Abstract
Although substance abuse treatment programs are important contact points for providing health services for hepatitis B virus (HBV) and hepatitis C virus (HCV) infections, availability of services in these programs has not been well characterized. This study evaluated the spectrum of HBV and HCV services offered by substance abuse treatment programs within the National Drug Abuse Treatment Clinical Trials Network. Our survey of substance abuse treatment program administrators covered availability of testing for HBV and HCV; hepatitis A virus (HAV) and HBV immunization; and HCV medical and non-medical services. There were also questions covering clarity of guidelines for HBV and HCV testing; and HAV and HBV immunization. Differences between methadone and non-methadone programs were examined. Despite the importance of substance abuse in sustaining the hepatitis epidemics, few programs offer comprehensive HBV and HCV testing or HCV healthcare services. Interventions to improve access to hepatitis services for substance abusers are needed.
1. INTRODUCTION
1.1 Prevalence of HBV & HCV in the United States
Hepatitis B virus (HBV) and hepatitis C virus (HCV) are major public health problems in the United States (US) and worldwide, and these infections are the leading causes of chronic liver disease, cirrhosis, and hepatocellular carcinoma; and the most frequent indication for liver transplantation (Lai, Ratziu, Yuen, & Poynard, 2003; Custer, Sullivan, Hazlet, Iloeje, Veenstra, & Kowdley, 2004; Lok, & McMahon, 2007; National Institutes of Health, 2002; Strader, Wright, Thomas, & Seeff, 2004; Global Burden of Hepatitis C Working Group, 2004; Shepard, Finelli, & Alter, 2005; Donato, Boffetta, & Puoti, 1998; Shi, Zhu, Liu, & Xie, 2005; Shepard, Finelli, & Alter, 2005). In the US, the Centers for Disease Control and Prevention (CDC) estimates that there are 1.25 million persons with HBV infection and over 4 million with HCV infection (McQuillan, Coleman, Kruszon-Moran, Moyer, Lambert, & Margolis, 1999; Almasio, & Amoroso, 2003).
1.2 Substance Abuse Treatment Programs Can Reduce HBV & HCV Transmission
Substance abusers are disproportionately affected by HBV and HCV, and are largely responsible for sustaining the epidemics of viral hepatitis in the US (Shepard, Finelli, & Alter, 2005; Centers for Disease Control and Prevention, 1998; Tortu, Neaigus, McMahon, & Hagen, 2001; Murrill, Weeks, Castrucci, Weinstock, Bell, Spruill, & Gwinn, 2002; Goldstein, Alter, Williams, Moyer, Judson, Mottram, Fleenor, Ryder, & Margolis, 2002; Quaglio, Lugoboni, Pajusco, Sarti, Talamini, Lechi, Mezzelani, & Des Jarlais, 2003; Koblin, Factor, Wu, & Vlahov, 2003; Tortu, McMahon, Pouget, Hamid, 2004; Garfein, Bower, Loney, Hutin, Xia, Jawanda, Groom, Nainan, Murphy, & Bell, 2004; Sulkowski, & Thomas, 2005). Substance abuse treatment programs are effective in reducing the use and abuse of illicit substances (Hubbard, Craddock, & Anderson, 2003), and can also be effective in reducing transmission of viral hepatitis. These programs provide an opportunity to offer testing and treatment for HBV and HCV, as well as vaccination against hepatitis A virus (HAV) and HBV. However, despite the large number of substance abuse treatment programs in the US, substance use disorders continue to remain an important mode of transmission of viral hepatitis.
1.3 HBV & HCV Services in Substance Abuse Programs and Study Aims
Surprisingly little is known about HBV and HCV health services offered by substance abuse treatment programs in the US. The primary aim of this portion of the Infections and Substance Abuse Study (NIDA CTN-0012) was to determine the availability and comprehensiveness of HBV and HCV testing, HAV and HBV vaccinations, and other healthcare services for hepatitis within substance abuse treatment programs in the US.
2. METHODS
2.1 Study Population
Survey responses for this report were provided by treatment program administrators (program directors or managers) from substance abuse treatment programs within the National Drug Abuse Treatment Clinical Trials Network (NIDA CTN) in the US. The NIDA CTN mission is to improve the quality of drug abuse treatment throughout the country using evidence based medicine and science as the vehicle.
All 319 substance abuse treatment program administrators within the NIDA CTN were provided with an Information Sheet and a Definitions Sheet prior to participation that described the objectives of the study and defined terms covered by the survey. Individuals were only excluded if they refused to complete the survey.
