Abstract
In Brazil, the increasing prevalence of HIV infection in young people makes it critical to know its distribution in university communities. In this cross-sectional study, we evaluated the impact of STI/HIV testing campaigns on university campuses from 2013 to 2017. The participants took part in rapid testing for HIV, syphilis, hepatitis B and C, and counseling sessions. A total of 2691 people participated in the campaigns. Of these, 79.4% were single, and 50.3% were women. The median age was 24 years old, and 77.9% of participants had ≥12 years of formal education. Most reported having unprotected sex in the last year (87.4%). The positivity rates for HIV, syphilis, hepatitis B virus, and hepatitis C virus were 0.56%, 1.20%, 0.19%, and 0.11%, respectively. The characteristics associated with HIV infection were being men who have sex with men (MSM) (aOR = 12.06; 95% CI = 3.83–37.99) and having <12 years of schooling (aOR = 3.28; 95% CI = 1.03–10.38). Factors associated with syphilis seropositivity were older age (aOR = 1.06; 95% CI = 1.03–1.09), multiple partners (aOR = 2.44; 95% CI = 1.08–5.50), and being MSM (aOR = 5.40; 95% CI = 2.49–11.72). Positivity for hepatitis B tended to decrease with the years of testing (p = 0.023) and for hepatitis C to increase with age (p = 0.035). Our study observed a high vulnerability to HIV and syphilis infection in a university community, which needs an early prevention strategy, including regular testing, continuing sexual education, easy access to condoms, and pre- and postexposure HIV prophylaxis.
Background
HIV infections have been considered stable in Brazil, but in recent years, a spike of new infections has been observed among young people in the 20–29 years age group.1,2
A study of HIV infections among men who have sex with men (MSM) in twelve Brazilian cities revealed an increase in the prevalence of infection in 2016 (18.4%) compared to the prevalence found in a study conducted with the same methodology in 10 Brazilian cities in 2009 (12.1%). 3 This increase was probably due to prevention shortcomings, including a decrease in promotion and distribution of condoms and low rates of HIV testing among key populations. 4
The increase in the numbers of new infections has been associated with risk-taking behaviors resulting from a lower risk perception of HIV infection, the existence of individuals with undiagnosed infection, and poor adherence to antiretroviral therapy in diagnosed patients. 1 Men are less likely to be tested for HIV, or to seek antiretroviral treatment, but are more likely to die from AIDS-related complications than women. 5
In Brazil, the acquired syphilis detection rate also increased from two cases per 100,000 population in 2010 to 42.5 cases per 100,000 population in 2016. Several factors are associated with this increase, including a reduction in condom use, lack of awareness regarding sexually transmitted infections, and a worldwide shortage of penicillin. 6 In a cross-sectional study with 8071 young participants from 119 primary care units in Brazil, the prevalence of self-reported syphilis was 2.9% and was associated with age, lower socioeconomic class, being a smoker, not using a condom for the first sexual intercourse, and having had a same-sex sexual experience. 7
The prevalence of hepatitis B virus and hepatitis C virus (HCV) is low among young people in Brazil, but infection among this group is associated with sexual intercourse, inconsistent condom use, history of sexually transmitted infections (STIs), and multiple partners.8,9
One strategy for early detection of HIV and other STIs in the young population is to conduct university-based testing events. On-site rapid testing campaigns at university campuses have achieved high HIV testing rates in university populations.10,11 The approach can be used for epidemiological surveillance and to expand access to diagnosis and treatment.12,13 In this context, the Ministry of Health in Brazil has provided resources for testing and awareness campaigns.
The increasing incidence of HIV infection in young Brazilians makes it critical to know the distribution of the disease within the university populations, which are younger and possibly have increased risk behaviors. The city of São Carlos (SP) is a college town, with three major institutions (Federal University of São Carlos—UFSCar, University of São Paulo—USP, and the University Center Central Paulista—UNICEP), adding more than 25,000 to the city’s population.
