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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e3180ca8f12
Article

Hepatitis B Infection and Vaccination Among High-Risk Noninjection Drug-Using Women: Baseline Data From the UNITY Study

Koblin, Beryl A. PhD*; Xu, Guozhen BS*; Lucy, Debbie MS*; Robertson, Verna RNP-MSN*; Bonner, Sebastian PhD†; Hoover, Donald R. PhD‡; Fortin, Princess MPH†; Latka, Mary PhD†

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Author Information

From the *Laboratory of Infectious Disease Prevention, New York Blood Center; †Center for Urban Epidemiologic Studies, New York Academy of Medicine, New York, New York; and ‡Department of Statistics, Rutgers University, New Brunswick, New Jersey

The authors thank Nikki Englert, Sean Lawrence, and Evelyn Rivera for their work and devotion in conducting this study, the Project ACHIEVE Community Advisory Board for their advice and contributions, and the study participants who gave their time and effort.

Supported by the National Institute on Drug Abuse, NIH (R01 DA017482) (to New York Blood Center).

Correspondence: Beryl A. Koblin, PhD, Laboratory of Infectious Disease Prevention, New York Blood Center, 310 E.67th St., New York, NY 10021. E-mail: bkoblin@nybloodcenter.org.

Received for publication February 1, 2007, and accepted April 29, 2007.

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Abstract

Objectives: Few studies of hepatitis B virus (HBV) infection and hepatitis B vaccination have focused on women, and specifically, women who are at high risk. This study was designed to assess the extent of HBV infection and vaccination, level of knowledge about hepatitis B, motivators and barriers to accepting vaccination and uptake of hepatitis B vaccine.

Design: From March 2005 to June 2006, 402 HIV-negative noninjection drug-using women at sexual risk were recruited, interviewed, and tested for markers of HBV infection.

Results: Based on serologic testing, 16.7% were previously vaccinated against HBV, 31.1% were previously infected and 52.2% were still susceptible to HBV. Knowledge of HBV infection, transmission, and prevention was low with a mean of 6.1 of 12 knowledge items correctly identified as true or false; a substantial percent of women were not sure of the correct answer. Of the women still susceptible, 69.0% started the hepatitis B vaccine series after counseling given through the study.

Conclusion: This study illustrates that there continues to be gaps in current strategies for administering hepatitis B vaccine among female populations at sexual risk. Interventions are needed for this population to increase awareness and knowledge of hepatitis B, its transmission, impact on health and the availability of a safe and effective vaccine, supplemented by community programs for adult vaccination.

THE INCIDENCE OF ACUTE HEPATITIS B cases has declined in all age groups in the United States, with the most dramatic declines in those under the age of 20. Although there have also been declines in incidence among adults, adults have the highest hepatitis B incidence in the United States.1 Sexual transmission accounts for a large proportion of infection with hepatitis B virus (HBV) in the United States,1–3 and among women, heterosexual exposure is the most common risk factor.1,2 Among 25–39-year-old women attending clinics for sexually transmitted infections (STIs), the prevalence of prior HBV infection has ranged from 10 to 40%, depending on age, history of syphilis, and number of male sex partners.4–6

Hepatitis B vaccine, which is safe and highly effective, was licensed in the United States in 1982.7 The initial national hepatitis B immunization strategy adopted in 1985 focused on vaccinating persons at high risk for infection.7,8 However, other than health-care workers, a few high-risk individuals were vaccinated,2 and thus the strategy of universal immunization of infants was adopted in 1991.9 Since this strategy has only been in effect for 16 years, older adolescents and high-risk adults still remain targets for immunization. Hepatitis B vaccine is recommended for persons with multiple sex partners or a history of STIs, men who have sex with men, injection drug users, those who are incarcerated, and household and sexual contacts of HBV-infected persons.10 Current recommendations are to conduct universal vaccination in settings where high proportions of persons are likely to be at risk, including STI/HIV testing and treatment facilities, drug-abuse treatment and prevention settings, health-care settings targeting injection drug users and men who have sex with men, and correctional facilities.11 Based on the National Health Interview Survey in the United States, the percent of adults at high risk reporting that they had received hepatitis B vaccine increased from 30% in 2000 to 45% in 2004.10

