The potential of an artificial intelligence for diagnosing MRI images in rectal cancer: multicenter collaborative trial.

Artificial intelligence MRI Rectal cancer

Journal

Journal of gastroenterology
ISSN: 1435-5922
Titre abrégé: J Gastroenterol
Pays: Japan
ID NLM: 9430794

Informations de publication

Date de publication:
31 Jul 2024
Historique:
received: 24 04 2024
accepted: 20 06 2024
medline: 1 8 2024
pubmed: 1 8 2024
entrez: 31 7 2024
Statut: aheadofprint

Résumé

An artificial intelligence-based algorithm we developed, mrAI, satisfactorily segmented the rectal tumor, rectum, and mesorectum from MRI data of rectal cancer patients in an initial study. Herein, we aimed to validate mrAI using an independent dataset. We utilized MRI images collected in another nationwide research project, "Open versus Laparoscopic Surgery for Advanced Low Rectal Cancer Patients". MRIs from 467 cases with upfront surgery were utilized; six radiologists centralized the MRI evaluations. The diagnostic accuracies of mrAI and the radiologists for tumor depth were compared using pathologic diagnosis as a reference. For all cases, centralized diagnosis demonstrated 84.2% sensitivity, 37.7% specificity, and 73.7% accuracy; mrAI exhibited 70.6% sensitivity, 61.3% specificity, and 68.5% accuracy. After limiting MRIs to those acquired by a Philips scanner, with an inter-slice spacing of ≤ 6 mm-both conditions similar to those used in the development of mrAI-the performance of mrAI improved to 76.8% sensitivity, 76.7% specificity, and 76.7% accuracy, while the centralized diagnosis showed 81.8% sensitivity, 36.7% specificity, and 71.3% accuracy. Regarding relapse-free survival, the prognosis for tumors staged ≥ T3 was significantly worse than for tumors staged ≤ T2 (P = 0.0484) in the pathologic diagnosis. While no significant difference was observed between ≥ T3 and ≤ T2 tumors in the centralized diagnosis (P = 0.1510), the prognosis for ≥ T3 was significantly worse in the mrAI diagnosis (P = 0.0318). Proper imaging conditions for MRI can enhance the accuracy of mrAI, which has the potential to provide feedback to radiologists without overestimating tumor stage.

Sections du résumé

BACKGROUND BACKGROUND
An artificial intelligence-based algorithm we developed, mrAI, satisfactorily segmented the rectal tumor, rectum, and mesorectum from MRI data of rectal cancer patients in an initial study. Herein, we aimed to validate mrAI using an independent dataset.
METHODS METHODS
We utilized MRI images collected in another nationwide research project, "Open versus Laparoscopic Surgery for Advanced Low Rectal Cancer Patients". MRIs from 467 cases with upfront surgery were utilized; six radiologists centralized the MRI evaluations. The diagnostic accuracies of mrAI and the radiologists for tumor depth were compared using pathologic diagnosis as a reference.
RESULTS RESULTS
For all cases, centralized diagnosis demonstrated 84.2% sensitivity, 37.7% specificity, and 73.7% accuracy; mrAI exhibited 70.6% sensitivity, 61.3% specificity, and 68.5% accuracy. After limiting MRIs to those acquired by a Philips scanner, with an inter-slice spacing of ≤ 6 mm-both conditions similar to those used in the development of mrAI-the performance of mrAI improved to 76.8% sensitivity, 76.7% specificity, and 76.7% accuracy, while the centralized diagnosis showed 81.8% sensitivity, 36.7% specificity, and 71.3% accuracy. Regarding relapse-free survival, the prognosis for tumors staged ≥ T3 was significantly worse than for tumors staged ≤ T2 (P = 0.0484) in the pathologic diagnosis. While no significant difference was observed between ≥ T3 and ≤ T2 tumors in the centralized diagnosis (P = 0.1510), the prognosis for ≥ T3 was significantly worse in the mrAI diagnosis (P = 0.0318).
CONCLUSION CONCLUSIONS
Proper imaging conditions for MRI can enhance the accuracy of mrAI, which has the potential to provide feedback to radiologists without overestimating tumor stage.

