Seroepidemiological survey of hepatitis C virus among commercial sex workers and pregnant women in Kinshasa, Democratic Republic of Congo

C Laurenta, D Henzelb, C Mulanga-Kabeyaa,c, G Maertensd, B Larouzéb,e and E Delaportea,f

a Laboratoire des Rétrovirus, Institut de Recherche pour le Développement (IRD), Montpellier, France.
b Institut de Médecine et d'Epidémiologie Africaines, Hôpital Bichat-Claude Bernard, Paris, France.
c Projet Sida, Kinshasa, RDC.
d Innogenetics, Ghent, Belgium.
e INSERM U444, Hôpital Saint Antoine, Paris, France.
f Service des Maladies Infectieuses et Tropicales, CHU Gui de Chauliac, Montpellier, France.

Eric Delaporte, Laboratoire des Rétrovirus, IRD, 911 Avenue Agropolis, BP 5045, 34032 Montpellier Cedex 1, France. E-mail: Eric. Delaporte{at}mpl.ird.fr


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background Studies conducted mainly in industrialized countries have shown that the transmission of hepatitis C virus (HCV) is mainly parenteral, and have emphasized the role of nosocomial transmission. In Equatorial Africa, the respective contributions of parenteral and non-parenteral routes of transmission are unknown. The potential role of sexual transmission in this area of high HCV endemicity, where sexually transmitted infections (STI) are frequent, is suggested by the fact that HCV infection is rare in infants and young adolescents, but increases thereafter with age. The present study, conducted in Democratic Republic of Congo, was designed to determine the prevalence of HCV infection and associated sexual risk factors in two female populations with different sexual behaviour.

Methods Cross-sectional studies conducted among commercial sex workers (CSW; n = 1144) and pregnant women (n = 1092) in the late 1980s in Kinshasa showed a high frequency of at-risk sexual behaviour, STI and human immunodeficiency virus (HIV) infection, particularly among CSW. We screened samples collected during these epidemiological studies for antibodies to HCV using a second-generation ELISA with confirmation by a third-generation LIA. We also assessed sociodemographic variables, medical history, STI markers and sexual behaviour, and their potential association with HCV infection.

Results The overall prevalence of anti-HCV was 6.6% (95% CI : 5.2–8.2) among CSW and 4.3% (95% CI : 3.2–5.7) among pregnant women (age-adjusted OR = 1.5, 95% CI : 1.0–2.1, P = 0.05). Multivariate analysis showed that the presence of anti-HCV among CSW was independently associated with a previous history of blood transfusion (P < 0.001), age >30 years (P < 0.001) and the presence of at least one biological marker of STI (P < 0.03). No such links were found among pregnant women (although the history of blood transfusions was not investigated in this group). Anti-HCV was not associated with sociodemographic variables or sexual behaviour in either group, or with individual markers of STI. Despite the high-risk sexual behaviour and the higher prevalence of STI in CSW, the difference in HCV seroprevalence between CSW and pregnant women (6.6% versus 4.3%) was small, particularly when compared with the difference in the seroprevalence of HIV (34.1% versus 2.8%).

Conclusion The role of sexual transmission in the spread of HCV seems to be limited. Parenteral transmission (including blood transfusion and injections), possibly related to the treatment of STI, probably plays a major role.

Keywords Africa, hepatitis C virus, epidemiology, pregnant women, commercial sex workers, sexual transmission, blood transfusion


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Infection by hepatitis C virus (HCV) is now recognized as a major worldwide public health problem, owing to its high prevalence1 and to the high risk of chronicity, potentially leading to liver cirrhosis and hepatocellular carcinoma.2 The distribution and spread of HCV are heterogeneous, particularly in sub-Saharan Africa. We and others have reported high HCV seroprevalence rates, ranging from 10% to 20% among adults, in Eastern Gabon3,4 and South Cameroon.5,6

Studies conducted mainly in industrialized countries have shown that the main mode of HCV transmission is the parenteral route, and that intravenous drug use (IDU) and nosocomial transmission play important roles.7 Although HCV sexual transmission may occur, it is considered a minor route.8

In Equatorial Africa, where IDU is rare, the respective contributions of parenteral and non-parenteral routes of HCV transmission are unknown. The potential role of HCV sexual transmission in this area of high HCV endemicity and high prevalence of sexually transmitted infections (STI) is suggested by the fact that HCV infection is rare in infants and young adolescents, but tends thereafter to increase with age.3,5

In 1988 and 1990, in Kinshasa (Democratic Republic of Congo), epidemiological studies of STI and human immunodeficiency virus (HIV) infection among women have been conducted by Projet SIDA, in collaboration with the Centers for Disease Control and Prevention, Atlanta, USA and the Institute of Tropical Medicine in Antwerp, Belgium. Based on data and samples collected during these surveys, we investigated the seroprevalence and sexual risk factors associated with HCV among commercial sex workers (CSW) and pregnant women to document the potential role of HCV sexual transmission.


    Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The population selection, data collection and laboratory procedures used during the initial surveys have been extensively described elsewhere.9,10

Data collection
A total of 1233 CSW seen in 1988 at the Women's Health Center of Project SIDA were recruited. Prostitutes from various areas of Kinshasa had been visited by a team of social workers at their work place to invite them to participate in the study. After they gave informed verbal consent, women who considered themselves prostitutes were interviewed by a nurse and examined by a physician. Demographic data and information on sexual behaviour and the medical history were collected using a standardized questionnaire. Blood samples and vaginal and endocervical specimens were collected for laboratory diagnosis.

From March to August 1990, 1166 pregnant women were selected at random (every fifth woman with their consent) during their first antenatal visit to four antenatal clinics. Interview and clinical examination including swab tests and serum collection were performed in the same way as CSW. Both studies were approved by the National Ethical Committee of the Ministry of Health of Zaire.

Laboratory procedures
Briefly, direct microscopic examination of vaginal smears was used to detect Trichomonas vaginalis and Candida albicans. Neisseria gonorrhoeae was identified by culture on modified Thayer-Martin medium. Chlamydia trachomatis antigen was detected in endocervical specimens by means of EIA (Chlamydiazyme Abbott, North Chicago, IL, USA). Syphilis was diagnosed by using the RPR test (Becton Dickinson) and TPHA (Fujirebio, Japan). The HIV testing was performed using an ELISA technique (Vironostika; Organon Teknika, Boxtel, The Netherlands) with western blot confirmation (Dupont, Wilmington, DE). The Papanicolau (PAP) staining technique was used to detect cytological evidence of human papillomavirus infection. When a genital ulcer was present, a specimen was cultured for Herpes simplex on Vero cells and Haemophilus ducreyi was detected on Mueller-Hinton medium.

In addition, for the purposes of the present study, sera stored at –20°C until tested were screened in 1995 for antibodies to HCV (anti-HCV) using a second-generation enzyme immunoassay (HCV EIA 2.0, Ortho Diagnostics, Roissy, France). All positive samples were confirmed using a third-generation line immunoassay (Innolia HCV Ab III, Innogenetics, Ghent, Belgium).

Statistical analysis
Data were analysed using EPIINFO 6.04 (Centers for Disease Control and Prevention, Atlanta, USA) and Logistic Regression 3.11Ef (Dallal GE, Andover, USA) software. The {chi}2 test and, when appropriate, Fisher's exact test, were used to compare the distribution of qualitative variables according to HCV serostatus. For continuous variables, comparisons were based on analysis of variance (ANOVA) when the distribution was normal, and otherwise on the non-parametric Kruskal-Wallis test. Variables associated (P < 0.25) with anti-HCV in univariate analysis were entered in a multiple logistic regression model. The Hosmer-Lemeshow statistic was used to assess the goodness-of-fit of the final model.11


    Results
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Prevalence of and risk factors for HCV infection among commercial sex workers
The mean age of CSW (n = 1144) was 25.8 ± 0.2 years (range: 14–55 years). A total of 874 CSW (76.4%) were not born in Kinshasa, including 298 (26.0%) who were born in Province Equateur and 183 (16.0%) in Province Orientale. The median length of prostitution was 3 years and the median number of clients per day was 2. This high-risk behaviour explains the high STI prevalence rate: 77.1% (n = 882) of the women (95% CI : 74.5–79.5%) had at least one STI marker. A history of blood transfusion during the last 10 years was reported by 12.1% (n = 137) of the prostitutes. In this population the HIV seroprevalence was 34.1% (390/1144; 95% CI : 31.3–36.9%).