2.2 Study Design
The Infections and Substance Abuse Study was a cross-sectional, descriptive, and exploratory survey examination of the range of available services associated with 3 infection groups in substance abuse treatment settings within the CTN. The study began in March 2003 and ended in January 2005. A comprehensive description of the design of this study has been published previously (Brown, Kritz, Goldsmith, Bini, Rotrosen, Baker, Robinson, & McAuliffe, 2006). Data for this report came from surveys returned by program administrators. The administrator survey had sections entitled Structure and Service Setting, Patient Characteristics, Staff Characteristics, Reimbursement Issues, Practices, Program Guidelines, Barriers, and Opinions.
For this report, which looked specifically at HBV and HCV, we assessed the availability and types of hepatitis tests offered at each facility. We also assessed the availability of HAV and HBV vaccinations. In addition, we evaluated the availability of 7 healthcare services (offered either on-site or via contractual agreement with another provider), including 4 medical services (medical history/physical examination, biological testing, medical treatment, medical monitoring) and 3 non-medical services (patient education, patient risk assessment, patient counseling). Finally, we asked about availability of written guidelines for HBV and HCV testing and HAV and HBV vaccinations. Specifically, we asked whether written guidelines for each of these items were: 1=Clear; 2=Somewhat clear; 3=Unclear; 4=Don’t know if guidelines exist; 5=No guidelines exist; 6=Program/service not offered.
Approval of this study was obtained from each Institutional Review Board with jurisdiction over the participating substance abuse treatment programs.
2.3 Outcomes Measures
The primary focus of this report is the availability of HBV and HCV testing in participating substance abuse treatment programs. The specific types of HBV tests assessed in this study included HBV surface antigen (HBsAg), HBV surface antibody (HBsAb), HBV core antibody (HBcAb), HBV e antigen (HBeAg), HBV e antibody (HBeAb), and HBV DNA testing. For HCV, we assessed the availability of HCV antibody, HCV recombinant immunoblot assay (RIBA), HCV qualitative polymerase-chain-reaction (PCR), HCV quantitative PCR, and HCV genotype testing. In addition, we also assessed the availability of other blood testing (complete blood count, serum chemistries, and hepatic panel).
The secondary outcome measures of this report included the proportion of substance abuse treatment programs that offered each of the 7 healthcare services for HCV, and whether the availability of these services differed between methadone and non-methadone programs.
Other secondary outcomes included the proportion of substance abuse treatment programs that offered vaccinations for HAV and HBV, and whether the proportion of programs that offered HBV and HCV testing and HAV and HBV vaccinations differed between programs that did and did not have clear or somewhat clear written guidelines regarding hepatitis testing.
2.4 Statistical Analysis
The survey sections used for this report consisted of Yes/No and multiple choice questions. The proportion of respondents providing a given answer was used to summarize each question. For the multiple choice questions, the categories of responses were collapsed into a broader set of categories (e.g., service offered either on-site or by contractual agreement with another provider; and clear or somewhat clear guidelines). Methadone and non-methadone programs were compared on the provision of services measures of interest, since previous research indicates that methadone programs are more likely to employ medical providers than non-methadone programs (Brown, Kritz, Goldsmith, Bini, Robinson, Alderson, & Rotrosen, 2007).
Categorical variables were expressed as proportions and compared using the Chi-square test or Fisher’s exact test. To minimize the possibility of type 1 error, Bonferroni corrections were applied. The p-value was set at 0.003 (0.05/16) for the comparison between methadone and non-methadone programs for HBV/HCV testing and HAV/HBV vaccination services offered. The p-value was set at 0.003 (0.05/16) for the comparison between methadone and non-methadone programs for HCV-related healthcare services offered. The p-value was set at 0.004 (0.05/14) for the comparison between existence/non-existence of clear or somewhat clear guidelines for HBV/HCV testing and HAV/HBV vaccination services. Statistical analyses were performed using SAS software version 9.1 for Windows.
3. RESULTS
3.1 Characteristics of the Substance Abuse Treatment Programs Surveyed
Of the 319 treatment program administrators surveyed, 269 individuals (84.3%) from geographically diverse locations in the United States returned surveys. The majority of substance abuse treatment programs were private not-for-profit, free-standing facilities. A substantial number of programs offered outpatient, outreach, and other support services, but far fewer offered inpatient/residential services or outpatient pharmacotherapy, such as methadone. In addition, program size, and medical and non-medical staffing patterns varied considerably.
3.2 Availability of HBV & HCV Testing and HAV & HBV Vaccinations in Substance Abuse Treatment Programs
As shown in Table 1, basic testing, consisting of complete blood count, serum chemistries, and liver function tests either on-site or by contractual agreement with another provider was done at about one-third of all substance abuse treatment programs.
Table 1.
