{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T12:03:55Z","timestamp":1790597035647,"version":"4.1.0"},"reference-count":43,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T00:00:00Z","timestamp":1790208000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Background\/Objectives: Sarcopenia predicts increased morbidity and mortality in gastrointestinal (GI) cancer. This study evaluated the longitudinal association between changes in the skeletal muscle index (SMI) and serum procollagen type III N-terminal peptide (PIIINP), together with sarcopenia and malnutrition screening tools (SARC-F, SARC-CalF, MUST), during chemotherapy for GI cancer. Methods: In this prospective single-center study, 170 patients with GI cancer were assessed at baseline and month 6; 48 died, and longitudinal analyses included the 122 survivors. SMI was derived from bioelectrical impedance analysis (Tanita SC-330) using the Janssen equation, and serum PIIINP was measured at both time points. The primary endpoint was the association between the percentage changes in SMI and PIIINP. Results: BMI, SMI, and handgrip strength decreased and SARC-F and SARC-CalF scores increased significantly (all p &lt; 0.001); the prevalence of low muscle mass rose from 29% to 52%, and PIIINP increased significantly. The percentage changes in SMI and PIIINP were strongly inversely correlated (\u03c1 = \u22120.733, p &lt; 0.001). In the parsimonious multivariable model, the percentage change in PIIINP (\u03b2 = \u22120.47) and month-6 albumin (\u03b2 = 0.31) were independently associated with the change in SMI (R2 = 0.37); the albumin association was model-dependent and not retained in the expanded model. Conclusions: In patients with GI cancer receiving chemotherapy, progressive muscle loss over six months was accompanied by a rise in the circulating collagen turnover marker PIIINP. Because the study was observational, restricted to survivors, and based on a non-muscle-specific marker, causal and muscle-specific inferences are unwarranted; PIIINP nonetheless merits further evaluation as a monitoring biomarker.<\/jats:p>","DOI":"10.3390\/nu18193149","type":"journal-article","created":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T13:26:11Z","timestamp":1790256371000},"page":"3149","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Longitudinal Association Between the Change in Serum Procollagen Type III N-Terminal Peptide (PIIINP) and Skeletal Muscle Loss in Patients with Gastrointestinal Cancer Receiving Chemotherapy: A Prospective Cohort Study"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-1715-0230","authenticated-orcid":false,"given":"Mehmet Erdin\u00e7","family":"Esenkaya","sequence":"first","affiliation":[{"name":"Department of Medical Oncology, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2520-5953","authenticated-orcid":false,"given":"\u00d6zlem","family":"\u00d6zdemir","sequence":"additional","affiliation":[{"name":"Department of Medical Oncology, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6988-9205","authenticated-orcid":false,"given":"Mustafa","family":"De\u011firmenci","sequence":"additional","affiliation":[{"name":"Department of Medical Oncology, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0888-9177","authenticated-orcid":false,"given":"Kaan","family":"Kuzu","sequence":"additional","affiliation":[{"name":"Department of Medical Biochemistry, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-4347-263X","authenticated-orcid":false,"given":"K\u00fcbra","family":"Ekiz Seyhan","sequence":"additional","affiliation":[{"name":"Department of Medical Biochemistry, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8474-6763","authenticated-orcid":false,"given":"G\u00fcrkan","family":"G\u00fcl","sequence":"additional","affiliation":[{"name":"Department of Medical Oncology, Izmir City Hospital, Izmir 35540, T\u00fcrkiye"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1093\/ageing\/afy169","article-title":"Sarcopenia: Revised European Consensus on Definition and Diagnosis","volume":"48","author":"Bahat","year":"2019","journal-title":"Age Ageing"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/j.jamda.2019.12.012","article-title":"Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment","volume":"21","author":"Chen","year":"2020","journal-title":"J. Am. Med. Dir. Assoc."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Emori, T., Itonaga, M., Ashida, R., and Kitano, M. (2025). Sarcopenia in Gastrointestinal Cancers. Int. J. Clin. Oncol., 30.","DOI":"10.1007\/s10147-025-02915-x"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1016\/j.clnu.2017.07.010","article-title":"Prevalence and Predictive Value of Pre-Therapeutic Sarcopenia in Cancer Patients: A Systematic Review","volume":"37","author":"Pamoukdjian","year":"2018","journal-title":"Clin. Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"7964","DOI":"10.1002\/cam4.3428","article-title":"Sarcopenia and Adverse Health-related Outcomes: An Umbrella Review of Meta-analyses of Observational Studies","volume":"9","author":"Xia","year":"2020","journal-title":"Cancer Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.ejca.2015.12.030","article-title":"Prognostic Value of Sarcopenia in Adults with Solid Tumours: A Meta-Analysis and Systematic Review","volume":"57","author":"Shachar","year":"2016","journal-title":"Eur. J. Cancer"},{"key":"ref_7","first-page":"207","article-title":"GLIM Criteria for the Diagnosis of Malnutrition\u2014A Consensus Report from the Global Clinical Nutrition Community","volume":"10","author":"Cederholm","year":"2019","journal-title":"Clin. Nutr."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S1470-2045(10)70218-7","article-title":"Definition and Classification of Cancer Cachexia: An International Consensus","volume":"12","author":"Fearon","year":"2011","journal-title":"Lancet Oncol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"C241","DOI":"10.1152\/ajpcell.00173.2013","article-title":"Cellular Mechanisms of Tissue Fibrosis. 4. Structural and Functional Consequences of Skeletal Muscle Fibrosis","volume":"305","author":"Lieber","year":"2013","journal-title":"Am. J. Physiol.-Cell Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"C1283","DOI":"10.1152\/ajpcell.00448.2025","article-title":"Profibrotic Immune Cells and Fibro-Adipogenic Progenitors Contribute to Skeletal Muscle Extracellular Matrix Remodeling and Fibrosis in Cancer Cachexia","volume":"329","author":"Cardaci","year":"2025","journal-title":"Am. J. Physiol.-Cell Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1002\/jcsm.12441","article-title":"Tumour-derived Transforming Growth Factor-\u03b2 Signalling Contributes to Fibrosis in Patients with Cancer Cachexia","volume":"10","author":"Lima","year":"2019","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"694","DOI":"10.12968\/hmed.2018.79.12.694","article-title":"The Enhanced Liver Fibrosis (ELF) Test in Diagnosis and Management of Liver Fibrosis","volume":"79","author":"Day","year":"2018","journal-title":"Br. J. Hosp. Med."},{"key":"ref_13","first-page":"687","article-title":"Effect of Muscle Mass on Toxicity and Survival in Patients with Colon Cancer Undergoing Adjuvant Chemotherapy","volume":"23","author":"Jung","year":"2015","journal-title":"Support. Care Cancer"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1002\/jcsm.12916","article-title":"Prognostic Utility of Self-reported Sarcopenia (SARC-F) in the Multiethnic Cohort","volume":"13","author":"Wu","year":"2022","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"E149","DOI":"10.1519\/JPT.0000000000000420","article-title":"Appendicular Skeletal Muscle Mass in Older Adults Can Be Estimated With a Simple Equation Using a Few Zero-Cost Variables","volume":"47","author":"Buccheri","year":"2024","journal-title":"J. Geriatr. Phys. Ther."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1430","DOI":"10.1016\/j.clnu.2004.09.012","article-title":"Bioelectrical Impedance Analysis\u2014Part II: Utilization in Clinical Practice","volume":"23","author":"Kyle","year":"2004","journal-title":"Clin. Nutr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1002\/jcsm.12871","article-title":"Validation of a Proxy-reported SARC-F Questionnaire for Current and Retrospective Screening of Sarcopenia-related Functional Impairments","volume":"13","author":"Maurus","year":"2022","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1093\/ajcn\/nqy244","article-title":"Validated Screening Tools for the Assessment of Cachexia, Sarcopenia, and Malnutrition: A Systematic Review","volume":"108","author":"Miller","year":"2018","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1016\/j.jamda.2016.08.004","article-title":"Enhancing SARC-F: Improving Sarcopenia Screening in the Clinical Practice","volume":"17","author":"Menezes","year":"2016","journal-title":"J. Am. Med. Dir. Assoc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1017\/S000711451100571X","article-title":"Validation of the Malnutrition Universal Screening Tool (MUST) in Cancer","volume":"108","author":"Camilo","year":"2012","journal-title":"Br. J. Nutr."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1093\/gerona\/glaa197","article-title":"Circulating Procollagen Type III N-Terminal Peptide and Physical Function in Adults from the Long Life Family Study","volume":"76","author":"Santanasto","year":"2021","journal-title":"J. Gerontol. Ser. A"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1007\/s11357-023-00894-3","article-title":"Muscle Quality, Physical Performance, and Comorbidity Are Predicted by Circulating Procollagen Type III N-Terminal Peptide (P3NP): The InCHIANTI Follow-up Study","volume":"46","author":"Pellegrino","year":"2023","journal-title":"GeroScience"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"111523","DOI":"10.1016\/j.exger.2021.111523","article-title":"Association between Plasma Procollagen Type III N-Terminal Peptide (P3NP) Levels and Physical Performance in Elderly Men: The Korean Frailty and Aging Cohort Study (KFACS)","volume":"154","author":"Shin","year":"2021","journal-title":"Exp. Gerontol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"151","DOI":"10.21614\/chirurgia.3291","article-title":"Serum Biomarkers and CT-Derived Muscle Indices in Sarcopenia Associated with Pancreatic Neoplasm: A Comparative Clinical Study","volume":"121","author":"Gherghescu","year":"2026","journal-title":"Chirurgia"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1002\/cam4.2787","article-title":"Loss of Skeletal Muscle Index and Survival in Patients with Metastatic Colorectal Cancer: Secondary Analysis of the Phase 3 CAIRO3 Trial","volume":"9","author":"Kurk","year":"2020","journal-title":"Cancer Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/S0140-6736(07)61602-X","article-title":"The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for Reporting Observational Studies","volume":"370","author":"Altman","year":"2007","journal-title":"Lancet"},{"key":"ref_27","unstructured":"Amin, M.B., American Joint Committee on Cancer, and American Cancer Society (2017). AJCC Cancer Staging Manual, Springer. [8th ed.]