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Am. J. Trop. Med. Hyg., 72(6), 2005, pp. 762-767
Copyright © 2005 by The American Society of Tropical Medicine and Hygiene

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RISK FACTORS ASSOCIATED WITH HEPATITIS C AMONG PATIENTS CO-INFECTED WITH HUMAN IMMUNODEFICIENCY VIRUS: A CASE-CONTROL STUDY

MARIA CÁSSIA JACINTHO MENDES-CORREA, ANTONIO ALCI BARONE, AND REINALDO JOSÉ GIANINI
Casa da AIDS, Division of Infectious and Parasitic Diseases, Hospital das Clinicas, Laboratory of Medical Investigation in Hepatitis, and Laboratory of Medical Investigation in Epidemiology and Statistics, Medical School, University of São Paulo, São Paulo, Brazil


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A case-control study was carried out to assess the risk factors associated with hepatitis C in patients infected with human immunodeficiency virus. One hundred eighteen patients tested positive for hepatitis C virus (HCV) and were included as cases, and 117 tested negative for HCV and were included as controls. Information was collected through a questionnaire. The risk factors that showed a significant association with co-infection by multivariate analysis were an age of 30–39 years (odds ratio [OR] = 4.65, 95% confidence interval [CI] = 1.31–16.43), an age of 40–49 years (OR = 6.48, 95% CI = 1.70–24.78), an age > 50 years (OR = 7.50, 95% CI = 1.54–36.68), use of intravenous drugs (OR = 25.46, 95% CI = 4.91–131.88), use of inhaled illicit drugs (OR = 3.56, 95% CI = 1.22–10.44), anal intercourse (OR = 3.93, 95% CI = 1.27–12.13), a sexual partner with a history of liver disease (OR = 5.45, 95% CI = 1.33–22.32), a sexual partner with a history of blood transfusions (OR = 4.79, 95% CI = 0.95–24.19), and sexual partner with a history of intravenous drug use (OR = 3.46, 95% CI = 1.24–9.65).


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients infected with human immunodeficiency virus (HIV) have prevalence rates for infection with hepatitis C virus (HCV) higher than those in the general population. Different studies have shown that prevalence ranges from 11% to 90% in different parts of the world.1–7 The prevalence of HCV in the HIV-positive population differs geographically because of the distribution of risk factors that determines its transmission. In Brazil, there are few data concerning patients seropositive for both HIV and HCV. However, this prevalence ranges from 17.7% to 53% in different studies.8–10 Patients with parenteral transmission risk factors, intravenous drug users (IDUs), and recipients of blood and blood products show a higher prevalence of co-infection with HIV and HCV.11

A decrease in the number of new cases of infection with HIV among IDUs has been observed in Brazil and other parts of the world.12,13 Another factor contributing to a lower incidence of co-infection with HIV and HCV is adequate control of parenteral transmission associated with transfusion of blood or its derivatives. However, the longer survival of HIV-infected patients as a result of the increased effectiveness of anti-retroviral treatments indicates that the prevalence of patients co-infected with HIV and HCV will continue to be high in the near future, with many of these patients being potential candidates for specific treatment of infection with HCV.

The large reservoir of individuals infected with HCV provides a source of transmission to others at risk. Risk-modifying educational programs have been shown to be effective in preventing HIV transmission and are likely to be useful for decreasing HCV transmission. There are few studies in the literature that carefully describe risk factors for transmission of HCV in the co-infected group of patients. There are descriptive studies,3,8 but few analytical studies showing the association between strength and magnitude of the effect of the various risk factors reported by patients (compared with controls).

The purpose of the present study was to better understand the possible association between different variables of exposure related to HCV transmission in patients co-infected with HIV.


PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
We conducted a case-control study with a similar proportion of controls and cases in which we analyzed data collected from individual interviews using a structured questionnaire, medical charts, and specific laboratory tests. The questionnaire contained questions about variables of exposure. To select these variables, we took into account the exposure factors of HCV transmission reported in the literature, the biologic plausibility of the possible associations, and availability of data. The variables selected for the study were grouped into different categories: demographic (sex and age), patient history (blood transfusion, surgery, acupuncture, tattooing, body piercing, handling of blood, and hospitalization), patient sexual behavior (sexual orientation, sexually transmitted diseases, number of sexual partners, anal intercourse [it was not asked if this was forced or receptive], and history of sexual partners), liver disease, HIV status, blood transfusion, use of intravenous drugs, and use of illicit drugs (intravenous or inhaled). The classification of these variables is shown in Tables 1Go–3GoGo.


