Sexually Transmitted Diseases:
Low Rates of Hepatitis Screening and Vaccination of HIV-Infected MSM in HIV Clinics
Hoover, Karen W. MD, MPH*; Butler, Mary PhD†; Workowski, Kimberly A. MD*,‡; Follansbee, Stephen MD§; Gratzer, Beau MPP¶,‖; Hare, C. Bradley MD**; Johnston, Barbara MD††; Theodore, John L. PhD††; Tao, Guoyu PhD*; Smith, Bryce D. PhD*; Chorba, Terence MD, MPA*; Kent, Charlotte K. PhD*; the Evaluation Group for Adherence to STD and Hepatitis Screening
From the *Centers for Disease Control and Prevention, Atlanta, GA; †Battelle Centers for Public Health Research and Evaluation, Seattle, WA; ‡Emory University School of Medicine, Atlanta, GA; §Kaiser Permanente, San Francisco, CA; ¶Howard Brown Health Center, Chicago, IL; ‖University of Illinois at Chicago School of Public Health, Chicago, IL; **San Francisco General Hospital Medical Center, San Francisco, CA; and ††St. Vincent Catholic Medical Centers, New York, NY
Evaluation Group for Adherence to STD and Hepatitis Screening: Mary Butler, Felix Carpio, Terence Chorba, Lauren Christiansen-Lindquist, John Cummins, Stephen Follansbee, Beau Gratzer, Brad Hare, Brenda Hernandez, Karen Hoover, Nidhi Jain, Barbara Johnston, Charlotte Kent, Clarissa Ospina Norvell, Bryce Smith, Guoyu Tao, John Theodore, Michael Wohlfeiler, and Kim Workowski.
None of the authors has conflicts of interest, or received support from the National Institutes of Health, Wellcome Trust, Howard Hughes Medical Institute, or the pharmaceutical or other industry.
Correspondence: Karen Hoover, MD, MPH, Division of Sexually Transmitted Disease Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Rd. NE MS E-80, Atlanta, Georgia 30333. E-mail: firstname.lastname@example.org.
Received for publication, August 3, 2011 and accepted December 1, 2011.
Background: HIV-infected men who have sex with men (MSM) are at increased risk of viral hepatitis because of similar behavioral risk factors for acquisition of these infections. Our objective was to estimate adherence to HIV management guidelines that recommend screening HIV-infected persons for hepatitis A, B, and C infection, and vaccinating for hepatitis A and B if susceptible.
Methods: We evaluated hepatitis prevention services received by a random sample of HIV-infected MSM in 8 HIV clinics in 6 US cities. We abstracted medical records of all visits made by the patients to the clinic during the period from 2004 to 2007, to estimate hepatitis screening and vaccination rates overall and by clinic site.
Results: Medical records of 1329 patients who had 14,831 visits from 2004 to 2006 were abstracted. Screening rates for hepatitis A, B, and C were 47%, 52%, and 54%, respectively. Among patients who were screened and found to be susceptible, 29% were vaccinated for hepatitis A and 25% for hepatitis B. The percentage of patients screened and vaccinated varied significantly by clinic.
Conclusions: Awareness of hepatitis susceptibility and hepatitis coinfection status in HIV-infected patients is essential for optimal clinical management. Despite recommendations for hepatitis screening and vaccination of HIV-infected MSM, rates were suboptimal at all clinic sites. These low rates highlight the importance of routine review of adherence to recommended clinical services. Such reviews can prompt the development and implementation of simple and sustainable interventions to improve the quality of care.
