Gunn, Robert A. MD, MPH*†; Lee, Marjorie A. MPH†; Murray, Paula J. MPH†; Gilchick, Robert A. MD, MPH†; Margolis, Harold S. MD*
MEN WHO HAVE SEX with men (MSM)1–3 and other persons who have multiple sex partners or a history of having sexually transmitted diseases (STDs)4,5 are at an increased risk of acquiring hepatitis B infection. With the licensure of hepatitis B vaccine in 1981, the Centers for Disease Control and Prevention (CDC) published recommendations for the vaccination of persons with risk factors for infection, including MSM.6 Subsequent updating of the hepatitis B vaccine recommendations expanded the prevention strategy to achieve the elimination of hepatitis B virus (HBV) transmission in the United States. This resulted in the universal vaccination of infants and catch-up vaccination of all children and adolescents and continued vaccination of MSM and other high-risk adults.7–8 However, vaccinating high-risk adolescents and adults has always been problematic.
The National Health Interview Survey 2000 data showed that only 31% of high-risk adults report having received ≥1 dose of hepatitis B vaccine.9 Many studies of MSM vaccination coverage, including some done in the last 5 years, showed that less than 50% (range 15%–46%) reported having received ≥1 dose of hepatitis B vaccine.10–15 However, MSM disproportionately account for approximately 15% of reported cases of acute symptomatic hepatitis B.5,16 Vaccination of this at-risk group should be a high-priority prevention service and opportunities and methods employed to deliver hepatitis B vaccination to this population are in need of evaluation.
In February 1998, the San Diego County STD program began a project to evaluate the administration of hepatitis B vaccine in a variety of provider sites throughout the community serving both high and lower-risk clients.17 At-risk MSM often seek health care and prevention services at public sexually transmitted disease (STD) clinics, social services' centers for MSM (gay and lesbian centers), HIV counseling and testing sites, HIV treatment clinics, and men's health clinics. The overall hepatitis B vaccination acceptance and completion rates at many of these sites in San Diego county have been recently reported.17 In this paper, hepatitis B vaccination acceptance, series completion, and coverage among MSM and other clients receiving STD services at the main San Diego County STD clinic during the period February 1998–December 2003 are reported.
The main 5-day-a-week public STD clinic, which serves the urban center of San Diego, has approximately 12,000 “new” visits annually (first visit or any visit >30 days after a previous visit) made by approximately 8000 persons. Beginning February 11, 1998, all clients received a hepatitis B fact sheet and were offered hepatitis B vaccine without additional charge. Clients could obtain their first dose of vaccine only in conjunction with an STD clinic examination. All clients were asked to complete a one-page STD/hepatitis risk assessment questionnaire at their first visit and at any subsequent new client visit. The risk assessment questionnaire was reviewed by staff clinicians and HIV counselors to assess each client's hepatitis, STD, and HIV risk and to recommend vaccination and hepatitis serologic testing, when indicated. Risk assessment data from the initial visit were entered into an Epi-Info database, and vaccination status was updated when subsequent doses of vaccine were administered.
Initial anecdotal reports suggested that clients had questions and concerns about vaccination and staff recommended that specific informational counseling would likely improve vaccine acceptance and reduce discussion time with clinicians and nursing staff. Beginning October 1999, counselors trained in hepatitis risk assessment attempted to see all new visit clients, review their risk assessment questionnaire, and counsel them about the risk and sequelae of HBV infection and the importance of vaccination. The safety of the vaccine was only addressed if the patient expressed concerns about it. Because of scheduling issues, counselor availability, and maintaining efficient patient flow, only about 50% of the clients were seen by a counselor. The hepatitis counselors were available for only 15 months (October 1999–December 2000) and beginning January 2001 the task of providing hepatitis counseling was transferred to HIV counselors who included hepatitis B information in the HIV pretest counseling session. Approximately 50% of new visit clients were seen by HIV counselors for HIV services.
Clients starting vaccination were given an International “yellow” Vaccination Card and were told to return for a “vaccination only” visit, which meant they had only minimal waiting time (approximately 10–15 minutes). However, no telephone or written reminders were sent except during a 26-month period (September 1998–October 2000) when 2 case managers, hired specifically for this task, attempted to contact and remind all high-risk clients (e.g., MSM, persons with a history of injecting drugs, and others with high-risk sexual behavior) who were overdue (>45 days) for their next dose of vaccine. Case managers attempted to contact clients by telephone or in some instances by a field visit. Case management success was recorded when an assigned client obtained the needed vaccine dose within 6 weeks from the initiation of the case management process.
