Sexually Transmitted Diseases

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Sexually Transmitted Diseases:

Hepatitis B Virus Infection Risk Factors and Immunity Among Sexually Transmitted Disease Clinic Clients

Trepka, Mary Jo MD, MSPH*; Weisbord, Joanna S. MSW, MPH†; Zhang, Guoyan MD, MPH*; Brewer, Toye MD‡

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*Office of Epidemiology and Disease Control, Miami-Dade County Health Department, Miami, Florida; CDC Public Health Prevention Specialist assigned to Office of Epidemiology and Disease Control, Miami-Dade County Health Department, Miami, Florida; and the Division of Infectious Diseases, Department of Medicine, University of Miami School of Medicine, Miami, Florida

Mary Jo Trepka has a new affiliation since completing this study: Department of Public Health, Florida International University, Miami, Florida. Joanna Weisbord also has a new affiliation: Boston Medical Center, Section of General Internal Medicine, Research Unit, Boston, Massachusetts.

This study was funded by the Florida Department of Health. The authors thank the following persons for their contributions to this study: Indra Pandya-Smith, MPH, Dolly Katz, PhD, Sterling Whisenhunt, Maria Nunez, MPH, Patrick Joseph, MPH, Sharmista Dutta, MPH, Katiana Pierre, Anita Martinez, RN, Ilsis Munoz, and Pedro Móntes de Oca from the Florida Department of Health; and David McNeely, MPH, Jose Rossique, MD, Jose Puerto, PA, Maria Inez Oliveira, ARNP, and Gabriele Cohen, ARNP, from the University of Miami.

Correspondence: Mary Jo Trepka, MD, MSPH, Department of Public Health, Florida International University, 11200 SW 8th Street, VH 216F, Miami, FL 33199. E-mail:

Received for publication April 28, 2003,

revised July 16, 2003, and accepted July 21, 2003.

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Background and Objectives: Hepatitis B virus (HBV) infection is a sexually transmitted infection that can be prevented with hepatitis B vaccination.

Goal: The goal was to determine prevalence and risk factors for HBV infection and immunity among sexually transmitted disease (STD) clinic clients.

Study Design: In this cross-sectional study, consenting adult STD clinic clients were interviewed regarding HBV risk factors and vaccination history, and blood was drawn for HBV serologic testing.

Results: Of the 682 participants, 154 (22.6%) had antibody to hepatitis B core antigen, indicating previous infection, and 64 (9.4%) had only antibody to hepatitis B surface antigen, indicating immunity as a result of hepatitis B vaccination. Only 130 (19.1%) of all participants reported receiving at least one dose of hepatitis B vaccine.

Conclusion: The majority of clients were susceptible to HBV, were at high risk for HBV infection, and would benefit from hepatitis B vaccination.

AN ESTIMATED 334,863 PERSONS were infected with hepatitis B virus (HBV) annually nationwide during 1988 to 1994, 1 and 0.4% had evidence of current HBV infection. 2 Among acute HBV cases identified in the Sentinel Counties Study of Viral Hepatitis during 1982 to 1998, 88% with an identified source of infection could be attributed to sexual transmission or injection drug use. 3 Therefore, the Centers for Disease Control and Prevention (CDC) Sexually Transmitted Diseases (STD) Treatment Guidelines recommend that all previously unvaccinated STD clinic clients be vaccinated with the hepatitis B vaccine. 4 We determined the prevalence of and risk factors for HBV infection and prevalence of immunity among Miami-Dade County Health Department (MDCHD) STD clinic clients.