HBV & HCV Testing and HAV & HBV Vaccination Services Offered by Substance Abuse Treatment Programs
| TEST/VACCINATION* | All Programs (%) N=269 |
Methadone Programs (%) N=89 |
Non-Methadone Programs (%) N=180 |
P-Value |
|---|---|---|---|---|
| Complete blood count ordered on all new patients | 34.5 | 58.6 | 22.2 | <0.001 |
| Serum chemistries ordered on all new patients | 33.1 | 58.1 | 20.5 | <0.001 |
| Liver function tests ordered on all new patients | 34.5 | 60.1 | 21.5 | <0.001 |
| HBV surface antigen testing | 20.5 | 41.2 | 10.4 | <0.001 |
| HBV surface antibody testing | 20.5 | 36.5 | 12.8 | <0.001 |
| HBV core antibody testing | 16.3 | 31.8 | 8.8 | <0.001 |
| HBV e antigen testing | 8.9 | 14.1 | 6.4 | 0.024 |
| HBV e antibody testing | 8.1 | 11.8 | 6.4 | 0.077 |
| HBV viral DNA testing | 3.9 | 7.4 | 2.3 | <0.036 |
| HCV antibody testing | 28.2 | 54.7 | 15.0 | <0.001 |
| HCV RIBA testing | 4.7 | 9.6 | 2.3 | 0.036 |
| HCV qualitative PCR testing | 4.7 | 9.5 | 2.3 | 0.026 |
| HCV quantitative PCR testing | 3.9 | 8.5 | 1.7 | <0.011 |
| HCV genotype testing | 6.2 | 14.1 | 2.3 | <0.001 |
| Other hepatitis testing | 2.7 | 4.7 | 1.9 | 0.072 |
| HAV and HBV vaccination for HCV-infected patients | 68.3 | 73.3 | 65.9 | 0.258 |
Refers to the service being offered either on-site or by contractual agreement with another provider
Bolded p values are statistically significant with Bonferroni correction
Testing to determine past or present infection with HBV or HCV either on-site or by contractual agreement with another provider ranged from 2.7% (Other hepatitis testing) to 28.2% (HCV antibody testing) with most rates <10% (Table 1). HBV and HCV testing was significantly more likely to be offered at methadone maintenance programs than non-methadone maintenance programs; however, the rate was less than half in almost all cases (Table 1).
Also shown in Table 1, HAV and HBV vaccination was offered either on-site or by contractual agreement with another provider at 68.3% of all substance abuse treatment programs.
3.3 Availability of HCV Healthcare Services in Substance Abuse Treatment Programs
For all patients in substance abuse treatment programs, HCV-related medical services (medical history and physical exam, biological testing, treatment, and monitoring) were offered either on-site or by contractual agreement with another provider at 50.0%, 34.4%, 28.9%, and 35.2% of all programs, respectively. HCV-related non-medical services (patient education, risk assessment, and counseling) were offered either on-site or by contractual agreement with another provider at 74.1%, 71.9%, and 58.9% of all programs, respectively (Table 2).
Table 2.
HCV Services Offered by Substance Abuse Treatment Programs
| HEALTHCARE SERVICE* | All Programs (%) (N=269) |
Methadone Programs (%) N=89 |
Non-Methadone Programs (%) N=180 |
P-Value |
|---|---|---|---|---|
| Patient medical history & physical exam | 50.0 | 83.3 | 38.0 | <0.001 |
| Patient biological testing | 34.4 | 63.4 | 24.0 | <0.001 |
| Patient treatment | 28.9 | 48.2 | 22.4 | <0.001 |
| Patient monitoring | 35.2 | 63.1 | 24.9 | <0.001 |
| Patient education | 74.1 | 88.1 | 73.7 | 0.009 |
| Patient risk assessment | 71.9 | 88.1 | 69.8 | 0.001 |
| Patient counseling | 58.9 | 82.1 | 52.6 | <0.001 |
Refers to the service being offered either on-site or by contractual agreement with another provider
Bolded p values are statistically significant with Bonferroni correction
Since previous studies have shown that the provision of medical and non-medical services differ between methadone and non-methadone programs, we evaluated whether the availability of HCV services also differed between these 2 groups of programs. As shown in Table 2, there was greater availability of all 7 HCV services at methadone vs. non-methadone programs, which was statistically significant; although for patient education, the statistical significance was lost with Bonferroni correction.
For HCV-infected patients, medical history and physical exam, counseling, treatment, and monitoring were offered either on-site or by contractual agreement with another provider at 37.6%, 43.4%, 18.2%, and 23.8% of programs, respectively (Table 3).
Table 3.