HIV-infected men who have sex with men (MSM) are at increased risk of acquiring viral hepatitis because of similar behavioral risk factors for acquisition of HIV and viral hepatitis and the high prevalence of viral hepatitis in this population. Among cases of acute viral hepatitis reported to the Centers for Disease Control and Prevention (CDC), a large percentage of hepatitis A, B, and C cases were among MSM, persons with multiple sexual partners, or persons who had sex with an infected partner.1 In the United States, hepatitis B infection and hepatitis C infection are common among HIV-infected MSM,2,3 and dual hepatitis B and C infections have been found in 3% to 5% of HIV-infected persons.4 MSM are at risk of acquiring sexually transmitted hepatitis A by engaging in sexual behaviors that involve oral-anal contact.5,6 Hepatitis B and C can be transmitted through sexual contact or injection-drug use. Although hepatitis C is transmitted by both sexual contact and percutaneous exposure to blood, sexual transmission is less efficient.7 Despite the apparent inefficiency of sexual transmission among discordant heterosexual couples, sexual transmission of hepatitis C has been reported among HIV-infected MSM in Europe and New York City and was associated with anal fisting, serosorting, group sex, multiple and anonymous sex partners, and the use of cocaine and other drugs during sex.8–10
Hepatitis A infection is usually not associated with adverse long-term outcomes and is spontaneously cleared. However, hepatitis A is more often fulminant in HIV and hepatitis C coinfected patients, increasing the importance of vaccination for hepatitis A in this population.7 Early diagnosis and treatment of hepatitis B and C infections is important in the clinical management of persons with HIV infection. Viral hepatitis tends to be more severe in patients coinfected with HIV. Compared to those with hepatitis B or C mono-infection, persons coinfected with HIV are more likely to develop chronic disease, and have an accelerated natural history of hepatitis C infection.11,12 In addition, it is important to diagnose hepatitis C early in infection, as interferon-based therapy is more effective in acute hepatitis C.7,13,14 Finally, to mitigate hepatic flare that might occur with immune reconstitution upon antiretroviral therapy (ART) initiation, hepatitis B coinfected patients who receive ART should be treated with antivirals that have activity against both viruses.7
Because of the high prevalence of coinfection and the possibility of severe sequelae, since 1999, national guidelines for the care of HIV-infected persons have recommended screening for hepatitis A, B, and C infection, and vaccinating for hepatitis A and B if susceptible.7,15–17 While prevaccination screening for hepatitis A is recommended for populations with a high seroprevalence of hepatitis A to increase the cost-effectiveness of vaccination, prevaccination screening for hepatitis B is important in HIV-infected patients to identify those who might be coinfected to optimize their clinical management.17 The objectives of this study were to evaluate adherence to hepatitis screening and vaccination guidelines in 8 HIV care clinics by estimating the percentage of HIV-infected MSM who were ever screened for hepatitis A, B, or C, and who received hepatitis A or B vaccine, while receiving care at these clinics.
We evaluated hepatitis screening and vaccination at 8 large HIV clinics that provided health services for HIV-infected MSM in 6 US cities: Atlanta, Chicago, Los Angeles, Miami, New York, and San Francisco. Clinics were designated as “A” through “H” to deidentify them. Clinics were selected to include Ryan White grantees, a mix of public and private clinics, and a racially and ethnically diverse study sample. During the study period, a range of 701 to 2010 HIV-infected MSM received care at each of the 8 clinics. We selected a random sample of patients for review and abstraction of their medical records, with a goal of 200 patients per clinic to provide at least a 10% sample from each clinic. Patients were eligible for inclusion if they were male, aged 18 years or older, HIV-infected, and reported a history of sex with men. Clinic staff conducted medical record reviews and abstractions, and entered data on worksheets that were developed to extract information on patients' demographic characteristics, insurance status, social and medical history, clinical complaints, physical examinations, and laboratory testing. We retrospectively abstracted all visits to the clinic including the initial visit, where hepatitis screening would likely occur, and all other visits that occurred earlier than the abstraction date. Deidentified patient data were entered into an Access database and were converted to SAS for analysis. The study was determined to be exempt from review by the Institutional Review Boards at CDC, Battelle, and each clinic.
We estimated patients' demographic characteristics, employment status, primary health insurance, AIDS Drug Assistance Program enrollment, their distribution by clinic, whether patients ever received ART, and their most recent HIV viral load and CD4 count. We also estimated the mean number, median number, and range of visits made by patients over the study period.
Patients' medical records were reviewed to assess if they were ever tested for hepatitis A, B, or C while in care at the clinic. Similar to the method used by the Health Resources and Services Administration for Ryan White performance measures,18 a patient was considered to have been tested for hepatitis A, B, or C if hepatitis screening status was documented in the chart. A patient was considered screened for hepatitis A, if hepatitis A antibody testing was documented in his medical record; hepatitis B, if hepatitis B surface antigen, surface antibody, and core antibody testing were documented; and hepatitis C, if hepatitis C antibody testing was documented.