Hepatitis B vaccination programs among populations at risk through sexual transmission or injection drug use have achieved a wide range of success, but commonly report lower completion rates for dose 2 and 3.4,12–23 Studies have found higher completion rates when one-on-one counseling is given before offering vaccine, when vaccine programs are integrated into overall health care programs and/or provided at convenient locations and with modest financial incentives, and with employment of reminder and retention strategies.24–27

Acceptance of hepatitis B vaccine among a variety of populations also correlates with individual-level factors including a desire to prevent HBV infection, knowing someone with hepatitis B, perceived susceptibility and benefits of immunization, understanding personal risk, and understanding of hepatitis B disease and the vaccine.20,28–31 Other factors facilitating vaccine acceptance include use of syringe exchange programs and recent contact with a health-care provider.12,13 Reasons for refusing hepatitis B vaccination include fear of needles, inconvenience, current pregnancy, concerns about adverse effects of the vaccine, perception as not being at risk for HBV infection, and distrust of the medical system.13,19,20,28,32

Few studies of HBV infection and hepatitis B vaccination have focused on women, and specifically, women who are at high risk for HBV infection. The UNITY study is a trial designed to test the efficacy of an enhanced HIV risk reduction intervention and an enhanced educational intervention to increase knowledge about HIV vaccine trials among high-risk noninjection drug-using women. In this study, women were also tested for markers of HBV infection, provided education about hepatitis B and, if needed, offered hepatitis B vaccine. Thus, the UNITY study provides an opportunity to better understand the knowledge and acceptance of hepatitis B vaccine. Using data from UNITY, we determined, among high-risk noninjection drug-using women, the extent of hepatitis B virus infection and vaccination at the baseline study visit; variables associated with prior hepatitis B vaccination; level of knowledge about hepatitis B; motivators and barriers to accepting vaccination with hepatitis B vaccine; and actual uptake of hepatitis B vaccine.

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Methods

Study Population

From March 2005 to June 2006, women in New York City were recruited for the UNITY study through street outreach, predominately in the South Bronx area; flyers placed in the local neighborhoods; and through referrals from previous studies, current study participants or friends, community agencies, and clinics. We were interested in enrolling women at sexual risk of HIV and who would be eligible for HIV vaccine efficacy trials. Therefore, the following eligibility criteria were used: tested HIV antibody negative; 18 years of age or older; reported noninjecting use of heroin, cocaine, or crack cocaine in the previous 6 months; had at least 1 instance of vaginal sex without a condom in the previous 3 months; no reported injection drug use in the previous 3 years; and not currently pregnant with no intent to become pregnant in the next 12 months.

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Data Collection

The data for this substudy were collected during the conduct of the overall UNITY study, which is designed to test the efficacy of an enhanced HIV risk reduction intervention and an educational intervention to increase knowledge about HIV vaccine trials. In the substudy, women were tested for markers of HBV infection, provided education about hepatitis B and, if needed, offered hepatitis B vaccine. At the initial visit, informed consent for screening was obtained. After consent, computer-assisted self-interviewing with an audio component (ACASI) was used to collect data for the UNITY study, including demographic characteristics, reproductive history, sexual behaviors, attitudes about safer sex, depression, alcohol and drug use, potential for domestic violence, and childhood abuse. Data were also collected on knowledge about hepatitis B vaccine and barriers and motivators to accepting the vaccine. These data were collected before any educational efforts about hepatitis B, and thus represent baseline knowledge among the women. For these analyses, a subset of measures was used as described below.