HCV Services Offered to HCV-infected Patients by Substance Abuse Treatment Programs (N=269)
| Medical histories & physical examination for HCV-infected patients | |
| Offered within substance abuse treatment program | 34.1% |
| Offered by contractual agreement with another provider | 3.5% |
| Offered by referral to community resource | 48.8% |
| Not offered | 13.6% |
| HCV counseling for HCV-infected patients | |
| Offered within substance abuse treatment program | 41.9% |
| Offered by contractual agreement with another provider | 1.5% |
| Offered by referral to community resource | 42.7% |
| Not offered | 13.9% |
| HCV treatment for HCV-infected patients | |
| Offered within substance abuse treatment program | 14.7% |
| Offered by contractual agreement with another provider | 3.5% |
| Offered by referral to community resource | 67.2% |
| Not offered | 14.7% |
| HCV treatment monitoring for HCV-infected patients | |
| Offered within substance abuse treatment program | 21.1% |
| Offered by contractual agreement with another provider | 2.7% |
| Offered by referral to community resource | 58.5% |
| Not offered | 17.7% |
3.4 Guidelines and HBV & HCV Testing and HAV & HBV Vaccination Services
As shown in Table 4, offering liver function, HBV, and HCV testing, and HAV and HBV vaccination either on-site or by contractual agreement with another provider ranged from 18.0% to 88.7% of substance abuse treatment programs with clear or somewhat clear regulatory guidelines. In substance abuse treatment programs where clear or somewhat clear regulatory guidelines did not exist, offers for testing and vaccination either on-site or by contractual agreement with another provider ranged from 1.9% to 59.8%. All 14 comparisons of testing/vaccination were statistically significant (p=0.017 to p≤0.001); although for 5 of the 14 comparisons, the statistical significance was lost with Bonferroni correction (Table 4).
Table 4.
Proportion of Substance Abuse Programs Offering HBV & HCV Testing and HAV & HBV Vaccination According to Presence or Absence of Clear or Somewhat Clear Guidelines for Hepatitis Testing (N=248)
| Test/Vaccination | Proportion of Programs Offering Testing* | P-Value | |
|---|---|---|---|
| Clear or Somewhat Clear Guidelines for Hepatitis Testing Exist |
Clear or Somewhat Clear Guidelines for Hepatitis Testing Do Not Exist |
||
| Liver function tests ordered on all new patients | 53.5% | 11.0% | <0.001 |
| HBV surface antigen testing | 75.0% | 16.4% | <0.001 |
| HBV surface antibody testing | 72.7% | 18.2% | <0.001 |
| HBV core antibody testing | 59.5% | 14.8% | <0.001 |
| HBV e antigen testing | 33.3% | 5.7% | <0.001 |
| HBV e antibody testing | 32.0% | 3.8% | <0.001 |
| HBV viral DNA testing | 18.0% | 1.9% | 0.005 |
| HCV antibody testing | 88.7% | 21.8% | <0.001 |
| HCV RIBA testing | 27.4% | 7.4% | 0.004 |
| HCV qualitative PCR testing | 24.7% | 5.7% | 0.007 |
| HCV quantitative PCR testing | 22.5% | 3.8% | 0.004 |
| HCV genotype testing | 24.7% | 5.6% | 0.007 |
| Other hepatitis testing | 19.2% | 2.0% | 0.008 |
| HAV and HBV vaccination to HCV-infected patients | 74.8% | 59.8% | 0.017 |
Refers to the service being offered either on-site or by contractual agreement with another provider
Bolded p values are statistically significant with Bonferroni correction
4. DISCUSSION
4.1 Summary of Our Findings
In the present study of 269 substance abuse treatment programs in the United States, we found that a substantial proportion of all programs do not offer HBV or HCV testing either on-site or by referral to another facility. This includes methadone maintenance programs in most instances. While the presence of program guidelines significantly improved the availability of HBV and HCV testing, a substantial majority of most of these services were not available in substance abuse treatment programs, whether they offered methadone maintenance or not. Considering the fact that our study only included programs within the NIDA CTN, where evidence-based practices would more likely be implemented than in other substance abuse treatment programs, the results are sobering. In view of the fact that treatment for chronic HBV and HCV infection has improved considerably over the past few years, these findings have important implications for the estimated 19.1 million current illicit substance users in the United States (Substance Abuse & Mental Health Services Administration NSDUH, 2005), and represent missed public health opportunities to diagnose, treat, and prevent further transmission of these infections, as has been the case with HIV disease (Hubbard, Marsden, Cavanaugh, Rachal, Ginzgurg, 1988; Metzger, Navaline, Woody, 1998; Sorensen, Copeland, 2000; Farrell, Gowing, Marsden, Ling, Ali 2005).
4.2 Previous Studies of HBV & HCV Services in Substance Abuse Treatment Programs
Despite the major public health importance of the HBV and HCV epidemics among substance abusers, few studies have comprehensively evaluated the range of health services offered for these infections in substance abuse treatment programs in the United States. Although estimates vary widely, these studies showed that a disappointingly high proportion of substance abuse treatment programs did not offer any testing for HCV (22.7% – 76.7%) (Substance Abuse & Mental Health Services Administration NSDUH, 2005; Substance Abuse & Mental Health Services Administration N-SSATS, 2005; Strauss, Astone, Des Jarlais, & Hagen, 2004). In our study, which covered a larger number of services, these findings were confirmed and extended to testing and services not previously reported.
