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Chang YP, Lee JY, Chen CY, Kao WY, Lin CL, Yang SS, Shih YL, Peng CY, Lee FJ, Tsai MC, Huang SC, Su TH, Tseng TC, Liu CJ, Chen PJ, Kao JH, Liu CH. Risk of Incident Type 2 Diabetes and Prediabetes in Patients With Direct Acting Antiviral-Induced Cure of Hepatitis C Virus Infection. Aliment Pharmacol Ther 2025; 61:1508-1518. [PMID: 39981689 DOI: 10.1111/apt.70029] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/23/2024] [Revised: 12/29/2024] [Accepted: 02/06/2025] [Indexed: 02/22/2025]
Abstract
BACKGROUND Data regarding the risk of incident type 2 diabetes (T2D) and prediabetes among patients with hepatitis C virus (HCV) achieving direct-acting antivirals (DAAs)-induced sustained virologic response (SVR12) remains limited. METHODS A total of 1079 patients, including 589 with normoglycemia and 490 with prediabetes, who underwent biannual fasting glucose and glycosylated haemoglobin (HbA1c) assessment for a median post-SVR12 follow-up of 5.5 years, were enrolled. We reported the crude (cIRs) and age-standardised incidence rates (ASIRs) of T2D and prediabetes. Factors associated with incident T2D and prediabetes were assessed using the Cox proportional hazards models. RESULTS The cIRs of T2D and prediabetes were 1.18 and 8.99 per 100 person-years of follow-up (PYFU), respectively. Additionally, the ASIRs of T2D and prediabetes were 1.09 (95% CI: 0.76-1.53) and 8.47 (95% CI: 7.23-9.90) per 100 PYFU. Prediabetes (adjusted hazard ratio [aHR]: 4.71; 95% confidence interval (CI): 2.55-8.70, p < 0.001), body mass index (BMI) per kg/m2 increase (aHR: 1.17; 95% CI: 1.09-1.26, p < 0.001) and liver stiffness measurement (LSM) per kPa increase (aHR: 1.05; 95% CI: 1.02-1.09, p = 0.001) were associated with a higher risk of incident T2D. Age per year increase (aHR: 1.02; 95% CI: 1.01-1.03, p < 0.001) was associated with a higher risk of incident prediabetes. CONCLUSION The incidence rates of T2D and prediabetes remain substantial among patients after HCV eradication. Lifestyle modification, drug therapy and regular monitoring of glycemic status are crucial for patients at risk of developing T2D and prediabetes following HCV clearance.
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Affiliation(s)
- Yu-Ping Chang
- Department of Internal Medicine, National Taiwan University Biomedical Park Hospital, Hsin-Chu, Taiwan
| | - Ji-Yuh Lee
- Department of Internal Medicine, National Taiwan University Hospital, Yunlin, Taiwan
| | - Chi-Yi Chen
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Ditmanson Medical Foundation Chiayi Christian Hospital, Chiayi, Taiwan
| | - Wei-Yu Kao
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Taipei Medical University Hospital, Taipei, Taiwan
- Graduate Institute of Metabolism and Obesity Sciences, Taipei Medical University, Taipei, Taiwan
- TMU Research Center for Digestive Medicine, Taipei Medical University, Taipei, Taiwan
- Taipei Cancer Center, Taipei Medical University, Taipei, Taiwan
| | - Chih-Lin Lin
- Department of Gastroenterology, Taipei City Hospital, Taipei, Taiwan
| | - Sheng-Shun Yang
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Taichung Veterans General Hospital, Taichung, Taiwan
- Ph.D. Program in Translational Medicine, National Chung Hsing University, Taichung, Taiwan
- Institute of Biomedical Sciences, National Chung Hsing University, Taichung, Taiwan
- Department of Post-Baccalaureate Medicine, College of Medicine, National Chung Hsing University, Taichung, Taiwan
| | - Yu-Lueng Shih
- Division of Gastroenterology, Department of Internal Medicine, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan
| | - Cheng-Yuan Peng
- Center for Digestive Medicine, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan
- School of Medicine, China Medical University, Taichung, Taiwan
| | - Fu-Jen Lee
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Fu Jen Catholic University Hospital, New Taipei City, Taiwan
| | - Ming-Chang Tsai
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, Chung Shan Medical University Hospital, Taichung, Taiwan
- School of Medicine, Chung Shan Medical University, Taichung, Taiwan
| | - Shang-Chin Huang
- Department of Internal Medicine, National Taiwan University Hospital Bei-Hu Branch, Taipei, Taiwan
| | - Tung-Hung Su
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
| | - Tai-Chung Tseng
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
- Department of Medical Research, National Taiwan University Hospital, Taipei, Taiwan
| | - Chun-Jen Liu
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
- Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Pei-Jer Chen
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
- Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Jia-Horng Kao
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
- Department of Medical Research, National Taiwan University Hospital, Taipei, Taiwan
- Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei, Taiwan
| | - Chen-Hua Liu
- Department of Internal Medicine, National Taiwan University Hospital, Yunlin, Taiwan
- Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
- Hepatitis Research Center, National Taiwan University Hospital, Taipei, Taiwan
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Goodman SH, Zahn M, Boden-Albala B, Lakon CM. Insurance Status, Comorbidity Diagnosis, and Hepatitis C Diagnosis Among Antibody-Positive Patients: A Retrospective Cohort Study. Health Serv Res Manag Epidemiol 2023; 10:23333928231175795. [PMID: 37197291 PMCID: PMC10184194 DOI: 10.1177/23333928231175795] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/19/2023] Open
Abstract
Background In California, laboratories report all hepatitis C (HCV)-positive antibody tests to the state; however, that does not accurately reflect active infection among those patients without a viral load test confirming a patient's HCV diagnosis. These public health surveillance disease incident records do not include patient details such as comorbidities or insurance status found in electronic medical records (EMRs). Objective This research seeks to understand how insurance type, insurance status, patient comorbidities, and other sociodemographic factors related to HCV diagnosis as defined by a positive viral load test among HCV antibody-positive persons from January 1, 2010 to March 1, 2020. Methods HCV antibody-positive individuals reported to the California Reportable Disease Information Exchange (CalREDIE), with a medical record number associated with the University of California, Irvine Medical Center, and an unrestricted EMR (n = 521) were extracted using manual chart review. Main Outcomes and measures HCV diagnosis as indicated in a patient's EMR in the problem list or disease registry. Results Less than a quarter of patients in this sample were diagnosed as having HCV in their EMR, with 0.4% of those diagnosed (5/116) patients with indicated HCV treatment in the medication field of their charts. After adjusting for multiple comorbidities, a multinomial logistic regression found that the relative risk ratios (RRRs) of HCV diagnosis found that patients with insurance were more likely to be diagnosed compared to those without insurance. When comparing uninsured patients to those with government insurance at the P < .05 level (RRR = 10.61 (95% confidence interval (CI): 4.14-27.22)) and those uninsured to private insurance (RRR = 6.79 (95% CI: 2.31-19.92). Conclusions These low frequencies of HCV diagnosis among the study population, particularly among the uninsured, indicate a need for increased viral load testing and linkage to care. Reflex testing on existing samples and improving HCV screening and diagnosis can help increase linkage to care and work towards eliminating this disease.
