The hepatitis B virus (HBV) is easily transmitted by sexual contact as well as by other exposures to infected blood and bodily fluids. Transmission of this virus can be effectively prevented by vaccination, and a vaccine against HBV has been available since the early 1980s.1,2 This vaccine is now composed of recombinant protein and is administered in a 3-dose series. It is generally well-tolerated, and is recommended for all children and adults in high-risk categories.3
Individuals seeking services at sexually transmitted disease (STD) clinics have a greater prevalence of exposure to HBV than the general population.4 HBV vaccination of STD clinic clients is recommended by the CDC.5 Although the number of STD clinics that offer this service is climbing,6 this vaccine is not universally available in STD clinics.
Rates of vaccine acceptance in STD clinics that offer this vaccine are significantly lower than those found among health care workers7,8 or those found in studies of adolescent HBV immunization programs.9,10 STD clinic studies show that one third or more of clients decline the vaccine11,12 and less than 50% complete the 3-dose vaccine series.13,14 While reasons for these low compliance rates have been explored in populations of men who have sex with men (MSM),12,14 no published studies on this topic have focused on heterosexual STD clinic populations. One study comparing heterosexual men to gay and bisexual men found lower rates of completion for the series among heterosexual men than among gay men (25 versus 47% series completion, respectively14); thus, further research on HBV vaccine acceptance among heterosexual populations is important.
To explore these issues, a study of HBV vaccine knowledge, attitudes, beliefs, and acceptance was conducted at a New York City Department of Health (NYCDOH) STD clinic. The clinic is located in northern Manhattan and offers a full array of STD services, including STD examination and treatment for men and women, behavioral counseling, disease investigation services, anonymous and confidential HIV counseling and testing and vaccination against HBV. The clinic population is racially, ethnically, and socioeconomically diverse.15
At this clinic, HBV vaccination is recommended to all clinic clients who have not previously been vaccinated. At the first vaccination visit, a blood specimen is collected for HBV serology and the first vaccine dose is administered. Based on HBV serology, the full vaccine series is offered to attendees who are seronegative. The HBV vaccine has been available at this clinic since 1995, and like all services at NYCDOH STD clinics, vaccine is provided free of charge.
Methods
Subjects
Between July and September 1997, a convenience sample of individuals 18 or older seeking examination or confidential testing services at the NYCDOH STD clinic were asked to participate in a survey of HBV vaccine knowledge, attitudes, beliefs, and behavior. Participants were notified of the study by an announcement in the clinic waiting room. Clinic attendees requesting anonymous HIV testing were excluded from the study as HBV vaccination (which requires the creation of a nonanonymous record) is not performed during an anonymous clinic visit. Clinic attendees requesting confidential HIV testing were not excluded from study participation; approximately 276 clinic attendees requested anonymous HIV testing during the study period, while approximately 397 attendees requested confidential HIV testing during this period.
Measures
During the planning phase of the study 5 focus groups were conducted to identify themes and constructs relevant to the decision to accept vaccination. All patients were eligible to participate in these groups, without regard to HBV vaccine status, and participants were paid $10. Eighteen people participated in these groups in 3 male-only and 2 female-only groups. One female focus group was conducted in Spanish. A discussion guide was used to facilitate these focus groups. A survey questionnaire was then developed based on the relevant constructs and domains identified in the focus groups. Those domains included: knowledge of HBV transmission and pathology, HBV risk perception, knowledge of and attitudes toward vaccines in general, knowledge of and attitudes toward the HBV vaccine specifically, social norms for vaccine acceptance, demographic data, and satisfaction with the provider and clinic visit. The outcome of interest was self-reported choice to accept the first dose of the HBV vaccine.
Although hepatitis B vaccination is recommended by the CDC for all STD clinic attendees, respondents who reported STD symptoms or had been requested to attend the clinic due to status as a contact to a known STD case were considered to be at increased risk due to evidence of exposure to an STD.
