Research
High-Yield Birth-Cohort Hepatitis C Virus Screening and Linkage to Care Among Underserved African Americans, Atlanta, Georgia, 2012–2013 Lesley S. Miller, MDa Francois Rollin, MD, MPHa Shelly-Ann Fluker, MDa Kristina L. Lundberg, MDa Brandi Park, MPHa Kristi Quairoli, PharmDb Nyiramugisha K. Niyibizi, MPHc Anne C. Spaulding, MD, MPHc
ABSTRACT Objective. Hepatitis C virus (HCV) infection disproportionately affects certain populations, including those born between 1945 and 1965 (i.e., baby boomers) and African Americans. As part of the Hepatitis Testing and Linkage to Care initiative, which promoted hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites, we conducted routine HCV screening to identify previously undiagnosed, primarily African American baby boomers with chronic hepatitis C infection and link them to care. Methods. We launched the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative at the Grady Memorial Hospital Primary Care Center and Grady Liver Clinic in Atlanta, Georgia, in October 2012, and present results from the first year. TILT-C faculty implemented an electronic medical record prompt and conducted educational sessions to boost HCV screening. A project coordinator tracked testing outcomes and linked HCV-positive patients to care. Results. Of 2,894 patients tested for anti-HCV, 201 (6.9%) tested positive. Men had a significantly higher (p,0.001) prevalence of HCV infection than women, with 106 of 1,091 (9.7%) men compared with 95 of 1,803 (5.3%) women testing anti-HCV positive. A total of 174 of 201 (86.6%) anti-HCVpositive patients received HCV ribonucleic acid (RNA) testing. Of 124 patients with a positive HCV RNA test, 122 were referred to care and 120 attended the first appointment. Conclusion. The TILT-C screening program was feasible and effective in detecting previously undiagnosed HCV infection and linking patients to care. The unexpectedly high prevalence of HCV infection in this primarily African American, baby boomer population underscores the need for aggressive HCV screening efforts in similar populations.
Emory University School of Medicine, Department of Medicine, Division of General Medicine and Geriatrics, Atlanta, GA
a
Grady Health System, Department of Clinical Pharmacy, Atlanta, GA
b
Emory University, School of Public Health, Department of Epidemiology, Atlanta, GA
c
Address correspondence to: Lesley S. Miller, MD, Emory University School of Medicine, Department of Medicine, Division of General Medicine and Geriatrics, 49 Jesse Hill Jr. Dr. SE, Atlanta, GA 30303; tel. 404-778-1635; fax 404-778-1601; e-mail . ©2016 Association of Schools and Programs of Public Health
84
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 85
Hepatitis C is a major public health problem in the United States, and black/African Americans are disproportionately affected.1 Data from the 2003–2010 National Health and Nutrition Examination Survey (NHANES) estimated that 2.2–3.2 million Americans are chronically infected with hepatitis C virus (HCV), representing 1% of the U.S. noninstitutionalized household population. One-quarter of infections are in black people and 81% of infections are among adults born between 1945 and 1965 (i.e., baby boomers, or the birth cohort). Estimated prevalence of chronic HCV infection in this birth cohort is 2.6%, which is sixfold greater than that of other adults.1,2 Importantly, NHANES likely underestimated the number of Americans infected because it did not survey incarcerated and homeless populations, two groups in which the prevalence of HCV infection is predicted to be higher than among the U.S. household population.3,4 HCV infection is the leading indicator for liver transplant, is a major cause of end-stage liver disease and hepatocellular carcinoma, and contributes to 15,000 deaths annually.5 A modeling study predicted that without increased screening and treatment, the incidence of end-stage liver disease from HCV could quadruple in the next 20 years.6 Total costs are predicted to rise from $6.5 billion in 2013 to $9.1 billion in 2024.7 New direct-acting antivirals have revolutionized the treatment of chronic HCV infection. Current all-oral therapies have the highest cure rates in history.8 For these treatments to achieve their full potential, more undiagnosed chronic HCV patients must be identified with improved screening. Until recently, HCV screening was based solely on risk-factor assessment, which was ineffective, evidenced by the fact that only half of those with chronic HCV infection are aware of their infection.9,10 Several studies also document poor provider adherence to HCV screening guidelines.11–14 Given that risk factor-based screening left many people undiagnosed and that most chronic HCV infection is found in those born between 1945 and 1965, the Centers for Disease Control and Prevention (CDC) updated its HCV screening guidelines in 2012 to add one-time screening in the birth cohort, acknowledging that birth-cohort screening is cost effective.10,15–17 In 2013, the U.S. Preventive Services Task Force also recommended HCV birth-cohort screening.18 We describe a program that implemented birthcohort HCV screening at Grady Memorial Hospital (GMH), an urban safety-net hospital in Atlanta, Georgia. The GMH Primary Care Center (PCC) is staffed by Emory University internal medicine residents (hereinafter, “residents”) and faculty, has 60,000 patient visits per year, and serves mostly underinsured and
uninsured African American patients. The Grady Liver Clinic (GLC), founded by general internists in 2002 to provide a conduit to chronic HCV infection care when specialty clinics were difficult to access, operates from the PCC.19 The GLC provides comprehensive care and treatment for patients with chronic HCV infection. Our program, Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C), demonstrated the feasibility of high-yield birth-cohort HCV screening and linkage to care in an underserved, predominantly African American population. METHODS TILT-C was funded through CDC’s Hepatitis Testing and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites. The TILT-C program established a three-step cascade: (1) HCV screening of appropriate patients (TILT-C Screen), (2) notification and appointment scheduling for HCV antibody (anti-HCV)-positive patients (TILT-C Link), and (3) a visit for comprehensive hepatitis C care (TILT-C Care). The goals for the project were to screen 2,000 patients for anti-HCV, test 85% of antiHCV-positive patients for HCV ribonucleic acid (RNA), and link 75% of HCV RNA-positive patients (i.e., those diagnosed with chronic HCV infection) to care. TILT-C Screen Starting in October 2012, all 137 residents with continuity practices in the PCC received a multicomponent educational intervention by a GLC/TILT-C physician. Residents received an e-mail introducing TILT-C, outlining its goals, and stressing that residents would be at the frontline of screening eligible patients. To be eligible for HCV screening, patients had to be born between 1945 and 1965 and not previously tested for HCV. Patients who were anti-HCV tested for an indication other than birth year (i.e., injection drug use [IDU], elevated liver enzymes) were excluded to avoid mixing a risk factor-based testing strategy with a birth-cohort testing strategy. Attached to the e-mail was the CDC recommendation for birth-cohort screening.15 Residents were advised to use a brief counseling script (Figure 1) to standardize the message about HCV testing. The faculty who supervised residents in the PCC received a similar e-mail, explaining TILT-C and encouraging them to support the program and screen in their faculty practices. Next, GLC/TILT-C faculty conducted one-on-one educational sessions with residents, reviewed birthcohort screening recommendations, and suggested
Public Health Reports / 2016 Supplement 2 / Volume 131
86 Research
Figure 1. Hepatitis C virus testing prompt including counseling script used in the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a
STOP! Was your patient born between 1945 and 1965? If yes, order HCV antibody today. HCV antibody results: no results HCV antibody ordered: YES NO “The CDC recently made new recommendations about hepatitis C testing. They recommend that all people born between 1945–1965 get tested one time for hepatitis C. Because you fall within this age group, I recommend that you get a hepatitis C test today.” a TILT-C was part of the Hepatitis Testing and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 33 U.S. sites.
