Prevalence of human immunodeficiency virus/hepatitis C virus co-infection in Brazil and associated factors: a review

REVIEW ARTICLE

Prevalence of human immunodeficiency virus/hepatitis C virus co-infection in Brazil and associated factors: a review

Valdete Meurer Kuehlkamp^I; Fabiana Schuelter-Trevisol^I,II,*

^IPostgraduate Program in Health Sciences, Universidade do Sul de Santa Catarina (UNISUL), Tubarão, SC, Brazil

^IICentro de Pesquisas Clínicas, Hospital Nossa Senhora da Conceição, Tubarão, SC, Brazil

ABSTRACT

The hepatitis C virus and human immunodeficiency virus share the same transmission routes, which makes co-infection an unfavorable condition for the natural history of both viral diseases. In this context, it should be highlighted that the knowledge of the extent of co-infection and associated risk factors is a vital tool for prevention and control over infectious diseases. The aim of this study was to review the literature, seeking to examine the prevalence of human immunodeficiency virus/hepatitis C virus co-infection reported in studies conducted in Brazil, and identify the main risk factors associated with co-infection.

The electronic search was conducted in the Medline, Lilacs and SciELO databases. The following keywords were used: human immunodeficiency virus and Hepatitis C or hepatitis C virus and Brazil. The search led to 376 articles, of which 69 were selected for data extraction. We excluded animal studies, reports or case series, review articles, letters to the editor, other types of hepatitis and those studies in which co-infected patients were intentionally selected for comparison to single infected individuals. As a result, 40 articles were reviewed. The majority of the population in these studies was male (71%) and young adults, with a mean age of 26.7 years. The prevalence of hepatitis C virus co-infection among individuals living with human immunodeficiency virus in the studies conducted in Brazil ranged from 3.3% (serum samples) to 82.4% (drug users), with an average of 20.3%. The findings reveal that the prevalence of human immunodeficiency virus/hepatitis C virus co-infection is highly variable, depending on the characteristics of the study population. Risk factors associated with human immunodeficiency virus/hepatitis C virus co-infection were injection drug use and blood transfusion.

Keywords: HIV; Hepatitis C; Co-infection; Brazil

Introduction

The human immunodeficiency virus (HIV) and hepatitis C virus (HCV) share the same transmission routes, which causes high rates of co-infection, and is a severe clinical condition for both viral diseases.¹

HIV is most commonly spread by sexual contact with an infected partner, through contact with infected blood, accidental sticks or vertical transmission.² HCV transmission occurs mostly through infected blood and blood products, but sexual, accidental and vertical transmission has been also evidenced.³

The HIV/HCV co-infection is a significant risk factor for liver fibrosis, since HIV seropositivity and low CD4+ count seems to accelerate this process.^4,5 The progression of fibrosis in HCV/HIV co-infected patients occurs with high frequency during an average estimated time of three years.⁶ Similarly, HCV infection has been shown to be associated with faster progression to acquired immunodeficiency syndrome (AIDS).⁷

In Brazil, according to the Epidemiological Bulletin on Viral Hepatitis (2011), co-infection rates reach a percentage of 11.4% in HIV-seropositive patients.⁸ This percentage shows regional variation being dependent on the characteristics of the study population. However, this estimate is based on cases reported by the Information System for Notifiable Diseases (SINAN), and may not be representative of the general population, since only AIDS cases are reported, and there is a relative delay between case detection and publishing of reports.⁸

Therefore, this study is intended to review this issue, seeking to examine the prevalence of HIV/HCV co-infection encountered in studies conducted in Brazil, and identify the main risk factors for this co-infection.

Methods

This is a narrative review on HIV/HCV co-infection in Brazil. The electronic search was conducted in the Medline, Lilacs and SciELO databases. The following keywords were used: HIV [MeSH] and HCV [textline] or Hepatitis C [MeSH] and Brazil [textline] in English and the corresponding words in Portuguese. The references of the selected articles were examined for possible inclusion of additional articles.

We included original scientific articles that presented data on the prevalence of HIV/HCV co-infection in different population groups, of both sexes, conducted in Brazil.

We excluded studies that addressed animal studies, reports or case series, review articles, letters to the editor, other types of hepatitis and those in which co-infected patients were intentionally selected for comparison to single-infected patients.

