braz j infect dis 2 0 1 9;2 3(1):2–7

The Brazilian Journal of

INFECTIOUS DISEASES
www.elsevier.com/locate/bjid

Original article

HIV testing and HIV knowledge among men who

have sex with men in Natal, Northeast Brazil

Monica Baumgardt Bay a,∗, Marise Reis de Freitas a, Marcia Cavalcante Vinhas Lucas b,
Elizabeth Cristina Fagundes de Souza b , Angelo Giuseppe Roncalli b
a Universidade Federal do Rio Grande do Norte, Departamento de Doenças Infecciosas, Natal, RN, Brazil
b Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Background: Men who have sex with men (MSM) account for the highest prevalence of HIV
Received 15 August 2018 in Brazil. HIV testing allows to implement preventive measures, reduces transmission, mor-
Accepted 13 January 2019 bidity, and mortality.
Available online 10 February 2019 Methods: We conducted a cross-sectional study to evaluate HIV testing during lifetime, fac-
tors associated with the decision to test, knowledge about HIV transmission, and use of
Keywords: condoms between MSM from the city of Natal, northeast Brazil.
HIV testing Results: Out of 99 participants, 62.6% had been tested for HIV during lifetime, 46.2% in the last
Men who have sex with men (MSM) year. The most frequent reported reason to be tested for HIV infection was curiosity (35.5%).
HIV knowledge Correct knowledge about HIV was observed in only 9.2% of participants. In multivariate
analysis, age (PR 0.95; 95%CI, 0.91–0.99; p = 0.041) and previous syphilis test (PR 4.21; 95%CI,
1.52–11.70; p = 0.006) were associated with HIV testing.
Conclusions: The frequency of HIV testing among MSM from Natal is rather low, especially
in younger MSM, and knowledge about HIV transmission is inappropriate.
© 2019 Sociedade Brasileira de Infectologia. Published by Elsevier España, S.L.U. This is
an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).

may be partly explained by the practices and behaviors associ-

Introduction ated with anal sex and the gut tropism of HIV.2,3 Besides that,
behavioral vulnerabilities act together increasing the chances
The overall prevalence of HIV infection in Brazil is estimated
of HIV infection between MSM, such as no condom use, prac-
at 0.4%, but the epidemic is highly concentrated in vulner-
tice of transactional sex, use of drugs during sex, and sex with
able populations, with 5.3% prevalence among sex workers
casual partners.4
and 19.8% in men who have sex with men (MSM) according to
In 2015, the Joint United Nations Program on HIV/AIDS
the last reports.1 The higher risk of HIV infection among MSM
(UNAIDS) proposed that by 2020, 90% of people living with
HIV should be aware of their HIV status, as the first part of
90-90-90 strategy to end AIDS epidemic.5 Early detection of
∗
Corresponding author. HIV allows initiating care for proper treatment, which impacts
E-mail address: [email protected] (M.B. Bay). in morbidity, mortality, and reduces further transmission.2 In
https://doi.org/10.1016/j.bjid.2019.01.003
1413-8670/© 2019 Sociedade Brasileira de Infectologia. Published by Elsevier España, S.L.U. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 b r a z j i n f e c t d i s . 2 0 1 9;2 3(1):2–7 3