After baseline data collection, participants received HIV and hepatitis B pretest counseling and education. Blood specimens were collected and tested for HIV antibody and markers of HBV infection. Approximately 2 weeks after screening, participants received their HIV and HBV marker test results and posttest counseling. Women who were HIV antibody negative were asked to enroll in the UNITY trial. Enrolled women who were found to be susceptible to HBV infection by serologic testing were offered hepatitis B vaccine. Participants with positive test results were given referrals for medical and social services, as needed. The study was approved by the Institutional Review Boards of the New York Blood Center and the New York Academy of Medicine.

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Measures
Demographic Characteristics

These variables included age, race/ethnicity, area of residence in New York City, place of birth, years of education, employment and income, health insurance, usual living situation, incarceration history and staying overnight in a shelter or group home, jail, drug treatment, or on the street at least once in the past year.

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Hepatitis B Related Measures

Adapted from HIV vaccine trial knowledge questions,33 participants were asked 12 knowledge questions about HBV infection, hepatitis B vaccine, and means of transmission of HBV for which they could respond “agree” (the statement was true), “disagree” (the statement was false), or “not sure.” Self-reported history of hepatitis was determined by the question “Have you ever been told you had any type of hepatitis or liver infection?” with follow-up questions about type of infectious hepatitis. Self-reported history of hepatitis B vaccination was determined by the question “Have you ever been offered the hepatitis B vaccine?” with follow-up questions about whether the vaccine was given, and the number of doses. Motivators and barriers for receiving hepatitis B vaccine were measured with 10 statements for which the participants answered how important each statement would be in their decision about being vaccinated with the hepatitis B vaccine. The responses were on a 4-point scale (not at all important, slightly important, somewhat important, very important). An additional 6 statements were presented for which the participant answered how concerned she was about different reasons why people do not get vaccinated, such as being afraid of needles. The responses were on a 3-point scale (not at all concerned, somewhat concerned, very concerned).

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Sexual Risk Behavior Measures

Participants were asked about 3 types of male partners with whom they had oral, vaginal, or anal intercourse in the previous 3 months: steady partner (a man you had sex with that you feel closest to in your heart), exchange partners (men you had sex with who gave you money or drugs or other services for having sex with them), and casual partners (nonsteady and nonexchange partners). For each type of partner, participants were asked about numbers of times they had had vaginal and anal intercourse and number of times a condom was used. Unprotected vaginal or anal sex was defined as not using a condom for all sexual acts.

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Drug Use Measures

Participants were asked the frequency of noninjection use of specific drugs in the previous 3 months on a 7-point scale (never, once a month or less, 2–3 times a month, once a week, 2–3 times a week, 4–6 times a week, every day). The drugs included in these analyses were crack cocaine, cocaine, and noninjection heroin. The women also were asked if they had ever injected drugs.

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Laboratory Testing

HIV antibodies were detected by enzyme-linked immunosorbant assay. Sera, which were reactive on first testing, were retested in duplicate. Repeatedly, reactive samples were confirmed by Western blot assay. Specimens were tested for hepatitis B surface antigen, antibody to hepatitis B surface antigen and antibody to hepatitis B core antigen (Immulite 2000, DPC or VITROS Immunodiagnostic HBsAg, anti-HBc and anti-HBs reagent packs, Ortho-Clinical Diagnostics). Women positive for hepatitis B surface antigen and/or antibody to hepatitis B core antigen were considered previously infected with HBV, women positive for antibody to hepatitis B surface antigen alone were considered previously vaccinated and those negative for all markers were considered susceptible to HBV infection.