4.3 Low Rates of HAV and HBV Vaccination Services
Another interesting and important finding was the relatively low proportion of substance abuse treatment programs offering vaccinations against HAV and HBV, given that injection and non-injection drug users are at high risk of HAV and HBV infection, and these infections can be effectively prevented by immunization (Goldstein, Alter, Williams, Moyer, Judson, Mottram, Fleenor, Ryder, & Margolis, 2002; Garfein, Bower, Loney, Hutin, Xia, Jawanda, Groom, Nainan, Murphy, & Bell, 2004; Centers for Disease Control and Prevention, 1999; O’Donovan, Cooke, Joce, Eastbury, Waite, & Stene-Johansen, 2001; Craig, & Schaffner, 2004; Spada, Genovese, Tosti, Mariano, Cuccuini, Proietti, Di Giuli, Lavagna, Crapa, Morace, Taffon, Mele, Rezza, & Rapicetta, 2005; Centers for Disease Control and Prevention, 2006).
Currently, the Centers for Disease Control and Prevention and others recommend that all substance abusers receive the HAV and HBV vaccine if they have not already been exposed or immunized (Centers for Disease Control and Prevention, 1999; Craig, Schaffner, 2004; Crowcroft, Walsh, Davison, & Gungabissoon, 2001; Hershey, Schowalter, & Bailey, 2005; Poland, & Jacobson, 2004; Poland, 2005; Quaglio, Lugoboni, Mezzelani, Des Jarlais, & Lechi, 2006). A substantial proportion of substance abusers have underlying chronic liver disease due to HCV infection and are at increased risk of acute liver failure and death if they were to become superinfected with HAV or HBV (Akriviadis, & Redeker, 1989; Vento, Garofano, Renzini, Cainelli, Casali, Ghironzi, Ferraro, & Concia, 1998; Koff, 2001; Cooksley, 2004; Reiss, & Keeffe, 2004; Keeffe, 2005). The presence of chronic liver disease due to HCV infection is also a clinical indication for HAV and HBV vaccination (Centers for Disease Control and Prevention, 1999; Centers for Disease Control and Prevention, 2006; Koff, 2001; Cooksley, 2004; Reiss, & Keeffe, 2004; Keeffe, 2005; Almasio, & Amoroso, 2003; Gaslightwala, & Bini, 2006) and, therefore, many substance abusers have a dual indication for both HAV and HBV vaccination. Failure to vaccinate these individuals against HAV and HBV represent missed opportunities for prevention.
4.4 Strengths and Weaknesses
The strengths of the present study include the large number of substance abuse treatment programs surveyed, the geographic diversity of these programs (Figure 1), the high response rates from treatment program administrators (84.3%) and the collection of comprehensive information about health services offered for HBV and HCV. In addition, our study is unique because we are unaware of any prior studies that have as comprehensively evaluated availability of testing and healthcare services for HIV, HCV, and STI in substance abuse treatment programs across the United States. The finding that a number of HBV and HCV testing, and HCV healthcare services are more readily available at methadone maintenance programs than non-methadone maintenance programs is consistent with a previous report from this study demonstrating that methadone maintenance programs have significantly more medical staff than non-methadone maintenance programs (Brown, Kritz, Goldsmith, Bini, Robinson, Alderson, & Rotrosen, 2007).
Figure 1.
Geographic Distribution of Substance Abuse Program Study Participants
Nonetheless, there are several limitations of this study to consider when interpreting our findings. First, we surveyed only substance abuse treatment programs within the CTN, and the services provided by these programs may differ from those associated with substance abuse treatment programs that do not participate in this network. However, this is unlikely because the distribution of the size and structure of the programs in our study were similar to the distribution of the 13,454 programs in the National Survey of Substance Abuse Treatment Services study (Substance Abuse & Mental Health Services Administration N-SSATS, 2005). Although there are some differences between CTN and non-CTN programs, there are also many similarities (Institute for Behavioral Research, 2005).
The self report nature of the study survey did not allow us to verify the accuracy of administrator responses. Some administrators may be more knowledgeable about their programs and/or have more access to hard data regarding survey questions than other administrators. To the extent that accuracy of responses was impacted, it represents a limitation.
4.5 Conclusions
We found that there was a lack of widespread availability of comprehensive testing and other health services for HBV and HCV both on-site or by referral to another facility in substance abuse treatment programs, whether offering methadone maintenance or not, in the United States. Since substance abuse treatment programs are an important point of contact to provide risk-reduction counseling, testing, and treatment for these infections, these identified shortcomings provide opportunities for public health intervention.