Brazil, HIV testing is recommended for all pregnant women partners, transactional sex, previous syphilis test, knowledge
and patients with diagnosis of tuberculosis, visceral leishma- of places were HIV testing is free, and adequate knowledge
niasis, or sexually transmitted infections.6 Studies estimated about HIV prevention, according to United Nations General
that the delay between infection and first CD4 count in Brazil Assembly Special Session on HIV/AIDS (UNGASS) indicator,
was 4.3 years, showing that a large proportion of individuals defined as the percentage of respondents giving correct
still started treatment late in the country.7 In Northeast Brazil answers to all the following five questions14 :
8800 new cases of AIDS are detected per year and in Natal the
mean CD4 count at diagnosis is 269 cells/mm3 , pointing to late Can having sex with only one faithful, uninfected partner
diagnosis of HIV.1 reduce the risk of HIV transmission? (yes);
Although the group of MSM accounts for the highest Can using condoms reduce the risk of HIV transmission?
prevalence of HIV in the country, there is no specific recom- (yes);
mendation for HIV testing in this population in Brazil.6 Data Can a healthy-looking person have HIV? (yes)
available from developed countries show that the proportion Can a person get HIV by using public toilets? (no)
of MSM never testing for HIV is generally below 30%.8,9 Since Can a person get HIV by sharing a meal with someone who
few studies evaluated HIV testing among MSM in Brazil, espe- is infected? (no)
cially in Northeast region, our study aimed to access the rate
and factors associated with HIV testing among MSM from A rapid test for HIV using hole blood was offered for
Natal city, Northeast Brazil. the participants at study site (Rapid Check HIV-1/2 and/or
Bio-Manguinhos HIV-1/2), with pre- and post-test counseling
and the result was given immediately, according to Brazilian
Materials and methods guidelines.15

Study design
Statistical analysis

This is a cross-sectional study, conducted in the city of Natal,

Sample size was calculated to be 95 subjects, assuming a
between August 2011 and December 2012. The primary objec-
prevalence of 60% for previous HIV testing during lifetime,
tive was to evaluate previous HIV testing among MSM from
95% confidence and a 10% error, based on previous data from
Natal during lifetime. Based on previous studies we anticipate
Adam et al. for 10 countries in Latin America.16 Descrip-
that younger age and lower education would be associated
tive analysis included central tendency measures calculated
with lack of testing,10,11
for continuous variables and proportions were calculated for
categorical variables. The association between previous HIV
Study sample testing and explanatory variables was assessed by univariate
analysis using Pearson’s Chi-square or Fischer exact test when
Participants were MSM aged 18 years old or more, residing appropriate. For continuous variables, Student’s “t” test was
or working in Natal. They were recruited using respondent- performed. Associations with a p-value less than 0.05 were
driven sampling (RDS) approach initially.12 Six MSM were considered significant. In order to verify the adjusted effect,
selected as initial seeds, chosen through focus group. The Poisson Regression Modeling with robust variance were per-
focus group was conducted with 15 MSM representatives of formed, including those variables with p-values less than 0.2.
artistic scene, student activism and social movement from Data were analyzed using SPSS (Statistical Package Software
Natal, the initial seeds were selected considering demographic for Social Science) version 20.0.
characteristics, like age and socioeconomic status, and net-
work size. Each seed was allowed to recruit three participants,
Ethics
using study coupons pre-printed with the study center phone
number and location. Staff screened subjects in the study site
The study was approved by the Ethic Research Committee of
for the following eligibility criteria: age over 18 years, living or
Federal University of Rio Grande do Norte (number 136/11). All
working in the city of Natal, and having engaged in anal inter-
participants signed a written informed consent.
course with another man in the previous year. Each included
participant received three coupons to invite more people for
the study. Results

Procedures By November 2012, 70 subjects were included using RDS,

despite many efforts of the study team to improve recruit-
The study was conducted at a health care facility inside the ment, including increase in the hours of operation of the
university. The study questionnaire consisted of objective study site and adding six more seeds. As our planed sample
questions to be self-administered and based on a behavioral was 95 MSM, we decided to include a venue-based sample of
instrument used previously with this population in Brazil.13 additional 31 subjects recruited during the gay pride event in
Participants responded to the questions in a private office. Natal city in December 2012. From 101 participants, two were
Questions included socioeconomic and demographic char- excluded because they answered less than 70% of the ques-
acteristics, history of HIV testing, reasons to do the test, use tionnaire, totaling a sample of 99 subjects. Sociodemographic
of condom in the last sexual relation, HIV status of sexual characteristics of participants are shown in Table 1. The mean
4 b r a z j i n f e c t d i s . 2 0 1 9;2 3(1):2–7