HCV 5 hepatitis C virus CDC 5 Centers for Disease Control and Prevention
documentation in the Epic brand (Epic Systems Corporation, Verona, Wisconsin) electronic health record (EHR). The TILT-C educational intervention guided residents to embed a dotphrase (i.e., a brief section of text) in their progress note template, which included the counseling script (Figure 1), to remind them to perform birth-cohort HCV screening on eligible patients. It automatically pulled in existing anti-HCV test results and prompted residents to document if an anti-HCV test had been ordered. Residents also received logo pens from CDC’s “Know More Hepatitis” awareness campaign, posters were hung in the clinic, and patients received “Know More Hepatitis” key chains to prompt inquiry about screening. After the educational intervention, residents screened birth-cohort patients. When a patient consented to screening, the resident ordered the anti-HCV test to be drawn at the onsite laboratory. Patients were advised to present to the laboratory immediately following the clinic appointment, but had the option of visiting the laboratory at any time in the next six months. TILT-C Link TILT-C Link proceeded in parallel with TILT-C Screen. The TILT-C project coordinator followed up PCC anti-HCV testing, relayed results to anti-HCV-positive patients, and arranged HCV RNA testing and linkage to care in the GLC. The coordinator manually reviewed charts, abstracted visits of all birth-cohort PCC patients, and extracted anti-HCV test results. The project coordinator then called patients with positive anti-HCV tests. Using a script, the coordinator
explained the positive test, the need for confirmatory HCV RNA testing, and arranged linkage to specialty care by giving the patient a date, time, and location for their visit at the GLC. Patients were considered “referred to care” if a GLC appointment was scheduled and “linked to care” if they attended the appointment. HCV RNA testing required an additional laboratory visit because reflex testing (i.e., automatic laboratory testing for HCV RNA on any anti-HCV-positive blood sample) was not available. For patient convenience, the HCV RNA test was often performed at the linkage visit. The GMH laboratory sent all anti-HCV-positive results to the Georgia Department of Public Health per laboratory protocol. Patients unavailable to receive results by telephone after three attempts received result letters. Per PCC protocol, residents provided anti-HCVnegative results within two weeks, and the coordinator noted negative results in the TILT-C database. For pending anti-HCV tests, the coordinator noted a future order if the resident ordered the test but the patient did not go to the laboratory. The coordinator periodically reviewed patients’ charts to determine test completion. PCC linkage. Patients may have had a return visit to their PCC provider prior to or instead of a GLC linkage visit. Progress notes from these visits were analyzed, and visits at which the anti-HCV result was noted and addressed (i.e., HCV noted in the assessment and plan, HCV RNA or genotype testing ordered, and/or patient referred to GLC) satisfied the requirements for a primary care linkage visit.
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 87
TILT-C Care Monthly linkage-to-care visits consisted of two components. Care 1 was a one-hour group educational session in which a GLC/TILT-C physician covered the diagnosis, epidemiology, transmission, and natural history of HCV and the importance of alcohol avoidance and vaccination for hepatitis A virus and hepatitis B virus. The physician also introduced the role of liver biopsy and detailed treatment options for HCV. Care 2 immediately followed Care 1 and was a GLC physician visit to evaluate risk factors for HCV infection, prior evaluation and treatment for hepatitis C, as well as hepatitis A virus and hepatitis B virus vaccination history. The physician also reviewed laboratory results and ordered liver imaging or biopsy for patients who needed it. Finally, the GLC physician provided individual counseling on avoidance of HCV transmission, risk reduction, and treatment options. Data management TILT-C data consisted of demographic characteristics, test results (i.e., anti-HCV, HCV RNA, and genotype), and linkage to care. For those linked to care, TILT-C data also included hepatitis C risk history and vaccination status, if recorded. The project coordinator extracted all TILT-C data from the EHR and submitted it into EvaluationWeb®, a secure, Internet-based database that facilitated data management for HepTLC programs.20 The database combined black or African American into one category (i.e., black/African American) and only allowed de-identified data to be entered. We analyzed data from all patients screened in the TILT-C program from October 5, 2012, to September 30, 2013. Analysis We examined relationships between demographic factors and the following outcomes: testing anti-HCV positive, obtaining HCV RNA testing, testing HCV RNA positive, and being linked to care (i.e., defined as attending the first medical appointment with the GLC or a primary care physician). We calculated age and birth-cohort subset by assuming each patient was born on January 1 of the recorded birth year. In EvaluationWeb, the Hispanic category of race was designated as “no race specified,” which allowed the Hispanic category to solely represent ethnicity and not race. We dichotomized the race variable into two levels for analysis: black/African American and non-black/African American, and treated the “no race specified/Hispanic” and “don’t know” categories as missing for this new binary race variable. The main
outcome of interest was linkage to GLC care. We examined associations between variables using Pearson’s c2 tests, with p,0.05 considered significant. We performed all analyses using SAS® version 9.3.21 RESULTS TILT-C met or exceeded all performance goals set by CDC. We screened 2,894 birth-cohort adults for anti-HCV, tested 174 of 201 (86.6%) anti-HCV-positive patients for HCV RNA, and linked 122 of 124 (98.4%) patients with chronic HCV infection to care. Screening for HCV in the 1945–1965 birth cohort resulted in 201 of 2,894 (6.9%) patients testing anti-HCV positive. The mean age of anti-HCV-positive patients was 59 years. Men were more likely than women to be anti-HCV positive (χ2520.80; p,0.001). Rates of anti-HCV positivity among black/African Americans and non-black/African Americans were similar. Of the 174 patients tested for HCV RNA, 124 (71.3%) were HCV RNA positive, and black/African Americans were more likely to be HCV RNA positive than non-black/African Americans (χ255.64; p50.018). HCV RNA test results did not vary significantly by sex (Table 1). Patients with anti-HCV-positive test results with either confirmed HCV RNA or pending HCV RNA testing were referred to a primary care physician or specialty care visit at GLC (Table 2). Per project protocol, we only analyzed HCV RNA-positive (i.e., viremic) patients for linkage to care. Of 124 viremic patients, 122 (98.4%) were referred to follow-up care and two were lost to follow-up. Of the 122 patients referred to care, 120 (98.4%) were linked to care—98 patients to GLC and 22 patients to primary care—and two patients were referred to the GLC but did not attend their first appointment (Figure 2). Comparing linkage to GLC with all other outcomes combined, black/African Americans were more likely than non-black/African Americans to visit the GLC (χ2511.87; p50.001). Thirty-five of the 98 patients who were linked to the GLC and three of the 22 patients linked to primary care reported a history of IDU, none of whom reported current use. Seventy GLC patients and seven primary care patients had no history of hepatitis A virus or hepatitis B virus vaccination. The diligence in querying about these matters differed by setting, which partially explained differences in the proportion of patients with reported histories of IDU or vaccination. Among those analyzed for HCV genotype, genotype 1 was reported in 103 of 108 (95.4%) patients. No significant associations were found among IDU history, vaccination history, or genotype.