Acknowledgments
This study was supported by the National Institute on Drug Abuse (NIDA)/National Institutes of Health via the National Drug Abuse Treatment Clinical Trials Network (U10-DA13046). We are indebted to the efforts of administrators, clinicians, and investigators of the 17 universities and medical centers along with the participating community-based substance abuse treatment programs of the National Drug Abuse Treatment Clinical Trials Network.
Footnotes
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
References
- Akriviadis EA, Redeker AG. Fulminant hepatitis A in intravenous drug users with chronic liver disease. Annals of Internal Medicine. 1989;110:838–839. doi: 10.7326/0003-4819-110-10-838. [DOI] [PubMed] [Google Scholar]
- Almasio PL, Amoroso P. HAV infection in chronic liver disease: a rationale for vaccination. Vaccine. 2003;21:2238–2241. doi: 10.1016/s0264-410x(03)00139-7. [DOI] [PubMed] [Google Scholar]
- Armstrong GL, Wasley A, Simard EP, McQillan GM, Kuhnert WL, Alter MJ. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Annals of Internal Medicine. 2006;144:705–714. doi: 10.7326/0003-4819-144-10-200605160-00004. [DOI] [PubMed] [Google Scholar]
- Brown LS, Jr, Kritz SA, Goldsmith RJ, Bini EJ, Rotrosen J, Baker S, Robinson J, McAuliffe P. Characteristics of substance abuse treatment programs providing services for HIV/AIDS, hepatitis C virus infection, and sexually transmitted infections: the National Drug Abuse Treatment Clinical Trials Network. Journal of Substance Abuse Treatment. 2006;30:315–321. doi: 10.1016/j.jsat.2006.02.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown LS, Kritz S, Goldsmith RJ, Bini EJ, Robinson J, Alderson D, Rotrosen J. Health Services for HIV/AIDS, HCV, and Sexually Transmitted Infections in Substance Abuse Treatment Programs. Public Health Reports. 2007;122:441–51. doi: 10.1177/003335490712200404. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Centers for Disease Control and Prevention. Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease. Morbidity & Mortality Weekly Report. 1998;47:1–39. [PubMed] [Google Scholar]
- Centers for Disease Control and Prevention. Prevention of hepatitis A through active or passive immunization: Recommendations of the Advisory Committee on Immunization Practices (ACIP) Morbidity & Mortality Weekly Report. 1999;48:1–37. [PubMed] [Google Scholar]
- 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 II: immunization of adults. Morbidity & Mortality Weekly Report. 2006;55:1–33. [PubMed] [Google Scholar]
- Cooksley G. The importance and benefits of hepatitis A prevention in chronic liver disease patients. Journal of Gastroenterology and Hepatology. 2004;19(Suppl):S17–S20. doi: 10.1111/j.1440-1746.2003.03394.x. [DOI] [PubMed] [Google Scholar]
- Craig AS, Schaffner W. Prevention of hepatitis A with the hepatitis A vaccine. New England Journal of Medicine. 2004;350:476–481. doi: 10.1056/NEJMcp031540. [DOI] [PubMed] [Google Scholar]
- Crowcroft NS, Walsh B, Davison KL, Gungabissoon U. Guidelines for the control of hepatitis A virus infection. Communicable Disease and Public Health. 2001;4:213–227. [PubMed] [Google Scholar]
- Custer B, Sullivan SD, Hazlet TK, Iloeje U, Veenstra DL, Kowdley KV. Global epidemiology of hepatitis B virus. Journal of Clinical Gastroenterology. 2004;38:S158–S168. doi: 10.1097/00004836-200411003-00008. [DOI] [PubMed] [Google Scholar]
- Donato F, Boffetta P, Puoti M. A meta-analysis of epidemiological studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma. International Journal of Cancer. 1998;75:347–354. doi: 10.1002/(sici)1097-0215(19980130)75:3<347::aid-ijc4>3.0.co;2-2. [DOI] [PubMed] [Google Scholar]
- Farrell M, Gowing L, Marsden J, Ling W, Ali R. Effectiveness of drug dependence treatment in HIV prevention. International Journal of Drug Policy. 2005;16:67–75. [Google Scholar]
- Garfein RS, Bower WA, Loney CM, Hutin YJF, Xia G, Jawanda J, Groom AV, Nainan OV, Murphy JS, Bell BP. Factors associated with fulminant liver failure during an outbreak among injection drug users with acute hepatitis B. Hepatology. 2004;40:865–873. doi: 10.1002/hep.20383. [DOI] [PubMed] [Google Scholar]