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Statistical Analysis

Using baseline data, we determined the proportion of women who had serologic evidence of HBV infection and of hepatitis B vaccination. Contingency tables and exact tests compared the proportions of women with serologic markers of hepatitis B vaccination by baseline demographics and risk behaviors. Analyses of variance compared continuous variables by demographic characteristics. We determined the level of knowledge about hepatitis B by calculating the mean number of items correct on the knowledge questionnaire. To determine whether the women were answering the knowledge questions better than guessing, we calculated the difference between sum of the number correct and the sum of the number incorrect. Since on average, the difference would be zero if a person guessed at the answers, the probability of this difference being different from zero was calculated using a t test and calculation of the 95% confidence interval around the mean difference. We compared the mean number of items correct among the groups defined by HBV serologic testing (previously infected, previously vaccinated, and susceptible) using analysis of variance. The proportion of women correctly identifying each knowledge item as true or false was calculated and the proportions correct for each item among the 3 serologic groups were compared using exact tests.

Among the women found to be susceptible to HBV infection, we calculated the proportion who indicated that specific motivators or barriers were “very important” or for which they were “very concerned.” Finally, we calculated the proportion of susceptible women accepting hepatitis B vaccine and used contingency tables and exact tests to compare the proportion vaccinated by selected demographic characteristics and risk behaviors. Multivariate logistic regression was used to identify independently significant variables associated with starting the hepatitis B vaccine series.

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Results

Screening and Enrollment

From March 2005 through June 2006, 430 women were screened and of those, 403 (93.7%) were found to be HIV antibody negative. One of these women was not tested for hepatitis B markers. Of the remaining 402 women, 51.0% were referred by a current study participant or friend, 30.0% were recruited through street outreach, 12.0% by posted flyers and the remaining 7.0% by a variety of other methods. The mean age of the participants was 42.3 years; most of the women were either black or Latina, 66.0% had less than a high school degree, 94.5% were unemployed, and 91.4% had an annual household income of less than $12,000 (Table 1). A majority (59.6%) had a history of being incarcerated sometime in their life and 19.0% had spent overnight in jail at least once in the past year. Most women (85.0%) had health insurance.

Table 1
Table 1
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With regard to sexual risk behaviors in the 3 months before the visit, 30.1% of women reported 4 or more casual male partners and 84.9% reported having at least 1 male partner with whom they received money or drugs for sex (Table 1). Almost all women reported having unprotected vaginal intercourse and 31.4% reported having unprotected anal intercourse. Recent drug use (in the prior 3 months) was common, and a lifetime history of injection drug use was reported by 13.4% of the women (Table 1).

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Markers of Hepatitis B Virus Infection or Vaccination

Based on serologic testing, 67 (16.7%) were found to be previously vaccinated against hepatitis B, 125 (31.1%) were previously infected and 210 (52.2%) were still susceptible to HBV. No chronic carriers were identified. By self-report, 24.1% of women reported they had had hepatitis B vaccine. Only 4.5% reported they had ever been told they had hepatitis B and an additional 4.7% had been told they had hepatitis but did not know what type. Of the 97 women who reported that they had received hepatitis B vaccine, only 39.2% had markers indicating previous vaccination. Of the 37 women who had ever been told they had hepatitis B or had hepatitis but did not know what type, 78.4% had markers of a previous HBV infection. Only 36.7% of the 210 susceptible women indicated that they had ever been offered hepatitis B vaccine.

The mean age of women who had serologic evidence of vaccination (38.5 years) was significantly lower than for women who had been previously infected (45.5 years) (P <0.0001) or still susceptible (41.5 years) (P = 0.01). The proportion of women who had a lifetime history of injection drug use was significantly lower among women who were vaccinated (12.1%), compared with that of women who had been previously infected (24.0%) (P = 0.05). There were no significant differences in the proportion vaccinated by any other demographic characteristic or risk behaviors.