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TABLE 1
Distribution of cases and controls according to sociodemographic-and history-related variables*
 

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TABLE 2
Distribution of cases and controls according to sexual behavior–and use of illicit drugs–related variables*
 

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TABLE 3
Distribution of cases and controls according to sexual partner history–related variables*
 
The enrolled patients were selected from those registered at the Casa da AIDS in Sao Paulo, Brazil, a specific ambulatory setting directed to HIV-infected patients and their sexual partners. Different tests are ordered for all patients during the first visit, including serology for hepatitis B virus (HBV) and HCV. The patients with a diagnosis of HCV infection are referred to the Study Group of Viral Hepatitis at the Casa da AIDS, which operates in the same building and is staffed by four physicians . From January 1999 to July 2001, 235 patients were invited to participate in the study. All patients had been diagnosed with HIV infection and showed negative test results for hepatitis B surface antigen (HBsAg), hepatitis B e antigen (HBeAg), or antibodies to hepatitis B core antigen (HBc).

The exclusion criterion used was any patient positive for HBsAg, HBeAg, or antibodies to HBc. We excluded individuals with evidence of serologic markers of current or previous infection with HBV because transmission of this virus is associated with many factors that are also associated with transmission of hepatitis C.14

A total of 118 patients showed positive serology for HCV infection or were positive for HCV by a nested polymerase chain reaction (112 patients) and were included in the study. These patients were selected in chronologic order of care provided by the Study Group of Viral Hepatitis at the Casa da AIDS as of January 1999 up to the total number of interviews required to complete the size of the sample. In July 2000, we selected patients to form the control group. Using the schedule of the Casa da AIDS, we selected all eligible patients and checked their test results for HBV and HCV. Patients who were negative for antibodies to HCV in at least two different tests and who showed negative results for HBsAg, HBeAg, and antibodies to HBc were selected as controls. The patients were then invited to come for an interview and 117 were selected as controls. Two trained physicians administered the questionnaire. The local Ethics Committee reviewed and approved the study. All patients who participated in the study signed an informed consent term. Serologic testing for HIV, HCV, and HBV was performed according to standard procedures using licensed assays.

For HIV, we used an enzyme immunosorbent assay (EIA) and two commercial enzyme-linked immunosorbent assays (Organon Technika, Tournault, Belgium and Embrabio, Sao Paulo, Brazil) for confirmation. Specimens testing positive on the EIA and those with discordant or indeterminate results were confirmed by Western blot analysis. For hepatitis B, we used an EIA to determine positivity for HbsAg, antibody to HBs, total antibody to HBc, HBeAg, and antibody to HBe. For hepatitis C, we used third-generation EIAs for antibodies to HCV. To test for the presence of HCV RNA, we used a nested polymerase chain reaction according to the method of Garson and others,15,16 except that 25 cycles at 94°C for 40 seconds and 55°C for 40 seconds were used.

To calculate the sample size, we considered the following parameters: a 95% confidence level, a test power = 0.80, a prevalence of intravenous drug use in 20% of the HIV-infected patients, and an odds ratio (OR) between the case group and the control group concerning use of intravenous drugs = 2.5. The prevalence of IDUs in the HIV-infected population was estimated based on the study of 27 units that provide health care to HIV-infected patients in the state of Sao Paulo, where 20% reported previous use of intravenous drugs.17 We used this parameter as a population estimate for patients not infected with HCV. These parameters led to a sample size of 210 patients (105 in each group). Since we anticipated that patients might withdraw from the study, we included 10% additional patients. Therefore, the final sample size was 230 patients (115 patients in each group).

