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Garry JD, Kundu S, Annis J, Alcorn C, Eden S, Smith E, Greevy R, Maron BA, Freiberg M, Brittain EL. Incidence of Pulmonary Hypertension in the Echocardiography Referral Population. Ann Am Thorac Soc 2025; 22:679-688. [PMID: 39680898 PMCID: PMC12051908 DOI: 10.1513/annalsats.202407-716oc] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2024] [Accepted: 12/13/2024] [Indexed: 12/18/2024] Open
Abstract
Rationale: Incidence rates for pulmonary hypertension using diagnostic data in patients with cardiopulmonary disease are not known. Objectives: To determine incidence rates of, risk factors for, and mortality hazard associated with pulmonary hypertension among patients referred for transthoracic echocardiography. Methods: A retrospective cohort study was conducted using data from the U.S. Department of Veterans Affairs (VA) (1999-2020) and Vanderbilt University Medical Center (1994-2020). Pulmonary hypertension was defined as pulmonary artery systolic pressure >35 mm Hg, with prevalent cases excluded. Heart failure and chronic obstructive pulmonary disease were the primary exposures of interest. The primary outcome was incident pulmonary hypertension. Secondarily, we examined mortality rate after incident diagnosis. Results: We identified 245,067 VA patients (94% men, 20% Black) and 117,526 Vanderbilt patients (46% men, 11% Black) without pulmonary hypertension, of whom 38,882 VA patients and 8,061 Vanderbilt patients developed pulmonary hypertension. Only 18-19% of patients with echocardiography-based pulmonary hypertension also had diagnostic codes. The hazard of pulmonary hypertension was fourfold higher in patients with heart failure and chronic obstructive pulmonary disease compared with patients without either. Mortality rates increased from pulmonary artery systolic pressure of 35-45 mm Hg and then plateaued. Independent risk factors for incident pulmonary hypertension included older age, male sex, Black race, and cardiometabolic comorbidities. Conclusions: Pulmonary hypertension incidence rates estimated by diagnostic data are higher than code-based rates. Heart failure and chronic obstructive pulmonary disease strongly associate with incident pulmonary hypertension. Pulmonary artery systolic pressure >45 mm Hg at diagnosis is associated with high mortality. New pulmonary hypertension on echocardiography is an important prognostic sign.
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Affiliation(s)
| | - Suman Kundu
- Vanderbilt Institute of Clinical and Translational Research, and
| | - Jeffrey Annis
- Vanderbilt Institute of Clinical and Translational Research, and
| | - Chuck Alcorn
- School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania
| | - Svetlana Eden
- Department of Biostatistics, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Emily Smith
- Vanderbilt Institute of Clinical and Translational Research, and
| | - Robert Greevy
- Department of Biostatistics, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Bradley A. Maron
- Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland
- The University of Maryland-Institute for Health Computing, Bethesda, Maryland; and
| | - Matthew Freiberg
- Division of Cardiovascular Medicine
- Veterans Affairs Tennessee Valley Healthcare System, Nashville, Tennessee
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Haque LY, Fiellin DA, Tate JP, Esserman D, Bhattacharya D, Butt AA, Crystal S, Edelman EJ, Gordon AJ, Lim JK, Tetrault JM, Williams EC, Bryant K, Cartwright EJ, Rentsch CT, Justice AC, Lo Re V, McGinnis KA. Association Between Alcohol Use Disorder and Receipt of Direct-Acting Antiviral Hepatitis C Virus Treatment. JAMA Netw Open 2022; 5:e2246604. [PMID: 36515952 PMCID: PMC9856353 DOI: 10.1001/jamanetworkopen.2022.46604] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/17/2022] [Accepted: 10/19/2022] [Indexed: 12/15/2022] Open
Abstract
IMPORTANCE Direct-acting antiviral (DAA) treatment for hepatitis C virus (HCV) infection is associated with lower mortality and is effective in individuals with alcohol use disorder (AUD). However, despite recommendations, patients with AUD may be less likely to receive DAAs. OBJECTIVE To assess the association between alcohol use and receipt of DAA treatment among patients with HCV within the Veterans Health Administration (VHA). DESIGN, SETTING, AND PARTICIPANTS This cohort study included 133 753 patients with HCV born from 1945 to 1965 who had completed the Alcohol Use Disorders Identification Test-Consumption (AUDIT-C) questionnaire and had at least 1 outpatient visit in the VHA from January 1, 2014, through May 31, 2017, with maximal follow-up of 3 years until May 31, 2020; DAA receipt; or death, whichever occurred first. EXPOSURES Alcohol use categories generated using responses to the AUDIT-C questionnaire and International Classification of Diseases, Ninth Revision and International Statistical Classification of Diseases and Related Health Problems, Tenth Revision diagnoses: current AUD, abstinent with AUD history, at-risk drinking, lower-risk drinking, and abstinent without AUD history. Demographic, other clinical, and pharmacy data were also collected. MAIN OUTCOMES AND MEASURES Associations between alcohol use categories and DAA receipt within 1 and 3 years estimated using Cox proportional hazards regression stratified by calendar year. RESULTS Of 133 753 patients (130 103 men [97%]; mean [SD] age, 60.6 [4.5] years; and 73 493 White patients [55%]), 38% had current AUD, 12% were abstinent with a history of AUD, 6% reported at-risk drinking, 14% reported lower-risk drinking, and 30% were abstinent without a history of AUD. Receipt of DAA treatment within 1 year was 7%, 33%, 53%, and 56% for patients entering the cohort in 2014, 2015, 2016, and 2017, respectively. For patients entering in 2014, those with current AUD (hazard ratio [HR], 0.72 [95%, CI, 0.66-0.77]) or who were abstinent with an AUD history (HR, 0.91 [95% CI, 0.84-1.00]) were less likely to receive DAA treatment within 1 year compared with patients with lower-risk drinking. For those entering in 2015-2017, patients with current AUD (HR, 0.75 [95% CI, 0.70-0.81]) and those who were abstinent with an AUD history (HR, 0.76 [95% CI, 0.68-0.86]) were less likely to receive DAA treatment within 1 year compared with patients with lower-risk drinking. CONCLUSIONS AND RELEVANCE This cohort study suggests that individuals with AUD, regardless of abstinence, were less likely to receive DAA treatment. Improved access to DAA treatment for persons with AUD is needed.
