.3)
No	211 (68.1)	46 (21.8)	105 (49.8)	60 (28.4)
Laboratory diagnosis of STIb					X2=0.3, df=2	.981
Yes	88 (28.4)	21 (23.8)	42 (47.7)	25 (28.5)
No	222 (71.6)	51 (23.0)	106 (47.8)	65 (29.2)
Laboratory diagnosis of HIV					X2=0.7, df=2	.698
Positive	37 (11.9)	8 (21.6)	20 (54.1)	9 (24.3)
Negative	273 (88.1)	64 (23.4)	128 (46.9)	81 (29.7)

^aSmall discrepancies in subtotals and totals are due to rounding and/or missing values.

^bSyphilis, rectal chlamydia, and/or rectal gonorrhea.

Discussion

Even though MSM and TW are the key populations in the HIV epidemic in Peru, we found that only 39% of our sample reported testing for HIV every 6 months, as recommended by both international and national guidelines [19,22]; 20% of our sample had never had an HIV test. Several other studies had evaluated HIV testing behavior among MSM in Peru, and even though these studies were conducted 6 to 7 years before ours, the proportion of participants who had never had an HIV test was similar. In 2007, 15% of MSM who were enrolled from a STI clinic in Lima and 19% who were recruited from neighborhoods surrounding the city reported that they had never undergone HIV testing.[23] In 2008, only 6% of MSM who were recruited from low-income neighborhoods of Lima reported testing every 6 months, and 20% of the sample had never tested.[10] Among MSM responding to an internet-based survey in 2008, one half indicated that they had never tested.[24] Men who are sampled via an internet survey, however, may be less likely to test than those recruited from STI or other clinics, because HIV testing in Peru is provided almost exclusively at health care facilities. Overall, services and prevention messages targeting key populations in Peru remain limited in scope, which could help explain why rates of HIV testing do not appear to have changed much over time.

These results are concerning because a large proportion of our participants reported engaging in high-risk sexual behavior. In the past 3 months, about three quarters of our sample had more than 1 sex partner, and slightly more reported having unprotected anal intercourse. Some studies have shown that MSM who report more high-risk behavior are themselves more likely to test.[25,26] However, we found an inconsistent relationship between reported high-risk behavior and testing, which could be due to several factors, including an inaccurate perception of risk. For example, a high proportion of MSM and TW who had unprotected anal sex (primarily receptive sex) or a history of syphilis did not believe they were at high risk for HIV acquisition. It is possible that a lack of understanding of risk was due to low levels of knowledge, which could be the result of limited messaging about HIV prevention. In addition, factors that we did not measure may have contributed to how participants assessed their risk, such as knowledge of a partner’s HIV status.[13,27]

Overall, perceived risk has not been found to be a consistent predictor of testing behavior among MSM.[15–17, 28, 29]. In our study, there was an inverse relationship between perceived risk and frequent testing. It is likely that contextual factors also play a role in determining who seeks testing. For example, in our sample, MSM and TW with a history of syphilis may have been more likely to test for HIV because such testing is provided primarily at health facilities. In addition, MSM in Peru who already feel stigmatized for being gay may wish to avoid the additional discrimination that comes with being identified as HIV infected. This is consistent with a study of MSM and TW in New York City, in which those who said they would be stigmatized if identified as HIV infected were less likely to test.[29,30] In Peru, even though ART is widely available, it has been shown that HIV stigma may affect the adherence to treatment, affecting benefits of suppressed viral load.[31]

Our study had several limitations. First, our primary outcome measure—frequency of HIV testing—was based on its definition in the Peruvian HIV guidelines.[8] This definition is imprecise, however. We did not specify a time frame or the number of times someone needed to have tested to be considered a frequent tester. Second, we used only a single-item measure of HIV risk perception; more complex measures have been used to evaluate a broader range of dimensions of perceived risk.[32] Third, we did not ask questions about stigma or discrimination, which might have otherwise revealed whether fear of an HIV-positive test result and the potential stigma associated with it were related to avoidance of testing. Fourth, study participants were recruited at 2 STI clinics and screened for being at risk for syphilis infection, and therefore may not have been representative of MSM and TW who were not accessing care. Finally, our questionnaire was administered using CAPI to reduce social desirability bias, so we could not explore a more nuanced understanding of sexual and testing behavior or perceived risk.

Conclusions

Results from our study indicate that high-risk MSM and TW in Peru undergo HIV testing infrequently. Being unaware of their HIV status prevents those who are HIV infected from accessing treatment, for their own benefit as well as to reduce transmission to others.[33] Because testing in Peru is primarily facility-based, expansion to other venues and implementation of self-testing programs could increase coverage among this high-risk group.[34,35] Use of social media and more up-to-date information and communication methods could also encourage testing and treatment [36–40] as well as improve understanding of the importance of achieving an undetectable viral load.[41] Reducing stigma is complex and difficult, but engagement of HIV-infected MSM and TW in educational campaigns at the community level, and improving the sensitivity of health care providers, are still needed in Peru.[42–46] Overall, efforts to reach and to provide information and care to MSM and TW in Peru remain underresourced despite it being decades since the beginning of the HIV epidemic in this region. Even though the Peruvian Health Authorities proposed greater inclusion of gender and sexual minorities within the health services, interventions to ensure that this happens have not been implemented widely.[47]