{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T09:24:37Z","timestamp":1787304277108,"version":"build-2736575974"},"reference-count":34,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T00:00:00Z","timestamp":1787270400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J. Clin. Med.","JCM"],"abstract":"<jats:p>Objective: In ulcerative colitis (UC), endoscopic assessment remains central to disease monitoring, but repeated colonoscopy is invasive and resource-intensive. This study evaluated the association and discriminatory performance of the systemic immune\u2013inflammation index (SII; platelet \u00d7 neutrophil\/lymphocyte) and the hemoglobin\u2013albumin\u2013lymphocyte\u2013platelet (HALP; hemoglobin \u00d7 albumin \u00d7 lymphocyte\/platelet) score for endoscopic activity in UC and explored whether azathioprine use modified these associations. Methods: Among 428 retrospectively reviewed patients with UC, 218 met the inclusion criteria. Mayo-defined activity (endoscopic score \u2265 2) and Rachmilewitz EAI-defined activity (score \u2265 4) were analyzed as separate outcomes. Laboratory parameters were compared between active disease and remission groups. Receiver operating characteristic (ROC) analyses, multivariable logistic regression, sensitivity analyses accounting for disease duration and treatment category, and azathioprine interaction analyses were performed. Results: According to the Mayo and Rachmilewitz EAI definitions, 80 (36.7%) and 150 (68.8%) patients, respectively, had active disease. For Mayo-defined activity, CRP showed the highest discrimination (AUC = 0.720), followed by SII (AUC = 0.692), whereas HALP showed limited discrimination (AUC = 0.598). In the primary multivariable Mayo model, CRP, SII, younger age, and male sex were independently associated with activity, whereas HALP and azathioprine use were not. Adding SII to CRP produced only a small numerical increase in AUC (0.720 to 0.752), and adding HALP produced essentially no further change. No significant interaction between azathioprine use and SII or HALP was identified. Conclusion: SII was associated with endoscopic activity but showed only modest discriminatory performance, while HALP had limited discriminatory and independent predictive value. CRP remained the strongest individual biomarker. SII and HALP should therefore be interpreted as adjunctive inflammatory indices rather than substitutes for established biomarkers or endoscopic assessment.<\/jats:p>","DOI":"10.3390\/jcm15166464","type":"journal-article","created":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T08:14:01Z","timestamp":1787300041000},"page":"6464","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Endoscopic Activity Prediction in Ulcerative Colitis Using Hemogram-Derived Inflammatory Indices: Impact of Azathioprine Use on Diagnostic Performance"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7514-1962","authenticated-orcid":false,"given":"Muhammed","family":"Kaya","sequence":"first","affiliation":[{"name":"Department of Gastroenterology, Hitit University Corum Erol Olcok Training and Research Hospital, 19040 Corum, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3857-1648","authenticated-orcid":false,"given":"G\u00f6khan","family":"Evren","sequence":"additional","affiliation":[{"name":"Department of Nephrology, Faculty of Medicine, Uluda\u011f University, 16240 Bursa, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9032-0977","authenticated-orcid":false,"given":"\u0130brahim","family":"Durak","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Faculty of Medicine, Hitit University, 19030 Corum, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6279-1018","authenticated-orcid":false,"given":"Tolga","family":"D\u00fczenli","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Faculty of Medicine, Samsun University, 55080 Samsun, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2197-7473","authenticated-orcid":false,"given":"H\u00fcseyin","family":"K\u00f6seo\u011flu","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Faculty of Medicine, Samsun University, 55080 Samsun, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3443-1987","authenticated-orcid":false,"given":"Mustafa","family":"Sade\u00e7olak","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology, Faculty of Medicine, Hitit University, 19030 Corum, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1016\/j.crohns.2012.09.003","article-title":"Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 1: Definitions and diagnosis","volume":"6","author":"Dignass","year":"2012","journal-title":"J. Crohn\u2019s Colitis"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1136\/gutjnl-2015-309598","article-title":"Beyond endoscopic mucosal healing in UC: Histological remission better predicts corticosteroid use and