The aim of the present study was to assess the impact of testing campaigns on the diagnosis of STIs (including HIV) and to identify factors associated with the risk of contracting STIs in a community of predominantly university students and staff.
Methods
Since 2013, a team of researchers from the UFSCar and the São Carlos Municipal STD/AIDS Program have been promoting counseling and testing campaigns for syphilis, HIV, and hepatitis B and C on university campuses in São Carlos city. A cross-sectional study of epidemiological and serological data from these “Fique Sabendo” testing campaigns was carried out in university communities from 2013 to 2017, in São Carlos, SP, Brazil.
Participants were invited to the campaign through advertisements on the universities’ webpages, emails to the university community, announcements and interviews on Radio and TV UFSCar programs, and campaign posters and flyers. The campaigns were centered at facilities within the university campuses with the participation of teachers, health students, as well as primary care professionals, trained by the researchers. Participation in the campaigns was completely voluntary, and the form used for pretest counseling included formal consent for interview and testing.
This study was approved by the Human Research Ethics Committee (HREC) of the UFSCar (CAAE: 29135114.8.0000.5504/2016), with the consent and participation of the São Carlos Department of Health. The HREC waived the need for informed consent because the study analyzed data of notifiable infectious diseases. The data were stored on a protected online platform at the end of each campaign for research purposes. To ensure confidentiality, names and any personally identifiable information were omitted for statistical analysis.
The campaigns were carried out annually during the week of World AIDS Day. They were announced to the university communities, but all those who attend university campuses were able to participate. Thus, the population comprised undergraduate and graduate students, academics, administrative personnel, outsourced security and cleaning staff, and occasionally the general population. The interviews and rapid testing were conducted on-site, at university facilities. On Saturdays, there were testing shifts outside the campuses, for participants who could not to attend during business hours.
The first three years of the campaign were centralized at the UFSCar campus, with alternative service shifts on Saturdays at the São Carlos Chronic Infection Care Center and at the Urgent Care Service, to serve the public that could not be there during the week. University Center Central Paulista activities were incorporated at night from the second year of the campaign, and at USP, they were incorporated on a fixed day in the week from the third year.
Although the campaign was centered at university campuses, there was a progressive incorporation of primary healthcare units (USF and UBS) of São Carlos, of the Irmandade Santa Casa de Misericórdia Hospital, of a state technical school (ETEC), and of a state high school. This expansion was due to the progressive training of professionals from the municipal health network of São Carlos. These units accounted for 13.9% of the population sample.
The participants were subjected to pretest standard counseling sessions to identify demographic characteristics (gender, age, race, years of formal education, and marital status), previous HIV testing, hierarchical self-reported risk behavior, history of use of psychoactive substances, history of sexually transmitted diseases, and sexual practices. Sexual practices were assessed using a multiple-choice questionnaire including the sex of partners (men, women, both men and women, and transgender people), the range of number of sexual partners in the last 12 months, and sexual identity. Once allowed, rapid tests for HIV, hepatitis B and C, and syphilis were performed. The history of hepatitis vaccination was also assessed, and participants were referred to complete the vaccine series as needed. Participants received counseling about safer sex and safer injecting practices and serological results interpretation.
The results and eventual diagnostic disclosure were performed only by qualified and specialized professionals, in a protected space (individual rooms or collective rooms with partitions or dividers), allowing confidentiality, privacy, attention to the user, and facilitation of the expression of feelings. At the end, prevention materials were provided (guidance material and test network information, lubricating gel, and both male and female condoms). The counseling and other activities were discussed and standardized by training sessions held in the weeks preceding the campaigns.
For HIV rapid testing, participants underwent immunochromatographic screening tests on finger-stick whole blood, except in the year 2015, when tests were made on oral fluid. The screening tests used were Rapid CheckTM (2013), BioeasyTM (2014), BiomanguinhosTM (2015 and 2016), and BioClinTM (2017). The reagent results were confirmed by a second immunochromatographic test of different methodology or by Western blot. Participants with reagent tests were referred for follow-up at our outpatient clinic.
