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“The only thing necessary for these diseases to the triumph is for good people and governments to do nothing.”

    

Hepatitis C Virus Infection in Young, Low-Income Women: The Role of Sexually Transmitted Infection as a Potential Cofactor for Hepatitis C Virus Infection

April 2002, Vol 92, No. 4 | American Journal of Public Health 670-676
© 2002  

 

Kimberly A. Page-Shafer, PhD, MPH, Barbara Cahoon-Young, PhD, Jeffrey D. Klausner, MD, MPH, Scott Morrow, PhD, Fred Molitor, PhD, Juan Ruiz, MD, DrPH and Willi McFarland, MD PhD for the Young Women's Survey Team

Kimberly A. Page-Shafer is with the Center for AIDS Prevention Studies, Department of Medicine, University of California San Francisco, Calif. Barbara Cahoon-Young is with East Bay Liver Clinic, Oakland, Calif. Jeffrey D. Klausner is with the Division of STD Control, San Francisco Department of Public Health, San Francisco, Calif. Scott Morrow is with San Mateo County Department of Public Health, Redwood City, Calif. Fred Molitor and Juan Ruiz are with the Office of AIDS, HIV/AIDS Epidemiology Branch, California Department of Health Services, Sacramento, Calif. Willi McFarland is with the HIV Epidemiology Unit, San Francisco Department of Public Health, San Francisco, Calif.

Correspondence: Requests for reprints should be sent to Kimberly A. Page-Shafer, PhD, MPH, Center for AIDS Prevention Studies, UCSF, 74 New Montgomery St, Suite 500, San Francisco, CA 94105 (e-mail: kshafer@psg.ucsf.edu).


   ABSTRACT

 
Objectives. We evaluated risk for hepatitis C virus (Hepatitis C Virus) infection in women residing in low-income neighborhoods of northern California.

Methods. A population-based sample of 1707 women, aged 18 to 29, were surveyed and screened for sexually transmitted infections and Hepatitis C Virus.

Results. Women infected with Hepatitis C Virus (2.5%) were more likely to have a history of injection and noninjection drug use, to exchange sex for money or drugs, and to have sexually transmitted infections. Hepatitis C Virus was independently associated with history of injection drug use, herpes simplex virus type 2 (HSV-2) infection, and heroin and cocaine use.

Conclusions. Injection drug use is the highest risk exposure for Hepatitis C Virus, but HSV-2 and noninjection drug use contribute significantly to increased risk. Hepatitis C Virus prevention programs in impoverished areas should integrate drug treatment and sexually transmitted infection control.

INTRODUCTION

 
Hepatitis C virus (Hepatitis C Virus) is the most important cause of acute and chronic liver disease in the United States. An estimated 4 million people, 1.8% of the US general population, are Hepatitis C Virus infected.1 Persistent infection develops in more than 85% of the persons exposed. Chronic hepatitis develops in 50% to 70% of the infected persons, and 10% to 20% of these may go on to develop cirrhosis.2 Liver failure and hepatocellular carcinomas necessitating liver transplantation are some of the most severe consequences of Hepatitis C Virus infection. An estimated 8000 to 10 000 deaths per year are attributed to Hepatitis C Virus-associated liver disease, a figure expected to triple in the next 10 to 20 years.3 Given the current low response to treatment (< 50%),4,5 primary prevention remains the most important public health control strategy to reduce Hepatitis C Virus-related morbidity.

Hepatitis C Virus infection is most easily acquired parenterally. As a result, prevalence is highest among injection drug users (IDUs) and hemophiliacs.6–8 Nonparenteral transmission of Hepatitis C Virus appears to be inefficient.7–14 Past research has documented the cofactor role of sexually transmitted infections in amplifying the acquisition and transmission of HIV and hepatitis B virus (HBV),15–17 but this interrelationship has not been well examined for Hepatitis C Virus. High rates of sexually transmitted infections and Hepatitis C Virus coinfection among IDUs suggest that ulcerative or nonulcerative urogenital infections may be cofactors for Hepatitis C Virus transmission. However, investigation of sexually transmitted infections as potential cofactors for sexual transmission of Hepatitis C Virus is hampered by the confounding effects of concomitant high-risk sexual behavior and injection practices.18 Lack of data on the determinants of sexual transmission of Hepatitis C Virus has limited the development of guidelines for sexual partners who may be at risk for transmitting or acquiring Hepatitis C Virus.9,19

The current study examined Hepatitis C Virus in the Young Women's Survey, a population-based sample of young women recruited in lowincome, multiethnic neighborhoods of northern California.20 Analysis focused on sexual behavior and sexually transmitted infections as risk factors for Hepatitis C Virus and their associated population attributable fractions.