Table 1 – Sociodemographic characteristics of 99 MSM Table 3 – Places of HIV testing reported by MSM.
from Natal.
Places n %
Variables Mean/n SD/%
Public service 32 51.6
Age (years) 29.1 9.7 Blood bank 6 9.7
Years of study 11.5 2.2 Private service 11 17.7
Month income (US dollars) 494 465 Work place 5 8.1
Other 8 12.9
Race
Total 62 100
White 25 27.5
Mulatto/black 66 72.5

Occupation mentioned by 71.9%. Only 13.1% were aware of the HIV status
Employed 62 62.6
of sexual partners. Of the 63 MSM who agreed to perform an
Unemployed 37 37.4
HIV test, six turned out positive (9.5%) [Table 1].
Use of condom in last anal sex In univariate analysis, age (PR 0.93; 95% CI, 0.88–0.97;
Yes 68 71.9
p < 0.001) and previous syphilis test (PR 1.85; 95% CI, 1.41–2.44;
No 27 28.1
p < 0.001) were associated with HIV testing. Knowing a place
Previous HIV test where the HIV test could be done free-of-charge was also asso-
Yes 62 62.6 ciated with HIV testing (PR 1.69; 95%CI, 1.05–2.71; p = 0.017), as
No 37 37.4
most MSM did the test in public services (Table 5). In adjusted
Previous syphilis test analysis, resulted from Poisson modeling, the variables “age”,
Yes 34 35.4 “previous syphilis test”, and “knowing where HIV test was
No 62 64.6
free” where included in a stepwise logistic regression analysis.
HIV test in the study In the final predictive model only “age” and “previous syphilis
Positive 6 9.2 test” remained independently associated with previous HIV
Negative 59 90.8
testing (Table 5).
Know where to test for HIV for free
Yes 72 73.5
No 26 26.5 Discussion

Our study found that 62.6% of MSM from Natal had been tested
for HIV before. This rate was higher than the national aver-
Table 2 – Reason for having done HIV test among MSM.
age of 37% estimated for the general population in 201113
Reason n % and the 51.6% found by Brito et al. in MSM from 10 Brazilian
Curiosity 22 35.5 cities in 2009.10 These rates are rather disappointing as MSM
Self perception to be at risk for HIV infection 11 17.7 is a group with a high prevalence of HIV infection. The World
Medical recommendation 10 16.2 Health organization and the Centers for Disease Control and
Blood donation 7 11.3 Prevention (CDC) in United States, recommend that persons
Requested at work 6 9.7 at high risk for HIV infection should be screened for HIV at
Partner wish 3 4.8
least annually.17,18 It should be pointed out that testing at any
Total 62 100
time was accounted for, rather than being restricted to the last
year. If only testing in the previous year were considered the
age was 29.1 years (SD 9.7 years), 73.3% identified themselves rate would be even lower (46.2%). Previous studies conducted
as mulatto or black, mean monthly income was 494 US dollars in Argentina, Peru, and China showed HIV testing rates vary-
(SD 465 dollars), and 61.5% were employed. Participants had a ing between 48% and 58%,9,11,19 but studies from United States
mean of 11.5 years of schooling (SD 2.2 years). and Puerto Rico had a much better result (82–90%).20,21
Out of 99 participants, 62.6% (CI 95% 52.5–71.7%) had been Lack of knowledge about HIV transmission is one of the rea-
tested for HIV, 46.2% (CI 35.5–57%) in the last year. The most sons that lead to low perceived risk of being infected. Hall et al.
frequent reason to be tested was curiosity (35.5%), 17.7% found that testing was higher among high school students
because they perceived themselves to be at risk for HIV if they were taught at school about AIDS or HIV.22 Although
infection, and 16.2% were asked to be tested by a health pro- adequate knowledge about HIV transmission was not signif-
fessional (Table 2). The most frequent place for testing was icantly associated with HIV testing, it is noteworthy the low
public services mentioned by 52.4% (Table 3). Only 9.2% of par- level of knowledge, despite the high educational level. The per-
ticipants had adequate knowledge about HIV transmission. centage of adequate knowledge in a study with the Brazilian
The questions with the highest percentages of wrong answers general population was much higher, reaching 57.1%,13 but
were “Can a person get HIV by sharing a meal with someone Guimarães et al. indicate a decrease in the proportion of MSM
who is infected?” (66.7% marked ‘yes’) and “Can a person get with adequate HIV knowledge from 35.2% in 2009 to 23.7%
HIV by using public toilets?” (22.9% marked ‘yes’) [Table 4]. in 2016.23 Campaigns carried out by the Ministry of Health
Transactional sex was frequent, as 42% reported having in Brazil have focused primarily on condom use as a way to
received money in exchange for sex in the previous six avoid HIV infection, leaving aside clarification on situations
months. Use of condom in the last anal intercourse was that have no risk of transmission, such as sharing a meal or
 b r a z j i n f e c t d i s . 2 0 1 9;2 3(1):2–7 5