Duplicate articles were excluded. We started reading the titles, then the abstracts, and later the full texts. Exclusion criteria were applied in all stages, always by consensus between two readers.

The selected articles were analyzed to characterize the study: year of publication, location and period of data collection, type of study, study population and sampling (number of investigated subjects, mean age and gender of participants), prevalence rates of HIV, HCV and HIV/HCV co-infection, and risk factors associated with the presence of co-infection.

HIV-infected individuals were considered those who had positive anti-HIV serology. HCV-infected individuals were considered those who had positive anti-HCV serology. The coinfection rates were taken directly from the articles, and when this information was not provided, they were calculated by dividing the number of individuals who had serological markers for HIV and HCV by the total number of participants in the study.

To calculate the mean age and the prevalence of HIV/HCV co-infection, we used descriptive statistics to find the weighted mean, taking into account the sample size of each study.

Results

The search led to 376 articles, of which 69 were selected for data extraction. After applying the exclusion criteria, 40 articles remained (Fig. 1). This study period covered articles published between April 1999 and June 2012.

Of the 40 articles analyzed, 36 were cross-sectional studies (one multisite), three cohort studies (two historical cohorts) and a descriptive study.

In total, we studied 48,791 subjects; of these, 28,819 (59.0%) were pregnant women, 13,483 (27.6%) were subjects or blood samples from HIV-infected patients, 2780 (5.7%) were individuals under restriction of freedom, 550 (1.1%) drug users, 3159 (6.6%) individuals with other characteristics, such as alcoholics, homeless people, garbage collectors, or patients attending various outpatient clinics.

Demographic characteristics available in the selected studies showed that the majority of participants were men (71%).^9-34 Of the 40 selected articles, men predominated in the samples of 26, with only one³⁵ showing a predominance of women. The samples of seven studies comprised only women.^35-41 The mean age was 26.7 years among the papers that presented this information.^{9-18,20-23,25,26,28,30-37,40-43} Eight of the selected papers had no data regarding gender and age of the participants.^38,39,44-49

In 20 articles,^{9-12,14-17,19-21,23,25,26,34,43-47} the study population consisted entirely of HIV-infected individuals or serum samples, and showed HIV/HCV co-infection rates ranging from 3.3%¹¹ to 54.7%⁴⁷ (Table 1), with an average of 19.5%. Including the studies with pregnant women^36,40 and injection drug users,²⁹ whose participants were all infected with HIV as well, the weighted mean of HIV/HCV co-infection was 20.3% among 13,894 participants.

Five papers studied pregnant women, aiming to determine the prevalence of certain infectious diseases and/or verify the risk of vertical transmission.^36-40 In these studies, the prevalence of HIV/HCV co-infection ranged from 0.00007³⁷ to 27.6%³⁹ (Table 2).

Among drug users^18,29,35 the prevalence of HIV/HCV coinfection ranged from 15.1%³⁵ to 82.4%²⁹ (Table 3). Five studies assessing individuals in restraint of freedom^{24,28,32,33,48} found a prevalence of co-infection ranging from 1.6%²⁸ to 7.1%³² (Table 4).

The HIV/HCV co-infection rates ranged from 0.6%³⁰ among homeless people who used hostels to 82.4%²⁹ among injection drug users. Studies that have determined the prevalence of HIV/HCV co-infection in other populations are presented in Table 5.

Out of the 40 papers reviewed only 14 reported data on risk factors associated with HIV/HCV co-infection, and these highlighted the injection drug use as the main transmission mechanism,^{12,14,15,18,22,23,25,34,42,46} followed by blood transfusion.^9,17,23,25 Behavioral risks such as tattooing,^11,23 piercing¹¹ and exposure to infected blood,¹⁴ although to a lesser extent, as well as sexual exposure,¹² homosexuality,¹⁸ and older age^22,25 were positively associated with the presence of HIV/HCV co-infection.

Discussion

This review comprised 40 studies that surveyed a total of 48,791 Brazilians, including pregnant women, subjects or blood samples from HIV-infected patients, individuals under restriction of freedom, drug users, individuals with other characteristics, such as alcoholics, homeless people, garbage collectors, or patients attending various outpatient clinics. Due to this regional and population diversity, the prevalence of HIV/HCV co-infection had great amplitude. This variation is explained by the exposure to different risk factors for coinfection.²

Thus, we chose to group the participants with similar characteristics, creating subgroups to analyze the seroprevalence rates of HIV/HCV co-infection.