METHODS

 
Study Design
The Young Women's Survey was a single-stage, cluster-sample, population-based, door-to-door, cross-sectional survey designed to measure the prevalence of HIV, sexually transmitted diseases, and related risk behavior in young, low-income women in northern California. The Young Women's Survey study methods, study population, and primary outcomes have been described in detail elsewhere.20 Hepatitis C Virus testing was conducted on stored sera from participants in 4 counties: Alameda, San Francisco, San Joaquin, and San Mateo.

Study Subjects
The target population was young women residing in low-income neighborhoods. Eligibility criteria were being female, aged 18 to 29 years, fluent in English or Spanish, and a resident in the target area. The target area was defined as 1990 US census block groups below the 10th percentile for median household income. In the 4 counties included in the study of Hepatitis C Virus, a total of 19 270 inhabited dwellings were enumerated in 276 randomly selected street blocks within the target area. Contact was made with a resident in each of 15 943 dwellings (82.7%). Of the 2828 eligible women identified, 2096 (74.1%) were enrolled from April 1996 to January 1998. Sera were available for 1707 (81.4%) of the women who were interviewed.

Measures
A structured interviewer-administered survey was conducted to gather data on sociodemographic characteristics, sexual behavior, substance use, medical history, and other health-related factors. Response rates for most variables were greater than 99%. Blood and urine samples were obtained to test for HIV, syphilis, herpes simplex virus types 1 and 2 (HSV-1, HSV-2), HBV, gonorrhea, and chlamydia.

Laboratory Methods
Antibody to Hepatitis C Virus (anti-Hepatitis C Virus) was detected with a third-generation enzyme immunoassay (EIA-3.0; Ortho Diagnostics Systems, Raritan, NJ). Specimens reactive by initial EIA-3.0 were confirmed with a strip recombinant immunoblot assay (RIBA 2.0; Chiron, Emeryville, Calif). Discrepant results (EIA+, RIBA–) were considered negative. HIV testing was conducted with enzyme immunoassay (EIA; Abbott Laboratories, Abbott Park, Ill) and confirmed by immunofluorescent antibody (IFA; Neufeld, Vienna, Austria). Antibody to hepatitis B core antigen (anti-HBc) was detected by EIA (Abbott Laboratories, Abbott Park, Ill), and hepatitis B surface antigen (HBsAg) was detected by microparticle EIA (Abbott Laboratories, Abbott Park, Ill). HSV-1 and HSV-2 specific antibodies were differentiated based on recombinant antigen bands for gG1, gB1, gG2, and gD2 with a strip recombinant immunoblot assay (RIBA HSV Type 1/Type 2 SIA; Chiron, Emeryville, Calif). Blood samples were tested for syphilis by rapid plasma reagin or VDRL tests; reactive specimens were confirmed by microhemagglutination test for Treponema pallidum. Ligase chain reaction (LCx; Abbott Laboratories, Abbott Park, Ill) was used to detect gonococcal and chlamydial DNA in urine specimens.

Statistical Methods
To account for the single-stage, cluster-sample survey design, we used Stata, Version 6.0, Survey (SVY) procedures to construct point prevalences, 95% confidence intervals (CIs), and odds ratios (ORs).21 Ninety-five-percent confidence intervals were adjusted to account for homogeneity within the primary sampling units (i.e., city blocks). Because crude prevalence estimates in the sample differed from the survey-adjusted estimates, we present only weighted percentages.

