Performance of the PRO-C3 collagen neo-epitope biomarker in non-alcoholic fatty liver disease

Anstee, 2013, Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis, Nat Rev Gastroenterol Hepatol, 10, 330, 10.1038/nrgastro.2013.41 Dulai, 2017, Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: Systematic review and meta-analysis, Hepatology, 65, 1557, 10.1002/hep.29085 Angulo, 2015, Liver Fibrosis, but No Other Histologic Features, Is Associated With Long-term Outcomes of Patients With Nonalcoholic Fatty Liver Disease, Gastroenterology, 149, 389, 10.1053/j.gastro.2015.04.043 Singh, 2015, Fibrosis Progression in Nonalcoholic Fatty Liver vs Nonalcoholic Steatohepatitis: A Systematic Review and Meta-analysis of Paired-Biopsy Studies, Clin Gastroenterol Hepatol, 13, 643, 10.1016/j.cgh.2014.04.014 McPherson, 2015, Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: Implications for prognosis and clinical management, J Hepatol, 62, 1148, 10.1016/j.jhep.2014.11.034 Perrault, 1978, Liver biopsy: complications in 1000 inpatients and outpatients, Gastroenterology, 74, 103, 10.1016/0016-5085(78)90364-5 Ratziu, 2005, Sampling variability of liver biopsy in nonalcoholic fatty liver disease, Gastroenterology, 128, 1898, 10.1053/j.gastro.2005.03.084 Colloredo, 2003, Impact of liver biopsy size on histological evaluation of chronic viral hepatitis: the smaller the sample, the milder the disease, J Hepatol, 39, 239, 10.1016/S0168-8278(03)00191-0 Center for Drug Evaluation and Research (CDER), 2018 Friedman, 2018, A randomized, placebo-controlled trial of cenicriviroc for treatment of nonalcoholic steatohepatitis with fibrosis, Hepatology, 67, 1754, 10.1002/hep.29477 FDA Williams, 1988, Ratio of serum aspartate to alanine aminotransferase in chronic hepatitis. Relationship to cirrhosis, Gastroenterology, 95, 734, 10.1016/S0016-5085(88)80022-2 Angulo, 2007, The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD, Hepatology, 45, 846, 10.1002/hep.21496 McPherson, 2014, Serum immunoglobulin levels predict fibrosis in patients with non-alcoholic fatty liver disease, J Hepatol, 60, 1055, 10.1016/j.jhep.2014.01.010 McPherson, 2010, Simple non-invasive fibrosis scoring systems can reliably exclude advanced fibrosis in patients with non-alcoholic fatty liver disease, Gut, 59, 1265, 10.1136/gut.2010.216077 McPherson, 2013, Are simple noninvasive scoring systems for fibrosis reliable in patients with NAFLD and normal ALT levels?, Eur J Gastroenterol Hepatol, 25, 652, 10.1097/MEG.0b013e32835d72cf Ratziu, 2006, Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with non-alcoholic fatty liver disease, BMC Gastroenterol, 6, 6, 10.1186/1471-230X-6-6 Guha, 2008, Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: Validating the European Liver Fibrosis Panel and exploring simple markers, Hepatology, 47, 455, 10.1002/hep.21984 Dyson, 2013, Non-alcoholic fatty liver disease: non-invasive investigation and risk stratification, J Clin Pathol, 66, 1033, 10.1136/jclinpath-2013-201620 Cassinotto, 2016, Liver stiffness in nonalcoholic fatty liver disease: A comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy, Hepatology, 63, 1817, 10.1002/hep.28394 Loomba, 2014, Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study, Hepatology, 60, 1920, 10.1002/hep.27362 Chen, 2017, Diagnostic Performance of MR Elastography and Vibration-controlled Transient Elastography in the Detection of Hepatic Fibrosis in Patients with Severe to Morbid Obesity, Radiology, 283, 418, 10.1148/radiol.2016160685 Nielsen, 2013, The neo-epitope specific PRO-C3 ELISA measures true formation of type III collagen associated with liver and muscle parameters, Am J Transl Res, 5, 303 Niemela, 1985, Purification and characterization of the N-terminal propeptide of human type III procollagen, Biochem J, 232, 145, 10.1042/bj2320145 Leeming, 2017, Estimation of serum “true collagen type III formation” (Pro-C3) levels as a marker of non-alcoholic steatohepatitis in a prospective cohort, J Hepatol, 66, S154, 10.1016/S0168-8278(17)30582-2 Nielsen, 2017, 143308 Karsdal, 2016, Fibrogenesis assessed by serological type III collagen formation identifies patients with progressive liver fibrosis and responders to a potential antifibrotic therapy, Am J Physiol Gastrointest Liver Physiol, 311, G1009, 10.1152/ajpgi.00283.2016 Harrison, 2018, NGM282 improves fibrosis and NASH-related histology in 12 weeks in patients with biopsy-confirmed