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Affiliation(s)
- Lamia Y. Haque
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Yale Program in Addiction Medicine, Yale School of Medicine, New Haven, Connecticut
| | - David A. Fiellin
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Yale Program in Addiction Medicine, Yale School of Medicine, New Haven, Connecticut
- Department of Health Policy and Management, Yale School of Public Health, New Haven, Connecticut
| | - Janet P. Tate
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Veterans Affairs Connecticut Health Care System, West Haven
| | - Denise Esserman
- Department of Biostatistics, Yale School of Public Health, New Haven, Connecticut
| | - Debika Bhattacharya
- Department of Internal Medicine, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles
- Veterans Affairs Greater Los Angeles Health Care System, Los Angeles, California
| | - Adeel A. Butt
- Department of Medicine, Weill Cornell Medicine, New York, New York
- Department of Population Health Sciences, Weill Cornell Medicine, New York, New York
- Veterans Affairs Pittsburgh Healthcare System, Pittsburgh, Pennsylvania
| | - Stephen Crystal
- Center for Health Services Research, Rutgers University, New Brunswick, New Jersey
| | - E. Jennifer Edelman
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Yale Program in Addiction Medicine, Yale School of Medicine, New Haven, Connecticut
- Department of Social and Behavioral Sciences, Yale School of Public Health, New Haven, Connecticut
| | - Adam J. Gordon
- Informatics, Decision-Enhancement, and Analytic Sciences Center, Veterans Affairs Salt Lake City Health Care System, Salt Lake City, Utah
- Program for Addiction Research, Clinical Care, Knowledge, and Advocacy, Division of Epidemiology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City
| | - Joseph K. Lim
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
| | - Jeanette M. Tetrault
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Yale Program in Addiction Medicine, Yale School of Medicine, New Haven, Connecticut
| | - Emily C. Williams
- Seattle-Denver Center of Innovation for Veteran-Centered and Value-Driven Care, Veterans Affairs Puget Sound Health Care System, Seattle, Washington
- Health Services Research and Development, Veterans Affairs Puget Sound Health Care System, Seattle, Washington
- Department of Health Systems and Population Health, University of Washington, Seattle
| | - Kendall Bryant
- HIV/AIDS and Alcohol Research Program, National Institute on Alcohol Abuse and Alcoholism, Bethesda, Maryland
| | - Emily J. Cartwright
- Department of Medicine, Emory School of Medicine, Atlanta, Georgia
- Veterans Affairs Atlanta Health Care System, Atlanta, Georgia
| | - Christopher T. Rentsch
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Veterans Affairs Connecticut Health Care System, West Haven
- London School of Hygiene and Tropical Medicine, London, United Kingdom
| | - Amy C. Justice
- Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
- Department of Health Policy and Management, Yale School of Public Health, New Haven, Connecticut
- Veterans Affairs Connecticut Health Care System, West Haven
| | - Vincent Lo Re
- Division of Infectious Diseases, Department of Medicine, Perelman School of Medicine, Philadelphia, Pennsylvania
- Center for Clinical Epidemiology and Biostatistics, Perelman School of Medicine, Philadelphia, Pennsylvania
- Department of Biostatistics, Epidemiology, and Informatics, Perelman School of Medicine, Philadelphia, Pennsylvania
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Aday AW, Duncan MS, Patterson OV, DuVall SL, Alba PR, Alcorn CW, Tindle HA, Creager MA, Bonaca MP, Damrauer SM, Wells QS, Behroozian A, Beckman JA, Freiberg MS. Association of Sex and Race With Incident Peripheral Artery Disease Among Veterans With Normal Ankle-Brachial Indices. JAMA Netw Open 2022; 5:e2240188. [PMID: 36326762 PMCID: PMC9634499 DOI: 10.1001/jamanetworkopen.2022.40188] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/06/2022] Open
Abstract
IMPORTANCE Reported risk of incident peripheral artery disease (PAD) by sex and race varies significantly and has not been reported in national cohorts among individuals free of baseline PAD. OBJECTIVE To evaluate the association of sex and race, as well as prevalent cardiovascular risk factors, with limb outcomes in a national cohort of people with normal baseline ankle-brachial indices (ABIs). DESIGN, SETTING, AND PARTICIPANTS This cohort study was conducted using data from participants in the Veterans Affairs Birth Cohort Study (born 1945-1965), with follow-up data between January 1, 2000, and December 31, 2016. Baseline demographics were collected from 77 041 participants receiving care from the Veterans Health Administration with baseline ABIs of 0.90 to 1.40 and no history of PAD. Data were analyzed from October 2019 through September 2022. EXPOSURES Sex, race, diabetes, and smoking status. MAIN OUTCOMES AND MEASURES Incident PAD, defined as subsequent ABI less than 0.90, surgical or percutaneous revascularization, or nontraumatic amputation. RESULTS Of 77 041 participants with normal ABIs (73 822 [95.8%] men; mean [SD] age, 60.2 [5.9] years; 13 080 Black [18.2%] and 54 377 White [75.6%] among 71 911 participants with race and ethnicity data), there were 6692 incident PAD events over a median [IQR] of 3.9 [1.7-6.9] years. Incidence rates were lower for women than men (incidence rates [IRs] per 1000 person-years, 7.4 incidents [95% CI, 6.2-8.8 incidents] vs 19.2 incidents [95% CI, 18.7-19.6 incidents]), with a lower risk of incident PAD (adjusted hazard ratio [aHR], 0.49 [95% CI, 0.41-0.59]). IRs per 1000 person-years of incident PAD were similar for Black and White participants (18.9 incidents [95% CI, 17.9-20.1 incidents] vs 18.8 incidents [95% CI, 18.3-19.4]). Compared with White participants, Black participants had increased risk of total PAD (aHR, 1.09 [95% CI, 1.02-1.16]) and nontraumatic amputation (aHR, 1.20 [95% CI, 1.06-1.36]) but not surgical or percutaneous revascularization (aHR, 1.10 [95% CI, 0.98-1.23]) or subsequent ABI less than 0.90 (aHR, 1.04 [95% CI, 0.95-1.13]). Diabetes (aHR, 1.62 [95% CI, 1.53-1.72]) and smoking (eg, current vs never: aHR, 1.76 [95% CI, 1.64-1.89]) were associated with incident PAD. Incident PAD was rare among individuals without a history of smoking or diabetes (eg, among 632 women: IR per 1000 people-years, 2.1 incidents [95% CI, 1.0-4.5 incidents]) despite an otherwise-high-risk cardiovascular profile (eg, 527 women [83.4%] with hypertension). CONCLUSIONS AND RELEVANCE This study found that the risk of PAD was approximately 50% lower in women than men and less than 10% higher for Black vs White participants, while the risk of nontraumatic amputation was 20% higher among Black compared with White participants.
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Affiliation(s)
- Aaron W. Aday
- Vanderbilt Translational and Clinical Cardiovascular Research Center, Division of Cardiovascular Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Meredith S. Duncan
- Vanderbilt Translational and Clinical Cardiovascular Research Center, Division of Cardiovascular Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
- Department of Biostatistics, College of Public Health, University of Kentucky, Lexington
| | - Olga V. Patterson
- VA Informatics and Computing Infrastructure, VA Salt Lake City Health Care System, Salt Lake City, Utah
- Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City
| | - Scott L. DuVall
- VA Informatics and Computing Infrastructure, VA Salt Lake City Health Care System, Salt Lake City, Utah
- Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City
| | - Patrick R. Alba
- VA Informatics and Computing Infrastructure, VA Salt Lake City Health Care System, Salt Lake City, Utah
- Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City
| | - Charles W. Alcorn
- University of Pittsburgh School of Public Health, Pittsburgh, Pennsylvania
| | - Hilary A. Tindle
- Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Mark A. Creager
- Heart and Vascular Center, Dartmouth-Hitchcock Medical Center, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire
| | - Marc P. Bonaca
- Colorado Prevention Center Clinical Research, Division of Cardiovascular Medicine, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora
| | - Scott M. Damrauer
- Department of Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia
- Corporal Michael Crescenz VA Medical Center, Philadelphia, Pennsylvania
| | - Quinn S. Wells
- Vanderbilt Translational and Clinical Cardiovascular Research Center, Division of Cardiovascular Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Adam Behroozian
- Department of Biostatistics, College of Public Health, University of Kentucky, Lexington
- Now with Division of Cardiovascular Diseases, Scripps Clinic, La Jolla, California
| | - Joshua A. Beckman
- Vanderbilt Translational and Clinical Cardiovascular Research Center, Division of Cardiovascular Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
| | - Matthew S. Freiberg
- Vanderbilt Translational and Clinical Cardiovascular Research Center, Division of Cardiovascular Medicine, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee
- Veterans Affairs Tennessee Valley Healthcare System, Nashville
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Torgersen J, Newcomb CW, Carbonari DM, Rentsch CT, Park LS, Mezochow A, Mehta RL, Buchwalder L, Tate JP, Bräu N, Bhattacharya D, Lim JK, Taddei TH, Justice AC, Lo Re V. Protease inhibitor-based direct-acting antivirals are associated with increased risk of aminotransferase elevations but not hepatic dysfunction or decompensation. J Hepatol 2021; 75:1312-1322. [PMID: 34333102 PMCID: PMC8604762 DOI: 10.1016/j.jhep.2021.07.021] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/23/2020] [Revised: 07/14/2021] [Accepted: 07/18/2021] [Indexed: 12/04/2022]
Abstract
BACKGROUND & AIMS Cases of acute liver injury (ALI) have been reported among chronic HCV-infected patients receiving protease inhibitor (PI)-based direct-acting antiviral (DAA) regimens, but no analyses have compared the risk of ALI in patients receiving PI- vs. non-PI-based DAAs. Thus, we compared the risk of 3 ALI outcomes between patients (by baseline Fibrosis-4 [FIB-4] group) receiving PI-based or non-PI-based DAAs. METHODS We conducted a cohort study of 18,498 patients receiving PI-based DAA therapy (paritaprevir/ritonavir/ombitasvir±dasabuvir, elbasvir/grazoprevir, glecaprevir/pibrentasvir) matched 1:1 on propensity score to those receiving non-PI-based DAAs (sofosbuvir/ledipasvir, sofosbuvir/velpatasvir) in the 1945-1965 Veterans Birth Cohort (2014-2019). During exposure to DAA therapy, we determined development of: i) alanine aminotransferase (ALT) >200 U/L, ii) severe hepatic dysfunction (coagulopathy with hyperbilirubinemia), and iii) hepatic decompensation. We used Cox regression to determine hazard ratios (HRs) with 95% CIs for each ALI outcome within groups defined by baseline FIB-4 (≤3.25; >3.25). RESULTS Among patients with baseline FIB-4 ≤3.25, those receiving PIs had a higher risk of ALT >200 U/L (HR 3.98; 95% CI 2.37-6.68), but not severe hepatic dysfunction (HR 0.67; 95% CI 0.19-2.39) or hepatic decompensation (HR 1.01; 95% CI 0.29-3.49), compared to those receiving non-PI-based regimens. For those with baseline FIB-4 >3.25, those receiving PIs had a higher risk of ALT >200 U/L (HR, 2.15; 95% CI 1.09-4.26), but not severe hepatic dysfunction (HR, 1.23 [0.64-2.38]) or hepatic decompensation (HR, 0.87; 95% CI 0.41-1.87), compared to those receiving non-PI-based regimens CONCLUSION: While risk of incident ALT elevations was increased in those receiving PI-based DAAs in both FIB-4 groups, the risk of severe hepatic dysfunction and hepatic decompensation did not differ between patients receiving PI- or non-PI-based DAAs in either FIB-4 group. LAY SUMMARY Cases of liver injury have been reported among patients treated with protease inhibitor-based direct-acting antivirals for hepatitis C infection, but it is not clear if the risk of liver injury among people starting these drugs is increased compared to those starting non-protease inhibitor-based therapy. In this study, patients receiving protease inhibitor-based treatment had a higher risk of liver inflammation than those receiving a non-protease inhibitor-based treatment, regardless of the presence of pre-treatment advanced liver fibrosis/cirrhosis. However, the risk of severe liver dysfunction and decompensation were not higher for patients treated with protease inhibitor-based regimens.