Among patients ever screened for hepatitis A, B, or C, we estimated the percentages who were found to be previously exposed or immune and who were found to be unexposed or susceptible to infection. A patient was considered vaccinated for hepatitis A or B if one or more doses of vaccine administration were documented in his medical record. Among patients who were screened and found to be susceptible to hepatitis A or B, we estimated the percentage of patients who were vaccinated. Among patients who were vaccinated for hepatitis A or B, we estimated the percentage of patients who were never screened. To assess whether any patients were ever retested for hepatitis C, we estimated the percentage of patients who were screened and found to be unexposed to hepatitis C infection, and then retested at any subsequent visit. Among patients whose race and ethnicity was classified as white non-Hispanic, black non-Hispanic, and Hispanic, we estimated the hepatitis screening and vaccination rates. We compared screening and vaccination rates at each clinic during the study period, and the percentage of patients in racial and ethnic subpopulations at each clinic. Percentages of patients screened or vaccinated were compared using the χ2 test, and a 2-tailed P < 0.05 was considered statistically significant.
We reviewed medical records of 1329 patients who had 14,831 visits from 2004 to 2007. Over the study period, the mean number of visits per patient was 11 (standard deviation of 6), the median number was 10, and ranged from 1 to 52 visits. Most of the patients (87%) had multiple visits over more than a 1-year period. The mean age of patients in 2005 was 41 years and ranged from 19 to 73 years. Among patients in the study, 18% were black non-Hispanic and 28% were Hispanic; 36% had private insurance, 22% Medicaid, and 13% Ryan White coverage; and 23% were enrolled in AIDS Drug Assistance Program (Table 1). The percentage of patients in racial and ethnic subpopulations varied significantly by clinic: white non-Hispanic patients ranged from 3.1% to 73.5%, black non-Hispanic patients ranged from 4.2% to 47.2%, and Hispanic patients ranged from 4.4% to 79.9% (P < 0.001). Of the 8 clinics, 7 were Ryan White grantees.
Among those 1329 patients, the percentages of patients who were ever screened for viral hepatitis were: 47% for hepatitis A, 52% for hepatitis B, and 54% for hepatitis C (Table 2). Among the 627 patients screened for hepatitis A, 16% were documented as previously exposed or immune and 84% were susceptible. The hepatitis A vaccination rate was 29% (150/526) among those who were screened and found to be susceptible to infection, and was 17% (219/1329) among all patients. Of 219 patients who were vaccinated for hepatitis A, 69 (32%) were vaccinated without ever being tested for prior exposure or existing immunity. Among the 696 patients screened for hepatitis B, 18% were documented as previously exposed or immune and 82% were susceptible to infection. Of the patients who were exposed or immune, 8% were documented as chronically infected in their medical record. The hepatitis B vaccination rate among those found to be susceptible was 25% (139/568), and among all patients was 14% (185/1329). Of 185 patient who were vaccinated for hepatitis B, 46 (25%) were vaccinated without ever being tested for prior exposure or existing immunity. Among the 714 patients screened for hepatitis C and found to be unexposed (641), 13% were ever retested during the observation period.
Hepatitis A screening was higher among Hispanic patients (55%) than non-Hispanic white patients (45%) (P < 0.01) or non-Hispanic black patients (48%) (P = 0.10) (Table 3). Hepatitis A vaccination did not vary significantly by race or ethnicity. Screening and vaccination for hepatitis B, and screening for hepatitis C, did not vary significantly when comparing rates for white non-Hispanic, black non-Hispanic, and Hispanic patients. Within each clinic, hepatitis screening and vaccination did not differ by race and ethnicity (data not shown) except at a single clinic where black non-Hispanic patients (32.2%) were less likely to be screened for hepatitis B than white non-Hispanic patients (50.7%) (P = 0.01).
Screening rates varied significantly by clinic: hepatitis A screening ranged from 20% to 64% (P < 0.001), hepatitis B screening from 39% to 64% (P < 0.001), and hepatitis C screening from 37% to 68% (P < 0.001). Vaccination rates of susceptible patients also varied significantly by clinic: hepatitis A vaccination ranged from 2% to 64% (P < 0.001) and hepatitis B vaccination ranged from 1% to 78% (P < 0.001).