Hepatitis B vaccine was offered to all clients until December 31, 2002. Beginning January 1, 2003, offering vaccine was then limited, because of reduced funding for vaccine, to clients based on age (all clients <25 years old) and risk factors (MSM, history of being an injecting drug user (IDU), sex partner of an IDU, persons having ≥3 sex partners in the past 3 months, or female commercial sex worker). Clients were classified as vaccination ineligible if they reported partial or full completion of the vaccination series or gave a history of having had HBV infection. Persons who had started the vaccination series elsewhere and had not completed it, were offered additional doses but were not included in the data analysis as vaccination eligible.
The STD clinic used a 0, 1, and 4-month vaccination schedule. However, some clients completed the series over several years during return clinic visits for STD symptoms or screening. Series completion trends were analyzed in a baseline cohort of 2543 clients (MSM = 237, other clients = 2306) who had their first vaccine dose in the calendar year 1998 (10.5 month period February 11–December 31, 1998). Completion rates were determined on December 31st of each subsequent year; each client in the 1998 cohort had at least a 12-month follow-up before completion rates were calculated (the first follow-up vaccination completion status for the 1998 cohort determined on December 31, 1999). Yearly completion rates were for vaccine delivered in the STD clinic; the small number of clients in the cohort who may have received a second or third dose at a non-STD clinic site was unknown since such information was not routinely collected.
The hepatitis B vaccination coverage rate (percent of STD clinic attendees reporting having received ≥1 vaccine dose) among STD clinic clients during the initial project year (1998; a 12-month period, February 11, 1998–February 10, 1999) was compared with that in calendar year 2003. Since some clients attending in 2003 had visited the clinic in prior years and had previously been entered into the database, their updated risk assessment and STD clinic vaccination data were combined with the risk assessment and reported vaccination data of clients who had a first time visit in 2003 to provide the vaccination coverage for all 2003 attendees. Vaccine coverage for persons visiting the clinic in 1998 and those visiting for the first time in 2003 were determined from clients' report of prior vaccination. Vaccination coverage for clients visiting in 2003 who had visited the STD clinic in prior years was determined from both a client's report of vaccination and STD clinic vaccination administration data entered in their record. In both 1998 and 2003, only data from the first visit in each of those years were included in the analysis.
Patients at high risk for hepatitis B (MSM, IDUs, sex partner of IDU) were offered serologic testing, which was often obtained at the time the first dose of vaccine was given. Sera were tested for hepatitis B core antibody (anti-HBc) and, if positive, for hepatitis B surface antigen (HBs Ag) using standard test kits at the San Diego County Public Health Laboratory.
During the 6-year evaluation period, 21,631 clients completed an initial risk assessment questionnaire. Their vaccination status on initial visit to the STD clinic is shown in Table 1. Among MSM, 21% reported series completion, 3.8% had received 1 or 2 doses of vaccine, and 7.0% reported having had HBV infection, leaving 69% eligible to start vaccination. Among other clients, 13% reported series completion, 2.1% had received 1 or 2 doses of vaccine, and 1.7% reported prior HBV infection, leaving 84% eligible to start vaccination.
Overall, the vaccination acceptance rate among eligible clients was similar among MSM (69%) and other clients (68%) and did not vary substantially by year. However, during a 15-month period (October 1999–December 2000) when hepatitis counselors were available, the overall vaccine acceptance rate was 77%, which was a 15% increase from the 66% observed during the 19-month baseline period (February 1998–September 1999, rate ratio [RR] = 1.15, 95% confidence interval [CI] = 1.13–1.18; P <0.001). Also, during the period when counselors were available, clients who received counseling had a higher vaccine acceptance (80%) compared to those who did not receive this counseling (74%, RR = 1.08, 95% CI = 1.05–1.12; P <0.001).17
The 3-dose vaccination series completion was 33% and was higher among MSM than other clients (43% vs. 32%, RR = 1.4, 95% CI = 1.3–1.5; P <0.001) (Table 1). The acceptance and completion rates among MSM and others were similar by race/ethnicity (data not shown). Among both groups, the acceptance rate decreased as age increased, while the completion rates increased with increasing age (data not shown). The vaccination completion rate increased as the length of follow-up time increased (42% for clients vaccinated in 1998 compared to 24% for clients starting vaccination in 2002—all clients had at least 12-month follow-up). This was clearly shown in the cohort of persons starting vaccination in 1998 and followed over the subsequent 5 years (Fig. 1). Among both MSM and other clients, the series completion rates increased by 1–2 percentage points per year, with the MSM group attaining higher second- and third-dose completion compared to the other clients.