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Affiliation(s)
- Jessie Torgersen
- Division of Infectious Diseases, Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; Department of Biostatistics, Epidemiology, and Informatics, Center for Clinical Epidemiology and Biostatistics, Center for Pharmacoepidemiology Research and Training, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
| | - Craig W Newcomb
- Department of Biostatistics, Epidemiology, and Informatics, Center for Clinical Epidemiology and Biostatistics, Center for Pharmacoepidemiology Research and Training, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
| | - Dena M Carbonari
- Department of Biostatistics, Epidemiology, and Informatics, Center for Clinical Epidemiology and Biostatistics, Center for Pharmacoepidemiology Research and Training, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
| | - Christopher T Rentsch
- Department of Non-communicable Disease Epidemiology, London School of Hygiene & Tropical Medicine, London, UK; VA Connecticut Healthcare System, West Haven, CT, USA
| | - Lesley S Park
- Stanford Center for Population Health Sciences, Stanford University School of Medicine, Stanford, CA, USA
| | - Alyssa Mezochow
- Division of Infectious Diseases, Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
| | - Rajni L Mehta
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Lynn Buchwalder
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Janet P Tate
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Norbert Bräu
- James J. Peters VA Medical Center, Bronx, NY, USA; Icahn School of Medicine at Mount Sinai, New York, NY, USA
| | - Debika Bhattacharya
- VA Greater Los Angeles Healthcare System and David Geffen School of Medicine at UCLA, Los Angeles, CA, USA
| | - Joseph K Lim
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Tamar H Taddei
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA
| | - Amy C Justice
- VA Connecticut Healthcare System, West Haven, CT, USA; Department of Medicine, Yale School of Medicine, New Haven, CT, USA; Division of Health Policy and Management, Yale School of Public Health, New Haven, CT, USA
| | - Vincent Lo Re
- Division of Infectious Diseases, Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; Department of Biostatistics, Epidemiology, and Informatics, Center for Clinical Epidemiology and Biostatistics, Center for Pharmacoepidemiology Research and Training, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
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Tien A, Sahota A, Yang SJ, Balbuena R, Chang M, Lim C, Fong TL. Prevalence and Characteristics of Chronic Hepatitis C Among Asian Americans Are Distinct From Other Ethnic Groups. J Clin Gastroenterol 2021; 55:884-890. [PMID: 33074947 DOI: 10.1097/mcg.0000000000001447] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/04/2020] [Accepted: 09/12/2020] [Indexed: 01/22/2023]
Abstract
GOAL The goal of this study was to determine the prevalence and characteristics of chronic hepatitis C (CHC) among Asian Americans compared with other ethnicities. BACKGROUND Chronic hepatitis C virus (HCV) affects an estimated 2.7 million in the United States, but there are limited data on HCV among Asian Americans. STUDY A total of 3,369,881 adults over the age of 18 who were patients of the integrated health care system in Southern California and 4903 Asian participants at community hepatitis screenings were included in a cross-sectional study. Variables included HCV serology, HCV genotype, comorbidities, and coinfections. RESULTS The prevalence of CHC was 1.3% in the general population (8271 adults) and 0.6% among Asians. The prevalence of CHC was significantly higher in the 1945-1965 birth cohort with 2.7% (5876) in the general population and 1.0% (313) among Asians (P<0.001). Asians had the highest rates of hepatitis B coinfection (2.9% vs. 0.2%, P<0.001). The distribution of genotypes among Asians differed from the general population with the most common genotype being 1b (27.5%) and a higher presence of genotype 6 (9.5%) (P<0.001). The presence of cirrhosis was 17.6% in Asians. Disaggregated Asian data showed that CHC was highest among Vietnamese and Cambodian and that genotype 6 was predominant among these 2 subgroups. CONCLUSIONS The prevalence of chronic HCV was significantly lower in Asians compared with other ethnicities. However, disaggregated data among Asians showed the highest prevalence rates among adults from Vietnam and Cambodia.
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Affiliation(s)
| | - Amandeep Sahota
- Gastroenterology, Kaiser Permanente Los Angeles Medical Center
| | - Su-Jau Yang
- Department of Research and Evaluation, Southern California Kaiser Permanente, Pasadena, CA
| | - Ronald Balbuena
- Department of Research and Evaluation, Southern California Kaiser Permanente, Pasadena, CA
| | - Mimi Chang
- Asian Pacific Liver Center, St. Vincent Medical Center
| | - Carolina Lim
- Asian Pacific Liver Center, St. Vincent Medical Center
| | - Tse-Ling Fong
- Asian Pacific Liver Center, St. Vincent Medical Center
- Division of Gastrointestinal and Liver Diseases, Keck School of Medicine at University of Southern California, Los Angeles
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Li J, Armon C, Palella FJ, Tedaldi E, Novak RM, Fuhrer J, Simoncini G, Carlson K, Buchacz K. Hepatitis C Virus Testing Among Men With Human Immunodeficiency Virus Who Have Sex With Men: Temporal Trends and Racial/Ethnic Disparities. Open Forum Infect Dis 2021; 8:ofaa645. [PMID: 33889655 DOI: 10.1093/ofid/ofaa645] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/21/2020] [Accepted: 01/15/2021] [Indexed: 12/19/2022] Open
Abstract
Background National guidelines recommend that sexually active people with human immunodeficiency virus (PWH) who are men who have sex with men (MSM) be tested for hepatitis C virus (HCV) infection at least annually. Hepatitis C virus testing rates vary by race/ethnicity in the general population, but limited data are available for PWH. Methods We analyzed medical records data from MSM in the HIV Outpatient Study at 9 human immunodeficiency virus (HIV) clinics from January 1, 2011 through December 31, 2019. We excluded observation time after documented past or current HCV infection. We evaluated HCV antibody testing in each calendar year among HCV-seronegative MSM, and we assessed testing correlates by generalized estimating equation analyses. Results Of 1829 eligible MSM who were PWH, 1174 (64.2%) were non-Hispanic/Latino white (NHW), 402 (22.0%) non-Hispanic black (NHB), 187 (10.2%) Hispanic/Latino, and 66 (3.6%) of other race/ethnicity. Most were ≥40 years old (68.9%), privately insured (64.5%), with CD4 cell count/mm3 (CD4) ≥350 (77.0%), and with HIV viral load <200 copies/mL (76.9%). During 2011-2019, 1205 (65.9%) had ≥1 HCV antibody test and average annual HCV percentage tested was 30.3% (from 33.8% for NHB to 28.5% for NHW; P < .001). Multivariable factors positively associated (P < .05) with HCV testing included more recent HIV diagnosis, public insurance, lower CD4, prior chlamydia, gonorrhea, syphilis, or hepatitis B virus diagnoses, and elevated liver enzyme levels, but not race/ethnicity. Conclusions Although we found no disparities by race/ethnicity in HCV testing, low overall HCV testing rates indicate suboptimal uptake of recommended HCV testing among MSM in HIV care.