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Affiliation(s)
- Sara H. Goodman
- Department of Pediatrics – Infectious Diseases, Stanford University School of Medicine, Palo Alto, CA, USA
- Department of Health, Society, and Behavior, Program in Public Health Susan and Henry Samueli College of Health Sciences, University of California, Irvine, CA, USA
| | - Matthew Zahn
- Communicable Disease Control, Orange County Health Care Agency, Santa Ana, CA, USA
| | - Bernadette Boden-Albala
- Department of Health, Society, and Behavior, Program in Public Health Susan and Henry Samueli College of Health Sciences, University of California, Irvine, CA, USA
| | - Cynthia M. Lakon
- Department of Health, Society, and Behavior, Program in Public Health Susan and Henry Samueli College of Health Sciences, University of California, Irvine, CA, USA
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Carvalhal MMDL, Dias JLL, Gomes DL, Quaresma JAS. Hepatitis C virus eradication on glycemic control and insulin resistance. Rev Assoc Med Bras (1992) 2021; 67:1821-1824. [PMID: 34909956 DOI: 10.1590/1806-9282.20210752] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2021] [Accepted: 09/17/2021] [Indexed: 11/22/2022] Open
Abstract
OBJECTIVE To review data regarding the effects of hepatitis C virus eradication on glycemic control and insulin resistance. METHODS This is an integrative literature review, carried out in the PubMed, SciELO, and Lilacs databases. Studies published in the past five years that were fully available, written in English or Portuguese, and have addressed the effects of eradication of the hepatitis C virus on glycemic control and insulin resistance were selected. RESULTS Nine studies were selected. Among the results found, it was observed that there is no consensus on the effects of viral eradication on glycemic control and IR, as some authors show an eventual improvement in insulin resistance and glycemic control, while other studies indicate that there are no significant differences between the parameters evaluated after viral eradication. CONCLUSIONS Although there is a relationship between hepatitis C virus infection and the development of insulin resistance and type 2 diabetes mellitus and recent advances in research, it was observed that there is no consensus on improving insulin resistance and glycemic control after antiviral treatment, probably due to methodological differences between studies. However, it emphasizes the need to guide people diagnosed with hepatitis C, regarding changes in lifestyle, encouragement of multidisciplinary monitoring, and control of other risk factors.
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Jeong D, Karim ME, Wong S, Wilton J, Butt ZA, Binka M, Adu PA, Bartlett S, Pearce M, Clementi E, Yu A, Alvarez M, Samji H, Velásquez García HA, Abdia Y, Krajden M, Janjua NZ. Impact of HCV infection and ethnicity on incident type 2 diabetes: findings from a large population-based cohort in British Columbia. BMJ Open Diabetes Res Care 2021; 9:9/1/e002145. [PMID: 34099439 PMCID: PMC8186745 DOI: 10.1136/bmjdrc-2021-002145] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/22/2021] [Accepted: 05/09/2021] [Indexed: 12/15/2022] Open
Abstract
INTRODUCTION Increasing evidence indicates that chronic hepatitis C virus (HCV) infection is associated with higher risk of diabetes. Previous studies showed ethnic disparities in the disease burden of diabetes, with increased risk in Asian population. We described the incidence of type 2 diabetes related to HCV infection and assessed the concurrent impact of HCV infection and ethnicity on the risk of diabetes. RESEARCH DESIGN AND METHODS In British Columbia Hepatitis Testers Cohort, individuals were followed from HCV diagnosis to the earliest of (1) incident type 2 diabetes, (2) death or (3) end of the study (December 31, 2015). Study population included 847 021 people. Diabetes incidence rates in people with and without HCV were computed. Propensity scores (PS) analysis was used to assess the impact of HCV infection on newly acquired diabetes. PS-matched dataset included 117 184 people. We used Fine and Gray multivariable subdistributional hazards models to assess the effect of HCV and ethnicity on diabetes while adjusting for confounders and competing risks. RESULTS Diabetes incidence rates were higher among people with HCV infection than those without. The highest diabetes incidence rate was in South Asians with HCV (14.7/1000 person-years, 95% CI 12.87 to 16.78). Compared with Others, South Asians with and without HCV and East Asians with HCV had a greater risk of diabetes. In the multivariable stratified analysis, HCV infection was associated with increased diabetes risk in all subgroups: East Asians, adjusted HR (aHR) 3.07 (95% CI 2.43 to 3.88); South Asians, aHR 2.62 (95% CI 2.10 to 3.26); and Others, aHR 2.28 (95% CI 2.15 to 2.42). CONCLUSIONS In a large population-based linked administrative health data, HCV infection was associated with higher diabetes risk, with a greater relative impact in East Asians. South Asians had the highest risk of diabetes. These findings highlight the need for care and screening for HCV-related chronic diseases such as type 2 diabetes among people affected by HCV.
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Affiliation(s)
- Dahn Jeong
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Mohammad Ehsanul Karim
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Centre for Health Evaluation and Outcome Sciences, St Paul's Hospital, Vancouver, British Columbia, Canada
| | - Stanley Wong
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - James Wilton
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Zahid Ahmad Butt
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
- School of Public Health and Health Systems, University of Waterloo, Waterloo, Ontario, Canada
| | - Mawuena Binka
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Prince Asumadu Adu
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Sofia Bartlett
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
- Department of Pathology and Laboratory Medicine, The University of British Columbia, Vancouver, British Columbia, Canada
| | - Margo Pearce
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Emilia Clementi
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Amanda Yu
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Maria Alvarez
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Hasina Samji
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
- Faculty of Health Sciences, Simon Fraser University, Burnaby, British Columbia, Canada
| | | | - Younathan Abdia
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Mel Krajden
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
- Department of Pathology and Laboratory Medicine, The University of British Columbia, Vancouver, British Columbia, Canada
| | - Naveed Zafar Janjua
- School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
- Clinical Prevention Services, British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
- Centre for Health Evaluation and Outcome Sciences, St Paul's Hospital, Vancouver, British Columbia, Canada
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Shengir M, Elgara M, Sebastiani G. Metabolic and cardiovascular complications after virological cure in hepatitis C: What awaits beyond. World J Gastroenterol 2021; 27:1959-1972. [PMID: 34007133 PMCID: PMC8108037 DOI: 10.3748/wjg.v27.i17.1959] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/25/2021] [Revised: 03/06/2021] [Accepted: 04/12/2021] [Indexed: 02/06/2023] Open
Abstract
The association between chronic hepatitis C (CHC) infection and extrahepatic manifestations (EHMs), particularly cardiometabolic diseases, has been extensively examined. However, there has still been insufficient evaluation for these EHMs after virological cure. Several multidirectional mechanisms have been proposed explaining the ability of hepatitis C virus (HCV) developing EHMs, cardiometabolic ones, as well as the effect of antiviral therapy to resolve these EHMs. Data on these manifestations after achieving sustained virologic response (SVR) are still conflicting. However, current evidence suggests that reversal of hepatic steatosis and its coexistent hypocholesterolemia after successful viral eradication led to unfavorable lipid profile, which increases cardiovascular disease (CVD) risk. Additionally, most observations showed that metabolic alterations, such as insulin resistance and diabetes mellitus (DM), undergo some degree of reduction after viral clearance. These changes seem HCV-genotype dependent. Interferon-based antiviral therapy and direct acting antiviral drugs were shown to minimize incidence of DM. Large epidemiological studies that investigated the effect of SVR on CVD showed great discrepancies in terms of results, with predominant findings indicating that CVD events decreased in patients with SVR compared to non-responders or untreated ones. In this review, we present a summary of the current knowledge regarding extrahepatic sequelae of CHC following SVR, which may have an impact on healthcare providers’ clinical practice.