Clinic clients were approached by interviewers in the waiting room, told about the study goals, protocol, risks, and benefits, and asked to sign a consent form if they were willing to participate. This protocol received human subjects approval from the NYCDOH and Columbia University Institutional Review Boards. Consenting participants were interviewed by trained English and Spanish-speaking interviewers in a 2-part process. The first part of the survey was administered while participants waited for clinical evaluation and asked about knowledge of HBV transmission and associated morbidity, perceived risk of disease, having an acquaintance who had received HBV vaccine, trust in the medical care establishment, and attitudes toward vaccines. Questions were yes/no or multiple choice; multiple choice questions were open-ended. The second part of the survey was administered at the end of the clinic visit, after clinical evaluation, treatment, and (potentially) vaccination were completed, and asked about the visit satisfaction, clinician’s recommendation, acceptance or refusal of HBV vaccination, and future plans regarding vaccination.
Analysis
Fisher’s exact test or the chi-square test of independence were used to identify significant bivariate associations with acceptance of the first dose of the hepatitis B vaccine (acceptance of vaccination). Those variables that were statistically significant or marginally significant (a priori cutoff value of P < 0.2) and variables shown to act as confounders were entered into a multiple logistic regression model. All statistical analyses were carried out using the SPSS statistical package.
RESULTS
One hundred and ninety-four people participated in the survey; respondent characteristics are described in Table 1. Participants were 48% black (non-Hispanic), 25% Hispanic, and 12% white (non-Hispanic); 42% of study respondents were female. One hundred and sixty-one people completed both parts of the interview (83%). There were no significant differences between those completing only the previsit survey and those who completed both the pre- and post-visit survey between or with respect to age, gender, race/ethnicity, place of birth, or reasons for attending the clinic (P > 0.05 in all cases, Fisher’s exact test, 2-sided). All analyses are based on subjects completing both portions of the survey.
TABLE 1: Study Respondent Characteristics
Subjects were asked about their reason for visiting the clinic. Twenty-seven percent of clinic attendees indicated STD symptoms as the reason for the clinic visit, 22% were attending for HIV testing (confidential and anonymous testing not distinguished), and 17% were attending the clinic for hepatitis B vaccination.
Overall, 62% (100) of survey respondents had not previously been vaccinated against HBV. One third (33) of unvaccinated survey respondents were considered to be at increased risk for HBV. Forty-nine percent (49) of the unvaccinated clinic attendees received vaccination on the study day; 47% (16) of high-risk clinic attendees received vaccination against HBV on the study day.
Hepatitis B Knowledge
Table 2 presents knowledge, attitudes, intentions, and social norms associated with HBV vaccination. Study respondents were asked about hepatitis B disease. Eighty-eight percent of study respondents had heard of HBV. Only 38% of respondents correctly identified the liver as the site of HBV infection. Other commonly named body parts were eyes (26%) and skin (13%). Twenty-six percent responded “don’t know.” When asked about HBV transmission in a multiple response question, 53% of respondents identified sexual contact, 23% of respondents identified blood contact, and 10% identified sharing needles during drug use as potential routes of HBV transmission; other responses included “coughing and sneezing” (13%) and “saliva” (4%). Less than half (49%) of the respondents identified condom use as a way to protect themselves from HBV and 11% correctly responded that not sharing needles would protect against transmission of HBV. Survey respondents’ concern about contracting HBV was assessed by asking “How concerned are you that you might get hepatitis B?” Twenty percent of respondents were “not concerned” about contracting the hepatitis B virus.
TABLE 2: Knowledge, Attitudes, Intentions, and Social Norms about Hepatitis B Vaccination
Attitudes and Beliefs About Vaccination
Respondents were asked a series of questions about vaccination in general and HBV vaccination specifically. When asked about vaccines in general, 59% of those who responded described vaccines as “very good for your health,” 22% described vaccines as “somewhat good for your health,” 18% described vaccines as “both good and bad for your health,” and no respondents described vaccines as “bad for your health.” Among the reasons commonly cited for these opinions were: the possibility of side effects (22%), mistrust of the vaccine or the government (7%), and the fear that the vaccine contains small amounts of disease/virus (15%).
Ninety-one percent of the survey participants responded “yes” to the question “do you know what a vaccine is” and 65% of respondents indicated that they had heard of the HBV vaccine. In contrast to this level of vaccine awareness, when asked “what are some of the ways you can protect yourself from hepatitis B,” only 16% named vaccination as a protective measure. Thirty-three percent of study respondents indicated that they “knew anyone who has taken a vaccine to prevent hepatitis B.”