Analyses were carried out using Epi-Info 6.04b software (Centers for Disease Control and Prevention, Atlanta, GA). Co-infection with HIV and HCV was the dependent variable. The exposure variables selected for the study were the independent variables. We initially conducted an analysis of frequency distribution for each selected variable. To determine the number of sexual partners, we calculated the value closest to the median referring to the sum of sex partners in the control group during an individual’s lifetime. On this basis, we assigned the number of partners to two categories: up to eight sexual partners during one’s lifetime, and more than eight sexual partners. Only patients with more than eight sexual partners were considered to have been exposed. As shown in Table 2Go, we analyzed patients with up to eight partners (including in this category those who reported eight partners) and patients with more than eight partners. We conducted univariate analysis to test the association of each variable and co-infection (chi-square test), and calculated the OR (Cornfield’s method) and its estimated variation by the 95% confidence interval (CI). We used unconditional logistic regression with Stata software (Stata Corp., College Station, TX) for multivariate analyses that included the variables that had shown a level of significance < 0.20 for an association with co-infection in the univariate analysis. Final multivariate analysis also included also history variables: blood transfusion, surgery, acupuncture, body piercing, blood handling, and hospitalization. We excluded variables with a P value ≥ 0.05.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Tables 1Go–3GoGo show that the variables sex (males), age (30–39 years old), tattooing, sexual orientation (heterosexual), anal intercourse, number of sexual partners (> 8), partner with liver disease, HIV+ partner (unknown), partner with a history of blood transfusion (yes or unknown), partner is an IDU (yes or unknown), patient is a user of inhaled drugs, and patient is an IDU were associated with a higher risk of co-infection with HCV and HIV. Table 4Go shows the results of multivariate analysis (tattooing was excluded because it proved to be strongly associated with intravenous drug use and the latter was essential for the analysis). Each variable was simultaneously adjusted to the others. The independent risk factors that remained significantly associated with co-infection were an age of 30–39 years (OR = 4.65. 95% CI = 1.31–16.43), an of 40–49 years (OR = 6.48, 95% CI = 1.70–24.78), an age > 50 years (OR = 7.50, 95% CI = 1.54–36.68), use of intravenous illicit drugs (OR = 25.46, 95% CI = 4.91–131.88), use of inhaled illicit drugs (OR = 3.56, 95% CI = 1.22–10.44), anal intercourse (OR = 3.93, 95% CI = 1.27–12.13), a sexual partner with a history of chronic liver disease (OR = 5.45, 95% CI = 1.33–22.32), a sexual partner with a history of blood transfusion (OR = 4.79, 95% CI = 0.95–24.19) and a sexual partner who was an IDU (OR = 3.46, 95% CI = 1.24–9.65).


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TABLE 4
Risk factors associated with HCV infection in HIV+ patients by multivariate analysis (unconditional logistic regression)*
 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of our study demonstrated that HCV infection was associated with inhaled illicit drugs, an age > 30 years old, and a history of anal intercourse. In addition, our results confirm that intravenous drug use was the most important risk factor associated with HCV infection, as also reported by others.3,18,19 Our results confirm that sexual partners with risk factors for transmission of HCV were also associated with HCV infection. We expected the association between use of intravenous drugs and HCV infection. The use of illicit intravenous drugs is currently the main mechanism of HCV transmission and is quite common in the HIV-infected population. The present results also showed that the use of inhaled drugs was associated with co-infection. Transmission of HCV via intranasal entry during use of cocaine has been reported in the literature.20,21 The use of sharp instruments such as straws or straw-shaped money bills can cause mucosal bleeding in users. Thus, the transmission of the virus would occur through the friable and unprotected mucosal membrane of the drug users when sharing instruments. The lesions could have served as an entry for HCV, a fact that would explain the association of the events reported in our study.

With regard to the demographic variables, the association we observed with an age > 30 years old and HCV infection has also been reported in other regions of Brazil.22,23 It is interesting to point out that univariate analysis did not demonstrate an association of co-infection in patients > 50 years old. However, multivariate analysis demonstrated that the risk for co-infection increased with age beginning at 30 years, including patients > 50 years old. We were unable to determine the influence of any particular variable that would justify a modification of the importance of this risk factor after multivariate analysis. This probably occurred due to the sum of the confounding effects of other risk factors that are highly prevalent in the group 30–49 years old. Once these confounding effects were eliminated (by multivariate analysis), a higher risk (independent effect) appeared an age > 50 years old. Tattooing was strongly associated with HCV infection, but was not considered in the final analysis due to its strong association with intravenous drug use.

The importance of sexual activity in the transmission of HCV has not been well established and the results of different studies are controversial.18,24 Concerning sexual behavior–related variables, the final results of the logistic regression model showed that among the variables studied here, only anal intercourse (forced or receptive) remained associated with HCV infection. The association of the variable sexual orientation (heterosexual) with co-infection lost significance in the multivariate analysis. The same occurred with a variable number of sexual partners (> 8). Both variables were strongly associated with intravenous drug use, the highest strength association observed. Because of this, when adjusted to each other, only being an intravenous drug user continued to show significance. Other investigators have shown a correlation between anal intercourse and HCV infection.25,26 It is possible that infection with HCV, similar to HBV and HIV, through the anal mucosae is facilitated by the presence of traumatic genital ulcers or damage resulting from sexually transmitted diseases.