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Affiliation(s)
- Mohamed Shengir
- Department of Medicine, McGill University, Montreal, Quebec H3A0G4, Canada
| | - Mohamed Elgara
- Department of Internal Medicine, Hamad Medical Corporation, Doha 3050, Qatar
| | - Giada Sebastiani
- Department of Medicine, McGill University Health Center, Montreal, Quebec H4A3J1, Canada
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Sacco M, Saracco GM. The impact of direct-acting antiviral treatment on glycemic homeostasis in patients with chronic hepatitis C. Minerva Gastroenterol (Torino) 2021; 67:264-272. [PMID: 33856147 DOI: 10.23736/s2724-5985.21.02835-x] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/08/2022]
Abstract
BACKGROUND there is robust epidemiological evidence suggesting the link of chronic Hepatitis C Virus (HCV) infection with type 2 diabetes mellitus (DM). Viral clearance achieved by Direct Acting Antiviral Agents (DAAs) has been associated to significant improvements in glycometabolic control but data on the long-term effect of Sustained Virological Response on diabetic disease are limited. AIM the aim of this review is to evaluate the influence of SVR after DAA-based therapy on Insulin Resistance (IR) and DM incidence in non-diabetic patients, on the glycemic homeostasis in diabetic patients and on their long-term hepatic and metabolic outcomes. METHODS an electronic search of Embase, PubMed, MEDLINE, Ovid and the Cochrane Database of Systematic Reviews was performed for papers regarding the effect of DAAinduced SVR on the glycometabolic control and clinical outcomes of HCV-positive diabetic patients up to September 30, 2020. RESULTS among non-diabetic patients, a significant reduction in the risk of IR and DM was reported by the vast majority of the studies; the glycometabolic control significantly improved in diabetic patients during and immediately after the end of antiviral treatment. However, whether this beneficial effect is long lasting is still matter of debate. Furthermore, at variance with data obtained during the Interferon (IFN) era, DM does not seem to be an unfavourable predictive factor of Hepatocellular Carcinoma (HCC) in cured patients. CONCLUSIONS a favourable influence of DAA-induced SVR on IR and DM incidence and on glycemic control is reported by several studies. However, the long-term biochemical, metabolic and clinical impact of this endocrine benefit remains largely unknown.
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Affiliation(s)
- Marco Sacco
- Gastro-hepatoloy Unit, Department of Medical Sciences, University of Turin, Turin, Italy
| | - Giorgio M Saracco
- Gastro-hepatoloy Unit, Department of Medical Sciences, University of Turin, Turin, Italy -
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Sex Differences in Extrahepatic Outcomes After Antiviral Treatment for Hepatitis C. Am J Gastroenterol 2021; 116:576-583. [PMID: 33399360 DOI: 10.14309/ajg.0000000000001095] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/30/2020] [Accepted: 11/13/2020] [Indexed: 12/11/2022]
Abstract
INTRODUCTION Despite recognized differences in the rates of cardiovascular and renal disease between men and women in the general population, studies of the downstream effects of antiviral treatment for hepatitis C (HCV) have not investigated differences in outcomes based on sex. We analyzed sex differences in risk of acute coronary syndrome (ACS), end-stage renal disease (ESRD), and ischemic stroke by treatment and response in a large US-based multisite cohort of HCV patients. METHODS Observation started at the HCV diagnosis date (untreated) or last antiviral treatment start (treated). Treatment selection bias was addressed using an inverse probability-weighting approach. We estimated the effect of treatment on the cumulative incidence of outcomes using the Fine-Gray method (subdistribution hazard ratios [sHR] and 95% confidence intervals [95% CI]). Death was a competing risk. RESULTS Roughly 40% of 15,295 HCV patients were women. After controlling for other risk factors, sustained virological response (SVR) (interferon-based [IFN] or direct-acting antiviral [DAA]) significantly reduced risk of all outcomes, particularly among female patients. Female patients who achieved SVR after IFN-based treatment had significantly lower risk of ACS compared with male patients with SVR from either treatment type (sHR 0.45 [95% CI 0.35-0.59] vs 0.81 [95% CI 0.69-0.96, for DAA SVR] and sHR 0.72 [95% 0.62, 0.85, for IFN SVR]). Successful treatment seemed to be most protective against ESRD; female patients who achieved SVR were at 66%-68% lower risk than untreated patients (sHR 0.32 [95% CI 0.17-0.60 for DAA SVR] and 0.34 [95% CI 0.20-0.58 for IFN SVR]), whereas men were at 38%-42% lower risk (sHR 0.62 [95% CI 0.46-0.85 for DAA SVR] and 0.58 [95% CI 0.43-0.76 for IFN SVR]). IFN treatment failure significantly increased risk of all outcomes by 50%-100% among female patients. Compared with no treatment, female patients who experienced IFN treatment failure were at 63% increased risk of ACS (sHR 1.63 [95% CI 1.35-1.96]), almost twice the risk of ESRD (sHR 1.95 [95% CI 1.43-2.66]) and 51% increased risk of stroke (sHR 1.49 [95%CI 1.11-2.00]). DISCUSSION SVR reduced the risk of extrahepatic complications, particularly in females. The significantly increased risk associated with IFN TF in women-a subset who represented roughly 10% of that group-underscores the importance of prioritizing these patients for DAA treatment irrespective of the fibrosis stage.