Several guidelines have been published that recommend screening HIV-infected persons for hepatitis A, B, and C infection, and vaccinating susceptible persons for hepatitis A and B.7,15,18–20 These recommendations from multiple organizations underscore the importance of diagnosis, treatment, and prevention of viral hepatitis in HIV-infected persons. However, this retrospective chart review found less than optimal adherence to the recommendation for hepatitis screening and vaccination of HIV-infected MSM in HIV clinics. Our findings of low screening rates and low vaccination coverage for hepatitis A and B among HIV-infected MSM were similar to those found in other patient populations.21–23
Vaccination of susceptible HIV-infected persons for hepatitis A and B can prevent morbidity from hepatitis A and B infections. In HIV-infected patients, antibody response to hepatitis A vaccination should be assessed 1 month after vaccination and nonresponders should be revaccinated.7 Similarly, all HIV-infected patients should have hepatitis B surface antibody titers obtained 1 month after completion of the hepatitis B vaccine series to document a response.7 If an appropriate response is not observed, revaccination should be considered. The immunogenicity of hepatitis B vaccine is lower in HIV-infected adults than in seronegative healthy adults.3 The use of a double hepatitis B vaccine dose has been found to result in a higher seroconversion rate among patients with CD4 counts >350 cells/μL.7,24
Although susceptible patients can be vaccinated to protect them from infection with hepatitis A and B, currently, a vaccine is not available to prevent hepatitis C. Current guidelines recommend HIV-infected patients be screened for hepatitis C only once while in care. Some providers might consider retesting unexposed patients with ongoing risk behaviors, and the CDC's 2010 STD Treatment Guidelines suggest routine hepatitis C testing of HIV-infected persons.17 We found that some providers did retest unexposed patients for hepatitis C more frequently while in care. It might be prudent to counsel and educate patients about risk behaviors associated with infection, and to test those at-risk more frequently. Liver function tests that are serially monitored as part of ongoing care for those receiving ART can also be used to identify abnormalities that could be caused by acute hepatitis virus infection. In addition, safe-sex practices should be encouraged for all HIV-infected persons; barrier precautions (e.g., latex condoms) are recommended to reduce the risk for exposure to sexually transmitted pathogens, including hepatitis viruses.7
Our study has several limitations. If patients were screened or vaccinated for hepatitis in a clinic or location other than the HIV clinic, then our study would have underestimated the screening rate. If hepatitis screening or vaccinations were performed but not documented in patients' medical records, rates would have been underestimated. The proportion of medical records abstracted at each clinic differed, possibly resulting in over- or underrepresentation of screening and vaccination practices at any one clinic. We were unable to assess whether a patient received a completed vaccine series for hepatitis A or B, so we assumed that he was fully vaccinated if he ever received a dose. If patients did not complete the vaccine series, we would have overestimated the number of HIV-infected MSM who were no longer susceptible to hepatitis A or B. Since this study, screening and vaccination practices might have improved in response to reiteration of these recommendations in newer publications.7,15,17 Finally, our findings cannot be generalized to all providers of HIV care.
A recent IOM report found that viral hepatitis infections are not widely recognized as serious public health problems,20 and reminds us that prevention and control of viral hepatitis must remain a public health priority. Interventions are needed in HIV clinics to increase adherence to guidelines that have existed since 1999, for screening and vaccination of HIV-infected persons. It is important that clinics regularly review their data and implement interventions to improve quality. Quality improvement techniques developed by the Institute for Healthcare Improvement,25–27 that use a rapid-cycle improvement method, have been shown to increase important clinical preventive processes.28 Our study underscores the need for providers and clinics to evaluate their data and implement effective and sustainable interventions to increase hepatitis screening and vaccination.
1. Daniels D, Grytdal S, Wasley A. Surveillance for acute viral hepatitis—United States, 2007. MMWR Surveill Summ 2009; 58:1–27.
2. Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol 2006; 44:S6–S9.
3. Mast EE, Weinbaum CM, Fiore AE, et al.. 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 II: Immunization of adults. MMWR Recomm Rep 2006; 55:1–33; quiz CE1–4.
4. Soriano V, Barreiro P, Martin-Carbonero L, et al.. Treatment of chronic hepatitis B or C in HIV-infected patients with dual viral hepatitis. J Infect Dis 2007; 195:1181–1183.