Upon the analysis of aspects related to sexual partners, we observed that a history of liver disease, blood transfusion, and intravenous drug use were risk factors for HCV infection. Other investigators analyzed HCV transmission among sexual partners and observed an association between HCV transmission and the presence of IDU index partners.27,28 There may be a number of mechanisms involved in HCV transmission between sexual partners, especially those who have habits that result in a high risk of virus transmission. Transmission could also result from exposure to unreported parenteral risk factors or from sharing certain personal items, such as toothbrushes or razors, which can result in accidental exposure to the partner’s blood. However, it is not clear whether the sexual relationship per se would be involved in transmission of the virus.

Our sample consisted of a large number of intravenous or non-intravenous drug users. A number of studies have reported that the use of intravenous drugs or even inhaled drugs frequently leads to unprotected sexual practices.29,30 It is interesting to note that when a patient ignores the history of his or her sexual partner, the risk of co-infection is higher. These data apparently indicate a weak relationship of these factors, which may be affected by sexual behavior with multiple partners. Indeed, our group of patients was characterized by unprotected sexual practices with multiple partners, who in turn present their own risk factors, which tend to progressively increase the likelihood of transmitting HCV to each of the members involved in the relationship. Within this context, sexual transmission of HCV could be facilitated and assume an even greater epidemiologic importance if we compared our group to groups with less risky sexual practices. It is possible that the findings concerning the association between HCV and anal intercourse observed in our study is related to this type of sexual behavior in our specific population. Along the same lines of reasoning, the use of inhaled drugs could increase the likelihood of virus transmission.

Our study had some limitations. First, the information about risk factors was collected from individual interviews in a questionnaire that may vary in completeness and be more vulnerable to bias. An attempt was made to minimize recall bias by applying the same standardized questionnaire to cases and controls. Cases were as likely as controls to recall exposures potentially associated with HCV infection. Second, patients in the case group were selected among those referred for treatment at the hepatitis group of the Casa da AIDS. It is reasonable that these patients could be more symptomatic or that their abnormal laboratory results were more significant, since they all had been referred to our service. Thus, it is possible that the interviewed patients (who formed the case group of the study) represented a population of co-infected subjects with more severe manifestations of both infections. It is possible that the clinical evolution of the interviewed group was more accelerated than in asymptomatic patients who had not been referred to our service and, as a consequence, were not involved in the study. This could be a possible selection bias in our study. Third, the patients in the control group were not tested for HCV RNA to rule out occult infection by HCV in this population. Patients in the control group were selected after undergoing two third-generation immunoenzymatic tests for antibody to HCV that showed repeatedly negative results. Due to technical difficulties, we did not test for HCV RNA in all patients and case and controls. Occult infection with HCV may occur in HIV-infected patients, but it seems to be uncommon and is related to the level of immunosuppression in these patients. Its occurrence may be more frequent in situations of acute infection with HCV.31,32 However, it is possible that a patient selected for the control group had an occult HCV infection. We would like to add that among the 117 patients in the control group, only 13 had a CD4 cell count < 200 and only five patients had a CD4 cell count < 100. Thus, the possibility of having an occult HCV infection in the analyzed group was probably restricted to a very small group of patients.

Received April 10, 2004. Accepted for publication September 7, 2004.