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Butt AA, Yan P, Aslam S, Shaikh OS, Abou-Samra AB. Hepatitis C Virus (HCV) Treatment With Directly Acting Agents Reduces the Risk of Incident Diabetes: Results From Electronically Retrieved Cohort of HCV Infected Veterans (ERCHIVES). Clin Infect Dis 2021; 70:1153-1160. [PMID: 30977808 DOI: 10.1093/cid/ciz304] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/14/2019] [Accepted: 04/09/2019] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND The effects of interferon-based therapies for hepatitis C virus (HCV) upon the risk of diabetes are controversial. The effects of newer, directly acting antiviral agents (DAA) upon this risk are unknown. We sought to determine the effects of HCV treatment upon the risk and incidence of diabetes. METHODS Using the Electronically Retrieved Cohort of HCV Infected Veterans (ERCHIVES) database for persons with chronic HCV infection (n = 242 680), we identified those treated with a pegylated interferon and ribavirin regimen (PEG/RBV, n = 4764) or a DAA-containing regimen (n = 21 279), after excluding those with diabetes at baseline, those with a human immunodeficiency virus or hepatitis B virus coinfection, and those treated with both PEG/RBV and DAA regimens. Age-, race-, sex-, and propensity score-matched controls (1:1) were also identified. RESULTS Diabetes incidence rates per 1000 person-years were 20.6 (95% confidence interval [CI] 19.6-21.6) among untreated persons, 19.8 (95% CI 18.3-21.4) among those treated with PEG/RBV, and 9.89 (95% CI 8.7-11.1) among DAA-treated persons (P < .001). Among the treated, rates were 13.3 (95% CI 12.2-14.5) for those with a sustained virologic response (SVR) and 19.2 (95% CI 17.4-21.1) for those without an SVR (P < .0001). A larger reduction was observed in persons with more advanced fibrosis/cirrhosis (absolute difference 2.9 for fibrosis severity score [FIB-4] < 1.25; 5.7 for FIB-4 1.26-3.25; 9.8 for FIB-4 >3.25). DAA treatment (hazard ratio [HR] 0.53, 95% CI .46-.63) and SVR (HR 0.81, 95% CI .70-.93) were associated with a significantly reduced risk of diabetes. DAA-treated persons had longer diabetes-free survival rates, compared to untreated and PEG/RBV-treated persons. There was no significant difference in diabetes-free survival rates between untreated and PEG/RBV-treated persons. The results were similar in inverse probability of treatment and censoring weight models. CONCLUSIONS DAA therapy significantly reduces the incidence and risk of subsequent diabetes. Treatment benefits are more pronounced in persons with more advanced liver fibrosis.
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Affiliation(s)
- Adeel A Butt
- Veterans Health Administration Pittsburgh Healthcare System, Pennsylvania.,Weill Cornell Medical College, New York, New York.,Hamad Medical Corporation, Doha, Qatar
| | - Peng Yan
- Veterans Health Administration Pittsburgh Healthcare System, Pennsylvania
| | - Samia Aslam
- Veterans Health Administration Pittsburgh Healthcare System, Pennsylvania
| | - Obaid S Shaikh
- Veterans Health Administration Pittsburgh Healthcare System, Pennsylvania
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Goodman S, Zahn M, Bruckner T, Boden-Albala B, Lakon CM. Measuring Hazards of Undetectable Viral Load among Hepatitis C Antibody Positive Residents of a Large Southern California County. Health Serv Res Manag Epidemiol 2021; 8:23333928211066181. [PMID: 34926722 PMCID: PMC8671667 DOI: 10.1177/23333928211066181] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/03/2021] [Revised: 11/16/2021] [Accepted: 11/22/2021] [Indexed: 12/09/2022] Open
Abstract
Background Hepatitis C virus (HCV) infection is the most common bloodborne infection in the U.S. However, only a small proportion of persons are treated and cured. Previous research has not characterized sociodemographic characteristics of who receives treatment. We examined predictors of undetectable for HCV in Orange County, the sixth largest county in the United States, where HCV is the most commonly reported infection. METHODS From 2014 to 2020, we acquired public health surveillance data from 91,165 HCV antibody-positive care encounters from the California Reportable Disease Information Exchange (CalREDIE). We used a time-to-event proportional hazards framework to estimate individual and area-level correlates of time-to-HCV undetectable viral load among HCV + individuals. RESULTS Older adults (>65 years) showed an increased hazard of undetectable viral load relative to younger adults (HR = 2.00). In addition, residents of census tracts with greater enrollment in health insurance showed a greater likelihood of undetectable viral load (HR = 1.36). The moderating effect of higher tract median household income and higher tract levels of health insurance were more likely to have undetectable viral load and was statistically significant. CONCLUSION In a large urban county, HCV antibody-positive older adults appear much more likely to show undetectable viral load compared to younger adults. Residents in areas with higher quartiles of health insurance enrollment have an increased likelihood of undetectable viral load. The extent to which constraints impede HCV care requires further investigation, including follow-up studies on health insurance type to test the relationship of health insurance type to undetectable viral load.
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Affiliation(s)
- Sara Goodman
- Program in Public Health, Department of Health, Society, and Behavior, Susan and Henry Samueli College of Health Sciences, University of California, Irvine, Irvine, USA
| | - Matthew Zahn
- Communicable Disease Control, Orange County Health Care Agency, Santa Ana, California, USA
| | - Tim Bruckner
- Program in Public Health, Department of Health, Society, and Behavior, Susan and Henry Samueli College of Health Sciences, University of California, Irvine, Irvine, USA
- Center for Population, Inequality, and Policy, University of California, Irvine, Irvine, USA
| | - Bernadette Boden-Albala
- Program in Public Health, Department of Health, Society, and Behavior, Susan and Henry Samueli College of Health Sciences, University of California, Irvine, Irvine, USA
- School of Medicine, Department of Neurology, Susan and Henry Samueli College of Health Sciences, University of California, Irvine, Irvine, USA
- Program in Public Health, Department of Epidemiology and Biostatistics, University of California, Irvine, Irvine, USA
| | - Cynthia M. Lakon
- Program in Public Health, Department of Health, Society, and Behavior, Susan and Henry Samueli College of Health Sciences, University of California, Irvine, Irvine, USA
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Graf C, Welzel T, Bogdanou D, Vermehren J, Beckel A, Bojunga J, Friedrich-Rust M, Dietz J, Kubesch A, Mondorf A, Fischer S, Lutz T, Stoffers P, Herrmann E, Poynard T, Zeuzem S, Dultz G, Mihm U. Hepatitis C Clearance by Direct-Acting Antivirals Impacts Glucose and Lipid Homeostasis. J Clin Med 2020; 9:E2702. [PMID: 32825571 PMCID: PMC7564474 DOI: 10.3390/jcm9092702] [Citation(s) in RCA: 20] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/13/2020] [Revised: 08/13/2020] [Accepted: 08/14/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Chronic hepatitis C virus (HCV) infections are causally linked with metabolic comorbidities such as insulin resistance, hepatic steatosis, and dyslipidemia. However, the clinical impact of HCV eradication achieved by direct-acting antivirals (DAAs) on glucose and lipid homeostasis is still controversial. The study aimed to prospectively investigate whether antiviral therapy of HCV with DAAs alters glucose and lipid parameters. METHODS 50 patients with chronic HCV who were treated with DAAs were screened, and 49 were enrolled in the study. Biochemical and virological data, as well as noninvasive liver fibrosis parameters, were prospectively collected at baseline, at the end of treatment (EOT) and 12 and 24 weeks post-treatment. RESULTS 45 of 46 patients achieved sustained virologic response (SVR). The prevalence of insulin resistance (HOMA-IR) after HCV clearance was significantly lower, compared to baseline (5.3 ± 6.1 to 2.5 ± 1.9, p < 0.001), which is primarily attributable to a significant decrease of fasting insulin levels (18.9 ± 17.3 to 11.7 ± 8.7; p = 0.002). In contrast to that, HCV eradication resulted in a significant increase in cholesterol levels (total cholesterol, low-density lipoprotein cholesterol (LDL-C), and high-density lipoprotein (HDL-C) levels) and Controlled Attenuated Score (CAP), although BMI did not significantly change over time (p = 0.95). Moreover, HOMA-IR correlated significantly with noninvasive liver fibrosis measurements at baseline und during follow-up (TE: r = 0.45; p = 0.003, pSWE: r = 0.35; p = 0.02, APRI: r = 0.44; p = 0.003, FIB-4: r = 0.41; p < 0.001). CONCLUSION Viral eradication following DAA therapy may have beneficial effects on glucose homeostasis, whereas lipid profile seems to be worsened.