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Affiliation(s)
- Jun Li
- Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
| | - Carl Armon
- Cerner Corporation, Kansas City, Missouri, USA
| | - Frank J Palella
- Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA
| | - Ellen Tedaldi
- Lewis Katz School of Medicine at Temple University, Philadelphia, Pennsylvania, USA
| | - Richard M Novak
- University of Illinois College of Medicine, Chicago, Illinois, USA
| | - Jack Fuhrer
- Renaissance School of Medicine at Stony Brook University, Stony Brook, New York, USA
| | - Gina Simoncini
- Lewis Katz School of Medicine at Temple University, Philadelphia, Pennsylvania, USA
| | | | - Kate Buchacz
- Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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7
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Womack JA, Murphy TE, Bathulapalli H, Smith A, Bates J, Jarad S, Redeker NS, Luther SL, Gill TM, Brandt CA, Justice AC. Serious Falls in Middle-Aged Veterans: Development and Validation of a Predictive Risk Model. J Am Geriatr Soc 2020; 68:2847-2854. [PMID: 32860222 DOI: 10.1111/jgs.16773] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2020] [Revised: 07/13/2020] [Accepted: 07/14/2020] [Indexed: 12/27/2022]
Abstract
BACKGROUND/OBJECTIVES Due to high rates of multimorbidity, polypharmacy, and hazardous alcohol and opioid use, middle-aged Veterans are at risk for serious falls (those prompting a visit with a healthcare provider), posing significant risk to their forthcoming geriatric health and quality of life. We developed and validated a predictive model of the 6-month risk of serious falls among middle-aged Veterans. DESIGN Cohort study. SETTING Veterans Health Administration (VA). PARTICIPANTS Veterans, aged 45 to 65 years, who presented for care within the VA between 2012 and 2015 (N = 275,940). EXPOSURES The exposures of primary interest were substance use (including alcohol and prescription opioid use), multimorbidity, and polypharmacy. Hazardous alcohol use was defined as an Alcohol Use Disorders Identification Test - Consumption (AUDIT-C) score of 3 or greater for women and 4 or greater for men. We used International Classification of Diseases, Ninth Revision (ICD-9), codes to identify alcohol and illicit substance use disorders and identified prescription opioid use from pharmacy fill-refill data. We included counts of chronic medications and of physical and mental health comorbidities. MEASUREMENTS We identified serious falls using external cause of injury codes and a machine-learning algorithm that identified serious falls in radiology reports. We used multivariable logistic regression with general estimating equations to calculate risk. We used an integrated predictiveness curve to identify intervention thresholds. RESULTS Most of our sample (54%) was aged 60 years or younger. Duration of follow-up was up to 4 years. Veterans who fell were more likely to be female (11% vs 7%) and White (72% vs 68%). They experienced 43,641 serious falls during follow-up. We identified 16 key predictors of serious falls and five interaction terms. Model performance was enhanced by addition of opioid use, as evidenced by overall category-free net reclassification improvement of 0.32 (P < .001). Discrimination (C-statistic = 0.76) and calibration were excellent for both development and validation data sets. CONCLUSION We developed and internally validated a model to predict 6-month risk of serious falls among middle-aged Veterans with excellent discrimination and calibration.
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Affiliation(s)
- Julie A Womack
- VA Connecticut Healthcare System, West Haven.,Yale School of Nursing, Orange, Connecticut
| | - Terrence E Murphy
- Geriatrics Section, Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
| | - Harini Bathulapalli
- VA Connecticut Healthcare System, West Haven.,Yale Center for Analytic Services, Yale School of Medicine, New Haven, Connecticut
| | | | - Jonathan Bates
- VA Connecticut Healthcare System, West Haven.,Yale Center for Medical Informatics, Yale School of Medicine, New Haven, Connecticut
| | - Samah Jarad
- Yale Center for Medical Informatics, Yale School of Medicine, New Haven, Connecticut
| | | | - Stephen L Luther
- James A. Haley Veterans Hospital, Research Service, Tampa, Florida.,University of South Florida, College of Public Health, Tampa, Florida
| | - Thomas M Gill
- Geriatrics Section, Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
| | - Cynthia A Brandt
- VA Connecticut Healthcare System, West Haven.,Yale Center for Medical Informatics, Yale School of Medicine, New Haven, Connecticut
| | - Amy C Justice
- VA Connecticut Healthcare System, West Haven.,Department of Internal Medicine, Yale School of Medicine, New Haven, Connecticut
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8
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Do A, Esserman DA, Krishnan S, Lim JK, Taddei TH, Hauser RG, Tate JP, Re VL, Justice AC. Excess Weight Gain After Cure of Hepatitis C Infection with Direct-Acting Antivirals. J Gen Intern Med 2020; 35:2025-2034. [PMID: 32342483 PMCID: PMC7352003 DOI: 10.1007/s11606-020-05782-6] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/30/2019] [Accepted: 03/06/2020] [Indexed: 12/18/2022]
Abstract
BACKGROUND Cure from chronic hepatitis C virus (HCV) infection is readily achievable with direct-acting antivirals (DAA), but little is known about optimal management after treatment. Weight gained after DAA treatment may mitigate benefits or increase risk for liver disease progression. As the single largest sample of HCV-infected individuals receiving DAA treatment in the United States, the Veterans Affairs (VA) Birth Cohort is an ideal setting to assess weight gain after DAA treatment. METHODS We performed a prospective study of patients dispensed DAA therapy from January 2014 to June 2015. Weight change was calculated as the difference in weight from sustained virologic response (SVR) determination to 2 years later. Demographic, weight, height, prescription, laboratory, and diagnosis code data were used for covariate definitions. We used multiple logistic regression to assess the association between candidate predictors and excess weight gain (≥ 10 lbs) after 2 years. RESULTS Among 11,469 patients, 78.0% of patients were already overweight or obese at treatment initiation. Overall, SVR was achieved in 97.0% of patients. After 2 years, 52.6% of patients gained weight and 19.8% gained excess weight. In those with SVR, weight gain was as high as 38.2 lbs, with the top 10% gaining ≥ 16.5 lbs. Only 1% of those with obesity at treatment initiation normalized their weight class after 2 years. Significant predictors of post-SVR weight gain were SVR achievement, lower age, high FIB-4 score, cirrhosis, and weight class at treatment initiation. CONCLUSION Weight gain is common after DAA treatment, even among those who are overweight or obese prior to treatment. Major predictors include age, baseline weight, alcohol, cirrhosis, and SVR. Everyone receiving DAAs should be counseled against weight gain with a particular emphasis among those at higher risk.