Public Health Reports / 2016 Supplement 2 / Volume 131
88 Research
Table 1. Characteristics of patients tested for anti-HCV and HCV RNA during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a Characteristic
Number tested for anti-HCV (percent)b
Total Mean age, in years (standard deviation) Birth year, range 1940–1949 1950–1959 1960–1969 Sex Female Male Race American Indian/Alaska Native Asian Black/African American Not specified (Hispanic) Native Hawaiian/Pacific Islander White Don’t know Ethnicity Hispanic/Latino Not Hispanic/Latino Don’t know
Number anti-HCV positive (percent) b
2,894 52.5 (3.5)
Number HCV RNA positive (percent)b
201 58.9 (4.7)
124 59.0 (4.6)
468 (16.2) 1,579 (54.6) 847 (29.3)
25 (12.4) 135 (67.2) 41 (20.4)
15 (12.1) 84 (67.7) 25 (20.2)
1,803 (62.3) 1,091 (37.7)
95 (47.3) 106 (52.7)
55 (44.4) 69 (55.6)
9 18 2,670 33 2 146 16
0 0 186 2 0 13 0
(0.3) (0.6) (92.3) (1.1) (0.1) (5.0) (0.6)
33 (1.1) 2,813 (97.2) 48 (1.7)
(0.0) (0.0) (92.5) (1.0) (0.0) (6.5) (0.0)
0 0 118 1 0 5 0
2 (1.0) 196 (97.1) 3 (1.5)
(0.0) (0.0) (95.2) (0.8) (0.0) (4.0) (0.0)
1 (0.8) 123 (99.2) 0 (0.0)
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
Percentages may not total to 100 because of rounding.
b
anti-HCV 5 hepatitis C virus antibody HCV 5 hepatitis C virus RNA 5 ribonucleic acid
Table 2. Characteristics of patients testing anti-HCV positive and HCV RNA positive (n=124) who were linked to care during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a Characteristic Total Mean age, in years (standard deviation) Birth year, range 1940–1949 1950–1959 1960–1969 Sex Female Male Race Black/African American No race specified (Hispanic) White
No follow-up
Referred to a specialist; no visit
Visited a primary care physician
Visited Grady Liver Clinic
2 63 (1.4)
2 64 (1.4)
22 57.8 (4.8)
98 59.1 (4.5)
0 2 0
1 1 0
2 13 7
12 68 18
1 1
1 1
10 12
43 55
2 0 0
2 0 0
18 0 4
96 1 1
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
anti-HCV 5 antibody to hepatitis C virus HCV 5 hepatitis C virus RNA 5 ribonucleic acid
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 89
DISCUSSION The TILT-C project was successful in training residents to perform HCV screening, accurately identifying chronic HCV infection, and linking nearly all chronically infected patients to care. We implemented a new screening practice by introducing several interventions to prompt physicians to screen. First, EHR reminders appeared to be an important component, which supports a study by Shojania et al. demonstrating that Figure 2. Linkage-to-care cascade among patients testing HCV RNA positive during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a
2,894 anti-HCV tested
201 (6.9%) anti-HCV positive
2,693 (93.1%) anti-HCV negative
174 (86.6%) HCV RNA tested
27 (13.4%) not HCV RNA tested
124 (71.3%) HCV RNA positive
50 (28.7%) HCV RNA negative
120 (96.8%) linked to care
4 (3.2%) not linked to care
22 (18.3%) linked to primary care physician
98 (81.7%) linked to Grady Liver Clinic
2 (1.6%) referred to care
2 (1.6%) lost to follow-up
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
HCV 5 hepatitis C virus RNA 5 ribonucleic acid anti-HCV 5 antibody to hepatitis C virus
reminders reinforce screening behaviors.22 In addition, providing one-on-one resident education allowed us to personalize the intervention, potentially contributing to residents’ willingness to screen for HCV. Finally, internal medicine residents were ideal screeners, because birth-cohort HCV screening could be seamlessly added to the preventive health measures these residents were being trained to implement. Ideally, resident physicians will take these new practices with them beyond our training institution. Our program uncovered a high prevalence of chronic HCV infection and resulted in high linkageto-care rates for viremic patients. This success was due in part to our testing sequence. Without reflex RNA testing, most patients needed to present for a clinic visit at GLC or PCC for HCV RNA testing; therefore, linkage to care occurred for most viremic patients. The availability of a colocated hepatitis C specialty clinic may have contributed to high linkage-to-care rates because of patients’ familiarity with the clinic location, staff, and operations. Offering care to uninsured patients also was a critical component of our program. Importantly, we found that even those patients who were linked to primary care had robust linkage visits. Many residents at GMH had trained with GLC faculty and rotated through the clinic; as such, they knew the basics of HCV management and could perform a comprehensive initial hepatitis C visit in the primary care setting. Finally, the TILT-C project coordinator called patients, often repeatedly, to deliver HCV testing results and referrals to care. This personalized and proactive case management likely contributed to the high linkage-to-care rate. Limitations This study had several limitations. First, we only measured the number of patients screened, not the number eligible for screening; without this denominator, we could not fully determine the rate at which residents performed screening and, thus, if the intervention changed physician behavior. Second, we tested high numbers of patients based on high clinic volumes, but informal chart review revealed that not all residents consistently screened patients. A formal evaluation of residents’ screening rates and targeted feedback for underperformers may have led to higher screening rates. We also had limitations in our linkage protocol. At each stage of the care continuum, patients were lost to follow-up. Missed opportunities for patients who never presented to the laboratory for anti-HCV testing could have been avoided by implementing rapid testing at the point of care.
