{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T16:00:45Z","timestamp":1753891245100,"version":"3.41.2"},"reference-count":41,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,3,28]],"date-time":"2025-03-28T00:00:00Z","timestamp":1743120000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program","doi-asserted-by":"publisher","award":["2022YFC2603500","2022YFC2603505"],"award-info":[{"award-number":["2022YFC2603500","2022YFC2603505"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program","doi-asserted-by":"publisher","award":["2023YFC2306901","2023YFC2308105"],"award-info":[{"award-number":["2023YFC2306901","2023YFC2308105"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Med."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>The steatosis, activity, and fibrosis (SAF) score is a histological scoring system developed by the European Association for the Study of the Liver to evaluate liver biopsy samples in cases of non-alcoholic fatty liver disease (NAFLD). Based on histopathological results and SAF scores, NAFLD patients were categorized into mild, moderate, and severe groups. We compared the differences between these groups and identified the risk factors influencing lesion severity.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We gathered data from 539 NAFLD patients who underwent percutaneous liver biopsy confirmation at Beijing Ditan Hospital between January 2018 and December 2022. All biopsies were graded according to the SAF scoring system, and the severity of the disease was classified as mild, moderate, or severe. We compared the differences in gender, age, BMI, history of diabetes, history of hypertension, aspartate aminotransferase (AST), alanine aminotransferase (ALT), serum cholesterol levels, and other factors among NAFLD patients with varying degrees of disease severity. Additionally, we explored the risk factors that influenced the severity of lesions.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A total of 539 patients were enrolled in this study, with ages ranging from 6 to 79\u202fyears. Among them, there were 325 men and 214 women in an average age of 39\u202f\u00b1\u202f13\u202fyears. The patients were divided into three groups based on disease severity: mild NAFLD group (162 cases), moderate NAFLD group (210 cases), and severe NAFLD group (167 cases). The results showed significant differences between the three groups in terms of age composition, high-calorie diet, family history of hypertension, ALT, AST, GGT, total bile acids, cholinesterase, glycosylated albumin, blood glucose, uric acid, type III procollagen, serum human laminin, liver stiffness, and hepatic steatosis.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>BMI, uric acid, AST, type III procollagen, liver stiffness, and hepatic steatosis play critical roles in the progression of NAFLD and contribute to high pathological SAF scores in NAFLD patients.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmed.2025.1510679","type":"journal-article","created":{"date-parts":[[2025,3,28]],"date-time":"2025-03-28T07:12:47Z","timestamp":1743145967000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Exploring the severity and risk factors of non-alcoholic fatty liver disease using the SAF scoring system"],"prefix":"10.3389","volume":"12","author":[{"given":"Xinxin","family":"Li","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shiyu","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ziyu","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wen","family":"Deng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yaqin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Weihua","family":"Cao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xin","family":"Wei","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zixuan","family":"Gao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Linmei","family":"Yao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shuojie","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Yi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yao","family":"Xie","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Minghui","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2025,3,28]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1016\/S0025-6196(24)00530-5","article-title":"Non-alcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease","volume":"55","author":"Ludwig","year":"1980","journal-title":"Mayo Clin Proc"},{"key":"ref2","first-page":"14","article-title":"Research advances in metabolic-associated fatty liver disease-related hepatocellular carcinoma","volume":"14","author":"Jiang","year":"2022","journal-title":"Chin J Liver Dis"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1797","DOI":"10.1097\/HEP.0000000000000323","article-title":"AASLD practice guidance on the clinical assessment and management of non-alcoholic fatty liver disease","volume":"77","author":"Rinella","year":"2023","journal-title":"Hepatology"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1038\/nrgastro.2017.109","article-title":"Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention","volume":"15","author":"Younossi","year":"2018","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"101238","DOI":"10.1016\/j.molmet.2021.101238","article-title":"Metabolic-associated fatty liver disease and lipoprotein metabolism","volume":"50","author":"Heeren","year":"2021","journal-title":"Mol