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Affiliation(s)
- Albert Do
- Section of Digestive Diseases, Department of Internal Medicine , Yale University School of Medicine, 333 Cedar St, 1080 LMP, New Haven, CT, 06510, USA.
| | - Denise A Esserman
- Department of Biostatistics, Yale University School of Public Health, New Haven, CT, USA
| | - Supriya Krishnan
- Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, USA
- VA Connecticut Healthcare System, West Haven, CT, USA
| | - Joseph K Lim
- Section of Digestive Diseases, Department of Internal Medicine , Yale University School of Medicine, 333 Cedar St, 1080 LMP, New Haven, CT, 06510, USA
- VA Connecticut Healthcare System, West Haven, CT, USA
| | - Tamar H Taddei
- Section of Digestive Diseases, Department of Internal Medicine , Yale University School of Medicine, 333 Cedar St, 1080 LMP, New Haven, CT, 06510, USA
- VA Connecticut Healthcare System, West Haven, CT, USA
| | - Ronald G Hauser
- VA Connecticut Healthcare System, West Haven, CT, USA
- Department of Laboratory Medicine, Yale University School of Medicine, New Haven, USA
| | - Janet P Tate
- Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, USA
- VA Connecticut Healthcare System, West Haven, CT, USA
| | - Vincent Lo Re
- Division of Infectious Diseases, Department of Medicine, Perelman School of Medicine, University of Pennsylvania University of Pennsylvania, Philadelphia, PA, USA
- Center for Clinical Epidemiology and Biostatistics, Department of Biostatistics, Epidemiology, and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
| | - Amy C Justice
- Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, USA
- VA Connecticut Healthcare System, West Haven, CT, USA
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9
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Rentsch CT, Kidwai-Khan F, Tate JP, Park LS, King JT, Skanderson M, Hauser RG, Schultze A, Jarvis CI, Holodniy M, Re VL, Akgün KM, Crothers K, Taddei TH, Freiberg MS, Justice AC. Covid-19 Testing, Hospital Admission, and Intensive Care Among 2,026,227 United States Veterans Aged 54-75 Years. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2020:2020.04.09.20059964. [PMID: 32511595 PMCID: PMC7276022 DOI: 10.1101/2020.04.09.20059964] [Citation(s) in RCA: 303] [Impact Index Per Article: 60.6] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 04/12/2023]
Abstract
IMPORTANCE Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection causes coronavirus disease 2019 (Covid-19), an evolving pandemic. Limited data are available characterizing SARS-Cov-2 infection in the United States. OBJECTIVE To determine associations between demographic and clinical factors and testing positive for coronavirus 2019 (Covid-19+), and among Covid-19+ subsequent hospitalization and intensive care. DESIGN, SETTING, AND PARTICIPANTS Retrospective cohort study including all patients tested for Covid-19 between February 8 and March 30, 2020, inclusive. We extracted electronic health record data from the national Veterans Affairs Healthcare System, the largest integrated healthcare system in the United States, on 2,026,227 patients born between 1945 and 1965 and active in care. Exposures: Demographic data, comorbidities, medication history, substance use, vital signs, and laboratory measures. Laboratory tests were analyzed first individually and then grouped into a validated summary measure of physiologic injury (VACS Index). Main Outcomes and Measures: We evaluated which factors were associated with Covid-19+ among all who tested. Among Covid-19+ we identified factors associated with hospitalization or intensive care. We identified independent associations using multivariable and conditional multivariable logistic regression with multiple imputation of missing values. RESULTS Among Veterans aged 54-75 years, 585/3,789 (15.4%) tested Covid-19+. In adjusted analysis (C-statistic=0.806) black race was associated with Covid-19+ (OR 4.68, 95% CI 3.79-5.78) and the association remained in analyses conditional on site (OR 2.56, 95% CI 1.89-3.46). In adjusted models, laboratory abnormalities (especially fibrosis-4 score [FIB-4] >3.25 OR 8.73, 95% CI 4.11-18.56), and VACS Index (per 5-point increase OR 1.62, 95% CI 1.43-1.84) were strongly associated with hospitalization. Associations were similar for intensive care. Although significant in unadjusted analyses, associations with comorbid conditions and medications were substantially reduced and, in most cases, no longer significant after adjustment. CONCLUSIONS AND RELEVANCE Black race was strongly associated with Covid-19+, but not with hospitalization or intensive care. Among Covid-19+, risk of hospitalization and intensive care may be better characterized by laboratory measures and vital signs than by comorbid conditions or prior medication exposure.
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Affiliation(s)
- Christopher T Rentsch
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, UK, WC1E 7HT
| | - Farah Kidwai-Khan
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Internal Medicine, Yale School of Medicine, New Haven, CT, US, 06520
| | - Janet P Tate
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Internal Medicine, Yale School of Medicine, New Haven, CT, US, 06520
| | - Lesley S Park
- Stanford Center for Population Health Sciences, Stanford University School of Medicine, Stanford, CA, US, 94305
| | - Joseph T King
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Neurosurgery, Yale School of Medicine, New Haven, CT, US, 06520
| | - Melissa Skanderson
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
| | - Ronald G Hauser
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Laboratory Medicine, Yale School of Medicine, New Haven, CT, US, 06520
| | - Anna Schultze
- Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, UK, WC1E 7HT
| | - Christopher I Jarvis
- Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, UK, WC1E 7HT
| | - Mark Holodniy
- VA Palo Alto Healthcare System, US Department of Veterans Affairs, Palo Alto, CA, US, 94304
- Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine, Stanford, CA, US, 94305
| | - Vincent Lo Re
- Division of Infectious Diseases, Department of Medicine and Center for Clinical Epidemiology and Biostatistics, Department of Biostatistics, Epidemiology, and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, US, 19104
| | - Kathleen M Akgün
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Internal Medicine, Yale School of Medicine, New Haven, CT, US, 06520
| | - Kristina Crothers
- VA Puget Sound Health Care System and Department of Medicine, University of Washington School of Medicine, Seattle, WA, US, 98104
| | - Tamar H Taddei
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Internal Medicine, Yale School of Medicine, New Haven, CT, US, 06520
| | - Matthew S Freiberg
- Geriatric Research Education and Clinical Center (GRECC), US Department of Veterans Affairs, Tennessee Valley Health Care System, Nashville, TN, US 37212
- Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, US, 37232
| | - Amy C Justice
- VA Connecticut Healthcare System, US Department of Veterans Affairs, West Haven, CT, US, 06516
- Department of Internal Medicine, Yale School of Medicine, New Haven, CT, US, 06520
- Center for Interdisciplinary Research on AIDS, Yale School of Public Health, New Haven, CT, US, 06511
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10
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Tsay CJ, Lim JK. Assessing the Effectiveness of Strategies in US Birth Cohort Screening for Hepatitis C Infection. J Clin Transl Hepatol 2020; 8:25-41. [PMID: 32274343 PMCID: PMC7132023 DOI: 10.14218/jcth.2019.00059] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/18/2019] [Revised: 02/04/2020] [Accepted: 02/25/2020] [Indexed: 12/15/2022] Open
Abstract
Chronic hepatitis C infection in the USA is a highly morbid condition and current guidelines recommend one-time screening among the birth cohort (1945-1965). Understanding strategies to optimize screening can help inform future hepatitis C virus (HCV) screening guidelines. A focused literature search was performed using PubMed and manual abstract review from major hepatology conferences over the past 2 years. The search strategy involved using Medical Subject Headings terms for hepatitis C, screening, birth cohort, baby boomers, and 1945-1965. The review was limited to data from the USA. A total of 327 articles were identified and 36 abstracts were included, with studies published between 2012-2019. Strategies including clinician education, electronic medical record alerts, reflex HCV RNA testing, point-of-care testing, multisite (outpatient, inpatient, emergency department, endoscopy suite) initiatives, direct patient solicitation, and utilization of non-physician providers have increased HCV screening rates. However, broad implementation remains less than optimal. Barriers include lack of patient acceptance to screening and engagement in the HCV care cascade. The Veterans Affairs Healthcare System has achieved higher birth cohort screening rates through an integrated approach requiring high-level engagement by leadership and institutional commitment. Multiple strategies for increasing birth cohort screening have been successful, but overall rates of HCV screening remain low. These strategies can inform public health efforts to implement emerging national recommendations for expansion of HCV screening to all U.S. adults age 18 or older.