NASH, which is preceded by significant decreases in hepatic steatosis, liver transaminases and fibrosis markers at 6 weeks, J Hepatol, 68, S65, 10.1016/S0168-8278(18)30352-0 Daniels, 2019, ADAPT: An algorithm incorporating PRO-C3 accurately identifies patients with NAFLD and advanced fibrosis, Hepatology, 69, 1075, 10.1002/hep.30163 Caussy, 2019, Collagen Formation Assessed by N-Terminal Propeptide of Type 3 Procollagen Is a Heritable Trait and Is Associated With Liver Fibrosis Assessed by Magnetic Resonance Elastography, Hepatology, 70, 127, 10.1002/hep.30610 Wilson, 2002, The relationship between consultation length, process and outcomes in general practice: a systematic review, Br J Gen Pract, 52, 1012 Smith, 2011, Thinking lean: implementing DMAIC methods to improve efficiency within a cystic fibrosis clinic, J Healthc Qual, 33, 37, 10.1111/j.1945-1474.2010.00130.x Vallet-Pichard, 2007, FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. comparison with liver biopsy and fibrotest, Hepatology, 46, 32, 10.1002/hep.21669 Wai, 2003, A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C, Hepatology, 38, 518, 10.1053/jhep.2003.50346 Harrison, 2008, Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease, Gut, 57, 1441, 10.1136/gut.2007.146019 Leeming, 2013, Novel serological neo-epitope markers of extracellular matrix proteins for the detection of portal hypertension, Aliment Pharmacol Ther, 38, 1086, 10.1111/apt.12484 Kleiner, 2005, Design and validation of a histological scoring system for nonalcoholic fatty liver disease, Hepatology, 41, 1313, 10.1002/hep.20701 Nguyen, 2012 Lambert, 2008, How to measure the diagnostic accuracy of noninvasive liver fibrosis indices: The area under the ROC curve revisited, Clin Chem, 54, 1372, 10.1373/clinchem.2007.097923 DeLong, 1988, Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach, Biometrics, 44, 837, 10.2307/2531595 Younossi, 2016, Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes, Hepatology, 64, 73, 10.1002/hep.28431 Estes, 2018, Modeling the epidemic of nonalcoholic fatty liver disease demonstrates an exponential increase in burden of disease, Hepatology, 67, 123, 10.1002/hep.29466 Estes, 2018, Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016-2030, J Hepatol, 69, 896, 10.1016/j.jhep.2018.05.036 Bedossa, 2012, Histopathological algorithm and scoring system for evaluation of liver lesions in morbidly obese patients, Hepatology, 56, 1751, 10.1002/hep.25889 Bedossa, 2014, Utility and appropriateness of the fatty liver inhibition of progression (FLIP) algorithm and steatosis, activity, and fibrosis (SAF) score in the evaluation of biopsies of nonalcoholic fatty liver disease, Hepatology, 60, 565, 10.1002/hep.27173 Zhou, 2005, Nonparametric estimation of ROC curves in the absence of a gold standard, Biometrics, 61, 600, 10.1111/j.1541-0420.2005.00324.x Rutjes, 2007, Evaluation of diagnostic tests when there is no gold standard. A review of methods, Health Technol Assess, 11, iii, 10.3310/hta11500 Luo, 2018, An Evaluation of the Collagen Fragments Related to Fibrogenesis and Fibrolysis in Nonalcoholic Steatohepatitis, Sci Rep, 8, 10.1038/s41598-018-30457-y Musso, 2011, Meta-analysis: natural history of non-alcoholic fatty liver disease (NAFLD) and diagnostic accuracy of non-invasive tests for liver disease severity, Ann Med, 43, 617, 10.3109/07853890.2010.518623 Koehler, 2016, Presence of diabetes mellitus and steatosis is associated with liver stiffness in a general population: The Rotterdam study, Hepatology, 63, 138, 10.1002/hep.27981 Caballeria, 2018, High Prevalence of Liver Fibrosis Among European Adults With Unknown Liver Disease: A Population-Based Study, Clin Gastroenterol Hepatol, 16, 1138, 10.1016/j.cgh.2017.12.048 Bhala, 2011, The natural history of nonalcoholic fatty liver disease with advanced fibrosis or cirrhosis: an international collaborative study, Hepatology, 54, 1208, 10.1002/hep.24491 Ascha, 2010, The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis, Hepatology, 51, 1972, 10.1002/hep.23527 Wanless, 1990, Fatty liver hepatitis (steatohepatitis) and obesity: an autopsy study with analysis of risk factors, Hepatology, 12, 1106, 10.1002/hep.1840120505 Halligan, 2015, Disadvantages of using the area under the receiver operating characteristic curve to assess imaging tests: a discussion and proposal for an alternative approach, Eur Radiol, 25, 932, 10.1007/s00330-014-3487-0