- Gaslightwala I, Bini EJ. Vaccination against hepatitis A in patients with chronic liver disease. Current Hepatitis Reports. 2006;5:49–53. [Google Scholar]
- Global Burden of Hepatitis C Working Group. Global burden of disease (GBD) for hepatitis C. Journal of Clinical Pharmacology. 2004;44:20–29. doi: 10.1177/0091270003258669. [DOI] [PubMed] [Google Scholar]
- Goldstein ST, Alter MJ, Williams IT, Moyer LA, Judson FN, Mottram K, Fleenor M, Ryder PL, Margolis HS. Incidence and risk factors for acute hepatitis B in the United States, 1982–1998: implications for vaccination programs. Journal of Infectious Diseases. 2002;185:713–719. doi: 10.1086/339192. [DOI] [PubMed] [Google Scholar]
- Hershey JH, Schowalter L, Bailey SB. Public health perspective on vaccine-preventable hepatitis: integrating hepatitis A and B vaccines into public health settings. American Journal of Medicine. 2005;118(Suppl 10A):100S–108S. doi: 10.1016/j.amjmed.2005.07.028. [DOI] [PubMed] [Google Scholar]
- Hubbard RL, Craddock SG, Anderson J. Overview of 5-year followup outcomes in the drug abuse treatment outcome studies (DATOS) Journal of Substance Abuse Treatment. 2003;25:125–134. doi: 10.1016/s0740-5472(03)00130-2. [DOI] [PubMed] [Google Scholar]
- Hubbard RL, Marsden ME, Cavanaugh E, Rachal JV, Ginzgurg HM. Role of drug abuse treatment in limiting the spread of AIDS. Reviews of Infectious Diseases. 1988;10:377–384. doi: 10.1093/clinids/10.2.377. [DOI] [PubMed] [Google Scholar]
- Institute for Behavioral Research. NTCS Report No. 10. University of Georgia; Athens, GA: 2005. Clinical Trials Network Summary & Comparison Report. [Google Scholar]
- Keeffe EB. Acute hepatitis A and B in patients with chronic liver disease: prevention through vaccination. American Journal of Medicine. 2005;118(Suppl 10A):21S–27S. doi: 10.1016/j.amjmed.2005.07.013. [DOI] [PubMed] [Google Scholar]
- Koblin BA, Factor SH, Wu Y, Vlahov D. Hepatitis C virus infection among noninjecting drug users in New York City. Journal of Medical Virology. 2003;70:387–390. doi: 10.1002/jmv.10407. [DOI] [PubMed] [Google Scholar]
- Koff RS. Risks associated with hepatitis A and hepatitis B in patients with hepatitis C. Journal of Clinical Gastroenterology. 2001;33:20–26. doi: 10.1097/00004836-200107000-00006. [DOI] [PubMed] [Google Scholar]
- Lai CL, Ratziu V, Yuen MF, Poynard T. Viral hepatitis B. Lancet. 2003;362:2089–2094. doi: 10.1016/S0140-6736(03)15108-2. [DOI] [PubMed] [Google Scholar]
- Lok AS, McMahon BJ. Chronic hepatitis B. Hepatology. 2007;45:507–539. doi: 10.1002/hep.21513. [DOI] [PubMed] [Google Scholar]
- Metzger DS, Navaline H, Woody GE. Drug abuse treatment as AIDS prevention. Public Health Reports. 1998;113:97–106. [PMC free article] [PubMed] [Google Scholar]
- McQuillan GM, Coleman PJ, Kruszon-Moran D, Moyer LA, Lambert SB, Margolis HS. Prevalence of hepatitis B virus infection in the United States: the National Health and Nutrition Examination Surveys, 1976 through 1994. American Journal of Public Health. 1999;89:14–18. doi: 10.2105/ajph.89.1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murrill CS, Weeks H, Castrucci BC, Weinstock HS, Bell BP, Spruill C, Gwinn M. Age-specific seroprevalence of HIV, hepatitis B virus, and hepatitis C virus infection among injection drug users admitted to drug treatment in 6 US cities. American Journal of Public Health. 2002;92:385–387. doi: 10.2105/ajph.92.3.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- National Institutes of Health. National Institutes of Health Consensus Development Conference Statement: Management of hepatitis C: 2002--June 10–12, 2002. Hepatology. 2002;36:S3–20. doi: 10.1053/jhep.2002.37117. [DOI] [PubMed] [Google Scholar]
- O’Donovan D, Cooke RP, Joce R, Eastbury A, Waite J, Stene-Johansen K. An outbreak of hepatitis A amongst injecting drug users. Epidemiology and Infection. 2001;127:469–473. doi: 10.1017/s0950268801006185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poland GA, Jacobson RM. Clinical practice: prevention of hepatitis B with the hepatitis B vaccine. New England Journal of Medicine. 2004;351:2832–2838. doi: 10.1056/NEJMcp041507. [DOI] [PubMed] [Google Scholar]