Public Health Reports / 2016 Supplement 2 / Volume 131
90 Research
Finally, although the GLC provides antiviral therapy, it was beyond the scope of this project to follow patients through this final stage of the care cascade. In addition, this project took place during a time of transition in antiviral therapies, when many patients deferred therapy while waiting for approval of new medications with more favorable side effects and efficacy profiles. We plan to report treatment outcomes for this cohort when they become available. Based on historical outcomes of treatment uptake and cure rates in the GLC,19 we anticipate high rates of retention in care and treatment success at this final stage of the care cascade. CONCLUSION In the TILT-C program, birth-cohort HCV screening for undeserved patients in an academic primary care setting was feasible and yielded new diagnoses of chronic HCV infection. An onsite, primary care-based hepatitis C clinic facilitated high rates of linkage to specialty care. This program can be used as a model for primary care providers caring for underserved patient populations with a high prevalence of HCV. This demonstration project was conducted in the context of public health practice; as such, the Emory University Institutional Review Board (IRB) deemed the project non-human subjects research and waived IRB review.
REFERENCES 1. Denniston MM, Jiles RB, Drobeniuc J, Klevens RM, Ward JW, McQuillan GM, et al. Chronic hepatitis C virus infection in the United States, National Health and Nutrition Examination Survey 2003 to 2010. Ann Intern Med 2014;160:293-300. 2. Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 2006;144:705-14. 3. Gelberg L, Robertson MJ, Arangua L, Leake BD, Sumner G, Moe A, et al. Prevalence, distribution, and correlates of hepatitis C virus infection among homeless adults in Los Angeles. Public Health Rep 2012;127:407-21. 4. Varan AK, Mercer DW, Stein MS, Spaulding AC. Hepatitis C seroprevalence among prison inmates since 2001: still high but declining. Public Health Rep 2014;129:187-95.
5. Ly KN, Xing J, Klevens RM, Jiles RB, Ward JW, Holmberg SD. The increasing burden of mortality from viral hepatitis in the United States between 1999 and 2007. Ann Intern Med 2012;156:271-8. 6. Rein DB, Wittenborn JS, Weinbaum CM, Sabin M, Smith BD, Lesesne SB. Forecasting the morbidity and mortality associated with prevalent cases of pre-cirrhotic chronic hepatitis C in the United States. Dig Liver Dis 2011;43:66-72. 7. Razavi H, Elkhoury AC, Elbasha E, Estes C, Pasini K, Poynard T, et al. Chronic hepatitis C virus (HCV) disease burden and cost in the United States. Hepatology 2013;57:2164-70. 8. Kohli A, Shaffer A, Sherman A, Kottilil S. Treatment of hepatitis C: a systematic review. JAMA 2014;312:631-40. 9. Pyenson BS, Fitch KV, Iwasaki K. Consequences of hepatitis C virus (HCV): costs of a baby boomer epidemic of liver disease. Seattle: Milliman, Inc.; 2009. 10. Rein DB, Smith BD, Wittenborn JS, Lesesne SB, Wagner LD, Roblin DW, et al. The cost-effectiveness of birth-cohort screening for hepatitis C antibody in U.S. primary care settings. Ann Intern Med 2012;156:263-70. 11. Roblin DW, Smith BD, Weinbaum CM, Sabin ME. HCV screening practices and prevalence in an MCO, 2000–2007. Am J Manag Care 2011;17:548-55. 12. Spradling PR, Rupp L, Moorman AC, Lu M, Teshale EH, Gordon SC, et al. Hepatitis B and C virus infection among 1.2 million persons with access to care: factors associated with testing and infection prevalence. Clin Infect Dis 2012;55:1047-55. 13. Linas BP, Hu H, Barter DM, Horberg M. Hepatitis C screening trends in a large integrated health system. Am J Med 2014;127:398-405. 14. Southern WN, Drainoni ML, Smith BD, Koppelman E, McKee MD, Christiansen CL, et al. Physician nonadherence with a hepatitis C screening program. Qual Manag Health Care 2014;23:1-9. 15. Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Teo CG, at al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945–1965 [published erratum appears in MMWR Recomm Rep 2012;61(43):886]. MMWR Recomm Rep 2012;61(RR-4):1-32. 16. McGarry LJ, Pawar VS, Panchmatia HR, Rubin JL, Davis GL, Younossi ZM, et al. Economic model of a birth cohort screening program for hepatitis C virus. Hepatology 2012;55:1344-55. 17. Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Ward JW. Hepatitis C virus testing of persons born during 1945–1965: recommendations from the Centers for Disease Control and Prevention. Ann Intern Med 2012;157:817-22. 18. Moyer VA; U.S. Preventive Services Task Force. Screening for hepatitis C virus infection in adults: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2013;159:349-57. 19. Miller L, Fluker SA, Osborn M, Liu X, Strawder A. Improving access to hepatitis C care for urban, underserved patients using a primary care-based hepatitis C clinic. J Natl Med Assoc 2012;104:244-50. 20. Luther Consulting LLC. EvaluationWeb®: Version 5. Carmel (IN): Luther Consulting LLC; 2013. 21. SAS Institute, Inc. SAS®: Version 9.3. Cary (NC): SAS Institute, Inc.; 2011. 22. Shojania KG, Jennings A, Mayhew A, Ramsay CR, Eccles MP, Grimshaw J. The effects of on-screen, point of care computer reminders on processes and outcomes of care. Cochrane Database Syst Rev 2009;(3):CD001096.