Multiple logistic regression analysis, adjusting for the survey design, was used to identify independent correlates of Hepatitis C Virus infection based on factors significant in bivariate analyses, a priori hypotheses (such as coinfection with HIV or HBV), and other variables of interest or potential confounders (such as age, race/ethnicity, and county). Models were examined with both a backward and a forward stepwise process. Variables were retained in the models if they reached a significance level of .05 or less. The final multiple logistic model and aflogit procedures21 employing Stata statistical software were used to obtain estimates of adjusted population attributable fraction and corresponding 95% confidence intervals with an approach based on unconditional logistic regression.22,23 The 95% confidence intervals associated with the population attributable fraction estimates were adjusted for probability weights but not for the cluster weights.


   RESULTS

 
Prevalence of Anti-Hepatitis C Virus, by Social and Demographic Characteristics
The population-based estimate of Hepatitis C Virus prevalence among women aged 18 to 29 years in low-income neighborhoods of the 4-county target area was 2.5% (95% CI = 1.4, 3.6) (Table 1). The estimate is based on the 40 Hepatitis C Virus RIBA-confirmed specimens of a total of 63 found to be positive with EIA-3.0. More than a third (39.2%) of the subjects were African American, 31.9% were Latina, 15.4% were White, 6.7% were Asian or Pacific Islander, and 6.7% indicated other or mixed race/ethnicity. Most women (70.5%) were born in the United States; 16.9% were born in Mexico, and 12.5% were born in other countries. The median age was 23.9 years (interquartile range = 21.0–26.7).

    


TABLE 1 —Prevalence of Hepatitis C Virus (Hepatitis C Virus) Infection, by Demographic Characteristics, in Women Aged 18 to 29 Years From Low-Income Neighborhoods of 4 Northern California Counties, April 1996–January 1998

 

Population Prevalence of Variable, %a


 

Population Prevalence of Hepatitis C Virus Antibody, % (95% CI)a,b


 

OR (95% CI)a


 

        Total

 

2.5 (1.4, 3.6)b

 

County of residence

    Alameda

30.0

3.8 (1.7, 6.0)

8.9 (2.6, 29.7)*

    San Francisco

27.9

4.3 (1.4, 7.1)

10.0 (2.8, 35.4)*

    San Joaquin

13.2

1.4 (0.1, 2.7)

Referent

    San Mateo

28.9

0 (NAc)

NAc

Monthly household income, $

    0–499

25.9

5.1 (2.4, 7.8)

 5.6 (2.1, 14.7)*

    500–999

33.7

2.2 (0.8, 3.7)

2.4 (0.9, 6.2)

    1000–2999

33.0

1.1 (0.2, 2.1)

Referent

    >= 3000

7.3

0 (NAc)

NAc

Race/ethnicity

    White

15.4

3.8 (1.1, 6.4)

5.3 (1.3, 21.5)***

    African American

39.2

4.0 (2.0, 5.9)

5.6 (1.8, 17.5)**

    Asian or Pacific Islander

6.7

0.9 (0, 2.5)

1.2 (0.1, 11.6)

    Other

6.7

1.7 (0, 4.0)

2.3 (0.4, 15.0)

    Latina

31.9

0.7 (0, 1.6)

Referent

Education

    < High school

40.6

3.1 (1.4, 4.8)

5.7 (0.9, 36.8)

    High school graduate

27.0

2.6 (1.1, 4.1)

4.7 (0.7, 32.1)

    Vocational or some college

22.2

2.4 (0.7, 4.0)

4.3 (0.5, 35.0)

    >= College degree

10.2

0.6 (0, 1.7)

Referent

Marital status

    Currently married

19.4

1.9 (0, 4.1)

0.7 (0.2, 2.2)

    Previously married

8.4

4.9 (1.1, 8.6)

1.8 (0.8, 4.3)

    Unmarried partnership

10.1

0.6 (0, 1.7)

0.2 (0.3, 1.4)

    Single

62.1

2.7 (1.4, 4.0)

Referent


 


 

Note. CI = confidence interval; OR = odds ratio.

aAll prevalence estimates, 95% CIs, and ORs are adjusted for the survey design.

bAnti-Hepatitis C Virus confirmed in n = 40.

cNot able to calculate survey-adjusted CIs or ORs when no infections were detected.

*P <=.001; **P <=.01; ***P <=.05.



