{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T05:10:29Z","timestamp":1789189829266,"version":"build-2803163510"},"reference-count":43,"publisher":"Japanese Society for Magnetic Resonance in Medicine","issue":"4","funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP23K14871"],"award-info":[{"award-number":["JP23K14871"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["MRMS","magn reson med sci"],"published-print":{"date-parts":[[2026]]},"DOI":"10.2463\/mrms.mp.2026-0041","type":"journal-article","created":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T22:12:13Z","timestamp":1789164733000},"page":"n\/a","source":"Crossref","is-referenced-by-count":0,"title":["Multi-pool Model\u2013based Amide Proton Transfer Imaging for Tumor Characterization and Risk Stratification in Endometrial Carcinoma"],"prefix":"10.2463","volume":"25","author":[{"given":"Yasukage","family":"Takami","sequence":"first","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takashi","family":"Norikane","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenichi","family":"Tanaka","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Riku","family":"Morita","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuri","family":"Manabe","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsumasa","family":"Murao","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katsuya","family":"Mitamura","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuka","family":"Yamamoto","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenji","family":"Kanenishi","sequence":"additional","affiliation":[{"name":"Department of Perinatology and Gynecology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsuharu","family":"Miyoshi","sequence":"additional","affiliation":[{"name":"GE HealthCare, Hino, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshihiro","family":"Nishiyama","sequence":"additional","affiliation":[{"name":"Department of Radiology, Faculty of Medicine, Kagawa University, Kita-gun, Kagawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1295","reference":[{"key":"1","doi-asserted-by":"crossref","unstructured":"1. Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2024; 74:229\u2013263.","DOI":"10.3322\/caac.21834"},{"key":"2","doi-asserted-by":"crossref","unstructured":"2. Lortet-Tieulent J, Ferlay J, Bray F, Jemal A. International patterns and trends in endometrial cancer incidence, 1978\u20132013. J Natl Cancer Inst 2018; 110:354\u2013361.","DOI":"10.1093\/jnci\/djx214"},{"key":"3","doi-asserted-by":"crossref","unstructured":"3. Berek JS, Matias-Guiu X, Creutzberg C, et al. FIGO staging of endometrial cancer: 2023. Int J Gynaecol Obstet 2023; 162:383\u2013394.","DOI":"10.1002\/ijgo.14923"},{"key":"4","doi-asserted-by":"crossref","unstructured":"4. Bosse T, Peters EEM, Creutzberg CL, et al. Substantial lymph-vascular space invasion (LVSI) is a significant risk factor for recurrence in endometrial cancer\u2014A pooled analysis of PORTEC 1 and 2 trials. Eur J Cancer 2015; 51:1742\u20131750.","DOI":"10.1016\/j.ejca.2015.05.015"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5. Morice P, Leary A, Creutzberg C, Abu-Rustum N, Darai E. Endometrial cancer. Lancet 2016; 387:1094\u20131108.","DOI":"10.1016\/S0140-6736(15)00130-0"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6. Concin N, Matias-Guiu X, Cibula D, et al. ESGO-ESTRO-ESP guidelines for the management of patients with endometrial carcinoma: Update 2025. Lancet Oncol 2025; 26:e423\u2013e435.","DOI":"10.1016\/S1470-2045(25)00167-6"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7. Morisada T, Kobayashi Y, Nagase S, et al. Japan Society of Gynecologic Oncology 2023 guidelines for treatment of uterine body neoplasm. J Gynecol Oncol 2025; 36:e119.","DOI":"10.3802\/jgo.2025.36.e119"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8. Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol 1983; 15:10\u201317.","DOI":"10.1016\/0090-8258(83)90111-7"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9. Creasman WT, Kohler MF, Odicino F, Maisonneuve P, Boyle P. Prognosis of papillary serous, clear cell, and grade 3 stage I carcinoma of the endometrium. Gynecol Oncol 2004; 95:593\u2013596.","DOI":"10.1016\/j.ygyno.2004.08.019"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10. Bak SE, Yoo JG, Lee SJ, Yoon JH, Park DC, Kim SI. Prognostic significance of histological grade in low-risk endometrial cancer. Int J Med Sci 2022; 19:1875\u20131878.","DOI":"10.7150\/ijms.77152"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11. Maheshwari E, Nougaret S, Stein EB, et al. Update on MRI in evaluation and treatment of endometrial cancer. Radiographics 2022; 42:2112\u20132130.","DOI":"10.1148\/rg.220070"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12. Rechichi G, Galimberti