Public Health Reports / 2016 Supplement 2 / Volume 131
High-Yield Birth-Cohort Hepatitis C Virus Screening and Linkage to Care Among Underserved African Americans, Atlanta, Georgia, 2012–2013 Lesley S. Miller, MDa Francois Rollin, MD, MPHa Shelly-Ann Fluker, MDa Kristina L. Lundberg, MDa Brandi Park, MPHa Kristi Quairoli, PharmDb Nyiramugisha K. Niyibizi, MPHc Anne C. Spaulding, MD, MPHc
ABSTRACT Objective. Hepatitis C virus (HCV) infection disproportionately affects certain populations, including those born between 1945 and 1965 (i.e., baby boomers) and African Americans. As part of the Hepatitis Testing and Linkage to Care initiative, which promoted hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites, we conducted routine HCV screening to identify previously undiagnosed, primarily African American baby boomers with chronic hepatitis C infection and link them to care. Methods. We launched the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative at the Grady Memorial Hospital Primary Care Center and Grady Liver Clinic in Atlanta, Georgia, in October 2012, and present results from the first year. TILT-C faculty implemented an electronic medical record prompt and conducted educational sessions to boost HCV screening. A project coordinator tracked testing outcomes and linked HCV-positive patients to care. Results. Of 2,894 patients tested for anti-HCV, 201 (6.9%) tested positive. Men had a significantly higher (p,0.001) prevalence of HCV infection than women, with 106 of 1,091 (9.7%) men compared with 95 of 1,803 (5.3%) women testing anti-HCV positive. A total of 174 of 201 (86.6%) anti-HCVpositive patients received HCV ribonucleic acid (RNA) testing. Of 124 patients with a positive HCV RNA test, 122 were referred to care and 120 attended the first appointment. Conclusion. The TILT-C screening program was feasible and effective in detecting previously undiagnosed HCV infection and linking patients to care. The unexpectedly high prevalence of HCV infection in this primarily African American, baby boomer population underscores the need for aggressive HCV screening efforts in similar populations.
Emory University School of Medicine, Department of Medicine, Division of General Medicine and Geriatrics, Atlanta, GA
a
Grady Health System, Department of Clinical Pharmacy, Atlanta, GA
b
Emory University, School of Public Health, Department of Epidemiology, Atlanta, GA
c
Address correspondence to: Lesley S. Miller, MD, Emory University School of Medicine, Department of Medicine, Division of General Medicine and Geriatrics, 49 Jesse Hill Jr. Dr. SE, Atlanta, GA 30303; tel. 404-778-1635; fax 404-778-1601; e-mail . ©2016 Association of Schools and Programs of Public Health
84
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 85
Hepatitis C is a major public health problem in the United States, and black/African Americans are disproportionately affected.1 Data from the 2003–2010 National Health and Nutrition Examination Survey (NHANES) estimated that 2.2–3.2 million Americans are chronically infected with hepatitis C virus (HCV), representing 1% of the U.S. noninstitutionalized household population. One-quarter of infections are in black people and 81% of infections are among adults born between 1945 and 1965 (i.e., baby boomers, or the birth cohort). Estimated prevalence of chronic HCV infection in this birth cohort is 2.6%, which is sixfold greater than that of other adults.1,2 Importantly, NHANES likely underestimated the number of Americans infected because it did not survey incarcerated and homeless populations, two groups in which the prevalence of HCV infection is predicted to be higher than among the U.S. household population.3,4 HCV infection is the leading indicator for liver transplant, is a major cause of end-stage liver disease and hepatocellular carcinoma, and contributes to 15,000 deaths annually.5 A modeling study predicted that without increased screening and treatment, the incidence of end-stage liver disease from HCV could quadruple in the next 20 years.6 Total costs are predicted to rise from $6.5 billion in 2013 to $9.1 billion in 2024.7 New direct-acting antivirals have revolutionized the treatment of chronic HCV infection. Current all-oral therapies have the highest cure rates in history.8 For these treatments to achieve their full potential, more undiagnosed chronic HCV patients must be identified with improved screening. Until recently, HCV screening was based solely on risk-factor assessment, which was ineffective, evidenced by the fact that only half of those with chronic HCV infection are aware of their infection.9,10 Several studies also document poor provider adherence to HCV screening guidelines.11–14 Given that risk factor-based screening left many people undiagnosed and that most chronic HCV infection is found in those born between 1945 and 1965, the Centers for Disease Control and Prevention (CDC) updated its HCV screening guidelines in 2012 to add one-time screening in the birth cohort, acknowledging that birth-cohort screening is cost effective.10,15–17 In 2013, the U.S. Preventive Services Task Force also recommended HCV birth-cohort screening.18 We describe a program that implemented birthcohort HCV screening at Grady Memorial Hospital (GMH), an urban safety-net hospital in Atlanta, Georgia. The GMH Primary Care Center (PCC) is staffed by Emory University internal medicine residents (hereinafter, “residents”) and faculty, has 60,000 patient visits per year, and serves mostly underinsured and
uninsured African American patients. The Grady Liver Clinic (GLC), founded by general internists in 2002 to provide a conduit to chronic HCV infection care when specialty clinics were difficult to access, operates from the PCC.19 The GLC provides comprehensive care and treatment for patients with chronic HCV infection. Our program, Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C), demonstrated the feasibility of high-yield birth-cohort HCV screening and linkage to care in an underserved, predominantly African American population. METHODS TILT-C was funded through CDC’s Hepatitis Testing and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites. The TILT-C program established a three-step cascade: (1) HCV screening of appropriate patients (TILT-C Screen), (2) notification and appointment scheduling for HCV antibody (anti-HCV)-positive patients (TILT-C Link), and (3) a visit for comprehensive hepatitis C care (TILT-C Care). The goals for the project were to screen 2,000 patients for anti-HCV, test 85% of antiHCV-positive patients for HCV ribonucleic acid (RNA), and link 75% of HCV RNA-positive patients (i.e., those diagnosed with chronic HCV infection) to care. TILT-C Screen Starting in October 2012, all 137 residents with continuity practices in the PCC received a multicomponent educational intervention by a GLC/TILT-C physician. Residents received an e-mail introducing TILT-C, outlining its goals, and stressing that residents would be at the frontline of screening eligible patients. To be eligible for HCV screening, patients had to be born between 1945 and 1965 and not previously tested for HCV. Patients who were anti-HCV tested for an indication other than birth year (i.e., injection drug use [IDU], elevated liver enzymes) were excluded to avoid mixing a risk factor-based testing strategy with a birth-cohort testing strategy. Attached to the e-mail was the CDC recommendation for birth-cohort screening.15 Residents were advised to use a brief counseling script (Figure 1) to standardize the message about HCV testing. The faculty who supervised residents in the PCC received a similar e-mail, explaining TILT-C and encouraging them to support the program and screen in their faculty practices. Next, GLC/TILT-C faculty conducted one-on-one educational sessions with residents, reviewed birthcohort screening recommendations, and suggested
Public Health Reports / 2016 Supplement 2 / Volume 131
86 Research
Figure 1. Hepatitis C virus testing prompt including counseling script used in the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a
STOP! Was your patient born between 1945 and 1965? If yes, order HCV antibody today. HCV antibody results: no results HCV antibody ordered: YES NO “The CDC recently made new recommendations about hepatitis C testing. They recommend that all people born between 1945–1965 get tested one time for hepatitis C. Because you fall within this age group, I recommend that you get a hepatitis C test today.” a TILT-C was part of the Hepatitis Testing and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 33 U.S. sites.