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Knowledge of Hepatitis B Infection and Vaccination

Of the 12 knowledge items, a mean of 6.1 (SD: 2.7) of the items were correctly identified as true or false. The mean difference in the sum of the number correct and the sum of the number incorrect was 3.9 and significantly different from zero (95% CI: 3.6–4.2). A high percent (90.1%) of women correctly answered that a blood test is the only way to be sure about having hepatitis B and about three-quarters (73.4%) knew that people with hepatitis B can spread the virus to others without knowing it (Table 2). Only about half of the women knew about treatments for hepatitis B and that it can be spread by unprotected sex and from pregnant women to their infants and that it is not caused by HIV. For a number of concepts, less than half of the women answered correctly such as prevention strategies (condoms, vaccines), symptoms of hepatitis B, chronic infection, and transmission routes. Except for 1 item, 20.2–49.5% of women were not sure of the correct answer (Table 2).

Table 2
Table 2
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The mean number of items correct was significantly higher for women who had serologic evidence of vaccination (6.9) compared with that for women who had been previously infected (6.0) (P = 0.02) or still susceptible (5.9) (P = 0.006). The proportion of women identifying specific knowledge items correctly was significantly different by serologic marker status for only 2 items. A higher proportion of women who were previously vaccinated (67.2%) knew that hepatitis B is not caused by HIV compared with that of women who were previously infected (55.2%) or susceptible (43.3%) (P = 0.002). A higher proportion of women who were previously vaccinated (44.8%) also knew that hepatitis B can be transmitted more easily than HIV compared with that of women who were previously infected (29.6%) or susceptible (28.6%) (P = 0.04).

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Motivators and Barriers to Accepting Hepatitis B Vaccine

At least three-quarters of the women who were susceptible to HBV infection stated that the preventive aspects of the vaccine, the safety and efficacy of the vaccine, free counseling, convenience of getting vaccine at the study site and helping to stop the spread of HBV were very important aspects in their decision making about whether to accept the vaccine (Table 3). Less than 30% of the women stated that monetary reimbursement for their study visit was an important motivator. The barriers endorsed by the largest proportion of women were the need to receive 3 doses (85.2%), minor side effects (61.2%), and fear of needles (35.6%) (Table 3).

Table 3
Table 3
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Uptake of Hepatitis B Vaccine

Of the 210 women who were susceptible to HBV infection, 158 women enrolled in the UNITY trial and were offered hepatitis B vaccine. Of those, 69 (43.7%) received their first dose of vaccine at their enrollment visit. An additional 40 women received their first dose at a subsequent study visit for a total of 109 (69.0%) women starting the hepatitis B vaccine series during the UNITY study. Of the 49 women not starting the vaccine series, 44.9% simply refused; the second most common reason (20.4% of women) was a desire to be vaccinated somewhere else.

Starting the vaccine series was significantly less likely for women who lived in Manhattan (48.0%) compared with those who lived in Bronx (71.9%) or other parts of the city (83.3%) (P = 0.04). A higher percent (72.0%) of women stating that it was very important to them “to get the vaccine here in this office” started the series compared with 56.3% of women for whom this motivator was not very important, although this association was statistically borderline (P = 0.09). Women who had stated at baseline that they were “very concerned” about being afraid of needles were significantly more likely to start the vaccine series (84.9%) compared with those who were not very concerned about fear of needles (60.2%) (P = 0.0018). Similarly, women who were “very concerned” about the statement “I don't think I need the hepatitis B vaccine” were significantly more likely to start the vaccine series (87.1%) compared with those who were not concerned about this statement (64.57%) (P = 0.015). Women did not think it was very important that they “would get a small amount of money each time” they came for a visit were more likely to start the series (73.5%) compared with women who thought it was important (56.1%) (P = 0.04). Starting the vaccine series was not significantly associated with other demographics, or sexual or drug-related risk behaviors. In multivariate analysis, controlling for place of residence, the motivators remaining significantly associated with starting the vaccine series were not being very concerned about getting money at each visit (OR= 2.4; 95% CI: 1.1, 5.3) and getting vaccine at the office (OR= 2.2; 95% CI: 1.0, 5.2).