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Affiliation(s)
- Cynthia J. Tsay
- Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, USA
| | - Joseph K. Lim
- Yale Liver Center, Section of Digestive Diseases, Yale University School of Medicine, New Haven, CT, USA
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11
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Hojat L, Avery A, Greco PJ, Kaelber DC. Doubling Hepatitis C Virus Screening in Primary Care Using Advanced Electronic Health Record Tools-A Non-Randomized Controlled Trial. J Gen Intern Med 2020; 35:498-504. [PMID: 31792863 PMCID: PMC7018893 DOI: 10.1007/s11606-019-05536-z] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/17/2019] [Revised: 07/26/2019] [Accepted: 10/11/2019] [Indexed: 12/09/2022]
Abstract
BACKGROUND Hepatitis C virus (HCV) infection is a major public health burden, affecting over 4 million people. The Centers for Disease Control and Prevention and the US Preventive Services Task Force guidelines recommend screening everyone born between 1945 and 1965, but screening rates remain low. OBJECTIVE To determine whether bulk ordering and electronic messaging to patients improves guideline-based HCV screening rates. DESIGN A non-randomized controlled trial of 1024 adults from November 2016 to March 2017. PARTICIPANTS Patients due for HCV screening with at least one primary care office visit in one of three primary care clinics and enrolled in the healthcare system's tethered personal health record (tPHR). INTERVENTIONS Control patients received normal care for HCV screening, consisting of passive HCV reminders to providers during face-to-face visits and passive HCV screening notification through the patient's tPHR. Intervention patients received normal care and also had HCV antibody tests ordered for them and customized messages sent through their tPHR inviting them to go directly to the lab for HCV screening over a 12-week period. MAIN MEASURES Percentage/number of patients receiving HCV antibody tests during the intervention period. Percentage/number of intervention group patients receiving HCV screening with other blood work. KEY RESULTS In the intervention group, 33% (168 of 514) completed HCV testing, compared with 19% (97 of 510) of controls (OR 1.7, 95% CI 1.2-2.1). Bulk lab ordering appeared to have a large impact while bulk messaging appeared to have a less significant role. CONCLUSIONS Leveraging population analytics and bulk ordering in an electronic health record with bulk messaging to a tPHR directly engages patients in blood screening tests and can significantly improve completion. This methodology has a broad range of applications including many recommended screening or disease-specific testing. This bulk ordering and direct-to-patient messaging approach improves patient screening while decreasing provider/staff work. TRIAL REGISTRATION MetroHealth IRB16-00776 (ClinicalTrials.gov).
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Affiliation(s)
- Leila Hojat
- Division of Infectious Diseases and HIV Medicine, University Hospitals Cleveland Medical Center, Case Western Reserve University, Cleveland, OH, USA.,Department of Medicine, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA
| | - Ann Avery
- Department of Medicine, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA
| | - Peter J Greco
- Department of Medicine, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA.,Center for Clinical Informatics Research and Education, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA
| | - David C Kaelber
- Department of Medicine, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA. .,Center for Clinical Informatics Research and Education, The MetroHealth System, Case Western Reserve University, Cleveland, OH, USA. .,Department of Pediatrics and Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, OH, USA.
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12
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Jain MK, Rich NE, Ahn C, Turner BJ, Sanders JM, Adamson B, Quirk L, Perryman P, Santini NO, Singal AG. Evaluation of a Multifaceted Intervention to Reduce Health Disparities in Hepatitis C Screening: A Pre-Post Analysis. Hepatology 2019; 70:40-50. [PMID: 30950085 DOI: 10.1002/hep.30638] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/18/2019] [Accepted: 03/25/2019] [Indexed: 12/30/2022]
Abstract
Hepatitis C virus (HCV) testing in persons born from 1945 to 1965 has had limited adoption despite guidelines, particularly among racial/ethnic minorities and socioeconomically disadvantaged patients, who have a higher prevalence of disease burden. We examined the effectiveness of a multifaceted intervention to improve HCV screening in a large safety-net health system. We performed a multifaceted intervention that included provider and patient education, an electronic medical record-enabled best practice alert, and increased HCV treatment capacity. We characterized HCV screening completion before and after the intervention. To identify correlates of HCV screening, we performed logistic regression for the preintervention and postintervention groups and used a generalized linear mixed model for patients observed in both preintervention and postintervention time frames. Before the intervention, 10.1% of 48,755 eligible baby boomer patients were screened. After the intervention, 34.6% of the 34,093 eligible baby boomers were screened (P < 0.0001). Prior to the intervention, HCV screening was lower among older baby boomers and providers with large patient panels and higher in high-risk subgroups including those with signs of liver disease (e.g., elevated transaminases, thrombocytopenia), human immunodeficiency virus-positive patients, and homeless patients. Postintervention, we observed increased screening uptake in older baby boomers, providers with larger patient panel size, and patients with more than one prior primary care appointment. Conclusion: Our multifaceted intervention significantly increased HCV screening, particularly among older patients, those engaged in primary care, and providers with large patient panels.
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Affiliation(s)
- Mamta K Jain
- Department of Internal Medicine, UT Southwestern Medical Center, Dallas, TX.,Parkland Health & Hospital System, Dallas, TX
| | - Nicole E Rich
- Department of Internal Medicine, UT Southwestern Medical Center, Dallas, TX.,Parkland Health & Hospital System, Dallas, TX
| | - Chul Ahn
- Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
| | - Barbara J Turner
- Department of Internal Medicine, UT Health Science Center, San Antonio, TX
| | - Joanne M Sanders
- Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
| | - Brian Adamson
- Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
| | - Lisa Quirk
- Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
| | - Patrice Perryman
- Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
| | - Noel O Santini
- Department of Internal Medicine, UT Southwestern Medical Center, Dallas, TX.,Parkland Health & Hospital System, Dallas, TX
| | - Amit G Singal
- Department of Internal Medicine, UT Southwestern Medical Center, Dallas, TX.,Parkland Health & Hospital System, Dallas, TX.,Department of Clinical Sciences, UT Southwestern Medical Center, Dallas, TX
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13
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Njei B, Esserman D, Krishnan S, Ohl M, Tate JP, Hauser G, Taddei T, Lim J. Regional and Rural-Urban Differences in the Use of Direct-acting Antiviral Agents for Hepatitis C Virus: The Veteran Birth Cohort. Med Care 2019; 57:279-285. [PMID: 30807449 PMCID: PMC6436819 DOI: 10.1097/mlr.0000000000001071] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/23/2023]
Abstract
BACKGROUND Veterans with hepatitis C virus (HCV) infection may face geographic obstacles to obtaining treatment. OBJECTIVE We studied the influence of region and rural versus urban residence on receipt of direct-acting antiretroviral (DAA) medications for HCV. SUBJECTS Veterans receiving care within Veterans Affairs Healthcare System born between 1945 and 1965. RESEARCH DESIGN This is a observational study using national electronic health record data. MEASURES Receipt of DAAs was defined as ≥1 filled prescription from January 1, 2014 to December 31, 2016. Region (South, Northeast, Midwest, and West) and residence (urban, rural-micropolitan, small rural towns, and isolated rural towns) variables were created using residential zone improvement plan codes and rural-urban commuting area (RUCA) codes. Multivariable models were adjusted for age, race, sex, severity of liver disease, comorbidities, and prior treatment experience. RESULTS Among 166,353 eligible patients 64,854 received, DAAs. Variation by rural-urban residence depended on region. In unadjusted analyses, receipt varied by rural-urban designations within Midwest, and West regions (P<0.05) but did not vary within the South (P=0.12). Southern rural small town had the lowest incidence of DAA receipt (40.1%), whereas the incidence was 52.9% in Midwestern isolated rural towns. In adjusted logistic analyses, compared with southern urban residents (the largest single group), southern rural small town residents had the lowest odds ratio, 0.85 (95% confidence interval, 0.75-0.93), and Midwestern residents from isolated and small rural towns had the highest odds (odds ratio, both 1.27) to receive treatment. CONCLUSIONS Substantial geographic variation exists in receipt of curative HCV treatment. Efforts are needed to provide more equitable access to DAAs.