Metab"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1016\/j.jhep.2021.10.013","article-title":"Distinct contributions of metabolic dysfunction and genetic risk factors in the pathogenesis of non-alcoholic fatty liver disease","volume":"76","author":"Luukkonen","year":"2022","journal-title":"J Hepatol"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"908","DOI":"10.1038\/s41591-018-0104-9","article-title":"Mechanisms of NAFLD development and therapeutic strategies","volume":"24","author":"Friedman","year":"2018","journal-title":"Nat Med"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"174","DOI":"10.3390\/antiox10020174","article-title":"Role of oxidative stress in the pathogenesis of non-alcoholic fatty liver disease: implications for prevention and therapy","volume":"10","author":"Arroyave-Ospina","year":"2021","journal-title":"Antioxidants (Basel)"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.cell.2018.08.020","article-title":"ER stress drives lipogenesis and Steatohepatitis via Caspase-2 activation of S1P","volume":"175","author":"Kim","year":"2018","journal-title":"Cell"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"761","DOI":"10.1136\/gutjnl-2019-319664","article-title":"Dietary cholesterol drives fatty liver-associated liver cancer by modulating gut microbiota and metabolites","volume":"70","author":"Zhang","year":"2021","journal-title":"Gut"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1038\/ajg.2009.587","article-title":"Predicting fibrosis worsening in obese patients with NASH through parenchymal fibronectin, HOMA-IR, and hypertension","volume":"105","author":"Sorrentino","year":"2010","journal-title":"Am J Gastroenterol"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1016\/j.jhep.2021.02.034","article-title":"Prospective evaluation of the prevalence of non-alcoholic fatty liver disease and steatohepatitis in a large middle-aged US cohort","volume":"75","author":"Harrison","year":"2021","journal-title":"J Hepatol"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1002\/hep.29367","article-title":"The diagnosis and management of non-alcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases","volume":"67","author":"Chalasani","year":"2018","journal-title":"Hepatology"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.jhep.2020.03.039","article-title":"A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement","volume":"73","author":"Eslam","year":"2020","journal-title":"J Hepatol"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"3451","DOI":"10.1093\/hmg\/ddaa162","article-title":"Insights into genetic variants associated with NASH-fibrosis from metabolite profiling","volume":"29","author":"Mann","year":"2020","journal-title":"Hum Mol Genet"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"828","DOI":"10.1016\/j.jhep.2019.12.008","article-title":"Clinical validation of the FLIP algorithm and the SAF score in patients with non-alcoholic fatty liver disease","volume":"72","author":"Nascimbeni","year":"2020","journal-title":"J Hepatol"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1080\/00365521.2016.1230779","article-title":"SAF score and mortality in NAFLD after up to 41 years of follow-up","volume":"52","author":"Hagstr\u00f6m","year":"2017","journal-title":"Scand J Gastroenterol"},{"key":"ref18","first-page":"757","article-title":"Chinese Diabetes Society. Chinese guidelines for the prevention and treatment of type 2 diabetes (2020 edition) (part 2)","volume":"41","year":"2021","journal-title":"Chin J Pract Intern Med"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"757","DOI":"10.19538\/j.nk202109","article-title":"Chinese Diabetes Society. Chinese guidelines for the prevention and treatment of type 2 diabetes (2020 edition) (part 1)","volume":"41","year":"2021","journal-title":"Chin J Pract Intern Med"},{"key":"ref20","first-page":"24","article-title":"2018 Chinese guidelines for the prevention and treatment of hypertension (revised edition)","volume":"24","year":"2019","journal-title":"Chin J Cardiovasc Med"},{"key":"ref21","first-page":"237","article-title":"Chinese guidelines for lipid management (2023)","volume":"38","author":"Wang","year":"2023","journal-title":"Chin Circ J"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1053\/j.gastro.2015.04.043","article-title":"Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with non-alcoholic fatty liver disease","volume":"149","author":"Angulo","year":"2015","journal-title":"Gastroenterology"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1002\/hep.28431","article-title":"Global epidemiology of non-alcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes","volume":"64","author":"Younossi","year":"2016","journal-title":"Hepatology"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.jfma.2021.01.004","article-title":"Predictors for incidence and remission of non-alcoholic fatty liver disease in obese children and adolescents","volume":"121","author":"Lin","year":"2022","journal-title":"J Formos Med Assoc"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"e0298800","DOI":"10.1371\/journal.pone.0298800","article-title":"Determinants of non-alcoholic fatty liver disease in young people: maternal, neonatal, and adolescent factors","volume":"19","author":"Nairz","year":"2024","journal-title":"PLoS