Identifiants

pubmed: 39085490
doi: 10.1007/s00535-024-02133-8
pii: 10.1007/s00535-024-02133-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Bahadoer RR, Dijkstra EA, van Etten B, et al. Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol. 2021;22:29–42.
doi: 10.1016/S1470-2045(20)30555-6 pubmed: 33301740
Conroy T, Bosset J-F, Etienne P-L, et al. Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 2021;22:702–15.
doi: 10.1016/S1470-2045(21)00079-6 pubmed: 33862000
Jin J, Tang Y, Hu C, et al. Multicenter, randomized, phase III trial of short-term radiotherapy plus chemotherapy versus long-term chemoradiotherapy in locally advanced rectal cancer (STELLAR). J Clin Oncol. 2022;40:1681–92.
doi: 10.1200/JCO.21.01667 pubmed: 35263150 pmcid: 9113208
Birgisson H, Pahlman L, Gunnarsson U, Glimelius B. Swedish Rectal Cancer Trial G Adverse effects of preoperative radiation therapy for rectal cancer: long-term follow-up of the Swedish Rectal Cancer Trial. J Clin Oncol. 2005;23:8697–705.
doi: 10.1200/JCO.2005.02.9017 pubmed: 16314629
Rombouts AJM, Hugen N, Elferink MAG, et al. Incidence of second tumors after treatment with or without radiation for rectal cancer. Ann Oncol. 2017;28:535–40.
doi: 10.1093/annonc/mdw661 pubmed: 27993790
Glynne-Jones R, Wyrwicz L, Tiret E, et al. Rectal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up†. Ann Oncol. 2017;28:iv22–40.
doi: 10.1093/annonc/mdx224 pubmed: 28881920
Benson AB, Venook AP, Al-Hawary MM, et al. Rectal cancer, version 2.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2022;20:1139–67.
doi: 10.6004/jnccn.2022.0051 pubmed: 36240850
Hamabe A, Ishii M, Kamoda R, et al. Artificial intelligence–based technology for semi-automated segmentation of rectal cancer using high-resolution MRI. PLoS ONE. 2022;17:e0269931.
doi: 10.1371/journal.pone.0269931 pubmed: 35714069 pmcid: 9205476
Hida K, Okamura R, Sakai Y, et al. Open versus laparoscopic surgery for advanced low rectal cancer: a large, multicenter, propensity score matched cohort study in Japan. Ann Surg. 2018;268:318–24.
doi: 10.1097/SLA.0000000000002329 pubmed: 28628565
Hida K, Nishizaki D, Sumii A, et al. Prognostic impact of lateral pelvic node dissection on the survival of patients in low rectal cancer subgroups based on lymph node size. Ann Surg Oncol. 2021;28:6179–88.
doi: 10.1245/s10434-021-10312-7 pubmed: 34255243
Sumii A, Hida K, Sakai Y, et al. Establishment and validation of a nomogram for predicting potential lateral pelvic lymph node metastasis in low rectal cancer. Int J Clin Oncol. 2022;27:1173–9.
doi: 10.1007/s10147-022-02157-1 pubmed: 35415787
Rouleau Fournier F, Motamedi MAK, Brown CJ, et al. Oncologic outcomes associated with MRI-detected extramural venous invasion (mrEMVI) in rectal cancer: a systematic review and meta-analysis. Ann Surg. 2022;275:303–14.
doi: 10.1097/SLA.0000000000004636 pubmed: 33491979
Chen S, Li N, Tang Y, et al. The prognostic value of MRI-detected extramural vascular invasion (mrEMVI) for rectal cancer patients treated with neoadjuvant therapy: a meta-analysis. Eur Radiol. 2021;31:8827–37.
doi: 10.1007/s00330-021-07981-z pubmed: 33993333
Birbeck KF, Macklin CP, Tiffin NJ, et al. Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg. 2002;235:449–57.
doi: 10.1097/00000658-200204000-00001 pubmed: 11923599 pmcid: 1422458
Group MS. Extramural depth of tumor invasion at thin-section MR in patients with rectal cancer: results of the MERCURY study. Radiology. 2007;243:132–9.
doi: 10.1148/radiol.2431051825
Burton S, Brown G, Daniels I, et al. MRI identified prognostic features of tumors in distal sigmoid, rectosigmoid, and upper rectum: treatment with radiotherapy and chemotherapy. J Radiat Oncol Biol Phys. 2006;65:445–51.
doi: 10.1016/j.ijrobp.2005.12.027
Kim H, Lim JS, Choi JY, et al. Rectal cancer: comparison of accuracy of local-regional staging with two- and three-dimensional preoperative 3-T MR imaging. Radiology. 2010;254:485–92.
doi: 10.1148/radiol.09090587 pubmed: 20093520
Akasu T, Iinuma G, Takawa M, Yamamoto S, Muramatsu Y, Moriyama N. Accuracy of high-resolution magnetic resonance imaging in preoperative staging of rectal cancer. Ann Surg Oncol. 2009;16:2787–94.
doi: 10.1245/s10434-009-0613-3 pubmed: 19618244
Al-Sukhni E, Milot L, Fruitman M, et al. Diagnostic accuracy of MRI for assessment of T category, lymph node metastases, and circumferential resection margin involvement in patients with rectal cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2012;19:2212–23.
doi: 10.1245/s10434-011-2210-5 pubmed: 22271205
Hashiguchi Y, Muro K, Saito Y, et al. Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020;25:1–42.
doi: 10.1007/s10147-019-01485-z pubmed: 31203527
Watanabe J, Kagawa Y, Chida K, et al. Phase III trial of short-course radiotherapy followed by CAPOXIRI versus CAPOX in locally advanced rectal cancer: the ENSEMBLE trial. ESMO Gastrointest Oncol. 2023;1:9–14.
doi: 10.1016/j.esmogo.2023.08.002
Moreno CC, Sullivan PS, Mittal PK. MRI evaluation of rectal cancer: staging and restaging. Curr Probl Diagn Radiol. 2017;46:234–41.
doi: 10.1067/j.cpradiol.2016.11.011 pubmed: 28089690
Taylor FG, Quirke P, Heald RJ, et al. Preoperative magnetic resonance imaging assessment of circumferential resection margin predicts disease-free survival and local recurrence: 5-year follow-up results of the MERCURY study. J Clin Oncol. 2014;32:34–43.
doi: 10.1200/JCO.2012.45.3258 pubmed: 24276776
Wong C, Fu Y, Li M, et al. MRI-based artificial intelligence in rectal cancer. J Magn Reson Imaging. 2023;57:45–56.
doi: 10.1002/jmri.28381 pubmed: 35993550
Takemasa I, Hamabe A, Miyo M, Akizuki E, Okuya K. Essential updates 2020/2021: advancing precision medicine for comprehensive rectal cancer treatment. Ann Gastroenterol Surg. 2022;7:198–215.
doi: 10.1002/ags3.12646 pubmed: 36998300 pmcid: 10043777
Smith NJ, Barbachano Y, Norman AR, Swift RI, Abulafi AM, Brown G. Prognostic significance of magnetic resonance imaging-detected extramural vascular invasion in rectal cancer. Br J Surg. 2008;95:229–36.
doi: 10.1002/bjs.5917 pubmed: 17932879
Brown G, Richards CJ, Bourne MW, et al. Morphologic predictors of lymph node status in rectal cancer with use of high-spatial-resolution MR imaging with histopathologic comparison. Radiology. 2003;227:371–7.
doi: 10.1148/radiol.2272011747 pubmed: 12732695
Lord AC, D’Souza N, Shaw A, et al. MRI-Diagnosed tumour deposits and EMVI status have superior prognostic accuracy to current clinical TNM staging in rectal cancer. Ann Surg. 2022;276:334–44.
doi: 10.1097/SLA.0000000000004499 pubmed: 32941279
Kotani D, Oki E, Nakamura Y, et al. Molecular residual disease and efficacy of adjuvant chemotherapy in patients with colorectal cancer. Nat Med. 2023;29:127–34.
doi: 10.1038/s41591-022-02115-4 pubmed: 36646802 pmcid: 9873552
Zhou J, Wang C, Lin G, et al. Serial circulating tumor DNA in predicting and monitoring the effect of neoadjuvant chemoradiotherapy in patients with rectal cancer: a prospective multicenter study. Clin Cancer Res. 2021;27:301–10.
doi: 10.1158/1078-0432.CCR-20-2299 pubmed: 33046514
Tie J, Cohen JD, Wang Y, et al. Serial circulating tumour DNA analysis during multimodality treatment of locally advanced rectal cancer: a prospective biomarker study. Gut. 2019;68:663–71.
doi: 10.1136/gutjnl-2017-315852 pubmed: 29420226
Ullah I, Yang L, Yin FT, et al. Multi-omics approaches in colorectal cancer screening and diagnosis, recent updates and future perspectives. Cancers. 2022;14:5545.
doi: 10.3390/cancers14225545 pubmed: 36428637 pmcid: 9688479
Gormly. Rectal MRI: the importance of high resolution T2 technique. Abdom Radiol. 2021;46:4090–5.
doi: 10.1007/s00261-021-03047-2