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Discussion

The UNITY study is one of the few studies to address hepatitis B infection and vaccination exclusively among high-risk inner-city noninjection drug-using women.6 Although no chronic cases of HBV infection were found, almost one-third of the women were already infected with hepatitis B virus, a percentage considerably higher than the 5% found in the general US population.3 Despite their high-risk behavior, only 17% had serologic evidence of being previously vaccinated, a level considerably lower than the 45% reported by high-risk adults in a national survey.10 Other studies, which included high-risk women, such as injection and noninjection drug users, street-recruited samples in high-risk areas or persons attending STI clinics found between 8–37% previously infected and 3–38% previously vaccinated.5,12–14,32,34–36 Findings from this more recently recruited sample illustrates that there continues to be gaps in the current strategies for administering hepatitis B vaccine. Although a high proportion of the women in this study had health insurance (most likely publicly funded), health-care providers may not be inquiring about potential risk behaviors, which would indicate a need for vaccination or a woman may be reluctant to disclose such risk behaviors to her provider. Furthermore, although there are no national programs that support vaccine purchase and administration for adults,10 many of the women had been in contact with shelters, the prison system, and drug treatment, all recommended settings for hepatitis B vaccine administration.11

Knowledge about key areas related to hepatitis B transmission and prevention was low among the women, an observation which has been made in other at-risk populations.12,13 On average, about half of the knowledge items were identified correctly, and although women who had been previously vaccinated had a significantly higher level of knowledge, this difference represented an average increase of only 1 knowledge item and thus knowledge was still low. Interventions to increase awareness and knowledge of hepatitis B, its transmission, impact on health and the availability of a safe and effective vaccine are needed for this at-risk population.

Over two-thirds of this group of high-risk women who were at risk for HBV infection agreed to initiate the vaccination series. A large proportion of women endorsed the motivators as very important. However, 1 motivator that distinguished women who accepted the vaccine series from those who did not was being able to get the vaccine at the study office, suggesting that convenience or level of comfort with the setting could be important factors in vaccine acceptance. Women who thought that financial reimbursement for visits was important were, however, less likely to start the vaccine series, suggesting that financial incentives found to be advantageous in other settings,27 were not for this study population.

The women in this study were not necessarily representative of noninjection drug-using women in New York City. The eligibility criteria were established to enroll HIV negative women who were at high risk of HIV infection, primarily through sexual contact. These eligibility criteria must be considered when reviewing the prevalence of prior HBV infection found in the study population. Regardless, HBV is efficiently transmitted by sexual contact,11 and thus, this population is an important target for hepatitis B vaccination. We also may have underestimated the percent of women who were previously vaccinated since antibody titers to hepatitis B surface antigen decline over time. Previous studies have indicated that 17–50% of vaccinated persons have low or undetectable titers 10–15 years after vaccination.11 However, a high proportion will retain immunologic memory and thus remain protected against HBV infection.37,38 Although we asked the women whether they had received hepatitis B vaccine, we do not have the date of vaccination to be able to estimate the percent of women who may be immune but with undetectable titers.

A variety of approaches have been examined to increase vaccine uptake among populations at high risk. Among injection drug users, hepatitis B vaccination efforts at syringe exchange programs have been one of the most successful strategies in achieving high rates (>90%) of initiation of the vaccine series27,32 illustrating the need to interface with persons at risk at convenient and trusted venues. Similarly, high rates of initiation of the vaccine series (83%) were achieved among sex workers when vaccine was provided at their workplace setting.6 Less success has been reported with persons attending STI clinics with 23–49% of persons accepting the vaccine.4,13,20 One common reason stated for not accepting vaccination in this setting was lack of time.13 Few studies have focused on noninjection drug users; 1 study in this population found an acceptance rate of 57% among male and female noninjection drug users using a referral and escort system.14 Overall, there is a need to develop strategies for increasing vaccination rates among high-risk noninjection drug-using women, which include communitywide education, one-on-one counseling, and integration into trusted and convenient community programs, potentially supplemented by organized community programs for adult hepatitis B vaccination.

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