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During January through March 2001, clients aged ≥18 years requesting a clinical evaluation for a new health problem at MDCHD's largest public STD clinic were asked to participate in the study. Health department staff interviewed the first 710 eligible and consenting clients regarding vaccination history and potential risk factors for viral hepatitis. After the interview, staff educated and counseled clients regarding hepatitis and hepatitis prevention, and blood was drawn for HBV and hepatitis C virus (HCV) serologic testing (antibody to hepatitis B surface antigen [anti-HBs], antibody to hepatitis B core antigen [anti-HBc], and antibody to HCV [anti-HCV] enzyme immunoassays [EIA]; Abbott Laboratories, Abbott Park, IL). Repeatedly reactive anti-HCV enzyme immunoassay tests were confirmed using recombinant immunoblot assay (RIBA 3.0; Chiron Corp., Emeryville, CA). HIV infection status was based on clients’ self-reported history. Race and ethnicity responses were combined and categorized into 4 groups: Haitian, non-Hispanic black (not Haitian), Hispanic, and non-Hispanic white, which included all other groups. Data were analyzed using Epi Info 6.0 5 and SAS software 8.02. 6 HBV infection was defined as being anti-HBc-reactive regardless of other HBV serum marker results. Immunity to HBV was defined as anti-HBs level of ≥10 mIU/mL. For the analysis of risk factors for HBV infection, clients with HBV infection were compared with clients who were negative for all HBV serum markers. This excluded clients who were immune (anti-HBs-positive) and had no evidence of HBV infection (anti-HBc-negative). All factors associated with HBV infection in the univariate analysis at P values of ≤0.1 (as determined by chi-squared or Fisher exact tests, as appropriate) were entered into the multivariate analysis except HCV and HIV infection, which were considered to be outcomes and not risk behaviors. A forward stepwise logistic regression was used, and all variables with P values of ≤0.05 were included in the final model. Institutional Review Board (IRB) approval to conduct this study was obtained from the University of Miami School of Medicine, Florida Department of Health, and CDC.

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Of 1365 eligible clients, 710 (52.0%) consented to participate. Reasons for refusing testing included time constraints, work commitments, and a belief of not being at risk for hepatitis. For 28 of the 710 consenting participants, no laboratory results were available because of insufficient blood sample or indeterminate results, leaving 682 (50.0% of eligible) clients with complete questionnaire and laboratory results. No significant difference existed in the sex, age, race, or ethnicity distributions between participants and all clients who were seen in the STD clinic during 2001.

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HBV Infection

Six (0.9%) of the participants were HBsAg-positive and anti-HBc-positive, indicating chronic infection; one participant knew of the infection. An additional 108 (15.8%) were anti-HBc-positive and anti-HBs-positive, and 40 (5.9%) were only anti-HBc-positive. Thus, 154 (22.6%) had evidence of infection; 6 (3.9%) knew of their infections. Of 680 participants with HCV test results, 32 (4.7%) had anti-HCV. Risk factors for HCV infection among participants have been reported elsewhere. 7 Of 673 participants reporting HIV infection status, 22 (3.3%) reported HIV infection. Of the 153 anti-HBc-positive clients with HCV test results, 18 (11.8%) had anti-HCV. Of the 151 anti-HBc-positive clients reporting HIV infection status, 13 (8.6%) reported HIV infection and 1 (0.7%) had anti-HCV and reported HIV infection.

The risk factor analysis compared clients who were anti-HBc-positive with those who were negative for all hepatitis B seromarkers, thus excluding 64 clients who were only anti-HBs-positive and leaving 618 in the analysis. Men were significantly (P = 0.03) more likely to be infected than women. In univariate analysis among men, being older than 24 years, Haitian compared with Hispanic ethnicity, not having a high school diploma, blood transfusion, injection drug use, ≥50 lifetime sex partners, history of STD diagnosis, exchanging sex for money, ever having sex with other men, HIV infection, and HCV infection were associated with HBV infection (Table 1). In multivariate analysis, being older than 24 years, being non-Hispanic black or Haitian, ever having sex with a man, having ≥50 lifetime sex partners, and not having a high school diploma were significantly associated with HBV infection (Table 2).

Table 1
Table 1
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Table 2
Table 2
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Among women, being non-Hispanic black compared with Hispanic, not having a high school diploma, being U.S.-born, injection drug use, having ≥50 lifetime sex partners, history of exchanging sex for money, and history of being in prison or jail ≥1 day were associated in univariate analysis with HBV infection (Table 1). In the multivariate analysis, history of injection drug use, being U.S.-born, being older than 24 years, not having a high school diploma, and being Haitian were significantly associated with HBV infection (Table 2).