Table 4 – Knowledge about HIV by MSM from Natal city, Brazil, 2012.
Question n %

Can a person get HIV by using public toilets?

Yes 22 22.9
No 57 59.4
Don’t know 17 17.7
Total 96 100

Can having sex with only one faithful, uninfected partner reduce the risk of HIV transmission?
Yes 78 78.8
No 16 16.2
Don’t know 5 5.1
Total 99 100

Can a healthy-looking person have HIV?

Yes 94 94.9
No 2 2.0
Don’t know 3 3.0
Total 99 100

Can using condoms reduce the risk of HIV transmission?

Yes 96 97.0
No 2 2.0
Don’t know 1 1.0
Total 99 100

Can a person get HIV by sharing a meal with someone who is infected?
Yes 66 66.7
No 17 17.2
Don’t know 16 16.2
Total 99 100

use of public toilets. In our country, AIDS is still a topic rarely 25 years or less was independently associated with higher
addressed in schools, and even when this approach is carried scores of risky behavior.27 A recent study from Germany also
out, it is usually not systematic. The school is often the only showed that younger age (<25 years) was associated with lower
place where young people can receive reliable information. rates of HIV testing.28 The very absence of testing could be a
However, most often school teachers are NOT well prepared, contributing factor to the increased number of infections in
and may end up delivering incomplete information. Alterna- this population, since people with HIV on antiretrovirals are
tive interventions like peer education and internet and social less likely to transmit the virus than those who do not use
media strategies to access MSM have proven to be useful in them, a category which include HIV carriers that have not been
studies from Peru and United States.19,24 In 2015, a team of diagnosed.29,30 The proposal of treatment as prevention relies
governmental, research, and non-governmental organizations on a model of universal testing, reinforcing that barriers to
in the city Curitiba in South Brazil launched and evaluated a HIV testing will become more relevant to the full spectrum of
multi-component implementation science project to improve HIV care. Maximizing testing opportunities and reducing bar-
HIV outcomes for MSM. This project, called “A Hora é Agora” riers to regular testing should be a central component of HIV
(“The Time is Now”) implemented a web-based platform and prevention programs.31
associated mobile application designed to provide HIV pre- This study has some limitations. The RDS technique was
vention information, allowing for self-assessment of risk and not effective for the population of MSM from Natal, as it has
delivering HIV self-test kits. The project exceeded all expecta- not reached the sample size initially calculated. Few seeds had
tions with 7352 HIV self-test requests over 24 months, as the enough waves to disperse the sample and make it closer to a
initial goal was to distribute 1000 test kits per year, and was probabilistic sample, even with all efforts from the research
able to reach a large percentage (31%) of MSM who had never team to improve recruitment. Similar difficulties have been
been tested before, with those between 18 and 28 years old reported with the use of RDS technique by researches in
reporting a higher percentage of first-time testers (36%) than Singapore.32 We ended up analyzing our entire group as a
those 29 years or older (18%).25 The same project is now being non-probabilistic sample as a consequence of these difficul-
implemented in the city of São Paulo.26 ties. Therefore, these results may not be representative of
Younger age was associated with never testing for HIV in the entire Natal MSM population. Some of the results that
this study, which is worrisome since the last national epi- did not show statistical significance may have been influ-
demiological report data showed that the HIV epidemic is enced by the sample size that may have not been sufficient
increasing in this group.1 A study evaluating sexual risk behav- to show associations. However, there is relevance to the study
ior among MSM from 10 Brazilian cities showed that to be aged because it represents a population that is difficult to access in
6 b r a z j i n f e c t d i s . 2 0 1 9;2 3(1):2–7