When respondents who had heard of the vaccine were asked “How effective do you think this vaccine would be in preventing hepatitis B?” only 58% of the respondents responded that the vaccine is “very effective.” When asked about vaccine availability, the majority of respondents indicated that the HBV vaccine was available: when asked how sure they were that they would be able to get the vaccine if they wanted it, 59% were very sure they could get it and 22% were somewhat sure; 14% were not sure.
Physician Recommendation
Sixty-four percent of respondents indicated that the vaccine was recommended to them by the physician.
Intention to Accept HBV Vaccine
Among the population that had not previously received the hepatitis B vaccine (n = 100), the majority of respondents (64%) planned to get the hepatitis B vaccine (respondents who indicated “I have thought about the hepatitis B vaccine and will get it” or “I have thought about the hepatitis B vaccine and will get it today”) in the previsit interview. Among the 64 respondents who had not been vaccinated and who planned to get the vaccine, 36 (56%) received the vaccine on the study day. Of the 28 respondents (44%) who planned to be vaccinated but did not accept vaccination on the study day, the reason most commonly cited for not accepting vaccination was lack of time (28% of this group).
Twenty-six previously unvaccinated respondents (26%) had no intention of accepting the vaccine at the previsit interview (these are patients who chose the following responses to this question: “never thought about getting the vaccine and no intention of getting it,” “have thought about getting the vaccine but too many barriers exist,” “have thought about getting the vaccine but decided against it”). Of this group, 28% (7) accepted vaccination; vaccination had been recommended by the clinician to all of these subjects. The remaining 72% (19) of the group planning to decline vaccination were not vaccinated; the most common reasons cited for not accepting vaccination were that the subject “wanted to know more about hepatitis B” (20%) and that the subject did not perceive that he/she was at risk for hepatitis B (20%).
Predictors of the Choice to Accept Vaccination
Of the 100 study subjects who had not been previously vaccinated, 49 (49%) accepted the vaccine on the study day. Table 3 presents bivariate associations with the choice to accept vaccination on the study day. The clinician’s recommendation and level of concern about contracting HBV were significant predictors of the vaccine acceptance.
TABLE 3: Bivariate Associations with Acceptance of Hepatitis B Vaccination N = 100*
Multivariate logistic regression was used to determine independent predictors of the choice to accept vaccination against HBV in this group; after excluding 16 subjects with missing data, we carried out regression analysis with a population of 84 vaccine-naive study respondents. Both predictors significantly associated with the vaccine choice (doctor’s recommendation, concern about HBV) as well as 2 variables (perception of vaccination, vaccinated acquaintance) with a marginal association with vaccine choice (p-value <0.20) were entered in the model. As some respondents indicated the “reason for visit” was to receive hepatitis B vaccination, a dummy variable indicating this was entered in the model; the variable describing the “intention to accept vaccine” was not used in the model as this question was asked after the discussion of hepatitis B vaccine in the questionnaire and therefore may not have represented the intention at the start of the clinic visit. Dummy variables indicating race/ethnicity were also entered in the model, as it was of interest a priori to evaluate whether these groups made different vaccine choices. All one-way interactions were evaluated.
Maximum likelihood analysis indicated that the reason for visit should be dropped from the model; the final model included variables indicating perceived susceptibility, doctor’s recommendation, perception of healthfulness of vaccination, and vaccinated acquaintance, as well as an interaction between Hispanic ethnicity and vaccinated acquaintance. A low Hosmer-Lemeshow goodness of fit test value (1.80) indicated that the model was appropriate for the data. Unadjusted and adjusted odds ratios for this population are presented in Table 4.
TABLE 4: Multivariate Associations with Acceptance of Hepatitis B Vaccine (N = 84)
DISCUSSION
Low rates of HBV vaccine acceptance among adults have been described in various settings. Often lack of acceptance is attributed, in part, to lack of access or resources to purchase the vaccine. This study, performed in a setting in which vaccine was free and available to all adult clinic clients, allows a more specific analysis of knowledge, attitudes, beliefs, social norms, intention, and provider influence on a choice to accept or decline vaccination. As this study was conducted prospectively, recall bias and shaping of responses to match behavior are unlikely to have affected the results reported here.