For syphilis rapid testing, participants underwent immunochromatographic screening tests on finger-stick whole blood. The tests used were BiomanguinhosTM (2013, 2014, and 2015) and AlereTM (2016 and 2017). Asymptomatic participants with reagent tests and with no previous history of treatment for syphilis or at risk of re-exposure were referred for Venereal Disease Research Laboratory (VDRL) and follow-up at primary health care units or at our institution. Participants with no previous history of syphilis received a VDRL request and a prescription of benzathine penicillin G according to the presence of signs and symptoms of the disease.
For hepatitis B testing, participants underwent the immunochromatographic VIKIATM HBsAg test on finger-stick whole blood. Participants with reactive tests were referred for follow-up at our outpatient clinic.
For hepatitis C testing, participants underwent immunochromatographic screening tests on finger-stick whole blood. The tests used were WAMATM (2013 and 2014) and AlereTM (2015, 2016, and 2017). Participants with reactive tests were referred for hepatitis C polymerase chain reaction and follow-up at our outpatient clinic.
Data from the database created at the end of each campaign were stored and analyzed using the Epi InfoTM version 7.2.2.6 statistical software. Quantitative variables were described using central tendency and dispersion measures. Absolute and relative frequencies were calculated for each categorical variable, including gender, skin color, level of education, marital status, history of psychoactive substance use, history of STIs, hierarchical HIV exposure classification, and rapid test results for each STI. The variable number of years of formal education was initially categorized into five groups (in complete years: none; 1–3; 4–7; 8–11; and 12 or more). Based on distributions and risk levels, the variable and number of sexual partners per year was initially categorized into eight categories (none; one; two; 3–5; 5–10; 11–20; 20–50; and 50 or more). The frequency of seropositivity for each STI was calculated according to the year of the campaign.
Univariate analysis was used in order to identify the factors associated with seropositivity for HIV, hepatitis B and C, and syphilis. Categorical variables were grouped in a dichotomous manner based on subgroups similarity. Comparisons between numeric variables were made using ANOVA or the Kruskal–Wallis test for two groups when appropriate. The categorical variables were expressed as absolute and relative frequencies and compared using 2-tailed Fisher’s exact test.
Variables that showed p values less than 0.15 in univariate analysis were retained for the multivariable analysis. The multiple logistic regression model started with the following variables for prediction: male versus female gender; age by year; white color versus other races; married/stable union versus other civil states; education level of up to 11 years versus 12 years or more of formal education; self-identified MSM versus other sexual orientations; and number of sexual partners category. A backward elimination was used to successively remove factors with the largest p value until all variables in the model had a p value less than 0.05.
Results
Characteristics of participants.
n: number of participants.
aHierarchical classification: intravenous drugs → oral or inhaled drugs → alcohol.
A total of 15 participants tested positive for HIV, seven of them reported being first-time testers. Eleven HIV-positive participants were followed up at our institution, and three chose to be treated elsewhere. One participant was lost follow-up and died four years later. Thirty-two participants tested positive for syphilis. Nine of them with reactive testing and without previous history of syphilis underwent confirmatory serological testing (VDRL and/or fluorescent treponemal antibody absorption test) and treatment at our outpatient clinic. Three patients with a previous history of treatment had a nonreactive VDRL or titer below 1: 4. Twenty patients with reactive testing decided not to perform the confirmatory test and treatment at our institution and were referred for treatment in primary care units, eight of whom had a previous history of treatment. Among the 32 participants who tested positive for syphilis and the 15 participants who tested positive for HIV, there were three patients who tested positive for both HIV and syphilis. Two participants who tested positive for syphilis received immediate treatment with benzathine penicillin G as one patient had a genital lesion compatible with primary syphilis and the other was coinfected with HIV. Three patients had positive rapid tests for hepatitis C and five for hepatitis B.