Factors not associated with infection among men or women included condom use, tattooing, and body piercing. Among injection drug users, needle sharing was not associated with infection. Among those who reported having had an STD, no specific STD was associated with HBV infection except for syphilis among men (P = 0.02) and herpes among women (P = 0.02). Being foreign-born was not associated with HBV infection. The 326 foreign-born participants who named their country of birth came from 37 different countries, with the majority from the Caribbean (n = 195, 59.8%) or Central America (n = 85, 26.1%).

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HBV Immunity

Of the 682 participants, 172 (25.2%) were anti-HBs-positive, indicating immunity. However, only 64 (37.2%) of the anti-HBs-positive clients were anti-HBc-negative, indicating that the majority of immunity resulted from previous infection and not vaccination. Unlike the prevalence HBV infection, immunity did not increase with age (among participants aged <25 years 24.2% [45 of 186], 25–34 years 24.9% [55 of 221], 35 or older 26.2% [72 of 275]).

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Hepatitis B Vaccination

Of the 682 participants, 130 (19.1%) reported a history of vaccination (at least 1 dose), including 39 (5.7%) who reported receiving 3 doses. Of 69 men reporting ever having sex with other men, 13 (18.8%) reported a history of vaccination. Vaccination history did not always correlate with anti-HBs results among anti-HBc-negative participants (n = 528). Of the 112 (21.2%) anti-HBc-negative participants reporting a history of vaccination, 38 (33.9%) were anti-HBs-positive; 22 (64.7%) of the 34 participants reporting receipt of 3 doses of vaccine were anti-HBs-positive. Of the 64 (12.1%) anti-HBc-negative participants who were anti-HBs-positive, 18 (28.1%) reported no history of vaccination.

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A total of 22.6% of STD clients had serologic evidence of HBV infection. This finding is similar to percentages (15–28%) determined among clients of other STD clinics in the United States. 8–10

Like in other surveys, 2,10 the prevalence of HBV infection increased with age. Focusing vaccination efforts on younger clients would be a way to decrease costs because younger clients are more likely to be anti-HBc-negative. 10 However, because more than 70% of clients in each age group were susceptible, focusing on younger clients would result in missed opportunities among older clients.

Consistent with national data, 2 being non-Hispanic black was associated with infection among men. Among men and women, being Haitian was associated with HBV infection, which is consistent with a serosurvey from a Florida agricultural community. 11 This highlights the importance of promoting the hepatitis B vaccine in a culturally and linguistically appropriate manner.

National data indicate that, compared with U.S.-born non-Hispanic whites and blacks, the prevalence of HBV infection is significantly higher among foreign-born non-Hispanic whites and blacks, but not among Mexican-Americans. 2 Being foreign-born was not associated with HBV infection among the MDCHD STD client population, which might be related to the fact that the majority (60%) of foreign-born clients were born in Caribbean countries. The Caribbean area is considered to be an area of low endemicity for HBV infection, except for the Dominican Republic and Haiti, which are considered to be of moderate endemnicity. 12

Among men and women, not graduating from high school was associated with HBV infection. National data indicate that having less than a high school education is associated with an increased prevalence of infection among non-Hispanics. 2 Educational information designed at an appropriate reading level is, therefore, critical.

Although having ≥50 lifetime sex partners and ever having sex with men were risk factors for HBV infection among men, among women, injection drug use but not number of sex partners was significantly associated with HBV infection in the multivariate analysis, which might be the result of a correlation between injection drug use and having ≥50 lifetime sex partners. Although history of incarceration was not associated with infection in the multivariate analysis, 54% of anti-HBc-positive participants had this history. Of people with acute HBV identified in the Sentinel Counties Study of Viral Hepatitis during 1996 to 1998, 29% reported a history of incarceration, 3 highlighting the importance of hepatitis B vaccination in correctional facilities as recommended by the CDC. 13

This study has certain limitations; first, because of the cross-sectional design, we do not know when the clients were infected. Some might have been infected during childhood before starting high-risk behaviors. A second limitation is the low participation rate. Although there were no significant demographic differences between participants and all STD clients during 2001, whether participants were more or less likely to have HBV infection than the entire STD client population is unknown. Choosing not to participate because of time constraints would probably not vary on the basis of disease status, unless it was not the true reason for not participating. However, the other common reason for not participating, a belief of not being at risk for hepatitis, would result in a higher apparent prevalence of HBV infection if the refusing clients were truly at lower risk. A third limitation is a potential lack of generalizability to populations outside the STD clinic, especially those with a lower percentage of foreign-born or minority clients.