In this STD clinic, where immunization against HBV has been offered since 1996, more than one third (37%) of study respondents had previously received at least one dose of the hepatitis B vaccine. On the day of the clinic visit 49% of those not previously vaccinated chose to accept the vaccine. Therefore, of the population surveyed, 68% had received at least one dose of vaccine against hepatitis B, a rate of vaccination which suggests that the vaccine made available at the clinic is reaching a significant proportion of the clinic population. However, among those not previously vaccinated and at high risk for HBV transmission (as indicated by the reason for clinic visit, as described), 53% chose not to receive the vaccine, indicating that barriers exist to the effective prevention of HBV transmission by vaccination in this setting.
Significant efforts have been made to educate clinic clients about the morbidity associated with HBV and the availability of HBV vaccine in the period since the vaccine was first made available in this clinic (1996). These educational interventions include oral presentations, materials made available in the clinic waiting area, and individual counseling by clinicians. Anecdotal evidence gathered from clinic patients suggests that patients find hepatitis confusing and have difficulty remembering the difference among the various types of hepatitis. Focus groups conducted with clinic clients revealed that although the term “hepatitis B” is known to clinic clients, routes of transmission are not well understood: only one focus group respondent (of 18) correctly identified a route of hepatitis B transmission, while many cited “in drink,” “swimming, talking,” “in the air,” and “coughing” as routes of transmission. However, it is important to note that the level of knowledge of HBV morbidity and routes of transmission was not associated with the choice to be vaccinated. Therefore, while a better understanding of hepatitis B outcomes and transmission is desirable, increased educational efforts in these areas alone are not likely to lead to increased vaccine acceptance.
Beliefs about risk of being infected with HBV were correlated with the choice to receive the vaccine, as demonstrated both by the fact that this variable was a significant predictor of vaccine choice in the multivariate analysis and by responses to the postvaccination discussion of motivation, where “to protect myself” was the most common reason given for choosing to be vaccinated. Therefore, information about transmission presented in the context of personal risk may be effective in leading clinic attendees at high risk to choose to be vaccinated against HBV.
This study indicates that familiarity with someone who had been immunized predicted acceptance of vaccination, suggesting that as a larger proportion of the population becomes vaccinated against HBV, acceptance of the vaccine will increase. This study also confirms that the recommendation of the physician is an effective motivator to vaccinate in this setting as in other settings.10,16,17 All clinic clients who had decided not to be vaccinated against HBV before their clinic visit and who subsequently accepted vaccination were encouraged to do so by their clinicians, emphasizing the importance of the provider-client counseling process to decisions about vaccination.
One-half of the unvaccinated study respondents did not choose to be vaccinated against hepatitis B on the day of the study. The analyses presented here suggest this choice is influenced by decisions about personal susceptibility and by the conversation between the clinic attendee and the clinician; these data also suggest that the assessment of vaccine safety plays a role in this decision.
Strikingly, 41% of respondents indicated that they were not entirely comfortable with vaccines in general, suggesting that fear of side effects, live virus inoculation, government manipulation, or other factors caused them to assess the vaccine as “both good and bad” or “somewhat good” for their health. This assessment of vaccine safety had a strong effect on the choice to receive the HBV vaccine. Mistrust of the influenza vaccine has been reported in a similar urban population,18 and this mistrust has deep roots in underserved communities.19 Focus group responses also indicated that mistrust of medical interventions exists in the community served by this clinic. These fears were articulated by one study participant as follows: “I do not trust doctors, why are they giving free vaccines in the inner city. Nothing is for free.” This study demonstrates the effect these fears have on vaccine choices, and points toward the importance of addressing these fears. Although these feelings are often informally addressed by clinic personnel, there are no educational materials or other formalized responses to these fears. Educational materials that directly address these fears, touching on regulation of vaccine manufacture and human subjects protections instituted to protect against the type of abuses that happened in the past, may help in increasing trust in the medical establishment and thereby increase vaccine acceptance.