The case management program (26 month period, September 1998–October 2000) monitored vaccine completion monthly and identified 1593 high-risk persons who were overdue for either vaccine dose 2 or 3. Among this group, 188 (12%) could not be located and only 8 (4.3%) of this group returned on their own and received the needed doses. Among the remaining 1405 high-risk clients who were contacted by a case manager, 377 (27%) received the needed vaccine dose with more success occurring when the case manager had direct contact (telephone or in-person discussion) with the client (41%) compared to indirect contact (telephone message or letter, 11%, RR = 3.7, 95% CI = 3.1–4.9; P <0.001, Table 2). The success rates among MSM clients (29%) and other high-risk clients (26%) were similar.
In 2003, partial or completed vaccination coverage was much higher than during the first year of the STD clinic program (45% vs. 11%, RR = 4.1, 95% CI = 3.7–4.4; P <0.001, Table 3). Comparing the coverage among clients who attended the STD clinic for the first time in 2003 with those having their first visit during the baseline year (1998) showed an almost threefold higher rate of having received some vaccine (29% vs. 11%, RR = 2.6, 95% CI = 2.4–2.9; P <0.001). Similar patterns were observed among MSM clients, a group with an overall higher level of vaccine coverage. The highest 2003 coverage rate (81%) occurred in clients who had multiple visits (return clients with ≥1 visit before 2003) for both MSM and other clients.
This evaluation of a hepatitis B vaccination program among STD clinic clients that spanned 6 years showed that the overall vaccine acceptance (69%) and completion rates (second dose, 55%, and third dose, 33%) were higher than previously reported acceptance rates (50%–44%)18,19 and 3-dose completion rates (31%–25%) found in other STD clinics19 (Klausner JD, report to CDC, unpublished data, 1997, personal communication, February 2006). Although these vaccine coverage rates were lower than observed from childhood and adolescent hepatitis B immunization, they could be considered acceptable for the transient nature of the population served by STD clinics and are comparable to the vaccine coverage rates in other adult populations.20,21 Although previous evaluations among STD clinic clients have shown lower acceptance and completion rates, these are difficult to compare because of variability of follow-up periods and methods used to improve vaccine acceptance and completion. Compared to published evaluations of hepatitis B vaccination in 2 other STD clinics, which both covered approximately 1.5 years19 (Klausner JD), this study was conducted over a 6-year period, and the higher completion rates in San Diego may reflect the institutionalization of the vaccination program and some effect of the case management services for high-risk clients that occurred for 26 months. However, since some persons used STD clinic services over many years, the higher completion rates may also be a result of the numerous opportunities to administer a second and third dose of vaccine during return STD clinic visits.
The 69% vaccine acceptance rate among MSM in San Diego during the evaluation period was slightly higher than previously reported in 2 other studies among STD clinic MSM clients—53% and 62%.19,22 Others have tried to determine the reasons for this relatively low acceptance rate and have concluded that vaccine refusal is a complex process with a wide variety of interrelated factors: knowledge about hepatitis and vaccine, perceived risk of infection, concern about health in general, vaccine safety, and structural issues, such as cost and time, and that client-centered counseling is needed to address specific concerns.10,11,22–26. In San Diego, brief hepatitis vaccination counseling (available for only 15 months) offered to all clients raised the acceptance rate among those counseled to 80% compared to 74% among those not counseled.17
The Healthy People 2010 Objective for hepatitis B vaccination of MSM is ≥60% fully immunized.27 In this evaluation, the overall completion rate among MSM was 43% and among the cohort followed for 5 years, 3-dose coverage reached 62%. These observations suggest that sustained availability of vaccination services markedly improves series completion rates and can achieve national goals. Although the case management program for high-risk persons, which included MSM, had some impact upon completion rates, this program was labor intensive and could not be sustained with available resources.