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Affiliation(s)
- Christiana Graf
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Tania Welzel
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Dimitra Bogdanou
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Johannes Vermehren
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Anita Beckel
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Jörg Bojunga
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Mireen Friedrich-Rust
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Julia Dietz
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Alica Kubesch
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Antonia Mondorf
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Sarah Fischer
- Infektiologikum, Center for Infectious Diseases, 60596 Frankfurt, Germany; (S.F.); (T.L.)
| | - Thomas Lutz
- Infektiologikum, Center for Infectious Diseases, 60596 Frankfurt, Germany; (S.F.); (T.L.)
| | - Philipp Stoffers
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Eva Herrmann
- Institute of Biostatistics and Mathematical Modeling, Goethe University Frankfurt, 60596 Frankfurt, Germany;
| | | | - Stefan Zeuzem
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Georg Dultz
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
| | - Ulrike Mihm
- Department of Internal Medicine, University Hospital Frankfurt, 60596 Frankfurt, Germany; (T.W.); (D.B.); (J.V.); (A.B.); (J.B.); (M.F.-R.); (J.D.); (A.K.); (A.M.); (P.S.); (S.Z.); (G.D.); (U.M.)
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Balasubramanyam M. Does COVID-19 Warn Us to Revisit Virus-Induced Diabetes? EXPLORATORY RESEARCH AND HYPOTHESIS IN MEDICINE 2020; 000:1-5. [DOI: 10.14218/erhm.2020.00046] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/15/2022]
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da Silva CB, Vieira DA, de Melo LF, Chagas ALS, Gomes AD, Faria Jr CLLD, Teixeira R, de Magalhães Queiroz DM, Rocha GA, Soares MMS, Bezerra JMT, Silva LD. Interleukin-6-174G/C polymorphism is associated with a decreased risk of type 2 diabetes in patients with chronic hepatitis C virus. World J Hepatol 2020; 12:137-148. [PMID: 32685106 PMCID: PMC7336292 DOI: 10.4254/wjh.v12.i4.137] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/29/2019] [Revised: 02/28/2020] [Accepted: 03/22/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Chronic hepatitis C (CHC) is associated with type 2 diabetes mellitus. Although the pathogenesis remains to be elucidated, a growing evidence has suggested a role of pro-inflammatory immune response. Increased serum concentrations of Interleukin 6 (IL-6) have been associated with insulin resistance, type 2 diabetes mellitus as well as advanced forms of liver disease in chronic hepatitis C infection.
AIM To investigate the frequency of IL-6-174G/C (rs1800795) single nucleotide polymorphism (SNP) in CHC patients and in healthy subjects of the same ethnicity. Associations between type 2 diabetes mellitus (dependent variable) and demographic, clinical, nutritional, virological and, IL-6 genotyping data were also investigated in CHC patients.
METHODS Two hundred and forty-five patients with CHC and 179 healthy control subjects (blood donors) were prospectively included. Type 2 diabetes mellitus was diagnosed according to the criteria of the American Diabetes Association. Clinical, biochemical, histological and radiological methods were used for the diagnosis of the liver disease. IL-6 polymorphism was evaluated by Taqman SNP genotyping assay. The data were analysed by logistic regression models.
RESULTS Type 2 diabetes mellitus, blood hypertension and liver cirrhosis were observed in 20.8% (51/245), 40.0% (98/245) and 38.4% (94/245) of the patients, respectively. The frequency of the studied IL-6 SNP did not differ between the CHC patients and controls (P = 0.81) and all alleles were in Hardy-Weinberg equilibrium (P = 0.38). In the multivariate analysis, type 2 diabetes mellitus was inversely associated with GC and CC genotypes of IL-6-174 (OR = 0.42; 95%CI = 0.22-0.78; P = 0.006) and positively associated with blood hypertension (OR = 5.56; 95%CI = 2.79-11.09; P < 0.001).
CONCLUSION This study was the first to show that GC and CC genotypes of IL-6-174 SNP are associated with a decreased risk of type 2 diabetes mellitus in patients chronically infected with hepatitis C virus. The identification of potential inflammatory mediators involved in the crosstalk between hepatitis C virus and the axis pancreas-liver remains important issues that deserve further investigations.