Table 5 – Univariate analysis of selected characteristics of MSM and prior HIV testing in Natal city, Brazil, 2012.
Variables Previous HIV test Total Unadjusted Adjustedb

Yes No n % pa PR p PR

n % n % Mean SD (CI 95%) (CI 95%)

Mean SD Mean SD

Occupation
Employed 39 66.1 20 33.9 59 61.5 0.48 1.23
Unemployed 21 56.8 16 43.2 37 38.5 (0.76–2.13)
Total 60 62.5 36 37.5 96 100
Age 31.8 10.0 24.4 6.9 29.1 9.7 <0.001 0.93 0.041 0.95
(0.88–0.97) (0.91–0.99)

Race
White 15 62.5 9 37.5 24 26.7 0.97 1.01
Non-White 41 62.1 25 37.9 66 73.3 (0.55–1.84)
Total 56 62.2 34 37.8 90 100
Years of schooling 11.5 2.1 11.4 2.4 11.5 2.2 0.714
Monthly income (US dollars) 528 511 434 370 494 465 0.359

Knowledge about HIV

Correct 6 66.7 3 33.3 9 9.2 0.82 1.11
Incorrect 56 62.9 33 37.1 89 90.8 (0.42–2.91)
Total 62 63.3 36 36.7 98 100

Transactional sex
No 38 69.1 17 30.9 55 57.9 0.34 1.37
Yes 23 57.5 17 42.5 40 42.1 (0.80–2.34)
Total 61 64.2 34 35.8 95 100

Previous syphilis test

Yes 31 91.2 3 8.8 34 35.8 <0.001 5.76 0.006 4.21
No 30 49.2 31 50.8 61 64.2 (1.90–17.45) (1.52–11.70)
Total 61 64.2 34 35.8 95 100

Know where HIV test is free

Yes 50 71.4 20 28.6 70 72.9 0.017 1.69
No 11 42.3 15 57.7 26 27.1 (1.05–2.71
Total 61 63.5 35 36.5 96 100

Use of condom in last anal sex

Yes 46 67.6 22 32.4 68 71.9 0.27 1.37
No 15 55.6 12 44.4 27 28.1 (0.79–2.37)
Total 61 64.2 34 35.8 95 100

a
For categorical variables, Chi-Square or Fisher Exact test; for continuous variables, Student’s “t” test.
b
Poisson Regression Modeling

a location where no similar study had been performed previ-

ously.
Sources of support

National Fund of Health, Ministry of Health, Brazil.

Conclusion

The study shows that HIV testing rates are low among this Conflicts of interest
sample of MSM, and younger age and previous syphilis test
were associated with never testing in multivariate analysis. The authors declare no conflicts of interest.
Knowing a place where the HIV test can be done free-of-charge
was associated with HIV testing in univariate analysis but lost references
significance in the multivariate model. Actions that prioritize
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