Authors’ addresses: Maria Jacintho Cássia Mendes-Correa, Hospital das Clínicas, Instituto Central, Avenida Enéas de Carvalho Aguiar 255, Quarto Andar, Divisão de Doenças Infecciosas e Parasitárias, São Paulo, Brazil, Telephone: 55-11-3069-6530, Fax: 55-11-3082-0427, E-mail: cassiamc{at}uol.com.br. Antonio Alci Barone, Instituto de Medicina Tropical, Avenida Dr. Enéas de Carvalho Aguiar 470, São Paulo, Brazil, Telephone: 55-11-3085-1601, E-mail: aabarone{at}uol.com.br. Reinaldo José Gianini, Faculdade de Medicina da Universidade de São Paulo, Avenida Doutor Arnaldo 455, São Paulo, Brazil, Telephone: 55-11-3066-7444, E-mail: reinaldo{at}sorocaba.pucsp.br.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Thomas DL, 2002. Hepatitis C and human immunodeficiency virus infection. Hepatology 36: S201–S209.[ISI][Medline]
  2. Sherman KE, Rouster SD, Chung RT, Rajicic N, 2002. Hepatitis C virus prevalence among patients infected with human immunodeficiency virus: a cross-sectional analysis of the US Adult AIDS Clinical Trials Group. Clin Infect Dis 34: 831–837.[ISI][Medline]
  3. Amin J, Kaye M, Skidmore S, Pillay D, Cooper DA, Dore GJ, 2004. HIV and hepatitis C coinfection within the CAESAR study. HIV Med 5: 174–179.[ISI][Medline]
  4. Ockenga J, Tillmann HL, Trautwein C, Stoll M, Manns MP, Schmidt RE, 1997. Hepatitis B and C in HIV-infected patients. Prevalence and prognostic value. J Hepatol 27: 18–24.[ISI][Medline]
  5. Fainboim H, Gonzalez J, Fassio E, Martinez A, Otegui L, Eposto M, Cahn P, Marino R, Landeira G, Suaya G, Gancedo E, Castro R, Brajterman L, Laplume H, 1999. Prevalence of hepatitis viruses in an anti-human immunodeficiency virus-positive population from Argentina. A multicentre study. J Viral Hepat 6: 53–57.
  6. Suwanagool S, Tieangrim S, Ratanasuwan W, Mekanantagosol S, Luengrojanakul P, Kunasol P, 1995. Seroprevalence of anti-HCV among HIV-infected persons and general population. J Med Assoc Thai 78: 611–617.[Medline]
  7. Opravil M, Hunziker R, Luthy R, Grob PJ, 1998. Chronic hepatitis B and C in HIV-infected patients. Dtsch Med Wochenschr 123: 753–760.[Medline]
  8. Mendes-Correa MC, Barone AA, Cavalheiro N, 2000. Prevalence of hepatitis B and C in the sera of patients with HIV infection in São Paulo, Brazil. Rev Inst Med Trop São Paulo 42: 81–85.[Medline]
  9. Etzel A, Shibata GY, Rozman M, Jorge ML, Damas CD, Segurado AA, 2001. HTLV-1 and HTLV-2 infections in HIV-infected individuals from Santos, Brazil: seroprevalence and risk factors. J Acquir Immune Defic Syndr 26: 185–190.
  10. Treitinger A, Spada C, Silva EL, Miranda AF, Oliveira OV, Silveira MV, Verdi JC, Abdalla DS, 1999. Prevalence of serologic markers of HBV and HCV infection in HIV-1 seropositive patients in Florianópolis, Brazil. Braz J Infect Dis 3: 1–5.[Medline]
  11. Zylberberg H, Pol S, 1996. Reciprocal interactions between human immunodeficiency virus and hepatitis C virus infections. Clin Infect Dis 23: 1117–1125.[ISI][Medline]
  12. Brito AM, Castilho EA, Szwarcwald CL, 2001. AIDS and HIV infection in Brazil: a multifaceted epidemic. Rev Soc Bras Med Trop 34: 207–217.[Medline]
  13. Sopelana P, Carrascosa C, Garcia-Benito P, 1998. Evolution of the prevalence of HIV-1 infection in drug addicts in the community of Madrid (1985–1986). Med Clin (Barc) 111: 257–258.[Medline]
  14. Jick H, Vessey MP, 1978. Case-control studies in the evaluation of drug-induced illness. Am J Epidemiol 107: 1–7.[Free Full Text]
  15. Garson JA, Tedder RS, Briggs M, Tuke P, Glazebrook JA, Trute A, Parker D, Barbara JA, Contreras M, Aloysius S, 1990. Detection of hepatitis C viral sequences in blood donations by "nested" polymerase chain reaction and prediction of infectivity. Lancet 335: 1419–1422.[ISI][Medline]
  16. Garson JA, Ring C, Tuke P, Tedder RS, 1990. Enhanced detection by PCR of hepatitis C virus RNA. Lancet 336: 878–879.[ISI][Medline]