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Affiliation(s)
- Cliviany Borges da Silva
- Sciences Applied to Adult Health Care Post-Graduate Programme, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Diego Alves Vieira
- Medical undergraduate student, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Luisa Freitas de Melo
- Medical undergraduate student, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Anna Luiza Soares Chagas
- Medical undergraduate student, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Adriana Dias Gomes
- Laboratory of Research in Bacteriology, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - César Lúcio Lopes de Faria Jr
- Laboratory of Research in Bacteriology, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Rosângela Teixeira
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Department of Internal Medicine, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Dulciene Maria de Magalhães Queiroz
- Laboratory of Research in Bacteriology, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Gifone Aguiar Rocha
- Laboratory of Research in Bacteriology, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Maria Marta Sarquis Soares
- Division of Endocrinology, Department of Internal Medicine, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Juliana Maria Trindade Bezerra
- Epidemiology of Infectious and Parasitic Diseases Laboratory, Department of Parasitology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
| | - Luciana Diniz Silva
- Outpatient Clinic of Viral Hepatitis, Instituto Alfa de Gastroenterologia, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
- Department of Internal Medicine, Faculdade de Medicina, Universidade Federal de Minas Gerais, Belo Horizonte 30130100, Minas Gerais, Brazil
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Mohanty A, Salameh S, Butt AA. Impact of Direct Acting Antiviral Agent Therapy upon Extrahepatic Manifestations of Hepatitis C Virus Infection. Curr HIV/AIDS Rep 2020; 16:389-394. [PMID: 31482299 DOI: 10.1007/s11904-019-00466-1] [Citation(s) in RCA: 31] [Impact Index Per Article: 6.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
Abstract
PURPOSE OF REVIEW Direct acting antiviral agents (DAAs) have emerged as simple, short, safe, and effective treatments for chronic hepatitis C (CHC) infection. CHC is a systemic disease with frequent and multiple extrahepatic manifestations. The beneficial effects of DAA treatment regimens extend beyond improvement in liver-related outcomes to amelioration of extra hepatic manifestations and are likely to have economic implications. The purpose of this review is to evaluate the effect of DAAs on extra hepatic manifestations of CHC virus infection. RECENT FINDINGS Recent studies indicate that DAAs are associated with reduction in all-cause mortality, even in patients without significant hepatic fibrosis. They are also associated with reduction in incident cardiovascular disease and diabetes. DAAs are the mainstay of treatment in HCV-associated cryoglobulinemia and lymphoma. Successful HCV therapy with DAAs also improves patient-related outcomes such as health-related quality of life. DAAs improve extrahepatic manifestations of CHC virus infection. Future studies are needed to evaluate the long-term durability of treatment response and for accounting amelioration of extrahepatic manifestations into the cost effectiveness of DAA regimens.
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Affiliation(s)
- Arpan Mohanty
- Boston University School of Medicine, Boston, MA, USA
| | | | - Adeel A Butt
- Hamad Medical Corporation, Doha, Qatar. .,VA Pittsburgh Healthcare System, Pittsburgh, PA, USA. .,Weill Cornell Medical College, New York, NY, USA. .,Weill Cornell Medical College, Doha, Qatar.
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The Effect of Viral Clearance Achieved by Direct-Acting Antiviral Agents on Hepatitis C Virus Positive Patients with Type 2 Diabetes Mellitus: A Word of Caution after the Initial Enthusiasm. J Clin Med 2020; 9:jcm9020563. [PMID: 32092892 PMCID: PMC7074145 DOI: 10.3390/jcm9020563] [Citation(s) in RCA: 22] [Impact Index Per Article: 4.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/11/2020] [Revised: 02/11/2020] [Accepted: 02/17/2020] [Indexed: 02/07/2023] Open
Abstract
The causal link between chronic hepatitis C and glycometabolic alterations has been confirmed by much biochemical, clinical, and epidemiological research work, but what is still controversial is the long-term clinical impact of sustained virologic response (SVR) achieved by direct-acting antiviral agents (DAAs) on patients with type 2 diabetes mellitus (DM). The aim of this paper is to summarize the biochemical and clinical consequences to DM of DAA-based therapy for hepatitis C virus (HCV) infection. An electronic search of Embase, PubMed, MEDLINE, Ovid, and the Cochrane Database of Systematic Reviews was conducted for publications assessing whether clearance of HCV achieved by interferon (IFN)-free antiviral therapy determines significant changes in glycometabolic control and clinical outcomes of diabetic patients. A beneficial effect of SVR obtained by DAA therapy on DM prevention and the short-term outcome of glycometabolic alterations are acknowledged by most of the studies. Whether this effect is maintained over the long term with a significant clinical impact on diabetic and liver disease is still a matter of debate.
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Rossi C, Jeong D, Wong S, McKee G, Butt ZA, Buxton J, Wong J, Darvishian M, Bartlett S, Samji H, Yu A, Binka M, Alvarez M, Adu PA, Tyndall M, Krajden M, Janjua NZ. Sustained virological response from interferon-based hepatitis C regimens is associated with reduced risk of extrahepatic manifestations. J Hepatol 2019; 71:1116-1125. [PMID: 31433302 DOI: 10.1016/j.jhep.2019.07.021] [Citation(s) in RCA: 23] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/14/2018] [Revised: 06/26/2019] [Accepted: 07/22/2019] [Indexed: 12/15/2022]
Abstract
BACKGROUND & AIMS HCV infection is associated with several extrahepatic manifestations (EHMs). We evaluated the impact of sustained virological response (SVR) on the risk of 7 EHMs that contribute to the burden of extrahepatic disease: type 2 diabetes mellitus, chronic kidney disease or end-stage renal disease, stroke, ischemic heart disease, major adverse cardiac events, mood and anxiety disorders, and rheumatoid arthritis. METHODS A longitudinal cohort study was conducted using data from the British Columbia Hepatitis Testers Cohort, which included ~1.3 million individuals screened for HCV. We identified all HCV-infected individuals who were treated with interferon-based therapies between 1999 and 2014. SVR was defined as a negative HCV RNA test ≥24 weeks post-treatment or after end-of-treatment, if unavailable. We computed adjusted subdistribution hazard ratios (asHR) for the effect of SVR on each EHM using competing risk proportional hazard models. Subgroup analyses by birth cohort, sex, injection drug exposure and genotype were also performed. RESULTS Overall, 10,264 HCV-infected individuals were treated with interferon, of whom 6,023 (59%) achieved SVR. Compared to those that failed treatment, EHM risk was significantly reduced among patients with SVR for type 2 diabetes mellitus (asHR 0.65; 95%CI 0.55-0.77), chronic kidney disease or end-stage renal disease (asHR 0.53; 95% CI 0.43-0.65), ischemic or hemorrhagic stroke (asHR 0.73; 95%CI 0.49-1.09), and mood and anxiety disorders (asHR 0.82; 95%CI 0.71-0.95), but not for ischemic heart disease (asHR 1.23; 95%CI 1.03-1.47), major adverse cardiac events (asHR 0.93; 95%CI 0.79-1.11) or rheumatoid arthritis (asHR 1.09; 95% CI 0.73-1.64). CONCLUSIONS SVR was associated with a reduction in the risk of several EHMs. Increased uptake of antiviral therapy may reduce the growing burden of EHMs in this population. LAY SUMMARY We estimated the rates of chronic comorbidities other than liver disease between those who were cured and those who failed treatment for hepatitis C virus (HCV) infection. Our findings showed that the rates of these non-liver diseases were largely reduced for those who were cured with interferon-based treatments. Early HCV treatments could provide many benefits in the prevention of various HCV complications beyond liver disease.