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Affiliation(s)
- Basile Njei
- Department of Gastroenterology and Hepatology, Yale University School of Medicine, VA Connecticut Healthcare System, 333 Cedar Street, New Haven, CT, 06516, (312) 415-7525,
| | - Denise Esserman
- Department of Biostatistics, Yale University School of Public Health, VA Connecticut Healthcare System, 300 George Street, New Haven, CT 06510-3210, (203)785-4297,
| | - Supriya Krishnan
- Department of Internal Medicine, Yale University School of Medicine, VA Connecticut Healthcare System, 950 Campbell Avenue, West Haven, CT, 06516, (203) 932-5711 ×5306,
| | - Michael Ohl
- University of Iowa Carver College of Medicine, Veterans Rural Health Resource Iowa City VA Medical Center, 601 Highway 6 West Iowa City, IA, 52246, (319)338-0581 ext. 3534,
| | - Janet P. Tate
- Department of Internal Medicine, Yale University School of Medicine, VA Connecticut Healthcare System, 950 Campbell Avenue, West Haven, CT,06516, (203) 932-5711 ×5371,
| | - George Hauser
- Center for Biomedical Data Science, Yale University School of Medicine, VA Connecticut Healthcare System, 950 Campbell Avenue, West Haven, CT, 06516 (203)932-5711 ×7140,
| | - Tamar Taddei
- Section of Digestive Diseases, Department of Internal Medicine, Yale University School of Medicine, VA Connecticut Healthcare System, 950 Campbell Ave., West Haven, CT, 06516, (203) 932-5711 ×4696,
| | - Joseph Lim
- Department of Internal Medicine Yale University School of Medicine, VA Connecticut Healthcare System, 333 Cedar Street, New Haven CT, 06510, New Haven CT, (203)737-6063,
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14
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Baumert TF, Berg T, Lim JK, Nelson DR. Status of Direct-Acting Antiviral Therapy for Hepatitis C Virus Infection and Remaining Challenges. Gastroenterology 2019; 156:431-445. [PMID: 30342035 PMCID: PMC6446912 DOI: 10.1053/j.gastro.2018.10.024] [Citation(s) in RCA: 141] [Impact Index Per Article: 23.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/26/2018] [Revised: 10/05/2018] [Accepted: 10/08/2018] [Indexed: 12/12/2022]
Abstract
Chronic infection with hepatitis C virus is a major cause of liver disease and hepatocellular carcinoma worldwide. After the discovery of hepatitis C virus 3 decades ago, the identification of the structure of the viral proteins, combined with high-throughput replicon models, enabled the discovery and development of direct-acting antivirals. These agents have revolutionized patient care, with cure rates of more than 90%. We review the status of direct-acting antiviral therapies for hepatitis C virus infection and discuss remaining challenges. We highlight licensed compounds, discuss the potential to shorten therapy even further, and review different options for treatment failure and resistance. We also provide an overview of clinical experience with generic agents and evidence for their efficacy. Finally, we discuss the need for new drugs and outline promising targets for future therapies.
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Affiliation(s)
- Thomas F Baumert
- INSERM, U1110, Institut de Recherche sur les Maladies Virales et Hépatiques, Strasbourg, France; Université de Strasbourg, Strasbourg, France; Pôle Hépato-digestif, Institut Hospitalo-Universitaire, Nouvel Hôpital Civil, Strasbourg, France.
| | - Thomas Berg
- Section of Hepatology, Clinic for Gastroenterology and Rheumatology, University Clinic Leipzig, Leipzig, Germany
| | - Joseph K Lim
- Section of Digestive Diseases and Yale Liver Center, Yale University School of Medicine, New Haven, Connecticut
| | - David R Nelson
- Department of Medicine, University of Florida, Gainesville, Florida.
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15
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Wray D, Coppin JD, Scott D, Jacob DA, Jinadatha C. Increased HCV Screening Yields Discordant Gains in Diagnoses Among Urban and Rural Veteran Populations in Texas: Results of a Statewide Quality Improvement Initiative. Jt Comm J Qual Patient Saf 2018; 45:112-122. [PMID: 30266248 DOI: 10.1016/j.jcjq.2018.06.005] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/12/2018] [Revised: 06/21/2018] [Accepted: 06/28/2018] [Indexed: 11/25/2022]
Abstract
BACKGROUND Chronic hepatitis C virus (HCV) infection is a significant health burden among military veterans. Our goals were to increase monthly HCV screenings, diagnoses, and sustained virologic responses (SVR) among 88,652 unscreened birth cohort Veterans in Texas. METHODS The interventions were enabled within six of the eight healthcare systems (HCSs) that compose Veteran's Integrated Service Network 17. The remaining two HCSs served as controls. The HCSs were separated into two groups: urban and rural; each composed of a control and three interventional HCSs. Decision support programming was embedded within the Computerized Patient Record System that prompted HCV screening among previously unscreened birth cohort patients. Clinical process design and educational efforts were enacted to enhance treatment capacity. RESULTS Monthly screenings increased 4.89 times (p < 0.001) and 2.97 times (p < 0.001) during the postinterventional period relative to control for urban and rural HCSs, respectively. For urban HCSs, diagnoses increased 1.58 (p < 0.001) times more than the control group during the postinterventional period, but there was no difference in number of diagnoses in the rural HCSs (p = 0.86). Monthly SVR increased 2.69 times more than the control group during the postinterventional period (p < 0.001). CONCLUSION Decision support improved HCV screening among birth cohort patients in both urban and rural HCSs. Increased screening boosted the monthly number of diagnoses in the urban HCSs, but not in the rural HCSs; which rebuts the utility of birth cohort screening among rurally residing veterans. These interventions significantly improved the rate of SVR achievement relative to control.
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Barocas JA, Wang J, White LF, Tasillo A, Salomon JA, Freedberg KA, Linas BP. Hepatitis C Testing Increased Among Baby Boomers Following The 2012 Change To CDC Testing Recommendations. Health Aff (Millwood) 2018; 36:2142-2150. [PMID: 29200354 DOI: 10.1377/hlthaff.2017.0684] [Citation(s) in RCA: 31] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Abstract
In 2012 the Centers for Disease Control and Prevention recommended routine testing for hepatitis C for people born in the period 1945-65. Until now, the recommendation's impact on hepatitis C screening rates in the United States has not been fully understood. We used an interrupted time series with comparison group design to analyze hepatitis C screening rates in the period 2010-14 among 2.8 million commercially insured adults in the MarketScan database. Hepatitis C screening rates increased yearly between 2010 and 2014, from 1.65 to 2.59 per 100 person-years. A 49 percent increase in screening rates among people born during 1945-65 followed the release of the recommendation, but no such increase was observed among adults born after 1965. The effect among the target population was sustained, and by twenty-four months after the recommendation's release, screening rates had increased 106 percent. We conclude that the hepatitis C testing policy change resulted in significantly increased testing among the target population and may have decreased the magnitude of the hepatitis C epidemic.