 
The prevalence of Hepatitis C Virus varied significantly by county of residence, income level, and race/ethnicity. Hepatitis C Virus prevalence was highest in the 2 most urban counties: San Francisco (4.3%; 95% CI = 1.4, 7.1) and Alameda (3.8%; 95% CI = 1.7, 6.0). Hepatitis C Virus prevalence increased with decreasing income, reaching 5.1% (95% CI = 2.4, 7.8) among women in the lowest income category (< $500 per month). By race/ethnicity, Hepatitis C Virus prevalence was highest among African Americans (4.0%; 95% CI = 2.0, 5.9).

Women for whom sera were not available did not differ significantly from women with sera with respect to age, education, income, or injection drug use history. However, women without sera available were more likely to be single and to have 2 or more male sex partners and less likely to be Latina ({chi}2 test, P < .05). The latter finding resulted from sera not being available for a disproportionate number of subjects from San Joaquin County.

Prevalence of Anti-Hepatitis C Virus, by Sexually Transmitted Infections and Sexual Behavior
Prevalence of Hepatitis C Virus was significantly higher among women with serologic markers for infection with syphilis (18.3%; 95% CI = 0, 41.7), HSV-2 (4.2%; 95% CI = 1.9, 6.4), HBV (8.3%; 95% CI = 3.2, 13.5), and HIV (63.5%; 95% CI = 0.8, 119.5) (Table 2). Prevalence of Hepatitis C Virus increased with increasing number of lifetime male sexual partners, from 0.4% (95% CI = 0, 1.3) among women with 1 partner to 3.9% (95% CI = 2.2, 5.7) among women with 5 or more partners. Only 2 women (0.1%) reported no male sexual partners, and 1 of these women had Hepatitis C Virus infection. Other sexual risk behaviors associated with increased Hepatitis C Virus prevalence were sex with an IDU (12.6%; 95% CI = 7.2, 18.0), exchange sex (trading sex for money, drugs, or other needs) (13.6%; 95% CI = 5.6, 18.6), and ever having anal sex (4.5%; 95% CI = 2.1, 7.0).


TABLE 2 —Prevalence of Hepatitis C Virus (Hepatitis C Virus) Infection, by Sexually Transmitted Infections and Reported Sexual Behavior, in Women Aged 18 to 29 Years From Low-Income Neighborhoods of 4 Northern California Counties, April 1996–January 1998

 

Population Prevalence of Variable, %a


 

Population Prevalence of Hepatitis C Virus Antibody, % (95% CI)a,b


 

Bivariate OR (95% CI)a


 

Chlamydia

3.2

 2.1 (2.0, 6.2)

0.8 (0.1, 6.0)

Syphilis

0.8

18.3 (0, 41.7)

9.1 (1.7, 46.8)**

Gonorrhea

0.8

 0 (NAc)

NAc

Herpes simplex virus type 2

34.2

 4.2 (1.9, 6.4)

10.4 (3.2, 34.3)*

Hepatitis B (core antibody or surface antigen)

8.8

 8.3 (3.2, 13.5)

4.1 (1.9, 8.8)*

HIV

0.2

63.5 (0.8, 119.5)

69.6 (6.1, 788.0)*

Lifetime male sex partners

    1

19.8

 0.4 (0, 1.3)

Referent

    2–4

26.2

 1.0 (0, 2.2)

1.4 (0.2, 8.5)

    >= 5

53.9

 3.9 (2.2, 5.7)

5.6 (1.3, 23.8)**

Sex with injection drug user

10.3

12.6 (7.2, 18.0)

10.4 (5.8, 18.6)*

Traded sex for money or drugs

12.1

13.6 (5.6, 18.6)

14.5 (7.1, 29.7)*

Anal sex

22.9

 4.5 (2.1, 7.0)

2.3 (1.3, 4.1)**


 


 

Note. CI = confidence interval; OR = odds ratio.

aAll prevalence estimates, 95% CIs, and ORs are adjusted for the survey design.

bAnti-Hepatitis C Virus confirmed in n = 40.

cNot able to calculate survey-adjusted CIs or ORs when no infections were detected.

*P <=.001; **P <=.01.