HCV 5 hepatitis C virus CDC 5 Centers for Disease Control and Prevention
documentation in the Epic brand (Epic Systems Corporation, Verona, Wisconsin) electronic health record (EHR). The TILT-C educational intervention guided residents to embed a dotphrase (i.e., a brief section of text) in their progress note template, which included the counseling script (Figure 1), to remind them to perform birth-cohort HCV screening on eligible patients. It automatically pulled in existing anti-HCV test results and prompted residents to document if an anti-HCV test had been ordered. Residents also received logo pens from CDC’s “Know More Hepatitis” awareness campaign, posters were hung in the clinic, and patients received “Know More Hepatitis” key chains to prompt inquiry about screening. After the educational intervention, residents screened birth-cohort patients. When a patient consented to screening, the resident ordered the anti-HCV test to be drawn at the onsite laboratory. Patients were advised to present to the laboratory immediately following the clinic appointment, but had the option of visiting the laboratory at any time in the next six months. TILT-C Link TILT-C Link proceeded in parallel with TILT-C Screen. The TILT-C project coordinator followed up PCC anti-HCV testing, relayed results to anti-HCV-positive patients, and arranged HCV RNA testing and linkage to care in the GLC. The coordinator manually reviewed charts, abstracted visits of all birth-cohort PCC patients, and extracted anti-HCV test results. The project coordinator then called patients with positive anti-HCV tests. Using a script, the coordinator
explained the positive test, the need for confirmatory HCV RNA testing, and arranged linkage to specialty care by giving the patient a date, time, and location for their visit at the GLC. Patients were considered “referred to care” if a GLC appointment was scheduled and “linked to care” if they attended the appointment. HCV RNA testing required an additional laboratory visit because reflex testing (i.e., automatic laboratory testing for HCV RNA on any anti-HCV-positive blood sample) was not available. For patient convenience, the HCV RNA test was often performed at the linkage visit. The GMH laboratory sent all anti-HCV-positive results to the Georgia Department of Public Health per laboratory protocol. Patients unavailable to receive results by telephone after three attempts received result letters. Per PCC protocol, residents provided anti-HCVnegative results within two weeks, and the coordinator noted negative results in the TILT-C database. For pending anti-HCV tests, the coordinator noted a future order if the resident ordered the test but the patient did not go to the laboratory. The coordinator periodically reviewed patients’ charts to determine test completion. PCC linkage. Patients may have had a return visit to their PCC provider prior to or instead of a GLC linkage visit. Progress notes from these visits were analyzed, and visits at which the anti-HCV result was noted and addressed (i.e., HCV noted in the assessment and plan, HCV RNA or genotype testing ordered, and/or patient referred to GLC) satisfied the requirements for a primary care linkage visit.
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 87
TILT-C Care Monthly linkage-to-care visits consisted of two components. Care 1 was a one-hour group educational session in which a GLC/TILT-C physician covered the diagnosis, epidemiology, transmission, and natural history of HCV and the importance of alcohol avoidance and vaccination for hepatitis A virus and hepatitis B virus. The physician also introduced the role of liver biopsy and detailed treatment options for HCV. Care 2 immediately followed Care 1 and was a GLC physician visit to evaluate risk factors for HCV infection, prior evaluation and treatment for hepatitis C, as well as hepatitis A virus and hepatitis B virus vaccination history. The physician also reviewed laboratory results and ordered liver imaging or biopsy for patients who needed it. Finally, the GLC physician provided individual counseling on avoidance of HCV transmission, risk reduction, and treatment options. Data management TILT-C data consisted of demographic characteristics, test results (i.e., anti-HCV, HCV RNA, and genotype), and linkage to care. For those linked to care, TILT-C data also included hepatitis C risk history and vaccination status, if recorded. The project coordinator extracted all TILT-C data from the EHR and submitted it into EvaluationWeb®, a secure, Internet-based database that facilitated data management for HepTLC programs.20 The database combined black or African American into one category (i.e., black/African American) and only allowed de-identified data to be entered. We analyzed data from all patients screened in the TILT-C program from October 5, 2012, to September 30, 2013. Analysis We examined relationships between demographic factors and the following outcomes: testing anti-HCV positive, obtaining HCV RNA testing, testing HCV RNA positive, and being linked to care (i.e., defined as attending the first medical appointment with the GLC or a primary care physician). We calculated age and birth-cohort subset by assuming each patient was born on January 1 of the recorded birth year. In EvaluationWeb, the Hispanic category of race was designated as “no race specified,” which allowed the Hispanic category to solely represent ethnicity and not race. We dichotomized the race variable into two levels for analysis: black/African American and non-black/African American, and treated the “no race specified/Hispanic” and “don’t know” categories as missing for this new binary race variable. The main
outcome of interest was linkage to GLC care. We examined associations between variables using Pearson’s c2 tests, with p,0.05 considered significant. We performed all analyses using SAS® version 9.3.21 RESULTS TILT-C met or exceeded all performance goals set by CDC. We screened 2,894 birth-cohort adults for anti-HCV, tested 174 of 201 (86.6%) anti-HCV-positive patients for HCV RNA, and linked 122 of 124 (98.4%) patients with chronic HCV infection to care. Screening for HCV in the 1945–1965 birth cohort resulted in 201 of 2,894 (6.9%) patients testing anti-HCV positive. The mean age of anti-HCV-positive patients was 59 years. Men were more likely than women to be anti-HCV positive (χ2520.80; p,0.001). Rates of anti-HCV positivity among black/African Americans and non-black/African Americans were similar. Of the 174 patients tested for HCV RNA, 124 (71.3%) were HCV RNA positive, and black/African Americans were more likely to be HCV RNA positive than non-black/African Americans (χ255.64; p50.018). HCV RNA test results did not vary significantly by sex (Table 1). Patients with anti-HCV-positive test results with either confirmed HCV RNA or pending HCV RNA testing were referred to a primary care physician or specialty care visit at GLC (Table 2). Per project protocol, we only analyzed HCV RNA-positive (i.e., viremic) patients for linkage to care. Of 124 viremic patients, 122 (98.4%) were referred to follow-up care and two were lost to follow-up. Of the 122 patients referred to care, 120 (98.4%) were linked to care—98 patients to GLC and 22 patients to primary care—and two patients were referred to the GLC but did not attend their first appointment (Figure 2). Comparing linkage to GLC with all other outcomes combined, black/African Americans were more likely than non-black/African Americans to visit the GLC (χ2511.87; p50.001). Thirty-five of the 98 patients who were linked to the GLC and three of the 22 patients linked to primary care reported a history of IDU, none of whom reported current use. Seventy GLC patients and seven primary care patients had no history of hepatitis A virus or hepatitis B virus vaccination. The diligence in querying about these matters differed by setting, which partially explained differences in the proportion of patients with reported histories of IDU or vaccination. Among those analyzed for HCV genotype, genotype 1 was reported in 103 of 108 (95.4%) patients. No significant associations were found among IDU history, vaccination history, or genotype.