One"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"e0140908","DOI":"10.1371\/journal.pone.0140908","article-title":"The prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and Meta-analysis","volume":"10","author":"Anderson","year":"2015","journal-title":"PLoS One"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"1457","DOI":"10.1002\/hep.30626","article-title":"Sex differences in non-alcoholic fatty liver disease: state of the art and identification of research gaps","volume":"70","author":"Lonardo","year":"2019","journal-title":"Hepatology"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"753","DOI":"10.1089\/ars.2021.0044","article-title":"Sex differences in non-alcoholic fatty liver disease: estrogen influence on the liver-adipose tissue crosstalk","volume":"35","author":"Mor\u00e1n-Costoya","year":"2021","journal-title":"Antioxid Redox Signal"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1038\/s41467-022-28138-6","article-title":"Formyl peptide receptor 2 determines sex-specific differences in the progression of non-alcoholic fatty liver disease and steatohepatitis","volume":"13","author":"Lee","year":"2022","journal-title":"Nat Commun"},{"key":"ref30","first-page":"947","article-title":"Guidelines for the prevention and treatment of non-alcoholic fatty liver disease (2018 updated edition)","volume":"34","year":"2018","journal-title":"J Clin Hepatol"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"115861","DOI":"10.1016\/j.bcp.2023.115861","article-title":"NLRP3 inflammasome in hepatic diseases: a pharmacological target","volume":"217","author":"Ramos-Tovar","year":"2023","journal-title":"Biochem Pharmacol"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"925","DOI":"10.1016\/j.jhep.2015.11.022","article-title":"Uric acid regulates hepatic steatosis and insulin resistance through the NLRP3 inflammasome-dependent mechanism","volume":"64","author":"Wan","year":"2016","journal-title":"J Hepatol"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"E1032","DOI":"10.1152\/ajpendo.00518.2020","article-title":"High uric acid induces liver fat accumulation via ROS\/JNK\/AP-1 signaling","volume":"320","author":"Xie","year":"2021","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"260","DOI":"10.14740\/gr685w","article-title":"Association of the non-alcoholic Hepatic Steatosis and its Degrees with the values of liver enzymes and homeostasis model assessment-insulin resistance index","volume":"8","author":"Cruz","year":"2015","journal-title":"Gastroenterol Res"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"e28443","DOI":"10.1097\/MD.0000000000028443","article-title":"Characteristics of peripheral blood gamma-glutamyl transferase in different liver diseases","volume":"101","author":"Xing","year":"2022","journal-title":"Medicine (Baltimore)"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"8494076","DOI":"10.1155\/2022\/8494076","article-title":"Gamma-Glutamyltransferase activity (GGT) is a long-sought biomarker of redox status in blood circulation: a retrospective clinical study of 44 types of human diseases","volume":"2022","author":"Bai","year":"2022","journal-title":"Oxidative Med Cell Longev"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"1287","DOI":"10.1002\/hep.31822","article-title":"Increased adipose tissue fibrogenesis, not impaired expandability, is associated with non-alcoholic fatty liver disease","volume":"74","author":"Beals","year":"2021","journal-title":"Hepatology"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"995749","DOI":"10.3389\/fmed.2022.995749","article-title":"Gamma-glutamyl transferase to high-density lipoprotein cholesterol ratio has a non-linear association with non-alcoholic fatty liver disease: a secondary prospective cohort study in non-obese Chinese adults","volume":"9","author":"Li","year":"2022","journal-title":"Front Med"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1186\/s12876-022-02598-y","article-title":"Assessing the longitudinal association between the GGT\/HDL-C ratio and NAFLD: a cohort study in a non-obese Chinese population","volume":"22","author":"Xie","year":"2022","journal-title":"BMC Gastroenterol"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"634","DOI":"10.21037\/atm-19-4516","article-title":"Association between ratio of \u03b3-glutamyl transpeptidase to high-density lipoprotein cholesterol and prevalence of non-alcoholic fatty liver disease and metabolic syndrome: a cross-sectional study","volume":"8","author":"Feng","year":"2020","journal-title":"Ann Transl Med"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"383","DOI":"10.2147\/DMSO.S342505","article-title":"Associations between GGT\/HDL and MAFLD: a cross-sectional study","volume":"15","author":"Xing","year":"2022","journal-title":"Diabetes Metab Syndr Obes"}],"container-title":["Frontiers in Medicine"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2025.1510679\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,28]],"date-time":"2025-03-28T07:12:58Z","timestamp":1743145978000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2025.1510679\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,28]]},"references-count":41,"alternative-id":["10.3389\/fmed.2025.1510679"],"URL":"https:\/\/doi.org\/10.3389\/fmed.2025.1510679","relation":{},"ISSN":["2296-858X"],"issn-type":[{"type":"electronic","value":"2296-858X"}],"subject":[],"published":{"date-parts":[[2025,3,28]]},"article-number":"1510679"}}