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Affiliation(s)
- Carmine Rossi
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
| | - Dahn Jeong
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Stanley Wong
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Geoffrey McKee
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Zahid Ahmad Butt
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Jane Buxton
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Jason Wong
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Maryam Darvishian
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Sofia Bartlett
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
| | - Hasina Samji
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Amanda Yu
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Mawuena Binka
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
| | - Maria Alvarez
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada
| | - Prince Asumadu Adu
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Mark Tyndall
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
| | - Mel Krajden
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, British Columbia, Canada
| | - Naveed Zafar Janjua
- British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada; School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada.
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Muñoz Díaz HA, Lúquez Mindiola AJ, Gómez Aldana AJ. Fisiopatología de la hepatitis C y diabetes mellitus. Hacia la cura de dos epidemias en el siglo XXI. REVISTA COLOMBIANA DE GASTROENTEROLOGÍA 2019; 34:277-287. [DOI: 10.22516/25007440.322] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 07/01/2024]
Abstract
La infección crónica por virus de la hepatitis C (VHC) y la diabetes mellitus (DM) son dos problemas de salud pública que impactan los sistemas de salud, con una alta carga económica global. La infección por VHC produce manifestaciones hepáticas tales como hepatitis, cirrosis y carcinoma hepatocelular; asimismo, se ha involucrado en la patogénesis de manifestaciones extrahepáticas, entre las cuales se ha asociado con alteraciones metabólicas como la DM. Estudios longitudinales y transversales han reportado mayor incidencia y prevalencia de DM en pacientes con infección crónica por VHC. La DM acelera la progresión histológica y clínica en pacientes con infección crónica por VHC y las complicaciones cardiovasculares. Recientemente se ha avanzado en el tratamiento y la introducción de nuevos medicamentos como los antivirales de acción directa, que mejoran el control glucémico en estos pacientes.
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Li J. Letter: HCV complication and type 2 diabetes management-the directional link is not yet defined. Authors' reply. Aliment Pharmacol Ther 2019; 49:1251-1252. [PMID: 30977180 DOI: 10.1111/apt.15247] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/09/2022]
Affiliation(s)
- Jia Li
- Department of Public Health Sciences, Henry Ford Health System, Detroit, MI
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Li J, Gordon SC, Rupp LB, Zhang T, Trudeau S, Holmberg SD, Moorman AC, Spradling PR, Teshale EH, Boscarino JA, Schmidt MA, Daida YG, Lu M, CHeCS Investigators. Sustained virological response to hepatitis C treatment decreases the incidence of complications associated with type 2 diabetes. Aliment Pharmacol Ther 2019; 49:599-608. [PMID: 30650468 PMCID: PMC6599612 DOI: 10.1111/apt.15102] [Citation(s) in RCA: 38] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/17/2018] [Revised: 09/12/2018] [Accepted: 11/28/2018] [Indexed: 12/15/2022]
Abstract
BACKGROUND The role of hepatitis C (HCV) eradication on the long-term complications of type 2 diabetes mellitus remains incompletely studied. AIM To investigate whether antiviral treatment impacted risk of acute coronary syndrome, end-stage renal disease, ischaemic stroke, and retinopathy among diabetic patients from the four US health systems comprising the Chronic Hepatitis Cohort Study (CHeCS). METHODS We included CHeCS HCV patients with diagnosis codes for type 2 diabetes who were on antidiabetic medications. Patients were followed until an outcome of interest, death, or last health system encounter. The effect of treatment on outcomes was estimated using the competing risk analysis (Fine-Gray subdistribution hazard ratio [sHR]), with death as a competing event. RESULTS Among 1395 HCV-infected patients with type 2 diabetes, 723 (52%) were treated with either interferon-based or direct-acting antivirals (DAAs); 539 (75% of treated) achieved sustained virological response (SVR). After propensity score adjustment to address treatment selection bias, patients with SVR demonstrated significantly decreased risk of acute coronary syndrome (sHR = 0.36; P < 0.001), end-stage renal disease (sHR = 0.46; P < 0.001), stroke (sHR = 0.34; P < 0.001), and retinopathy (sHR = 0.24; P < 0.001) compared to untreated patients. Results were consistent in subgroup analyses of DAA-treated patients and interferon-treated patients, an analysis of cirrhotic patients, as well as in sensitivity analyses considering cause-specific hazards, exclusion of patients with on-treatment retinopathy, and treatment status as a time-varying covariate. CONCLUSION Successful HCV treatment among patients with type 2 diabetes significantly reduces incidence of acute coronary syndrome, end-stage renal disease, ischaemic stroke, and retinopathy, regardless of cirrhosis. Our findings support the importance of HCV antiviral therapy among patients with type 2 diabetes to reduce the risk of these extrahepatic outcomes.
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Affiliation(s)
- Jia Li
- Department of Public Health Sciences, Henry Ford Health System, Detroit, Michigan
| | - Stuart C. Gordon
- Division of Gastroenterology and Hepatology, Henry Ford Health System, and Wayne State University School of Medicine, Detroit, Michigan
| | - Loralee B. Rupp
- Center for Health Policy and Health Services Research, Henry Ford Health System, Detroit, Michigan
| | - Talan Zhang
- Department of Public Health Sciences, Henry Ford Health System, Detroit, Michigan
| | - Sheri Trudeau
- Department of Public Health Sciences, Henry Ford Health System, Detroit, Michigan
| | - Scott D. Holmberg
- Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Anne C. Moorman
- Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Philip R. Spradling
- Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Eyasu H. Teshale
- Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
| | - Joseph A. Boscarino
- Department of Epidemiology & Health Services Research, Geisinger Clinic, Danville, Pennsylvania
| | - Mark A. Schmidt
- Center for Health Research, Kaiser Permanente-Northwest, Portland, Oregon
| | - Yihe G. Daida
- Center for Health Research, Kaiser Permanente-Hawai’i, Honolulu, Hawaii
| | - Mei Lu
- Department of Public Health Sciences, Henry Ford Health System, Detroit, Michigan
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Zhao Y, Xing H, Wang X, Ou W, Zhao H, Li B, Li Y, Duan Y, Zhuang L, Li W, Cheng D, Quan M, Zhang Y, Ji S. Management of Diabetes Mellitus in Patients with Chronic Liver Diseases. J Diabetes Res 2019; 2019:6430486. [PMID: 31915709 PMCID: PMC6931017 DOI: 10.1155/2019/6430486] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/16/2019] [Accepted: 11/09/2019] [Indexed: 02/06/2023] Open
Abstract
Diabetes mellitus (DM) is a common chronic disease affecting humans globally. During the last few years, the incidence of diabetes has increased and has received more attention. In addition to growing DM populations, DM complications are involving injuries to more organs, such as the heart and cerebral vessel damage. DM complications can reduce quality of life and shorten life spans and eventually also impede social and economic development. Therefore, effective measures to curb the occurrence and development of diabetes assist in improving patients' quality of life, delay the progression of DM in the population, and ease a social burden. The liver is regarded as an important link in the management and control of DM, including the alleviation of glucose metabolism and lipid metabolism and others via glucose storage and endogenous glucose generation from glycogen stored in the liver. Liver cirrhosis is a very common chronic disease, which often lowers the quality of life and decreases life expectancy. According to a growing body of research, diabetes shows a close correlation with hepatitis, liver cirrhosis, and liver cancer. Moreover, coexistence of liver complications would accelerate the deterioration of patients with diabetes. Liver cirrhosis and diabetes influence each other. Thus, in addition to pharmacological treatments and lifestyle interventions, effective control of cirrhosis might assist in a better management of diabetes. When it comes to different etiologies of liver cirrhosis, different therapeutic methods, such as antiviral treatment, may be more effective. Effective control of cirrhosis might be a strategy for better management of diabetes.