Public Health Reports / 2016 Supplement 2 / Volume 131
88 Research
Table 1. Characteristics of patients tested for anti-HCV and HCV RNA during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a Characteristic
Number tested for anti-HCV (percent)b
Total Mean age, in years (standard deviation) Birth year, range 1940–1949 1950–1959 1960–1969 Sex Female Male Race American Indian/Alaska Native Asian Black/African American Not specified (Hispanic) Native Hawaiian/Pacific Islander White Don’t know Ethnicity Hispanic/Latino Not Hispanic/Latino Don’t know
Number anti-HCV positive (percent) b
2,894 52.5 (3.5)
Number HCV RNA positive (percent)b
201 58.9 (4.7)
124 59.0 (4.6)
468 (16.2) 1,579 (54.6) 847 (29.3)
25 (12.4) 135 (67.2) 41 (20.4)
15 (12.1) 84 (67.7) 25 (20.2)
1,803 (62.3) 1,091 (37.7)
95 (47.3) 106 (52.7)
55 (44.4) 69 (55.6)
9 18 2,670 33 2 146 16
0 0 186 2 0 13 0
(0.3) (0.6) (92.3) (1.1) (0.1) (5.0) (0.6)
33 (1.1) 2,813 (97.2) 48 (1.7)
(0.0) (0.0) (92.5) (1.0) (0.0) (6.5) (0.0)
0 0 118 1 0 5 0
2 (1.0) 196 (97.1) 3 (1.5)
(0.0) (0.0) (95.2) (0.8) (0.0) (4.0) (0.0)
1 (0.8) 123 (99.2) 0 (0.0)
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
Percentages may not total to 100 because of rounding.
b
anti-HCV 5 hepatitis C virus antibody HCV 5 hepatitis C virus RNA 5 ribonucleic acid
Table 2. Characteristics of patients testing anti-HCV positive and HCV RNA positive (n=124) who were linked to care during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a Characteristic Total Mean age, in years (standard deviation) Birth year, range 1940–1949 1950–1959 1960–1969 Sex Female Male Race Black/African American No race specified (Hispanic) White
No follow-up
Referred to a specialist; no visit
Visited a primary care physician
Visited Grady Liver Clinic
2 63 (1.4)
2 64 (1.4)
22 57.8 (4.8)
98 59.1 (4.5)
0 2 0
1 1 0
2 13 7
12 68 18
1 1
1 1
10 12
43 55
2 0 0
2 0 0
18 0 4
96 1 1
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
anti-HCV 5 antibody to hepatitis C virus HCV 5 hepatitis C virus RNA 5 ribonucleic acid
Public Health Reports / 2016 Supplement 2 / Volume 131
Birth-Cohort HCV Screening 89
DISCUSSION The TILT-C project was successful in training residents to perform HCV screening, accurately identifying chronic HCV infection, and linking nearly all chronically infected patients to care. We implemented a new screening practice by introducing several interventions to prompt physicians to screen. First, EHR reminders appeared to be an important component, which supports a study by Shojania et al. demonstrating that Figure 2. Linkage-to-care cascade among patients testing HCV RNA positive during the Internal Medicine Trainees Identifying and Linking to Treatment for Hepatitis C (TILT-C) initiative, Grady Memorial Hospital, Atlanta, Georgia, October 2012 through September 2013a
2,894 anti-HCV tested
201 (6.9%) anti-HCV positive
2,693 (93.1%) anti-HCV negative
174 (86.6%) HCV RNA tested
27 (13.4%) not HCV RNA tested
124 (71.3%) HCV RNA positive
50 (28.7%) HCV RNA negative
120 (96.8%) linked to care
4 (3.2%) not linked to care
22 (18.3%) linked to primary care physician
98 (81.7%) linked to Grady Liver Clinic
2 (1.6%) referred to care
2 (1.6%) lost to follow-up
a TILT-C was part of the Hepatitis Testing and Linkage to Care initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites.
HCV 5 hepatitis C virus RNA 5 ribonucleic acid anti-HCV 5 antibody to hepatitis C virus
reminders reinforce screening behaviors.22 In addition, providing one-on-one resident education allowed us to personalize the intervention, potentially contributing to residents’ willingness to screen for HCV. Finally, internal medicine residents were ideal screeners, because birth-cohort HCV screening could be seamlessly added to the preventive health measures these residents were being trained to implement. Ideally, resident physicians will take these new practices with them beyond our training institution. Our program uncovered a high prevalence of chronic HCV infection and resulted in high linkageto-care rates for viremic patients. This success was due in part to our testing sequence. Without reflex RNA testing, most patients needed to present for a clinic visit at GLC or PCC for HCV RNA testing; therefore, linkage to care occurred for most viremic patients. The availability of a colocated hepatitis C specialty clinic may have contributed to high linkage-to-care rates because of patients’ familiarity with the clinic location, staff, and operations. Offering care to uninsured patients also was a critical component of our program. Importantly, we found that even those patients who were linked to primary care had robust linkage visits. Many residents at GMH had trained with GLC faculty and rotated through the clinic; as such, they knew the basics of HCV management and could perform a comprehensive initial hepatitis C visit in the primary care setting. Finally, the TILT-C project coordinator called patients, often repeatedly, to deliver HCV testing results and referrals to care. This personalized and proactive case management likely contributed to the high linkage-to-care rate. Limitations This study had several limitations. First, we only measured the number of patients screened, not the number eligible for screening; without this denominator, we could not fully determine the rate at which residents performed screening and, thus, if the intervention changed physician behavior. Second, we tested high numbers of patients based on high clinic volumes, but informal chart review revealed that not all residents consistently screened patients. A formal evaluation of residents’ screening rates and targeted feedback for underperformers may have led to higher screening rates. We also had limitations in our linkage protocol. At each stage of the care continuum, patients were lost to follow-up. Missed opportunities for patients who never presented to the laboratory for anti-HCV testing could have been avoided by implementing rapid testing at the point of care.