The overall HCV seroprevalence was 6.6% (95% CI : 5.2– 8.2%). As shown in Figure 1, HCV seroprevalence increased with age, from 2.8% in the 14–20-year age group to 21.3% in the over-40 year age group ({chi}2 for trends: P < 0.001). The seroprevalence rate was significantly higher in the >30 year age group than in the <=30 year age group (Table 1Go). A striking association was found between anti-HCV and a history of blood transfusion. Among the 137 CSW who reported one or more episodes of blood transfusion during the past 10 years, 13.1% (n = 18) were anti-HCV-positive, compared to 5.5% (n = 55) of those who had not been transfused (P < 0.001).


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Table 1 Relationship between HCV seropositivity and selected variables in commercial sex workers in Kinshasa, 1988 (univariate analysis)
 
Additional univariate analysis showed that level of education (P = 0.3), geographical area of origin (P = 0.1) and number of years spent in Kinshasa (P = 0.1) were not related to anti-HCV positivity. As regards behavioural variables, the HCV seroprevalence rate was only associated with the length of prostitution: CSW with more than 5 years in prostitution were at a higher risk of HCV infection (9.9% versus 5.4%, P = 0.007). No association was found between HCV infection and the following variables: number of clients per day, sexual practices, regular use of vaginal pharmaceutical or traditional products, history of one or more abortions and use of any contraceptive method during the past 5 years.

Among the STI markers, only syphilis seropositivity was associated with the presence of anti-HCV (P = 0.002). No difference in the HCV seroprevalence rate was observed according to HIV serostatus (7.4% versus 6.1%, P = 0.4). The HCV prevalence rate was higher among CSW who had at least one STI marker than in those with none (7.5% versus 3.4%, P = 0.02). The number of medical visits for symptoms of STI during the last year was not significantly associated with anti-HCV.

In multivariate analysis, only older age, a history of blood transfusion and the presence of at least one STI marker remained significantly associated with HCV infection (Table 2Go). The Hosmer-Lemeshow statistic showed the good fit of the final model (C = 5.012; 8 d.f.; P = 0.8).


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Table 2 Relationship between hepatitis C virus seropositivity and selected variables in commercial sex workers in Kinshasa, 1988 (multivariate analysis)
 
Prevalence of and risk factors for HCV among pregnant women
The pregnant women recruited for this study (n = 1092) were young (mean age: 25.6 ± 0.2, range: 14–45) and usually married (66.9%), including 225 women in polygamous marriages; 22.4% (n = 245) were single and only 9.9% (n = 108) reported living with one partner without being married. During the year preceding the survey, 19.9% (n = 217) of the women reported more than one sexual partner. Only 41 women (3.8%) declared using condoms regularly. At least one marker of STI was found in 427 pregnant women (39.1%). The history of blood transfusion was not investigated. The HIV seroprevalence rate was 2.8% (95% CI : 2.0–4.1%).

In this group the overall HCV seroprevalence rate was lower (4.3%, 95% CI : 3.2–5.7%) than in CSW (age-adjusted OR = 1.5, 95% CI : 1.0–2.1, P = 0.05) despite a similar age distribution in the two groups. No association was found between anti-HCV and the following variables: age, marital status, multiple sexual partners, condom use, STI markers including HIV and the presence of at least one STI marker (Table 3Go).


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Table 3 Relationship between HCV seropositivity and selected variables in pregnant women in Kinshasa, 1990 (univariate analysis)
 

    Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
This study of the seroprevalence of and risk factors for HCV infection among CSW and pregnant women in Kinshasa, DRC, showed a higher HCV seroprevalence among CSW than pregnant women (6.6% versus 4.3%, P = 0.05). Hepatitis C virus infection was not related to at-risk sexual behaviour or STI markers taken individually, but, among CSW, HCV infection was associated with the presence of at least one of these markers and a history of blood transfusion (a factor which was not investigated among pregnant women).

Most studies of HCV seroprevalence performed in Equatorial Africa including Eastern Gabon3,4 and South Cameroon5,6 were community based. Therefore, comparisons of their results with ours are difficult owing to differences in the population selection procedure. However, our results, obtained in a large population sample with a more accurate laboratory procedure, confirm the high HCV endemicity in this area. Pregnant women are not representative of the general population, but, as with HIV, they are a readily accessible sentinel group. Recent studies conducted in Ethiopia showed a close correlation between HCV seroprevalence in random samples and consecutively recruited pregnant women from the same community.12

The low HCV seroprevalence in younger CSW and the shape of the age-specific prevalence curve are not in favour of a strong impact of sexual transmission in this population with high-risk sexual behaviour, reflected by the high prevalence of STI markers and by the behavioural variables. This is consistent with a lack of any association between these variables and anti-HCV. The fact that the relationship between anti-HCV and age was not observed among pregnant women might be related to lower exposure to HCV, but the small sample size in the older age range should be taken into account in the interpretation of the results.