Of the 20 studies that had determined the prevalence of HCV co-infection among individuals living with HIV, the average co-infection rate was 19.5%, which is higher than the rate of 11.8% published by the Ministry of Health in the last Epidemiological Bulletin of Viral Hepatitis.⁸ This can be attributed to the fact that this estimate is based on cases reported by the SINAN, and may not be representative of the general population, since only AIDS cases are reported and there is a delay between case detection and publishing of reports.⁸

The HIV/HCV co-infection rates among individuals in restraint of freedom are higher than in the general population. Containment is considered a risk factor due to crowding into small enclosures, promiscuity and rape, illicit drug use, and sharing of personal hygiene objects. These factors create favorable conditions for infection with HIV, HCV and co-infection.⁵⁰

According to the demographic characteristics of the participants in the different studies, 71% were men, which is in accordance with the national and international data showing that men are the most affected group by HIV, HCV and, consequently, co-infection.^8,51,52 The mean age was 26.7 years, i.e., young adults, unlike some studies that showed older age populations.^7,15 This discrepancy can be explained by the inclusion of teenagers³³ and pregnant women,^36-40 e.g., women of childbearing age, and therefore, younger, coupled with the fact that several studies did not provide the age of the study population,^{19,38,39,44-49} which may have underestimated this figure.^{19,38,39,44-49} It should be emphasized, however, that the predominance of men and young population represents the sample described in the studies, and not the co-infection cases, since these data were not available. Nevertheless, one can assume that there was a demographic similarity among the detected co-infection cases.

The articles that addressed studies with pregnant women showed a great variation of co-infection rates, ranging between 0.00007 and 27.6%.^36-40 This variation can be explained by the fact that only Costa et al.³⁷ conducted research with large numbers of pregnant women to determine the prevalence of infection with HIV, HCV and co-infection, reaching rate values of 0.13%, 0.22% and 0.00007%, respectively. These findings diverge from some different studies included in the review, whose main objective was to verify the vertical transmission by studying subgroups of HIVand HCV-seropositive subjects or both, thereby increasing the rates found. In Brazil, the prevalence of HIV infection in pregnant women is estimated to be 0.41%.⁵³ There is no national estimate of the prevalence of HCV infection among pregnant women, but the rate of HCV vertical transmission is 0.3%.⁸

Injection drug use is a major mode of HIV and HCV transmission.⁵⁴ In all studies included in this review, injection drug users had high rates of co-infection. This high rate of transmission can be attributed to the sharing of drug preparation equipment, facilitating HIV and HCV transmission through the exposure to contaminated blood.⁵⁵ This pathway is the main route of transmission for HCV. Drug injection practices also predispose to other risky behaviors such as promiscuity, lack of condom use, homosexual intercourse, among others.⁵⁶

Different HIV/HCV co-infection rates were observed among the study population that participated in the studies included in this review. The heterogeneity of the studies did neither allow summarizing the prevalence of coinfection in each subgroup nor an overall prevalence. Therefore, we opted to calculate just the weighted average of HIV/HCV co-infection rate in people living with HIV. The variation of coinfection rates found in this study is justified by the peculiar characteristics of the diverse population groups that are exposed to different risk factors.

The studies that reported data on risk factors associated with HIV/HCV co-infection highlighted that drug injection practices were the main transmission mechanism,^{12,14,15,18,22,23,25,34,46,57} followed by blood transfusion.^9,17,23,25 Since the risk factors for HIV and HCV have close connection, these can be characterized as behavioral and biological factors.⁵⁸

The limitations of this review include missing information in some articles that could allow a more detailed analysis of the characteristics of the study populations and the risk factors for co-infection.

Conclusion

The data show that the prevalence of HIV/HCV co-infection is highly variable, depending on the prevalence of HIV and HCV infection, and the exposure to various risk factors in the study populations. The prevalence of HIV/HCV co-infection among people living with HIV was 20.3%. Risk factors associated with HIV/HCV co-infection were injection drug use and blood transfusion.

Conflict of interest

All authors declare to have no conflict of interest.

Received 27 September 2012

Accepted 29 October 2012

Available online 13 May 2013

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Publication Dates

• Publication in this collection
  16 Aug 2013
• Date of issue
  Aug 2013

History

• Received
  27 Sept 2012
• Accepted
  29 Oct 2012