This evaluation suggested that the vaccination coverage in the STD clinic may have also increased over time from effects of the communitywide hepatitis B vaccination program.17 In 1998, the vaccine coverage (≥1 dose of vaccine) was only 11% among STD clinic clients, which was slightly lower than the 19% found in the Miami Dade County STD clinic in 2001.28 In 2003, in San Diego, the vaccine coverage of new first-time clients was considerably higher compared to 1998 when the program began (29% vs. 11%, P <0.001). Clients returning to the STD clinic after visits in prior years had very high vaccine coverage (81%). These improved coverage rates are likely the result of combined vaccination efforts of the STD clinic and other sites serving high-risk clients.
MSM had an overall coverage rate (54%) in 2003 that was somewhat higher than other studies done in a variety of settings, which have shown vaccine coverage (≥1 dose) among MSM that was less than 50%, ranging from approximately 15% among young men12 to 46% among all MSM,14 with most coverage rates being in the 35%–45% range.10–15 These findings show that a substantial proportion of MSM clients who attended the San Diego STD clinic were being vaccinated, which should impact HBV transmission at the community level.
The findings from this program evaluation are somewhat limited because of the variability of specialized services (e.g., hepatitis counseling, case management of high-risk clients) that occurred in the 6-year period. However, the basic components of the hepatitis B vaccination service in the STD clinic have remained in place and offering hepatitis B vaccine is a routine service. Having regular vaccination implementation meetings, responding to staff suggestions, and providing feedback on vaccine coverage established the importance of this service that has helped sustain the program over many years. Unfortunately, CDC was unable to provide vaccine after 2001 and beginning January 1, 2003, vaccine was offered to clients based on risk and also to all clients <25 years of age, with clients <19 years of age receiving vaccine through the federal Vaccines for Children (VFC) program. Currently, hepatitis B vaccine is purchased through the county STD program; in 2003 the cost of vaccine was approximately $100,000.
Even though hepatitis B vaccine at no or low cost is not readily available to STD clinics, a minimal immunization program can be implemented in most STD clinics. STD clinics can provide vaccine to all adolescent clients, irrespective of their risk factors, with vaccine available through the VFC program.29 Guidance for initiating an immunization program in an STD clinic is available.30 Following the implementation of adolescent vaccination, a broader hepatitis B prevention program, which should include comprehensive counseling about hepatitis and the need for vaccination, can be developed. These first steps will familiarize staff with hepatitis prevention and vaccine handling and administration. Subsequently, trying to incorporate funding for vaccine that can be offered to MSM, and using a telephone reminder for MSM clients overdue for scheduled doses, would improve coverage for the highest risk clients. There is some evidence that more clinics that provide STD services are offering hepatitis B vaccine to high-risk clients.31 Hopefully, in the near future, a national program supported by federally funded vaccine will be initiated for high-risk adults, which should result in expanded hepatitis B vaccination services in STD clinics and should prepare clinic staff for the administration of any STD or HIV vaccine that becomes available.
1. Dietzman DE, Harnisch JP, Ray CG, et al. Hepatitis B surface antigen (HBs
AG) and antibody to HBs
AG prevalence in homosexual and heterosexual men. JAMA 1977; 238:2625–2626.
2. Schreeder MT, Thompson SE, Hadler SC, et al. Hepatitis B in homosexual men: Prevalence of infection and factors related to transmission. J Infect Dis 1982; 146:7–15.
3. Szmuness W, Much MI, Prince AM, et al. On the role of sexual behavior in the spread of hepatitis B infection. Ann Intern Med 1975; 83:489–493.
4. Alter MJ, Hadler SC, Margolis HS, et al. The changing epidemiology of hepatitis B in the United States: Need for alternative vaccination strategies. JAMA 1990; 263:1218–1222.
5. Goldstein ST, Alter MJ, Williams IT, et al. Incidence and risk factors for acute hepatitis B in the United States, 1982–1998: Implications for vaccination programs. J Infect Dis 2002; 185:713–719.
6. Centers for Disease Control and Prevention. Recommendation of the Immunization Practices Advisory Committee (ACIP) Inactivated hepatitis B virus vaccine. MMWR Morb Mortal Wkly Rep 1982; 31:317–322, 327–328.
7. Centers for Disease Control and Prevention Protection against viral hepatitis. Recommendations of the Immunization Practices Advisory Committee. MMWR Recomm Rep 1990; 39(RR-2):1–27.
8. Centers for Disease Control and Prevention: Hepatitis B virus: A comprehensive strategy for eliminating transmission in the United States through universal childhood vaccination: Recommendations of the Immunization Practices Advisory Committee. MMWR Morb Mortal Wkly Recomm Rep 1991; 40(RR-13):1–25.