Prevalence of Anti-Hepatitis C Virus, by Injection and Noninjection Drug Use
Table 3 shows the prevalence of Hepatitis C Virus among women by reported alcohol, noninjection drug, and injection drug use. Of note, the estimate of lifetime injection drug use in the target population was 4.4% (95% CI = 2.9, 5.9). Hepatitis C Virus infection was strongly associated with a history of injecting any drug (OR = 64.6; 95% CI = 33.0, 126.2, P < .001). Hepatitis C Virus infection was significantly more likely among women who reported sharing needles in the past 6 months compared with those who did not (66.7% vs 37.1%; OR = 3.3; 95% CI = 1.0, 11.0) but not among women who reported having ever shared a needle compared with those who did not (OR = 2.7; 95% CI = 0.8, 10.1). Among women with a history of injection drug use, the prevalence of Hepatitis C Virus increased significantly with age: 19.7% (95% CI = 5.5, 34.2) among those younger than 24 years and 55% (95% CI = 38.0, 72.0) among those 24 years and older (data not shown).


TABLE 3 —Prevalence of Hepatitis C Virus (Hepatitis C Virus) Infection, by Alcohol, Noninjection Drug, and Injection Drug Use, in Women Aged 18 to 29 Years From Low-Income Neighborhoods of 4 Northern California Counties, April 1996–January 1998

 

Population Prevalence of Variable, %a


 

Population Prevalence of Hepatitis C Virus Antibody, % (95% CI)a,b


 

OR (95% CI)a


 

History of injection drug use

4.4

 37.5 (26.4, 48.6)

 64.6 (33.0, 126.2)*

Shared needles (among those with a history of injection drug use)

    Ever

56.0

 51.4 (38.8, 63.9)

  2.7 (0.8, 10.1)

    Last 6 mo

38.5

 66.7 (47.2, 86.1)

  3.3 (1.0, 11.0)***

Alcohol

    Ever

78.0

  2.8 (1.6, 4.2)

  2.2 (0.8, 6.3)

    Last 6 mo

60.3

  2.8 (1.5, 4.1)

  1.3 (0.7, 2.7)

    Sex while high on

30.7

  4.3 (2.3, 6.4)

  2.6 (1.3, 5.3)**

Amphetamine

    Ever

12.3

  9.3 (4.7, 13.8)

  7.1 (4.0, 12.6)*

    Last 6 mo

5.0

 15.6 (8.3, 22.9)

  9.8 (5.6, 17.4)*

    Sex while high on

2.8

 19.7 (9.0, 30.3)

 11.8 (6.0, 23.3)*

Injected amphetamine

    Ever

2.2

 42.2 (26.5, 57.8)

 43.8 (18.8, 102.0)*

    Last 6 mo

1.0

 55.8 (34.8, 76.7)

 61.9 (21.9, 174.7)*

    Sex while high on

0.6

 50.0 (28.1, 71.9)

 44.0 (15.7, 123.5)*

Cocaine

    Ever

17.5

 12.1 (7.8, 16.4)

 27.6 (11.2, 67.9)*

    Last 6 mo

8.5

 21.1 (14.5, 27.7)

 32.9 (15.8, 68.5)*

    Sex while high on

5.2

 24.5 (15.4, 33.7)

 24.3 (11.2, 52.5)*

Injected cocaine

    Ever

1.6

 51.2 (33.2, 69.2)

 59.9 (25.5, 140.8)*

    Last 6 mo

0.9

 72.6 (51.0, 94.2)

135.5 (40.7, 451.2)*

    Sex while high on

0.2

100 (NAc)

NAc

Heroin

    Ever

5.1

 28.9 (18.8, 38.9)

 36.2 (18.8, 68.9)*

    Last 6 mo

2.2

 50.4 (36.9, 64.1)

 68.4 (32.7, 143.1)*

    Sex while high on

1.5

 51.7 (34.3, 69.1)

 59.2 (25.9, 135.0)*

Injected heroin

    Ever

2.8

 44.5 (32.5, 56.5)

 59.5 (28.5, 124.2)*

    Last 6 mo

1.7

 66.7 (56.1, 77.2)

140.6 (71.4, 276.6)*

    Sex while high on

1.2

 62.8 (51.2, 74.3)

 93.4 (47.7, 182.8)*

Ever on methadone treatment

1.2

 45.5 (21.3, 69.8)

 41.0 (13.0, 129.8)*


 


 

Note. CI = confidence interval; OR = odds ratio.

aAll prevalence estimates, 95% CIs, and ORs are adjusted for the survey design.

bAnti-Hepatitis C Virus confirmed in n = 40.

cNot able to calculate survey-adjusted CIs or ORs when the point estimate is 0 or 100%.