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Affiliation(s)
- Joshua A Barocas
- Joshua A. Barocas ( ) is an assistant in medicine in the Division of Infectious Diseases at Massachusetts General Hospital and an instructor in medicine at Harvard Medical School, both in Boston
| | - Jianing Wang
- Jianing Wang is a statistical analyst in the Division of Infectious Diseases at Boston Medical Center, in Massachusetts
| | - Laura F White
- Laura F. White is a senior biostatistician at the Boston University School of Public Health, in Massachusetts
| | - Abriana Tasillo
- Abriana Tasillo is a research assistant in the Division of Infectious Diseases at Boston Medical Center
| | - Joshua A Salomon
- Joshua A. Salomon is a professor of medicine at Stanford University, in California
| | - Kenneth A Freedberg
- Kenneth A. Freedberg is a professor of medicine in the Divisions of General Internal Medicine and Infectious Diseases and director of the HIV Research Program, Medical Practice Evaluation Center, at Massachusetts General Hospital, and a professor in the Department of Health Policy and Management at the Harvard T. H. Chan School of Public Health, in Boston
| | - Benjamin P Linas
- Benjamin P. Linas is an associate professor of medicine in the Division of Infectious Diseases at Boston Medical Center and an associate professor of epidemiology at the Boston University School of Public Health
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Yeboah-Korang A, Beig MI, Khan MQ, Goldstein JL, Macapinlac DM, Maurer D, Sonnenberg A, Fimmel CJ. Hepatitis C Screening in Commercially Insured U.S. Birth-cohort Patients: Factors Associated with Testing and Effect of an EMR-based Screening Alert. J Transl Int Med 2018; 6:82-89. [PMID: 29984203 PMCID: PMC6032190 DOI: 10.2478/jtim-2018-0012] [Citation(s) in RCA: 24] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/25/2023] Open
Abstract
BACKGROUND AND OBJECTIVES Hepatitis C virus (HCV) testing rates among U.S. birth-cohort patients have been studied extensively, limited data exists to differentiate birth-cohort screening from risk- or liver disease-based testing. This study aims to identify factors associated with HCV antibody (HCV-Ab) testing in a group of insured birth cohort patients, to determine true birth cohort testing rates, and to determine whether an electronic medical record (EMR)-driven Best Practice Alert (BPA) would improve birth cohort testing rates. METHODS All birth-cohort outpatients between 2010 and 2015 were identified. HCV-Ab test results, clinical, and demographic variables were extracted from the EMR, and factors associated with testing were analyzed by logistic regression. True birth-cohort HCV screening rates were determined by detailed chart review for all outpatient visits during one calendar month. An automated Best Practice Alert was used to identify unscreened patients at the point of care, and to prompt HCV testing. Screening rates before and after system-wide implementation of the BPA were compared. RESULTS The historic HCV-Ab testing rate was 11.2% (11,976/106,753). Younger age, female gender, and African American, Asian, or Hispanic ethnicity, and medical comorbidities such as chronic hemodialysis, HIV infection, and rheumatologic and psychiatric comorbidities were associated with higher testing rates. However, during the one-month sampling period, true age cohort-based testing was performed in only 69/10,089 patients (0.68%). Following the system-wide implementation of the HCV BPA, testing rates increased from 0.68% to 10.76% (P<0.0001). CONCLUSIONS We documented low HCV-Ab testing rates in our baby boomers population. HCV testing was typically performed in the presence of known risk factors or established liver disease. The implementation of an EMR-based HCV BPA resulted in a marked increase in testing rates. Our study highlights current HCV screening gaps, and the utility of the EMR to improve screening rates and population health.
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Affiliation(s)
| | | | | | | | | | | | - Amnon Sonnenberg
- Portland VA Medical Center and Oregon Health & Science University, Portland, OR, USA
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18
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Lim JK. Expanding Capacity to Treat Hepatitis C: Overcoming Barriers and New Innovations. CURRENT HEPATOLOGY REPORTS 2018; 17:83-87. [DOI: 10.1007/s11901-018-0400-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/15/2025]
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19
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Samuel ST, Martinez AD, Chen Y, Markatou M, Talal AH. Hepatitis C virus knowledge improves hepatitis C virus screening practices among primary care physicians. World J Hepatol 2018; 10:319-328. [PMID: 29527267 PMCID: PMC5838450 DOI: 10.4254/wjh.v10.i2.319] [Citation(s) in RCA: 17] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/01/2018] [Revised: 01/17/2018] [Accepted: 02/03/2018] [Indexed: 02/06/2023] Open
Abstract
AIM To understand the role of knowledge as a promoter of hepatitis C virus (HCV) screening among primary care physicians (PCP). METHODS A 45-item online questionnaire assessing knowledge of HCV natural history, risk factors, and treatment was distributed to 163 PCP. Logistic regression, adjusted for survey responses, assessed associations between PCP knowledge of HCV natural history and treatment and birth cohort (i.e., birth between 1945 and 1965) screening. Response stratification and weighting were used to account for nonresponse and to permit extension of responses to the entire survey population. Associations between various predictors including demographic characteristics, level of training, and HCV treatment experience and HCV knowledge were assessed. RESULTS Ninety-one individuals (55.8%) responded. Abnormal liver enzymes (49.4%), assessment of HCV-related risk factors (30.6%), and birth cohort membership (20%) were the leading HCV screening indications. Most PCP (64.7%) felt that the combination of risk-factor and birth cohort screening utilizing a self-administered survey while awaiting the physician (55.3%) were the most efficient screening practices. Implementation of birth cohort screening was associated with awareness of the recommendations (P-value = 0.01), knowledge of HCV natural history (P-value < 0.01), and prior management of HCV patients (P-value < 0.01). PCP with knowledge of HCV treatment was also knowledgeable about HCV natural history (P-value < 0.01). Similarly, awareness of age-based screening recommendations was associated with HCV treatment knowledge (P-value = 0.03). CONCLUSION Comprehensive knowledge of HCV is critical to motivate HCV screening. PCP-targeted educational interventions are required to expand the HCV workforce and linkage-to-care opportunities as we seek global HCV eradication.
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Affiliation(s)
- Sandeep T Samuel
- Department of Medicine, University at Buffalo, State University of New York, Buffalo, NY 14203, United States
| | - Anthony D Martinez
- Department of Medicine, University at Buffalo, State University of New York, Buffalo, NY 14203, United States
| | - Yang Chen
- Department of Biostatistics, University at Buffalo, State University of New York, Buffalo, NY 14214, United States
| | - Marianthi Markatou
- Department of Biostatistics, University at Buffalo, State University of New York, Buffalo, NY 14214, United States
| | - Andrew H Talal
- Department of Medicine, University at Buffalo, State University of New York, Buffalo, NY 14203, United States
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20
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Justice AC, Esserman D, Sarkar S, Levin FL, Skanderson M, Lim JK. Reply to: "Hepatitis C testing in U.S. veterans born 1945-1965: An update". J Hepatol 2017; 66:239. [PMID: 27717863 DOI: 10.1016/j.jhep.2016.09.019] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/26/2016] [Accepted: 09/27/2016] [Indexed: 12/04/2022]
Affiliation(s)
- Amy C Justice
- Department of Internal Medicine, VA Connecticut Healthcare System, West Haven, CT, USA; Department of Internal Medicine, Yale University School of Medicine, New Haven, CT, USA; Department of Health Policy and Management, Yale School of Public Health, New Haven, CT, USA.
| | - Denise Esserman
- Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA
| | - Souvik Sarkar
- Section of Digestive Diseases, Yale University School of Medicine, New Haven, CT, USA; Current affiliation: Division of Gastroenterology and Hepatology, University of California, Davis, CA, USA
| | - Forrest L Levin
- Department of Internal Medicine, VA Connecticut Healthcare System, West Haven, CT, USA
| | - Melissa Skanderson
- Department of Internal Medicine, VA Connecticut Healthcare System, West Haven, CT, USA
| | - Joseph K Lim
- Department of Internal Medicine, VA Connecticut Healthcare System, West Haven, CT, USA
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21
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Ross DB, Belperio PS, Chartier M, Backus LI. Hepatitis C testing in U.S. veterans born 1945-1965: An update. J Hepatol 2017; 66:237-238. [PMID: 27720804 DOI: 10.1016/j.jhep.2016.09.018] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/15/2016] [Accepted: 09/15/2016] [Indexed: 12/04/2022]
Affiliation(s)
- David B Ross
- Department of Veterans Affairs, HIV, Hepatitis, and Public Health Pathogens Programs, Washington, DC, USA.
| | - Pamela S Belperio
- Department of Veterans Affairs, Population Health Services, Palo Alto Health Care System, Palo Alto, CA, USA
| | - Maggie Chartier
- Department of Veterans Affairs, HIV, Hepatitis, and Public Health Pathogens Programs, Washington, DC, USA
| | - Lisa I Backus
- Department of Veterans Affairs, Population Health Services, Palo Alto Health Care System, Palo Alto, CA, USA
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22
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Pawlotsky JM. The end of the hepatitis C burden: Really? Hepatology 2016; 64:1404-1407. [PMID: 27486957 DOI: 10.1002/hep.28758] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/29/2016] [Revised: 07/24/2016] [Accepted: 07/28/2016] [Indexed: 01/02/2023]
Affiliation(s)
- Jean-Michel Pawlotsky
- National Reference Center for Viral Hepatitis B, C and D, Department of Virology, Henri Mondor Hospital, University of Paris-Est, Créteil, France. .,INSERM U955, Créteil, France.
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