S, Signorelli M, et al. Endometrial cancer: Correlation of apparent diffusion coefficient with tumor grade, depth of myometrial invasion, and presence of lymph node metastases. AJR Am J Roentgenol 2011; 197:256\u2013262.","DOI":"10.2214\/AJR.10.5584"},{"key":"13","doi-asserted-by":"crossref","unstructured":"13. Wu B, Warnock G, Zaiss M, et al. An overview of CEST MRI for non-MR physicists. EJNMMI Phys 2016; 3:19.","DOI":"10.1186\/s40658-016-0155-2"},{"key":"14","doi-asserted-by":"crossref","unstructured":"14. Takayama Y, Nishie A, Togao O, et al. Amide proton transfer MR imaging of endometrioid endometrial adenocarcinoma: Association with histologic grade. Radiology 2018; 286:909\u2013917.","DOI":"10.1148\/radiol.2017170349"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15. Ochiai R, Mukuda N, Yunaga H, et al. Amide proton transfer imaging in differentiation of type II and type I endometrial carcinoma: A pilot study. Jpn J Radiol 2022; 40:184\u2013191.","DOI":"10.1007\/s11604-021-01197-3"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16. Meng X, Zhang X, Tian S, et al. Evaluation of lymphovascular space invasion in endometrial carcinoma by APTw and mDixon-Quant. Acta Radiol 2024; 65:1440\u20131446.","DOI":"10.1177\/02841851241277339"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17. Meng N, Fang T, Feng P, et al. Amide proton transfer-weighted imaging and multiple models diffusion-weighted imaging facilitates preoperative risk stratification of early-stage endometrial carcinoma. J Magn Reson Imaging 2021; 54:1200\u20131211.","DOI":"10.1002\/jmri.27684"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18. Sun PZ, Sorensen AG. Imaging pH using the chemical exchange saturation transfer (CEST) MRI: Correction of concomitant RF irradiation effects to quantify CEST MRI for chemical exchange rate and pH. Magn Reson Med 2008; 60:390\u2013397.","DOI":"10.1002\/mrm.21653"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19. van Zijl PCM, Lam WW, Xu J, Knutsson L, Stanisz GJ. Magnetization transfer contrast and chemical exchange saturation transfer MRI. Features and analysis of the field-dependent saturation spectrum. Neuroimage 2018; 168:222\u2013241.","DOI":"10.1016\/j.neuroimage.2017.04.045"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20. Paech D, Zaiss M, Meissner JE, et al. Nuclear Overhauser Enhancement mediated chemical exchange saturation transfer imaging at 7 Tesla in glioblastoma patients. PLoS One 2014; 9:e104181.","DOI":"10.1371\/journal.pone.0104181"},{"key":"21","doi-asserted-by":"crossref","unstructured":"21. Liu D, Zhou J, Xue R, Zuo Z, An J, Wang DJ. Quantitative characterization of nuclear overhauser enhancement and amide proton transfer effects in the human brain at 7 tesla. Magn Reson Med 2013; 70:1070\u20131081.","DOI":"10.1002\/mrm.24560"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22. Zhou IY, Wang E, Cheung JS, Zhang X, Fulci G, Sun PZ. Quantitative chemical exchange saturation transfer (CEST) MRI of glioma using Image Downsampling Expedited Adaptive Least-squares (IDEAL) fitting. Sci Rep 2017; 7:84.","DOI":"10.1038\/s41598-017-00167-y"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23. Takami Y, Norikane T, Kimura N, et al. Relationship between multi-pool model-based chemical exchange saturation transfer imaging, intravoxel incoherent motion MRI, and <sup>11<\/sup>C-methionine uptake on PET\/CT in patients with gliomas. Magn Reson Imaging 2024; 111:148\u2013156.","DOI":"10.1016\/j.mri.2024.05.007"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24. Takami Y, Norikane T, Kimura N, et al. Multi-pool model-based amide proton transfer imaging in grading of gliomas and evaluating tumor proliferation: Comparison to apparent diffusion coefficient and magnetization transfer ratio asymmetry. Magn Reson Imaging 2025; 123:110488.","DOI":"10.1016\/j.mri.2025.110488"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25. Kim M, Gillen J, Landman BA, Zhou J, van Zijl PC. Water saturation shift referencing (WASSR) for chemical exchange saturation transfer (CEST) experiments. Magn Reson Med 2009; 61:1441\u20131450.","DOI":"10.1002\/mrm.21873"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33:159\u2013174.","DOI":"10.2307\/2529310"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27. Hosmer DW, Lemeshow S, Sturdivant RX. Applied logistic regression. 