*P <=.001; **P <=.01; ***P <=.05.



Ever and recent use of alcohol was not associated with increased Hepatitis C Virus prevalence, but having had sex while high on alcohol was (OR = 2.6; 95% CI = 1.3, 5.3). Hepatitis C Virus prevalence was significantly higher among women reporting use of amphetamine, cocaine, or heroin compared with women not using these drugs. For each of these drugs, Hepatitis C Virus prevalence was higher among those reporting recent use compared with ever use and among those reporting injecting compared with those not injecting. Of any risk factor measured, Hepatitis C Virus prevalence was highest among women reporting recent cocaine injection (72.6%; 95% CI = 51.0, 94.2), followed by those reporting recent heroin injection (66.7%; 95% CI = 56.1, 77.2).

Independent Risk Factors for Hepatitis C Virus Infection
In multivariate analyses (Table 4), the strongest independent associations with Hepatitis C Virus infection were history of injection drug use (adjusted OR = 4.9; 95% CI = 2.7, 9.2), serological evidence of HSV-2 infection (OR = 3.7; 95% CI = 1.2, 11.5), any use of heroin (OR = 5.6; 95% CI = 3.1, 10.2), any use of cocaine (OR = 3.4; 95% CI = 1.2, 9.5), and very low income (adjusted OR for income < $500 per month = 4.2; 95% CI = 1.2, 14.4) after adjustment for age. Sexual risk behavior did not reach statistical significance in the model. The associations found between Hepatitis C Virus infection and race/ethnicity were confounded by income and reported sexual risk behavior. African American women were most likely to have HSV-2 infection, to have lower income, and to report a history of trading sex for drugs or money and thus were at highest risk for Hepatitis C Virus infection. No significant interactions were found between age, racial/ethnic group, and sexual risk behaviors. HIV infection was a significant risk factor for Hepatitis C Virus in this study but was excluded from the model because of small numbers and the observation that parameter estimates of the other variables were not significantly changed by its inclusion. The adjusted odds ratio for Hepatitis C Virus infection associated with HIV infection was 7.5 (95% CI = 1.5, 37.0).


TABLE 4 —Independent Associations With Hepatitis C Virus Infection (Multivariate Analysis) and Associated Population Attributable Fractions for Women Aged 18 to 29 Years From Low-Income Neighborhoods of 4 Northern California Counties, April 1996–January 1998

 

Adjusted OR (95% CI)


 

Adjusted Population Attributable Fraction (95% CI)


 

History of injection drug use

4.9 (2.7, 9.2)

0.332 (–0.9, 0.8)

Herpes simplex virus type 2

3.7 (1.2, 11.5)

0.506 (–13.8, 1.0)

Heroin use (ever)

5.6 (3.1, 10.2)

0.394 (–1.1, 0.8)

Cocaine use (ever)

3.4 (1.2, 9.5)

0.442 (–9.2, 1.0)

Age (< 24 vs >=24)

2.5 (0.9, 7.2)

 

Monthly income, $

    < 500

4.2 (1.2, 14.4)

0.400 (–6.4, 1.0)

    500–999

1.5 (0.3, 6.9)

0.695 (–2.3, 0.7)

    >= 1000

Referent

 


 


 

Note. CI = confidence interval; OR = odds ratio.



Analyses among women with no history of injection drug use were conducted to evaluate risk factors associated with nonparenteral acquisition of Hepatitis C Virus infection. In this subset, 12 women (0.9%) were positive for anti-Hepatitis C Virus. Factors associated with Hepatitis C Virus among women non-IDUs were African American race/ethnicity, noninjection cocaine use, and lower income (Table 5). Cocaine use and exchange sex (e.g., trading sex for money or drugs) were highly collinear; however, cocaine use had a stronger association. Among women non-IDUs, African Americans were significantly more likely (OR = 27.5; 95% CI = 3.4, 221.5) to be positive for Hepatitis C Virus than were non–African American women, an association confounded by income level (the unadjusted OR was 36.0).