Univariate analysis of demographic characteristics associated with rapid test results for HIV, syphilis, hepatitis B, and hepatitis C in a university community—2013–2017, São Carlos.
n: number of participants.
aTwo-tailed Fisher’s exact test.
bANOVA.
Univariate analysis of behavioral characteristics associated with positive test results for HIV, syphilis, hepatitis B, and hepatitis C in a university community—2013–2017, São Carlos.
n: number of participants; MSM: men who have sex with men.
Heterosexual men, homosexual and heterosexual women.
Fisher’s exact test.
Two participants with first test positive, not confirmed by second test (2013 and 2015).
ANOVA.
Kruskal–Wallis test for two groups.
Multiple logistic regression of factors associated with reagent tests for HIV and syphilis in a university community—2013–2017, São Carlos.
MSM: men who have sex with men.
Discussion
The present study demonstrated the impact of testing campaigns at university campuses in detecting HIV infection and syphilis. The relatively higher detection rates for HIV (0.56%) and syphilis (1.2%) shown by the study contrast with the detection rates found in blood bank studies, where the detection rates for HIV vary from 0.05% to 0.18%, and for syphilis, from 0.13 to 0.57%.14,15 The prevalence rate of HIV infection in the total Brazilian population has also remained stable and estimated at 0.4%. 2
Although university communities are not formally considered as a key population for HIV infection, this population tends to engage in behaviors that put them at risk of STIs such as alcohol use, illicit drugs use, permissive attitudes toward casual sex, history of STI diagnosis, poor STI knowledge, and low STI and HIV testing rates.16–22 The importance of identifying university population as a STI at risk group was illustrated by a 2003 outbreak of HIV infection in North Carolina, USA. 23
The percentage of positive test results for HIV were particularly high in the early years of the campaign, reaching 0.88% in 2014. The high rates were probably due to the high vulnerability of this population and to the pent-up demand for HIV testing. This was an expected response, since on-site testing strategy has been described as an effective way to increase youth access to diagnosis of HIV infection and to insert them more quickly in health services. 24 To deal with the situation, the São Carlos STD/AIDS Program implemented a permanent counseling and testing service within the UFSCar campus and expanded the post-sexual exposure prophylaxis network.
Our study found out a HIV coinfection rate of 9.4% among participants with syphilis, which corresponded to a 20% syphilis coinfection rate among HIV-positive participants. A high prevalence of syphilis and HIV coinfection has been commonly detected in clinical practice, since the two diseases share the same transmission route.25,26 In addition, syphilis coinfection can increase HIV transmission, both by increasing viral spread by open mucosal sores and by increasing the patient’s viral load. HIV-positive patients tend to have unusual primary lesions, a higher rate of asymptomatic infection, more aggressive secondary syphilis, and early neurological involvement. 27 Therefore, it is in arguable that coinfection should be regarded as an important factor in the diagnosis and treatment of both infections.
The seropositivity rate for HIV and syphilis was higher in men who have sex with men. This is consistent with other studies that have found out that HIV seropositivity among MSM is associated with multiple sexual partners, unprotected sex, and diagnosis of other STIs.23,28
The low detection rate for hepatitis B (0.19%) in our predominantly university community is in line with the low incidence of the infection in young people in Brazil, particularly in the Southeast. 29 The decreasing prevalence observed over the years suggests an increasing and successful vaccination coverage in young people. 30
The hepatitis C positivity rate was also low (0.11%) and increased with age. This scenario was probably due to improved safety in transfusions of blood and blood products, reduced drug injection and needle sharing, improved sterilization of health and beauty equipment, increased use of disposable sharps, and increased screening and treatment of HCV infection in Brazil. 31
The main limitation of this study is the use of voluntary HIV and STI testing, which could have led to voluntary response bias. This selection bias may affect the external validity of the study, since the population at greatest risk may not have participated in the campaigns. Despite this limitation, the campaigns diagnosed at least one infection in 1.9% of participants. Another limitation is that the study encompasses the entire university community, not just students. However, university campuses are open to the community, which frequents and interacts with academics, students, and staff.