5. Henning KJ, Bell E, Braun J, et al.. A community-wide outbreak of hepatitis A: Risk factors for infection among homosexual and bisexual men. Am J Med 1995; 99:132–136.
6. Corey L, Holmes KK. Sexual transmission of hepatitis A in homosexual men: Incidence and mechanism. N Engl J Med 1980; 302:435–438.
7. Kaplan JE, Benson C, Holmes KH, et al.. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009; 58(RR-4):1–207.
8. Gotz HM, van Doornum G, Niesters HG, et al.. A cluster of acute hepatitis C virus infection among men who have sex with men—Results from contact tracing and public health implications. AIDS 2005; 19:969–974.
9. Urbanus AT, van de Laar TJ, Stolte IG, et al.. Hepatitis C virus infections among HIV-infected men who have sex with men: An expanding epidemic. AIDS 2009; 23:F1–F7.
10. van de Laar TJW, van der Bij AK, Prins M, et al.. Increase in HCV incidence among men who have sex with men in Amsterdam most likely caused by sexual transmission. J Infect Dis 2007; 196:230–238.
11. Graham CS, Baden LR, Yu E, et al.. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: A meta-analysis. Clin Infect Dis 2001; 33:562–569.
12. Thio CL, Seaberg EC, Skolasky R Jr, et al.. HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet 2002; 360:1921–1926.
13. Jaeckel E, Cornberg M, Wedemeyer H, et al.. Treatment of acute hepatitis C with interferon alfa-2b. N Engl J Med 2001; 345:1452–1457.
14. Kamal SM, Fouly AE, Kamel RR, et al.. Peginterferon alfa-2b therapy in acute hepatitis C: Impact of onset of therapy on sustained virologic response. Gastroenterology 2006; 130:632–638.
15. Aberg JA, Kaplan JE, Libman H, et al.. Primary care guidelines for the management of persons infected with human immunodeficiency virus: 2009 update by the HIV medicine association of the infectious diseases society of America. Clin Infect Dis 2009; 49:651–681.
16. 1999 USPHS/IDSA guidelines for the prevention of opportunistic infections in persons infected with human immunodeficiency virus. U.S. Public Health Service (USPHS) and Infectious Diseases Society of America (IDSA). MMWR Recomm Rep 1999; 48(RR-10):1–59–66, 61–66.
17. Workowski KA, Berman S. Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 2010; 59:1–110.
19. Health Resources and Services Administration. The HIV/AIDS Program: Legislation. Available at: http://hab.hrsa.gov/law/leg.htm
. Accessed November 19, 2010.
20. Institute of Medicine. Hepatitis and Liver Cancer: A National Strategy for Prevention and Control of Hepatitis B and C. Washington, DC: National Academy Press, 2010.
21. Tedaldi EM, Baker RK, Moorman AC, et al.. Hepatitis A and B vaccination practices for ambulatory patients infected with HIV. Clin Infect Dis 2004; 38:1478–1484.
22. Kellerman SE, Hanson DL, McNaghten AD, et al.. Prevalence of chronic hepatitis B and incidence of acute hepatitis B infection in human immunodeficiency virus-infected subjects. J Infect Dis 2003; 188:571–577.
23. MacKellar DA, Valleroy LA, Secura GM, et al.. Two decades after vaccine license: Hepatitis B immunization and infection among young men who have sex with men. Am J Public Health 2001; 91:965–971.
24. Fonseca MO, Pang LW, de Paula Cavalheiro N, et al.. Randomized trial of recombinant hepatitis B vaccine in HIV-infected adult patients comparing a standard dose to a double dose. Vaccine 2005; 23:2902–2908.
25. Berwick DM. Continuous improvement as an ideal in health care. N Engl J Med 1989; 320:53–56.
26. Shortell SM, O'Brien JL, Carman JM, et al.. Assessing the impact of continuous quality improvement/total quality management: concept versus implementation. Health Serv Res 1995; 30:377–401.
27. Kilo CM. A framework for collaborative improvement: lessons from the Institute for Healthcare Improvement's Breakthrough Series. Qual Manag Health Care 1998; 6:1–13.
28. Landon BE, Hicks LS, O'Malley AJ, et al.. Improving the management of chronic disease at community health centers. N Engl J Med 2007; 356:921–934.
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