Epidemiological data on HIV-infected patients and the importance of education regarding the infection rate. An analytical cross-sectional study

Abstract BACKGROUND: Sexually transmitted diseases (STIs) are an important public health problem in all countries. Knowledge of their relationship with the various socioeconomic levels is necessary for an understanding of their epidemiology and behavior in society. OBJECTIVE: To investigate the epidemiology of human immunodeficiency virus (HIV)-positive patients and to correlate education with history of sexually transmitted diseases, especially for syphilis. DESIGN AND SETTING: Analytical cross-sectional study carried out in the city of Juiz de Fora, Minas Gerais, Brazil. METHODS: The medical records of HIV/acquired immunodeficiency syndrome (AIDS) patients who started antiretroviral therapy (ART) between January 2010 and July 2018 were assessed. These patients were attended at the specialized assistance service for HIV/AIDS) of the Department of Sexually Transmitted Diseases (STD/AIDS) of the city of Juiz de Fora. In total, 335 patients were selected. RESULTS: In our sample, 73.13% were male; 57.36% were aged between 25 and 45 years and 24.23% were over 45 years of age. Regarding sexual orientation, 61.78% were homosexual. Regarding education, 52.88% had “unskilled education”, while 47.12% had “qualified education”. Analysis on the relationship between schooling and syphilis, a positive relationship between qualified schooling and syphilis was observed: odds ratio = 3.588; 95% confidence interval: 1.090-11.808. CONCLUSION: Homosexual male patients are most affected by HIV. Furthermore, this disease is not limited only to individuals with low education. Syphilis should be suspected in all individuals.


INTRODUCTION
Sexually transmitted infections (STIs) are a public health problem and affect the lives of people around the world. This situation is associated with high rates of transmission, often explained by the view that people are not well informed about the transmission of these diseases or ignore the mandatory precautionary measures for safe sex. Individuals infected with any STI are five to ten times more likely than non-infected individuals to acquire or transmit the human immunodeficiency virus (HIV) through sexual contact. 1 Many asymptomatic or undiagnosed individuals transmit HIV, syphilis and hepatitis B and C, either sexually or through contact with contaminated blood, as in the transmission of hepatitis C. 2 In Brazil and worldwide, HIV infection persists and is often associated with other STIs.
Co-infection with HIV and syphilis, for example, has synergistic action and increases the transmissibility of HIV. 3 According to the Brazilian Ministry of Health, syphilis cases have increased mainly among people with "qualified" education level. This also represents a major problem and risk with regard to the transmissibility of HIV. 4

OBJECTIVE
The objectives of this study were to outline the epidemiological data on HIV-positive patients, and to correlate these patients' education with occurrence of other STIs, such as syphilis, in Juiz

Adjusted analysis
We constructed a logistic regression model to determine the interaction between schooling and sexually transmitted infections.
First, statistical comparisons were made between schooling and other variables using the Wilcoxon signed-rank test for continuous data and Fisher's exact test, two-sided for nominal variables.
Then, the variables that were significantly correlated at P > 0.05 (age, sex and syphilis) were included in the logistic regression model. Adjusted odds ratios (OR) and 95% confidence intervals (95% CI) were calculated. The logistic regression was performed using the R Core Team software, version 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria).

RESULTS
This study evaluated 335 patients with HIV. The epidemiological characteristics of these patients are shown in Table 1. In order to investigate correlations between educational level and sexually transmitted infections, an odds ratio (OR) analysis was performed through logistic regression. The individuals analyzed were separated into two groups: the first was named "quali-  Given that skilled education is age and sex-dependent, a logistic regression analysis was performed, with adjustments for these variables ( Table 3). The difference between qualified and unskilled education was found to be nonsignificant in this adjusted model (P = 0.675), as was age (P = 0.581). However, being male (OR 3.9; P = 0.055) and being positive for syphilis (3.588; P = 0.035) were significantly correlated with qualified education. 26 men for every ten women. 5 In the sample studied, a ratio of 2.98 (M:F) was observed, i.e. close to 30 men for every 10 women.