The higher HCV seroprevalence rate among CSW compared to pregnant women may point to the existence of HCV sexual transmission, as CSW have more at-risk sexual behaviours and a higher prevalence of STI. However, the difference in the HCV seroprevalence rate between the two groups was small (4.3% and 6.6% in pregnant women and CSW), particularly when compared with that of HIV (2.8% versus 34.1%). The lack of association between HCV seroprevalence rate and HIV serostatus in CSW argues for a low sexual transmission impact since HIV is mainly sexually transmitted in this population. We only found an association between STI and HCV when all the STI markers were considered together.

The cross-sectional nature of our investigation makes it difficult to interpret the association (or lack of association) between STI and HCV infection, except for syphilis, which induces long-lasting antibodies (but syphilis was not associated with HCV after controlling for age). Other STI may have been acquired a few days or a few months previously, while HCV could have been acquired several years previously. Therefore, STI should be essentially considered as markers of high-risk sexual behaviours.

The fact that the CSW in our study were not frequently infected by HCV despite their high-risk sexual behaviour is consistent with the result of studies in industrialized countries. Hepatitis C virus infection has been shown to be more frequent among CSW,13 sexually promiscuous subjects,14 and patients with STI and HIV1517 infection, but in several studies intravenous drug use was a confounding variable.8 In stable couples with one infected partner, the probability of HCV infection of the other partner increases with time18,19 but it is much lower than for HIV (with the possible exception, due to the higher HCV viral load, of index subjects co-infected by HIV20,21). The limited epidemiological evidence of HCV sexual transmission is consistent with the fact that HCV genetic sequences are seldom detected in semen or vaginal secretions of infected people.22,23

In our study a role of confounding variables in the higher HCV seroprevalence rate among CSW than among pregnant women cannot be excluded. The common use of intramuscular (IM) injections of drugs (mostly antibiotics) to treat STI in Africa, particularly among CSW, might, at least in part, explain the higher rate of HCV infection in this group. In many instances, these IM treatments are given within the ‘informal’ health system, where sterilization practices are often inadequate. The role of parenteral injections in the spread of HCV has been documented in Egypt, where previous mass treatment for schistosomiasis is considered responsible for the very high HCV seroprevalence rate.24

Blood transfusion is a highly efficient means of HCV transmission25 and played a significant role in the spread of HCV among the CSW we investigated, as shown by the strong association between a history of blood transfusion and seropositivity for HCV. Despite efforts to reduce the number of blood transfusions to control the spread of HIV, blood transfusion might still play an important role in the spread of HCV in highly endemic areas such as Central Africa. Screening blood donors for HCV infection is not yet a routine practice in many African countries. Given the high risk of chronicity, and subsequent cirrhosis and hepatocellular carcinoma associated with HCV infection, screening for anti-HCV in blood banks would be a cost-effective measure.

In conclusion, if our results do not rule out the existence of HCV sexual transmission, they strongly suggest that, even in Equatorial Africa (a highly endemic area) this potential means of transmission does not play an important role in the spread of HCV.


KEY MESSAGES

  • A seroepidemiological survey of HCV was conducted in 1988–1990 in Kinshasa, Democratic Republic of Congo.
  • Despite the high-risk sexual behaviour and the higher prevalence of STI in commercial sex workers (CSW), the difference in HCV seroprevalence between CSW and pregnant women (6.6% versus 4.3%) was small, particularly when compared with the difference in the seroprevalence of HIV (34.1% versus 2.8%).
  • The role of sexual transmission in the spread of HCV seems to be limited.

 



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Figure 1 Hepatitis C virus (HCV) and human immunodeficiency virus (HIV) seroprevalence according to age among commercial sex workers in Kinshasa, 1988

 

    Acknowledgments
 
The HCV study was supported by a grant from the European Commission (DGXII, STD3 programme). We wish to thank the Department of Epidemiology and Microbiology of the Institute of Tropical Medicine of Antwerp, Belgium (M Laga, P Piot) as well as the staff of projet SIDA, Kinshasa (Nzila Nzilambi) for their contribution.


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 Introduction
 Materials and Methods
 Results
 Discussion
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