  17. Nemes MIB, Souza MFM, Kalichman AO, 2000. Prevalência da aderência e fatores associados. Coordenação Nacional de DST-AIDS. Aderência ao Tratamento por Antiretrovirais em Serviços Públicos no Estado de São Paulo. Brasilia: Ministério da Saúde.
  18. Seeff LB, Hoofnagle JH, 2003. Appendix: the National Institutes of Health Consensus Development Conference Management of Hepatitis C 2002. Clin Liver Dis 7: 261–287.[Medline]
  19. Segurado AC, Braga P, Etzel A, Cardoso MR, 2004. Hepatitis C virus coinfection in a cohort of HIV-infected individuals from Santos, Brazil: seroprevalence and associated factors. AIDS Patient Care STDS 18: 135–143.[ISI][Medline]
  20. Conry-Cantilena C, VanRaden M, Gibble J, Melpolder J, Shakil AO, Viladomiu L, Cheung L, DiBisceglie A, Hoofnagle J, Shih JW, 1996. Routes of infection, viremia, and liver disease in blood donors found to have hepatitis C virus infection. N Engl J Med 334: 1691–1696.[Abstract/Free Full Text]
  21. Page-Shafer KA, Cahoon-Young B, Klausner JD, Morrow S, Molitor F, Ruiz J, McFarland W, Young Womens Survey Group, 2002. Hepatitis C virus infection in young, low-income women: the role of sexually transmitted infection as a potential cofactor for HCV infection. Am J Public Health 92: 670–676.[Abstract/Free Full Text]
  22. Focaccia R, da Conceicao OJ, Sette H Jr, Sabino E, Bassit L, Nitrini DR, Lomar AV, Lorenco R, Vieira de Souza F, Kiffer CR, Santos EB, Gonzales MP, Saez-Alquezar A, Riscal JR, Fischer D, 1998. Estimated prevalence of viral hepatitis in the general population of the municipality of São Paulo, measured by a serologic survey of a stratified, randomized and residence-based population. Braz J Infect Dis 2: 269–284.[Medline]
  23. Brandao AB, Fuchs SC, 2002. Risk factors for hepatitis C virus infection among blood donors in southern Brazil: a case-control study. BMC Gastroenterol 2: 18.[Medline]
  24. NIH Consensus Statement, 2002. Management of Hepatitis C. Bethesda, MD: National Institutes of Health, 1–46.
  25. Ndimbie OK, Kingsley LA, Nedjar S, Rinaldo CR, 1996. Hepatitis C virus infection in a male homosexual cohort: risk factor analysis. Genitourin Med 72: 213–216.[ISI][Medline]
  26. Osmond DH, Charlebois E, Sheppard HW, Page K, Winkelstein W, Moss AR, Reingold A, 1993. Comparison of risk factors for hepatitis C and hepatitis B virus infection in homosexual men. J Infect Dis 167: 66–71.[ISI][Medline]
  27. Gabrielli C, Zannini A, Corradini R, Gafa S, 1994. Spread of hepatitis C virus among sexual partners of HCVAb positive intravenous drug users. J Infect 29: 17–22.[ISI][Medline]
  28. Hershow RC, Kalish LA, Sha B, Till M, Cohen M, 1998. Hepatitis C virus infection in Chicago women with or at risk for HIV infection: evidence for sexual transmission. Sex Transm Dis 25: 527–532.[ISI][Medline]
  29. Bastos FI, Lowndes CM, Castello-Branco LR, Linhares-de-Carvalho MI, Oelemann W, Bernier F, Morgado MG, Yoshida CF, Rozental T, Alary M, 2000. Sexual behaviour and infection rates for HIV, blood-borne and sexually transmitted infections among patients attending drug treatment centres in Rio de Janeiro, Brazil. Int J STD AIDS 11: 383–392.[Abstract/Free Full Text]
  30. van Empelen P, Schaalma HP, Kok G, Jansen MW, 2001.Predicting condom use with casual and steady sex partners among drug users. Health Educ Res 16: 293–305.[Abstract/Free Full Text]
  31. Thio CL, Nolt KR, Astemborski J, Vlahov D, Nelson KE, Thomas DL, 2000. Screening for hepatitis C virus in human immunodeficiency virus-infected individuals. J Clin Microbiol 38: 575–577.[Abstract/Free Full Text]
  32. George SL, Gebhardt J, Klinzman D, Foster MB, Patrick KD, Schmidt WN, Alden B, Pfaller MA, Stapleton JT, 2002. Hepatitis C virus viremia in HIV-infected individuals with negative HCV antibody tests. J Acquir Immune Defic Syndr 31: 154–162.



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