Auteurs

Atsushi Hamabe (A)

Department of Surgery, Surgical Oncology and Science, Sapporo Medical University, S1 W16, Chuo-Ku, Sapporo, 060-8543, Japan.
Department of Gastroenterological Surgery, Graduate School of Medicine, Osaka University, 2-2-E2 Yamadaoka, Suita, Osaka, 565-0871, Japan.

Ichiro Takemasa (I)

Department of Surgery, Surgical Oncology and Science, Sapporo Medical University, S1 W16, Chuo-Ku, Sapporo, 060-8543, Japan. itakemasa@sapmed.ac.jp.

Masayuki Ishii (M)

Department of Surgery, Surgical Oncology and Science, Sapporo Medical University, S1 W16, Chuo-Ku, Sapporo, 060-8543, Japan.

Koichi Okuya (K)

Department of Surgery, Surgical Oncology and Science, Sapporo Medical University, S1 W16, Chuo-Ku, Sapporo, 060-8543, Japan.

Koya Hida (K)

Department of Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Daisuke Nishizaki (D)

Department of Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Atsuhiko Sumii (A)

Department of Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Shigeki Arizono (S)

Department of Diagnostic Radiology, Kobe City Medical Center General Hospital, Kobe, Japan.

Shigeshi Kohno (S)

Department of Diagnostic Radiology, Kobe City Medical Center General Hospital, Kobe, Japan.

Koji Tokunaga (K)

Department of Diagnostic Radiology, Japanese Red Cross Wakayama Medical Center, Wakayama, Japan.

Hirotsugu Nakai (H)

Department of Radiology, Mayo Clinic, Rochester, MN, USA.

Yoshiharu Sakai (Y)

Department of Surgery, Osaka Red-Cross Hospital, Osaka, Japan.

Masahiko Watanabe (M)

Department of Surgery, Kitasato University Kitasato Institute Hospital, Tokyo, Japan.

Classifications MeSH