DISCUSSION
We separated transgender individuals from these proportions, in order to ascertain the prevalence of this population in the sample.    Table 3. Logistic regression results shows that some patients with STIs now have qualified education levels, i.e. that STIs are not just prevalent among individuals with less school education.
In addition, among men, over the period observed, it was found in another study that 51.3% of the cases were due to homosexual or bisexual exposure, while 31.4% were heterosexual. 5 In our sample, 61.78% of those infected were homosexuals, and 94.3% of them were male. Among women, it has been noted that 86.5% of the cases fall into the category of heterosexual exposure in Brazil. 5 In the sample of our study, 53% of the heterosexuals were female and about 95% of the bisexuals were female. This situation demonstrates that the population most affected is still that of individuals with homosexual sexual orientation and is concentrated more in the male sex, while in the heterosexual group there is a tendency towards equality between the groups, i.e. in this group the female and male sexes have similar distributions.

This situation is similar to what has been seen in the United
States. Homosexual and bisexual men together form a group that corresponded to 86% of new infections in the United States and its dependent territories in 2017. Homosexual exposure among men corresponded to 79% of the infections diagnosed that year, with or without an association with the use of injectable drugs, i.e. a proportion considerably higher than the 51.3% seen in Brazil. 6 However, regarding American women, 76% became infected through heterosexual exposure and another group of 21%, through injecting drugs. 6 HIV affects approximately 35 million people worldwide, and approximately 8.6% of them are co-infected with HBV. 7 The rates of HIV/HBV co-infection vary according to the origin of the population studied and the geographical location. 8,9 In a group of 297 patients evaluated at the Hospital de Clínicas, Universidade Federal do Paraná (UFPR), Brazil, the prevalence of hepatitis B markers was significantly associated with HIV infection, in comparison with the prevalence observed in the general population of the same geographical area. 10 Out of the 48 patients analyzed in our study, only one had positive HBV serological tests. In addition, the prevalence of HIV/HCV co-infection was low in the group analyzed here, and this was also observed in studies in Recife and Pará. 11,12 In a hospital in Porto Alegre, Brazil, anti-HCV was observed in 126 out of 330 cases (38.2%). 13 This situation confirms the idea that the prevalence of these associations depends on the geographical location.
In 2018, 158,051 cases of acquired syphilis were reported to SINAN. This condition has been subject to compulsory notification since 2010. Its detection rate increased from 34.1 to 75.8 cases per 100,000 inhabitants between 2015 and 2018. In 2018, among the cases in which the education level was reported, 39.5% of these individuals had reached at least high school education. 4 In the group analyzed here, a positive correlation with individuals with higher education levels was observed: these individuals were more likely to have contracted syphilis than individuals with lower education. The main limitation to this finding was the number of individuals from whom the rapid test results were notified (92 patients). Nonetheless, this relationship is extremely important from a public health point of view, given that it may indicate that campaigns to prevent these diseases are not being effective, since individuals with higher socioeducational levels do not follow preventive measures. It is worth mentioning that the population studied consisted of individuals with HIV and, therefore, presented higher risk of severe forms.
Education is associated with STIs, as observed in a previous survey conducted in São Paulo. 14 An association between past STIs and lower levels of schooling has been described in the literature. 15 However, because of the limitation of the size of the population studied, we were unable to add data from other STIs to the logistic regression analysis, such as hepatitis B and C.

CONCLUSION
Our analysis shows that HIV is still a prevalent disease in society, and is more prevalent among males and homosexuals. It is similarly distributed across all educational levels; i.e. individuals with qualified education have a prevalence similar to that of individuals with unskilled education. This demonstrates that this public health problem transcends socioeducational levels.
In addition, syphilis is an emerging problem in the context of public health, and it should receive special attention for the entire population. Its incidence is not restricted mainly to less-favored socioeducational groups.