."},{"key":"ref_28","unstructured":"World Health Organization (2000). Obesity: Preventing and Managing the Global Epidemic: Report of a WHO Consultation, World Health Organization."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1016\/j.clnu.2004.06.004","article-title":"Bioelectrical Impedance Analysis\u2014Part I: Review of Principles and Methods","volume":"23","author":"Kyle","year":"2004","journal-title":"Clin. Nutr."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1152\/jappl.2000.89.2.465","article-title":"Estimation of Skeletal Muscle Mass by Bioelectrical Impedance Analysis","volume":"89","author":"Janssen","year":"2000","journal-title":"J. Appl. Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1093\/aje\/kwh058","article-title":"Skeletal Muscle Cutpoints Associated with Elevated Physical Disability Risk in Older Men and Women","volume":"159","author":"Janssen","year":"2004","journal-title":"Am. J. Epidemiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.jamda.2013.05.018","article-title":"SARC-F: A Simple Questionnaire to Rapidly Diagnose Sarcopenia","volume":"14","author":"Malmstrom","year":"2013","journal-title":"J. Am. Med. Dir. Assoc."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1007\/s12603-018-1072-y","article-title":"Comparing SARC-F with SARC-CalF to Screen Sarcopenia in Community Living Older Adults","volume":"22","author":"Bahat","year":"2018","journal-title":"J. Nutr. Health Aging"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1038\/sj.bjc.6606087","article-title":"An Inflammation-Based Prognostic Score (mGPS) Predicts Cancer Survival Independent of Tumour Site: A Glasgow Inflammation Outcome Study","volume":"104","author":"Proctor","year":"2011","journal-title":"Br. J. Cancer"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B Stat. Methodol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1007\/s00441-018-2955-2","article-title":"Skeletal Muscle Fibrosis: An Overview","volume":"375","author":"Mahdy","year":"2019","journal-title":"Cell Tissue Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4224","DOI":"10.1210\/jc.2009-1434","article-title":"N-Terminal Propeptide of Type III Procollagen as a Biomarker of Anabolic Response to Recombinant Human GH and Testosterone","volume":"94","author":"Bhasin","year":"2009","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1007\/s13539-013-0120-z","article-title":"Biomarkers of Muscle Quality: N-terminal Propeptide of Type III Procollagen and C-terminal Agrin Fragment Responses to Resistance Exercise Training in Older Adults","volume":"5","author":"Fragala","year":"2014","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2889","DOI":"10.1016\/j.clnu.2019.12.024","article-title":"Comparison of the Prognostic Value of ECOG-PS, mGPS and BMI\/WL: Implications for a Clinically Important Framework in the Assessment and Treatment of Advanced Cancer","volume":"39","author":"Dolan","year":"2020","journal-title":"Clin. Nutr."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1186\/1475-2891-9-69","article-title":"Pretreatment Serum Albumin as a Predictor of Cancer Survival: A Systematic Review of the Epidemiological Literature","volume":"9","author":"Gupta","year":"2010","journal-title":"Nutr. J."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Izzo, A., Massimino, E., Riccardi, G., and Della Pepa, G. (2021). A Narrative Review on Sarcopenia in Type 2 Diabetes Mellitus: Prevalence and Associated Factors. Nutrients, 13.","DOI":"10.3390\/nu13010183"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2163","DOI":"10.1016\/j.biocel.2013.05.036","article-title":"Glucocorticoid-Induced Skeletal Muscle Atrophy","volume":"45","author":"Schakman","year":"2013","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"7587","DOI":"10.4081\/ejtm.2018.7587","article-title":"Chemotherapy-Induced Muscle Wasting: An Update","volume":"28","author":"Coletti","year":"2018","journal-title":"Eur. J. Transl. Myol."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/18\/19\/3149\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T11:47:59Z","timestamp":1790596079000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/18\/19\/3149"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,24]]},"references-count":43,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2026,10]]}},"alternative-id":["nu18193149"],"URL":"https:\/\/doi.org\/10.3390\/nu18193149","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,24]]}}}