Public Health Reports / 2016 Supplement 2 / Volume 131
90 Research
Finally, although the GLC provides antiviral therapy, it was beyond the scope of this project to follow patients through this final stage of the care cascade. In addition, this project took place during a time of transition in antiviral therapies, when many patients deferred therapy while waiting for approval of new medications with more favorable side effects and efficacy profiles. We plan to report treatment outcomes for this cohort when they become available. Based on historical outcomes of treatment uptake and cure rates in the GLC,19 we anticipate high rates of retention in care and treatment success at this final stage of the care cascade. CONCLUSION In the TILT-C program, birth-cohort HCV screening for undeserved patients in an academic primary care setting was feasible and yielded new diagnoses of chronic HCV infection. An onsite, primary care-based hepatitis C clinic facilitated high rates of linkage to specialty care. This program can be used as a model for primary care providers caring for underserved patient populations with a high prevalence of HCV. This demonstration project was conducted in the context of public health practice; as such, the Emory University Institutional Review Board (IRB) deemed the project non-human subjects research and waived IRB review.
REFERENCES 1. Denniston MM, Jiles RB, Drobeniuc J, Klevens RM, Ward JW, McQuillan GM, et al. Chronic hepatitis C virus infection in the United States, National Health and Nutrition Examination Survey 2003 to 2010. Ann Intern Med 2014;160:293-300. 2. Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 2006;144:705-14. 3. Gelberg L, Robertson MJ, Arangua L, Leake BD, Sumner G, Moe A, et al. Prevalence, distribution, and correlates of hepatitis C virus infection among homeless adults in Los Angeles. Public Health Rep 2012;127:407-21. 4. Varan AK, Mercer DW, Stein MS, Spaulding AC. Hepatitis C seroprevalence among prison inmates since 2001: still high but declining. Public Health Rep 2014;129:187-95.
5. Ly KN, Xing J, Klevens RM, Jiles RB, Ward JW, Holmberg SD. The increasing burden of mortality from viral hepatitis in the United States between 1999 and 2007. Ann Intern Med 2012;156:271-8. 6. Rein DB, Wittenborn JS, Weinbaum CM, Sabin M, Smith BD, Lesesne SB. Forecasting the morbidity and mortality associated with prevalent cases of pre-cirrhotic chronic hepatitis C in the United States. Dig Liver Dis 2011;43:66-72. 7. Razavi H, Elkhoury AC, Elbasha E, Estes C, Pasini K, Poynard T, et al. Chronic hepatitis C virus (HCV) disease burden and cost in the United States. Hepatology 2013;57:2164-70. 8. Kohli A, Shaffer A, Sherman A, Kottilil S. Treatment of hepatitis C: a systematic review. JAMA 2014;312:631-40. 9. Pyenson BS, Fitch KV, Iwasaki K. Consequences of hepatitis C virus (HCV): costs of a baby boomer epidemic of liver disease. Seattle: Milliman, Inc.; 2009. 10. Rein DB, Smith BD, Wittenborn JS, Lesesne SB, Wagner LD, Roblin DW, et al. The cost-effectiveness of birth-cohort screening for hepatitis C antibody in U.S. primary care settings. Ann Intern Med 2012;156:263-70. 11. Roblin DW, Smith BD, Weinbaum CM, Sabin ME. HCV screening practices and prevalence in an MCO, 2000–2007. Am J Manag Care 2011;17:548-55. 12. Spradling PR, Rupp L, Moorman AC, Lu M, Teshale EH, Gordon SC, et al. Hepatitis B and C virus infection among 1.2 million persons with access to care: factors associated with testing and infection prevalence. Clin Infect Dis 2012;55:1047-55. 13. Linas BP, Hu H, Barter DM, Horberg M. Hepatitis C screening trends in a large integrated health system. Am J Med 2014;127:398-405. 14. Southern WN, Drainoni ML, Smith BD, Koppelman E, McKee MD, Christiansen CL, et al. Physician nonadherence with a hepatitis C screening program. Qual Manag Health Care 2014;23:1-9. 15. Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Teo CG, at al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945–1965 [published erratum appears in MMWR Recomm Rep 2012;61(43):886]. MMWR Recomm Rep 2012;61(RR-4):1-32. 16. McGarry LJ, Pawar VS, Panchmatia HR, Rubin JL, Davis GL, Younossi ZM, et al. Economic model of a birth cohort screening program for hepatitis C virus. Hepatology 2012;55:1344-55. 17. Smith BD, Morgan RL, Beckett GA, Falck-Ytter Y, Holtzman D, Ward JW. Hepatitis C virus testing of persons born during 1945–1965: recommendations from the Centers for Disease Control and Prevention. Ann Intern Med 2012;157:817-22. 18. Moyer VA; U.S. Preventive Services Task Force. Screening for hepatitis C virus infection in adults: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2013;159:349-57. 19. Miller L, Fluker SA, Osborn M, Liu X, Strawder A. Improving access to hepatitis C care for urban, underserved patients using a primary care-based hepatitis C clinic. J Natl Med Assoc 2012;104:244-50. 20. Luther Consulting LLC. EvaluationWeb®: Version 5. Carmel (IN): Luther Consulting LLC; 2013. 21. SAS Institute, Inc. SAS®: Version 9.3. Cary (NC): SAS Institute, Inc.; 2011. 22. Shojania KG, Jennings A, Mayhew A, Ramsay CR, Eccles MP, Grimshaw J. The effects of on-screen, point of care computer reminders on processes and outcomes of care. Cochrane Database Syst Rev 2009;(3):CD001096.
Public Health Reports / 2016 Supplement 2 / Volume 131