There are several limitations inherent to this study. This study may incorporate a bias in that 2 interviews were required to complete the study and people who felt they had been at the clinic too long may have left before they completed the second portion of the study; in addition, although vaccination is free at this clinic, waiting times may have served to make vaccine inaccessible to those with time constraints. This study is not generalizable to the larger population, as the sample was drawn from STD clinic attendees. Limiting our study to this high-risk population decreases its applicability but focuses on a population in which significant transmission occurs. These results are therefore most useful to public health professionals serving similar populations. This study depends on self-report data for information about prior vaccination, which may be less accurate than medical records review; however, self-report of vaccination history has been reported to be reasonably accurate when compared to medical chart data.20 This study also depends on self-report of vaccination on the study day; as clinic attendees completed the second portion of the study immediately after the completion of the clinic appointment, confusion or inaccurate memory are unlikely to have influenced these reports.
CONCLUSION
These data suggest that improved education on vaccine efficacy and safety and a focus on personal risk and on the routine nature of HBV vaccination may increase the number of people receiving HBV vaccine at this urban STD Clinic. These data also emphasize, as have other studies, the importance of the clinician-patient encounter to vaccine choices. As an STD clinic-based hepatitis B vaccine program reaches people at high risk, improvement of vaccine acceptance at these sites is likely to reduce rates of hepatitis B transmission.
References
1. Francis DP, et al. Prevention of hepatitis B with vaccine: report from the Centers for Disease Control multi-center efficacy trial among homosexual men. Ann Intern Med 1982; 97.
2. Szmuness W, et al. Hepatitis B vaccine: demonstration of efficacy in a controlled clinical trial in a high-risk population in the United States. N Engl J Med 1980; 303:833–841.
3. CDC. Hepatitis B Fact Sheet. 2002.
4. Alter MJ, Margolis HS. The emergence of hepatitis B as a sexually transmitted disease. Sex Transm Dis 1990; 74:1529–1541.
5. CDC. Guidelines for treatment of sexually transmitted diseases. Mortal Morbid Wkly Report 1998; 47:101–103 (1988).
6. Wilson BC, et al. Hepatitis B vaccination in sexually transmitted disease (STD) clinics. Sex Transm Dis 2001; 28:148–152.
7. Doebbeling BN, Ferguson KJ, Kohout FJ. Predictors of hepatitis B vaccine acceptance in health care workers. Med Care 1996; 34:58–72.
8. Briggs MJ, Thomas J. Obstacles to hepatitis B vaccine uptake by health care staff. Public Health 1994; 108:137–148.
9. Moore-Caldwell SY, et al. Hepatitis B vaccination in adolescents. J Adolesc Health 1997; 20:294–299.
10. Rosenthal SL, et al. Hepatitis B vaccine acceptance among adolescents and their parents. J Adolesc Health 1995; 17:248–254.
11. Bhatti N, et al. Failure to deliver hepatitis B vaccine: confessions from a genitourinary medicine clinic. BMJ 1991; 303:97–101.
12. McCusker J, Hill EM, Mayer KH. Awareness and use of hepatitis B vaccine among homosexual male clients of a Boston community health center. Public Health Rep 1990; 5:59–64.
13. Dal-Re R, et al. Compliance with immunization against hepatitis B. A pragmatic study in sexually transmitted disease clinics. Vaccine 1995; 13:163–167.
14. Yuan L, Robinson G. Hepatitis B vaccination and screening for markers at a sexually transmitted disease clinic for men. Can J Public Health 1994; 85:338–341.
15. VanDevanter N, et al. Transfer of behavioral intervention technology to a sexually transmitted disease clinic. J Public Health Manage Pract 1999; 5:40–51.
16. Ashby-Hughes B, Nickerson N. Provider endorsement: the strongest cue in prompting high-risk adults to receive influenza and pneumococcal immunizations. Clin Excell Nurse Pract 1999; 3:97–104.
17. Nichol KL, MacDonald R, Hauge M. Factors associated with influenza and pneumococcal vaccination behavior among high-risk adults. J Gen Intern Med 1996; 11:673–677.
18. Armstrong K, et al. Barriers to influenza immunization in a low-income population. Am J Prevent Med 2001; 20:21–25.
19. Gamble VN. Under the shadow of Tuskegee: African Americans and health care. Am J Public Health 1997; 87:1773–1778.
20. Hutchinson BG. Measurement of influenza vaccination status of the elderly by mailed questionnaire: response rate, validity, and cost. Can J Public Health 1989; 80:271–275.