Conclusion
The university community, especially MSM, has been shown to be vulnerable to HIV infection and syphilis. High rates of HIV positivity were observed in the early years of college, and high rates of positivity for syphilis were associated with age and having three or more sexual partners per year. These results demonstrate the importance of implementing and maintaining programs for prevention and treatment of HIV infection and other STIs in high schools and university campuses. At the same time, efforts must be made to strengthen the partnership with the local health network, in order to refer patients to care as soon as possible.
Members of SANCAHIV Audit and Standards Subcommittee
Rede de São Carlos de Testagem para HIV (SANCAHIV): PROGRAMA MUNICIPAL DE DST/AIDS: Cintia Martins Ruggiero, Isabella Gerin de Oliveira Bomfim, Conceicao Walsimary Justa Uchoa, Fabiana Sayuri Tanikawa, Ana Maria Zabeu, Wania Cristina de Souza Moraes, Daniela Maria de Oliveira Falcão, Daniela Cristina Gomes, Márcia Milani, Lais Fernanda de Souza Pizzi, Vera Lúcia Simões Campos, Karla Elisabeth Hoffmann Rodrigues, Alessandra Cristina de Oliveira, Stefanie Leda, Bianca Bolzan Cieto, Ana Lúcia Bernardo Soares, Adriana Aparecida Blanco Minatti, Calógeras Antônio de Albergaria Barbosa, Carlos Fischer de Toledo, Bárbara Rezende Martins, and Robson Poul L Tiossi; UNIVERSIDADE FEDERAL DE SÃO CARLOS (UFSCar): (a) Departamento de Assistência à Saúde: Marta Maria Troiano Cury; (b) Departamento de Enfermagem: Simone Protti, Rosely Moralez de Figueiredo, Anamaria Napoleão, Isabella Gerin de Oliveira Bomfim, Mariana Ramos da Silva, Amanda Alessandra dos Reis, Ana Carolina Belmonte Assalin, Silas Zil, and Rafaela Camila Freitas da Silva; (c) Departamento de Medicina: Sigrid De Sousa dos Santos and Silvana Gama Florêncio Chachá; (d) Liga de Infectologia da UFSCar: Glória Selegatto, Lucas Sales Fidelis, Olívia S. Zanetti, Alexandre Botelho de Paula, Abner Carnizello Souza, and João Lucas Dourado do Val; (e) Departamento de Psicologia: Moira Scorse, Thales Cervi Mariana Gonçalves Fabrício, Camila Almeida Pinho, Renan Aparecido da Silva Reis, and Luana Alves Corrêa; UNIVERSIDADE DE SÃO PAULO (USP): Helen Cristina Pedrinho; CENTRO UNIVERSITÁRIO CENTRAL PAULISTA (UNICEP): Tânia Maria Marcondes, Denise Gili Ferreira, and Andrea dos Reis Fermiano; ETEC PAULINO BOTELHO: Cleide Maria da Costa, Professora Cristiane Leite de Almeida, Jandira Ferreira da Silva, and Gláucia Regina Lopes Negre.
Footnotes
Authors’ contributions
IGOB and SDSS conceived the study and participated in the design; IGOB, SDSS, CMR, and AAN participated in the testing campaigns; IGOB and SDSS performed the data collection, organization, and the preliminary statistical analysis; IGOB, SDSS, CMR, and AAN drafted the manuscript. All authors read and approved the final version of the manuscript.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was supported by Prefeitura Municipal de São Carlos, SP (Brazil)
Ethical approval
This study was approved by the Human Research Ethics Committee of the Federal University of São Carlos (CAAE: 29135114.8.0000.5504/2016), with the consent and participation of the São Carlos Department of Health, which waived the need for informed consent.
Data availability statement
The majority of data collected and analyzed for the study are included in the article. The complete data are available at the Brazilian STD/Aids campaigns data bank. Individual data will not be shared to ensure confidentiality and privacy, as required by the local Human Research Ethics Committee.