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Affiliation(s)
- Yingying Zhao
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Huichun Xing
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Xiaomei Wang
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Weini Ou
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Hong Zhao
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Ben Li
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Yue Li
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Ying Duan
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Liwei Zhuang
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Wei Li
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Danying Cheng
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Min Quan
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Yu Zhang
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
| | - Shibo Ji
- Department of Hepatology, Division 3, Beijing Ditan Hospital, Capital Medical University and Teaching Hospital of Peking University, 8 Jingshundong Street, Beijing 100015, China
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20
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Jafri S, Gordon SC. Epidemiology of Hepatitis C. Clin Liver Dis (Hoboken) 2018; 12:140-142. [PMID: 30988931 PMCID: PMC6385933 DOI: 10.1002/cld.783] [Citation(s) in RCA: 26] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/05/2018] [Accepted: 11/07/2018] [Indexed: 02/06/2023] Open
Affiliation(s)
- Syed‐Mohammed Jafri
- Department of Gastroenterology and HepatologyHenry Ford Health SystemDetroitMI
| | - Stuart C. Gordon
- Department of Gastroenterology and HepatologyHenry Ford Health SystemDetroitMI
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21
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Lanini S, Pisapia R, Capobianchi MR, Ippolito G. Global epidemiology of viral hepatitis and national needs for complete control. Expert Rev Anti Infect Ther 2018; 16:625-639. [PMID: 30067107 DOI: 10.1080/14787210.2018.1505503] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2022]
Abstract
INTRODUCTION The World Health Organization recognizes that viral hepatitis is not only a massive public health issue but also a huge opportunity to improve quality of life and equity at a global level. Viral hepatitis causes about 1.5 million deaths each year and significantly affects the quality of life of hundreds of millions of people. To date, frail individuals in high-income countries and people living in low-income settings are paying the heaviest tool. Areas covered. Here we present a broad discussion on current knowledge and topical issues about the hepatitis pandemic. The report includes a structured overview of global epidemiology, including the definition of specific local epidemic profiles for each hepatitis agents (HAV, HBV, HCV, and HEV), and a perspective about the critical actions needed for achieving a complete control. Expert commentary. The control of viral hepatitis is currently, ethically urgent and even economically convenient. There is a wide consensus that viral hepatitis can be controlled through comprehensive intervention tailored on local needs addressing the issue of viral hepatitis as a unique public health issue. These strategies should include: (1) primary prevention (including vaccination and improved infection control), (2) improving diagnosis rate, and (3) management of existing cases of infections.
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Affiliation(s)
- Simone Lanini
- a Dipartimento Epidemiologia, Ricerca Preclinica e Diagnostica Avanzata , National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy
| | - Raffaella Pisapia
- a Dipartimento Epidemiologia, Ricerca Preclinica e Diagnostica Avanzata , National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy
| | - Maria Rosaria Capobianchi
- a Dipartimento Epidemiologia, Ricerca Preclinica e Diagnostica Avanzata , National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy
| | - Giuseppe Ippolito
- a Dipartimento Epidemiologia, Ricerca Preclinica e Diagnostica Avanzata , National Institute for Infectious Diseases Lazzaro Spallanzani-IRCCS , Rome , Italy
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22
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Moorman AC, Rupp LB, Gordon SC, Zhong Y, Xing J, Lu M, Boscarino JA, Schmidt MA, Daida YG, Teshale EH, Spradling PR, Holmberg SD. Long-Term Liver Disease, Treatment, and Mortality Outcomes Among 17,000 Persons Diagnosed with Chronic Hepatitis C Virus Infection: Current Chronic Hepatitis Cohort Study Status and Review of Findings. Infect Dis Clin North Am 2018; 32:253-268. [PMID: 29778254 PMCID: PMC6211170 DOI: 10.1016/j.idc.2018.02.002] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
Abstract
Chronic Hepatitis Cohort Study (CHeCS) publications using data from "real-world" patients with hepatitis C virus (HCV) have described demographic disparities in access to care; rates of advanced liver disease, morbidity, and mortality (2.5%-3.5% per year during 2006-10, although only 19% of all CHeCS decedents, and just 30% of those with deaths attributed to liver disease, had HCV listed on death certificate); substantial comorbidities, such as diabetes, advanced liver fibrosis (29% prevalence), renal disease, and depression, and partial reversal of all these with successful antiviral therapy; patient risk behaviors; and use of noninvasive markers to assess liver disease.
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Affiliation(s)
- Anne C Moorman
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA.
| | - Loralee B Rupp
- Division of Gastroenterology and Hepatology, Henry Ford Health System, 2799 West Grand Boulevard, Detroit, MI 48202, USA
| | - Stuart C Gordon
- Division of Gastroenterology and Hepatology, Henry Ford Health System, 2799 West Grand Boulevard, Detroit, MI 48202, USA
| | - Yuna Zhong
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA
| | - Jian Xing
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA
| | - Mei Lu
- Public Health Sciences, Henry Ford Health System, 1 Ford Place -3A, Detroit, MI 48202, USA
| | - Joseph A Boscarino
- Department of Epidemiology and Health Services Research, Geisinger Clinic, 100 North Academy Avenue, Danville, PA 17822, USA
| | - Mark A Schmidt
- Kaiser Permanente-Center for Health Research, Northwest, Kaiser Permanente Northwest, 3800 North Interstate Avenue, Portland, OR 97227-1098, USA
| | - Yihe G Daida
- Kaiser Permanente-Center for Health Research, Hawaii, Kaiser Permanente Hawaii, 501 Alakawa Street, Suite 201, Honolulu, HI 9681, USA
| | - Eyasu H Teshale
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA
| | - Philip R Spradling
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA
| | - Scott D Holmberg
- Division of Viral Hepatitis, Centers for Disease Control and Prevention (CDC), Mailstop G-37, Atlanta, GA 30329, USA
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