Vaccination history did not always correlate with anti-HBs results with 28% of immune, anti-HBc-negative clients reporting no history of a hepatitis B vaccine. This could be the result of clients’ inability to recall their vaccination history accurately, although rarely anti-HBs can be present as the only serum marker in unvaccinated people with distant infections. 14 In healthy adults, 3 doses of HBV vaccine results in a protective antibody response in >90% of healthy adults <40 years of age. 4 Reasons why the 35% of anti-HBc-negative clients who reported completing the vaccination series were still susceptible to HBV include having an adequate titer in the past that since declined, being vaccinated at an older age, or having HIV infection, which can impair the response to hepatitis B vaccine. 4 Although only one of these clients reported being infected with HIV, some clients might have not been aware of their infection or did not report it.

Prevaccination antibody screening could be cost-effective in populations with a high prevalence of HBV infection 4 such as our population. An additional advantage to screening if HBsAg is included is the ability to identify clients with active HBV infections who are unaware of their infection, allowing for treatment referral and education of the clients and provision of postexposure prophylaxis to their contacts.

In 1997, mandatory HBV vaccination of all students in the seventh grade began in Florida, and currently, almost all students in grades 7 to 12 are vaccinated. However, most young adults who are older than the 12th grade cohort are unvaccinated. Until the majority of adults are universally vaccinated, acute HBV infections will continue to occur among adults, especially among groups at high risk (eg, STD clinic clients). Furthermore, communities with substantial immigrant populations such as Miami-Dade County will have a continuing need for vaccination of recently arrived adult immigrants who did not benefit from the school vaccination laws.

The proportion (19%) of participants who reported a history of hepatitis B vaccination was low, a finding similar to those involving other STD clinics in the United States. 15,16 Furthermore, only 6% had a history of completion of the hepatitis B series. Among male clients who reported having sex with men, the proportion reporting a history of vaccination was not higher than that among all participants, although they met 2 criteria for vaccination (attending a STD clinic and men having sex with men). The low proportion of all clients reporting a history of vaccination was supported by a low prevalence of immunity (12%) among clients who were not previously infected.

The low rate of vaccination among a population at high risk underscores the need to increase vaccination efforts. In every age and nearly every risk group, the majority of clients were susceptible to HBV (anti-HBs-negative), highlighting the need for STD clinics to offer hepatitis B vaccine to all clients. Nationwide, <10% of STD program and clinic managers reported that hepatitis B vaccine is offered to all clients. 17 Lack of funding and resources have been key barriers to vaccinating STD clinic clients. 17

The results of this study indicate that hepatitis B vaccination levels are inadequate, and efforts must be intensified within STD clinic settings. In addition, educational efforts to promote vaccination among STD clients should be designed to reach those who are at highest risk (eg, those without a high school diploma, non-Hispanic blacks, Haitians, men who have sex with men, and injection drug users).

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14. Bisharat N, Segol O, Raz R, et al. Isolated hepatitis B surface antibody as a sole marker for past HBV infection. J Infect 1998; 37: 201–202.

15. Centers for Disease Control and Prevention. Hepatitis B vaccination among high-risk adolescents and adults—San Diego, California, 1998–2001. MMWR Morb Mortal Weekly Rep 2002; 51: 618–621.

16. Staat MA, Tang YL, Fresia AE, et al. Susceptibility to vaccine-preventable diseases in a sexually transmitted disease clinic population. Sex Transm Dis 1998; 25: 331–334.

17. Wilson BC, Moyer L, Schmid G, et al. Hepatitis B vaccination in sexually transmitted disease (STD) clinics: a survey of STD programs. Sex Transm Dis 2001; 28: 148–152.

© Copyright 2003 American Sexually Transmitted Diseases Association


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