9. Centers for Disease Control and Prevention. Update: Recommendations to prevent hepatitis B virus transmission—United States. MMWR Morb Mortal Wkly Rep 1995; 44:574–575.
10. Jain N, Yusuf H, Wortley PM, et al. Factors associated with receiving hepatitis B vaccination among high-risk adults in the United States: An analysis of the national health interview survey 2000. Fam Med 2004; 36:480–486.
11. Rhodes SD, Hergenrather KC, Yee LJ. Increasing hepatitis B vaccination among young African-American men who have sex with men: Simple answers and difficult solutions. AIDS Patient Care STDS 2002; 16:519–525.
12. Rhodes SD, Diclemente RJ. Psychosocial predictors of hepatitis B vaccination among young African–Am gay men in the deep south. Sex Transm Dis 2003; 30:449–454.
13. MacKellar DA, Valleroy LP, Secura GM, et al. Two decades after vaccine license: Hepatitis B immunization among young men who have sex with men. Am J Public Health 2001; 91:965–971.
14. Choi KH, McFarland W, Neilands TB, et al. High level of hepatitis B infection and ongoing risk among Asian/Pacific Islander men who have sex with men, San Francisco, 2000–2001. Sex Transm Dis 2005; 32:44–48.
15. Dufour A, Remis RS, Aldry M, et al. Factors associated with hepatitis B vaccination among men having sexual relations with men in Montreal, Quebec, Canada. Sex Transm Dis 1999; 26:317–324.
17. Centers for Disease Control and Prevention. Incidence of acute hepatitis B—United States, 1990–2002. MMWR Morb Mortal Wkly Rep 2004; 52:1252–1254.
18. Centers for Disease Control. Hepatitis B vaccination among high-risk adolescents and adults—San Diego, California, 1998–2001. MMWR Morb Mortal Wkly Rep 2002; 51:618–621.
19. Samoff E, Dunn A, VanDevanter N, et al. Predictors of acceptance of hepatitis B vaccination in an urban sexually transmitted disease clinic. Sex Transm Dis 2004; 31:415–420.
20. Weinstock HS, Bolan G, Moran JS, et al. Routine hepatitis B vaccination in a clinic for sexually transmitted diseases. Am J Public Health 1995; 85:846–849.
21. Mahoney FJ, Stewart K, Wu H, et al. Progress toward the elimination of hepatitis B virus among healthcare workers in the United States. Arch Intern Med 1997; 157:113–119.
22. Centers for Disease Control and Prevention. Hepatitis B vaccination coverage among adults—United States, 2004. MMWR Morb Mortal Wkly Rep 2006; 55:509–511.
23. Rudy ET, Detels R, Douglas W, et al. Factors affecting hepatitis vaccination refusal at a sexually transmitted disease clinic among men who have sex with men. Sex Transm Dis 2003; 30:411–418.
24. deWit JB, Vet R, Schutten M, et al. Social-cognitive determinants of vaccination behavior against hepatitis B: An assessment among men who have sex with men. Prev Med 2005; 40:795–802.
25. Yee LJ, Rhodes SD. Understanding correlates of hepatitis B virus vaccination in men who have sex with men: What have we learned? Sex Transm Infect 2002; 78:374–377.
26. Handsfield HH. Hepatitis A and B immunization in persons being evaluated for sexually transmitted diseases. Am J Med 2005; 118(Suppl 10A):69S–74S.
27. Rich JD, Ching CG, Lally MA, et al. A review of the case for hepatitis B vaccination of high-risk adults. Am J Med 2003; 114:316–318.
29. Trepka MJ, Weisbord JS, Zhang G, et al. Hepatitis B virus infection risk factors and immunity among sexually transmitted disease clinic clients. Sex Transm Dis 2003; 30:914–918.
30. Centers for Disease Control and Prevention. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus infection in the United States: Recommendations of the Advisory Committee on Immunization Practices (ACIP), Part 1: Immunization of infants, children, and adolescents. MMWR Recomm Rep 2005; 54(RR-16):1–31. Erratum in: MMWR Morb Mortal Wkly Rep 2006; 55:158–159.
32. Gilbert LK, Bulger J, Scanlon K, et al. Integrating hepatitis B prevention into sexually transmitted diseases services: US sexually transmitted disease program and clinic trends—1997 and 2001. Sex Transm Dis 2005; 32:346–350.