hospitalisation over 6 years of follow-up","volume":"65","author":"Bryant","year":"2016","journal-title":"Gut"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1053\/j.gastro.2020.12.031","article-title":"STRIDE-II: An Update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): Determining Therapeutic Goals for Treat-to-Target strategies in IBD","volume":"160","author":"Turner","year":"2021","journal-title":"Gastroenterology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1093\/ecco-jcc\/jjz131","article-title":"Outcomes and Strategies to Support a Treat-to-target Approach in Inflammatory Bowel Disease: A Systematic Review","volume":"14","author":"Colombel","year":"2020","journal-title":"J. Crohn\u2019s Colitis"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1038\/ajg.2015.233","article-title":"Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): Determining Therapeutic Goals for Treat-to-Target","volume":"110","author":"Sandborn","year":"2015","journal-title":"Am. J. Gastroenterol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"17562848241251600","DOI":"10.1177\/17562848241251600","article-title":"Biomarkers in inflammatory bowel disease: A practical guide","volume":"17","author":"Clough","year":"2024","journal-title":"Ther. Adv. Gastroenterol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2218","DOI":"10.1002\/ibd.22917","article-title":"Fecal calprotectin is a surrogate marker for endoscopic lesions in inflammatory bowel disease","volume":"18","author":"Ferrante","year":"2012","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_8","first-page":"176","article-title":"Assessment of disease activity in ulcerative colitis by faecal calprotectin, a novel granulocyte marker protein","volume":"58","author":"Aadland","year":"1997","journal-title":"Digestion"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1136\/gutjnl-2019-318343","article-title":"A blood-based prognostic biomarker in IBD","volume":"68","author":"Biasci","year":"2019","journal-title":"Gut"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"710915","DOI":"10.1155\/2014\/710915","article-title":"Biomarkers of inflammatory bowel disease","volume":"2014","author":"Fengming","year":"2014","journal-title":"Dis. Markers"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"6212","DOI":"10.1158\/1078-0432.CCR-14-0442","article-title":"Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma","volume":"20","author":"Hu","year":"2014","journal-title":"Clin. Cancer Res."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Li, P., Wu, Y., Xiong, W., Cao, J., Chen, M., Yuan, Z., Guo, W., and Yang, B. (2025). Association between the immune-inflammation index and the severity and clinical outcomes of patients with inflammatory bowel disease: A systematic review and meta-analysis. BMC Gastroenterol., 25.","DOI":"10.1186\/s12876-025-04033-4"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e35197","DOI":"10.1097\/MD.0000000000035197","article-title":"The relationship between neutrophil lymphocyte ratio, platelet lymphocyte ratio, and depression in dialysis patients","volume":"102","author":"Tutan","year":"2023","journal-title":"Medicine"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"109496","DOI":"10.1016\/j.intimp.2022.109496","article-title":"Hemoglobin, albumin, lymphocyte, and platelet (HALP) score and cancer prognosis: A systematic review and meta-analysis of 13,110 patients","volume":"114","author":"Xu","year":"2023","journal-title":"Int. Immunopharmacol."},{"key":"ref_15","first-page":"2514","article-title":"A new index for predicting malignant causes in patients with extrahepatic biliary obstruction: The hemoglobin, albumin, lymphocyte, and platelet (HALP) score","volume":"27","author":"Eskin","year":"2023","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"334","DOI":"10.12998\/wjcc.v9.i2.334","article-title":"Effective immune-inflammation index for ulcerative colitis and activity assessments","volume":"9","author":"Zhang","year":"2021","journal-title":"World J. Clin. Cases"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1080\/03007995.2024.2316860","article-title":"Association between pan-immune inflammatory value and ulcerative colitis","volume":"40","year":"2024","journal-title":"Curr. Med. Res. Opin."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lin, H., Bai, Z., Wu, Q., Chu, G., Zhang, Y., Guo, X., and Qi, X. (2022). Inflammatory Indexes for Assessing the Severity and Disease Progression of Ulcerative Colitis: A Single-Center Retrospective Study. Front. Public Health, 10.","DOI":"10.3389\/fpubh.2022.851295"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"9987214","DOI":"10.1155\/2022\/9987214","article-title":"Serum Immune-Inflammation Index Assessment in the Patients with Ulcerative Colitis","volume":"2022","author":"Pakoz","year":"2022","journal-title":"Gastroenterol. Res. Pract."