- Poland GA. Evaluating existing recommendations for hepatitis A and B vaccination. American Journal of Medicine. 2005;118(Suppl 10A):16S–20S. doi: 10.1016/j.amjmed.2005.07.029. [DOI] [PubMed] [Google Scholar]
- Quaglio G, Lugoboni F, Pajusco B, Sarti M, Talamini G, Lechi A, Mezzelani P, Des Jarlais DC. Factors associated with hepatitis C virus infection in injection and noninjection drug users in Italy. Clinical Infectious Diseases. 2003;37:33–40. doi: 10.1086/375566. [DOI] [PubMed] [Google Scholar]
- Quaglio G, Lugoboni F, Mezzelani P, Des Jarlais DC, Lechi A. Hepatitis vaccination among drug users. Vaccine. 2006;24:2702–2709. doi: 10.1016/j.vaccine.2005.12.045. [DOI] [PubMed] [Google Scholar]
- Reiss G, Keeffe EB. Review article: hepatitis vaccination in patients with chronic liver disease. Alimentary Pharmacology & Therapeutics. 2004;19:715–727. doi: 10.1111/j.1365-2036.2004.01906.x. [DOI] [PubMed] [Google Scholar]
- Sharma P, Lok A. Viral hepatitis and liver transplantation. Seminars in Liver Disease. 2006;26:285–297. doi: 10.1055/s-2006-947298. [DOI] [PubMed] [Google Scholar]
- Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infectious Diseases. 2005;5:558–567. doi: 10.1016/S1473-3099(05)70216-4. [DOI] [PubMed] [Google Scholar]
- Shi J, Zhu L, Liu S, Xie F. A meta-analysis of case-control studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma in China. British Journal of Cancer. 2005;92:607–612. doi: 10.1038/sj.bjc.6602333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sorensen JL, Copeland AL. Drug abuse treatment as an HIV prevention strategy: a review. Drug & Alcohol Dependence. 2000;59:17–31. doi: 10.1016/s0376-8716(99)00104-0. [DOI] [PubMed] [Google Scholar]
- Spada E, Genovese D, Tosti ME, Mariano A, Cuccuini M, Proietti L, Di Giuli C, Lavagna A, Crapa GE, Morace G, Taffon S, Mele A, Rezza G, Rapicetta M. An outbreak of hepatitis A virus infection with a high case-fatality rate among injecting drug users. Journal of Hepatology. 2005;43:958–964. doi: 10.1016/j.jhep.2005.06.012. [DOI] [PubMed] [Google Scholar]
- Strader DB, Wright T, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C. Hepatology. 2004;39:1147–1171. doi: 10.1002/hep.20119. [DOI] [PubMed] [Google Scholar]
- Strauss SM, Astone JM, Des Jarlais D, Hagen H. A comparison of HCV antibody testing in drug-free and methadone maintenance treatment programs in the United States. Drug and Alcohol Dependence. 2004;73:227–236. doi: 10.1016/j.drugalcdep.2003.08.009. [DOI] [PubMed] [Google Scholar]
- Substance Abuse & Mental Health Services Administration. DHHS Publication No. SMA 05-4062. Rockville, MD: 2005. Results from the 2004 National Survey on Drug Use and Health: National Findings (Office of Applied Studies), NSDUH Series H-28. [Google Scholar]
- Substance Abuse & Mental Health Services Administration. DHHS Publication No. SMA 05-4112. Rockville, MD: 2005. National Survey of Substance Abuse Treatment Programs (N-SSATS): 2004. Data on Substance Abuse Treatment Facilities, DASIS Series: S-28. [Google Scholar]
- Sulkowski MS, Thomas DL. Epidemiology and natural history of hepatitis C virus infection in injection drug users: implications for treatment. Clinical Infectious Diseases. 2005;40(Suppl 5):S263–S269. doi: 10.1086/427440. [DOI] [PubMed] [Google Scholar]
- Tortu S, Neaigus A, McMahon J, Hagen D. Hepatitis C among noninjecting drug users: a report. Substance Use & Misuse. 2001;36:523–534. doi: 10.1081/ja-100102640. [DOI] [PubMed] [Google Scholar]
- Tortu S, McMahon JM, Pouget ER, Hamid R. Sharing of noninjection drug-use implements as a risk factor for hepatitis C. Substance Use & Misuse. 2004;39:211–224. doi: 10.1081/ja-120028488. [DOI] [PubMed] [Google Scholar]
- Vento S, Garofano T, Renzini C, Cainelli F, Casali F, Ghironzi G, Ferraro T, Concia E. Fulminant hepatitis associated with hepatitis A virus superinfection in patients with chronic hepatitis C. New England Journal of Medicine. 1998;338:286–290. doi: 10.1056/NEJM199801293380503. [DOI] [PubMed] [Google Scholar]