3rd edn. Hoboken, New Jersey: Wiley &amp; Sons; 2013.","DOI":"10.1002\/9781118548387"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28. Meng N, Wang X, Sun J, et al. Evaluation of amide proton transfer-weighted imaging for endometrial carcinoma histological features: A comparative study with diffusion kurtosis imaging. Eur Radiol 2021; 31:8388\u20138398.","DOI":"10.1007\/s00330-021-07966-y"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29. Bryant RG. The dynamics of water-protein interactions. Annu Rev Biophys Biomol Struct 1996; 25:29\u201353.","DOI":"10.1146\/annurev.bb.25.060196.000333"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30. Persson E, Halle B. Cell water dynamics on multiple time scales. Proc Natl Acad Sci USA 2008; 105:6266\u20136271.","DOI":"10.1073\/pnas.0709585105"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31. Salama A, Arafa M, ElZahaf E, et al. Potential role for a panel of immunohistochemical markers in the management of endometrial carcinoma. J Pathol Transl Med 2019; 53:164\u2013172.","DOI":"10.4132\/jptm.2019.02.12"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32. Terlikowska KM, Dobrzycka B, Terlikowski R, Sienkiewicz A, Kinalski M, Terlikowski SJ. Clinical value of selected markers of angiogenesis, inflammation, insulin resistance and obesity in type 1 endometrial cancer. BMC Cancer 2020; 20:921.","DOI":"10.1186\/s12885-020-07415-x"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33. Abbink K, Zusterzeel PLM, Geurts-Moespot A, van der Steen R, Span PN, Sweep FCGJ. Prognostic significance of VEGF and components of the plasminogen activator system in endometrial cancer. J Cancer Res Clin Oncol 2020; 146:1725\u20131735.","DOI":"10.1007\/s00432-020-03225-7"},{"key":"34","doi-asserted-by":"crossref","unstructured":"34. Jin X, Yan R, Li Z, et al. Evaluation of amide proton transfer-weighted imaging for risk factors in stage I endometrial cancer: A comparison with diffusion-weighted imaging and diffusion kurtosis imaging. Front Oncol 2022; 12:876120.","DOI":"10.3389\/fonc.2022.876120"},{"key":"35","doi-asserted-by":"crossref","unstructured":"35. Zhao Y, Zhao F, Cheng M, et al. Risk stratification prediction of endometrial cancer using microstructural mapping based on time-dependent diffusion MRI. Cancer Sci 2025; 116:1627\u20131637.","DOI":"10.1111\/cas.70036"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36. Stefansson IM, Salvesen HB, Akslen LA. Vascular proliferation is important for clinical progress of endometrial cancer. Cancer Res 2006; 66:3303\u20133309.","DOI":"10.1158\/0008-5472.CAN-05-1163"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37. Bredholt G, Mannelqvist M, Stefansson IM, et al. Tumor necrosis is an important hallmark of aggressive endometrial cancer and associates with hypoxia, angiogenesis and inflammation responses. Oncotarget 2015; 6:39676\u201339691.","DOI":"10.18632\/oncotarget.5344"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38. Yan BC, Xiao ML, Li Y, Wei Qiang J. The diagnostic performance of ADC value for tumor grade, deep myometrial invasion and lymphovascular space invasion in endometrial cancer: A meta-analysis. Acta Radiol 2019; 60:284185119841988.","DOI":"10.1177\/0284185119841988"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39. Scepanovic B, Andjelic N, Mladenovic-Segedi L, et al. Diagnostic value of the apparent diffusion coefficient in differentiating malignant from benign endometrial lesions. Front Oncol 2023; 13:1109495.","DOI":"10.3389\/fonc.2023.1109495"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: Applications and challenges in oncology. AJR Am J Roentgenol 2007; 188:1622\u20131635.","DOI":"10.2214\/AJR.06.1403"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41. Bharwani N, Miquel ME, Sahdev A, et al. Diffusion-weighted imaging in the assessment of tumour grade in endometrial cancer. Br J Radiol 2011; 84:997\u20131004.","DOI":"10.1259\/bjr\/14980811"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42. Rau TT, Bettschen E, B\u00fcchi C, et al. Prognostic impact of tumor budding in endometrial carcinoma within distinct molecular subgroups. Mod Pathol 2021; 34:222\u2013232.","DOI":"10.1038\/s41379-020-0626-9"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43. Ak\u00e7ay A, G\u00fcltekin MA, Alt\u0131nta\u015f F, et al. Updated endometrial cancer FIGO staging: The role of MRI in determining newly included histopathological criteria. Abdom Radiol (NY) 2024; 49:3711\u20133721.","DOI":"10.1007\/s00261-024-04398-2"}],"container-title":["Magnetic Resonance in Medical Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/mrms\/25\/4\/25_mp.2026-0041\/_pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T05:02:56Z","timestamp":1789189376000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/mrms\/25\/4\/25_mp.2026-0041\/_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026]]},"references-count":43,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2026]]}},"URL":"https:\/\/doi.org\/10.2463\/mrms.mp.2026-0041","relation":{},"ISSN":["1347-3182","1880-2206"],"issn-type":[{"value":"1347-3182","type":"print"},{"value":"1880-2206","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026]]},"article-number":"mp.2026-0041"}}