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Yan, J., Wu, J., Wang, R., Meng, P., Liu, A., and Xu, Y. (2025). The systemic immune-inflammation index is superior to predicting clinical remission and relapse for ulcerative colitis patients treated with vedolizumab. Front. Med., 12.","DOI":"10.3389\/fmed.2025.1524307"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.cca.2021.02.016","article-title":"Elevated systemic immune inflammation index level is associated with disease activity in ulcerative colitis patients","volume":"517","author":"Xie","year":"2021","journal-title":"Clin. Chim. Acta"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.gande.2024.10.003","article-title":"Systemic immune-inflammation index: Unveiling the diagnostic potential in ulcerative colitis through a comprehensive systematic review and meta-analysis","volume":"3","author":"Elgenidy","year":"2025","journal-title":"Gastroenterol. Endosc."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"502662","DOI":"10.1016\/j.gastrohep.2026.502662","article-title":"Unveiling hidden malnutrition in IBD: A cross-sectional multi-tool analysis reveals high prevalence beyond weight-based assessment","volume":"49","author":"Fissah","year":"2026","journal-title":"Gastroenterol. Hepatol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1136\/bmj.298.6666.82","article-title":"Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis: A randomised trial","volume":"298","author":"Rachmilewitz","year":"1989","journal-title":"BMJ"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2188","DOI":"10.1016\/j.cgh.2024.06.048","article-title":"AGA Clinical Practice Update on Endoscopic Scoring Systems in Inflammatory Bowel Disease: Commentary","volume":"22","author":"Buchner","year":"2024","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1136\/gut.2005.082909","article-title":"The Montreal classification of inflammatory bowel disease: Controversies, consensus, and implications","volume":"55","author":"Satsangi","year":"2006","journal-title":"Gut"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"29","DOI":"10.21037\/jlpm.2018.03.04","article-title":"Prognostic value of systemic immune-inflammation index (SII) in cancers: A systematic review and meta-analysis","volume":"3","author":"Tang","year":"2018","journal-title":"J. Lab. Precis. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1007\/s10238-024-01294-3","article-title":"The diagnostic role of the systemic inflammation index in patients with immunological diseases: A systematic review and meta-analysis","volume":"24","author":"Mangoni","year":"2024","journal-title":"Clin. Exp. Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"153","DOI":"10.18632\/oncotarget.28367","article-title":"What is hemoglobin, albumin, lymphocyte, platelet (HALP) score? A comprehensive literature review of HALP\u2019s prognostic ability in different cancer types","volume":"14","author":"Farag","year":"2023","journal-title":"Oncotarget"},{"key":"ref_30","first-page":"e24874","article-title":"Use of Azathioprine in Ulcerative Colitis: A Comprehensive Review","volume":"14","author":"Mallick","year":"2022","journal-title":"Cureus"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1783","DOI":"10.1111\/j.1572-0241.2008.01848.x","article-title":"Thiopurine-induced myelotoxicity in patients with inflammatory bowel disease: A review","volume":"103","author":"Gisbert","year":"2008","journal-title":"Am. J. Gastroenterol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1097\/MIB.0b013e318281f28f","article-title":"Safety of thiopurine therapy in inflammatory bowel disease: Long-term follow-up study of 3931 patients","volume":"19","author":"Chaparro","year":"2013","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1159\/000253850","article-title":"Do patients with ulcerative colitis diagnosed at a young age have more severe disease activity than patients diagnosed when older?","volume":"81","author":"Lee","year":"2010","journal-title":"Digestion"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2402","DOI":"10.1007\/s10620-012-2081-z","article-title":"Association of age at diagnosis and ulcerative colitis phenotype","volume":"57","author":"Quezada","year":"2012","journal-title":"Dig. Dis. Sci."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/15\/16\/6464\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,21]],"date-time":"2026-08-21T08:34:37Z","timestamp":1787301277000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/15\/16\/6464"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,21]]},"references-count":34,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2026,8]]}},"alternative-id":["jcm15166464"],"URL":"https:\/\/doi.org\/10.3390\/jcm15166464","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,21]]}}}