Crohn's Disease-Associated Anorectal Cancer Has a Poor Prognosis With High Local Recurrence: A Subanalysis of the Nationwide Japanese Study.


Journal

The American journal of gastroenterology
ISSN: 1572-0241
Titre abrégé: Am J Gastroenterol
Pays: United States
ID NLM: 0421030

Informations de publication

Date de publication:
01 09 2023
Historique:
received: 10 11 2022
accepted: 16 03 2023
medline: 31 8 2023
pubmed: 30 3 2023
entrez: 29 3 2023
Statut: ppublish

Résumé

Colorectal cancer (CRC) is one of the major life-threatening complications in patients with Crohn's disease (CD). Previous studies of CD-associated CRC (CD-CRC) have involved only small numbers of patients, and no large series have been reported from Asia. The aim of this study was to clarify the prognosis and clinicopathological features of CD-CRC compared with sporadic CRC. A large nationwide database was used to identify patients with CD-CRC (n = 233) and sporadic CRC (n = 129,783) over a 40-year period, from 1980 to 2020. Five-year overall survival (OS), recurrence-free survival (RFS), and clinicopathological characteristics were investigated. The prognosis of CD-CRC was further evaluated in groups divided by colon cancer and anorectal cancer (RC). Multivariable Cox regression analysis was used to adjust for confounding by unbalanced covariables. Compared with sporadic cases, patients with CD-CRC were younger; more often had RC, multiple lesions, and mucinous adenocarcinoma; and had lower R0 resection rates. Five-year OS was worse for CD-CRC than for sporadic CRC (53.99% vs 71.17%, P < 0.001). Multivariable Cox regression analysis revealed that CD was associated with significantly poorer survival (hazard ratio 2.36, 95% confidence interval: 1.54-3.62, P < 0.0001). Evaluation by tumor location showed significantly worse 5-year OS and RFS of CD-RC compared with sporadic RC. Recurrence was identified in 39.57% of CD-RC cases and was mostly local. Poor prognosis of CD-CRC is attributable primarily to RC and high local recurrence. Local control is indispensable to improving prognosis.

Identifiants

pubmed: 36988310
doi: 10.14309/ajg.0000000000002269
pii: 00000434-990000000-00711
pmc: PMC10453357
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1626-1637

Informations de copyright

Copyright © 2023 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of The American College of Gastroenterology.

Références

Freeman HJ. Colorectal cancer risk in Crohn's disease. World J Gastroenterol 2008;14(12):1810–1.
Yano Y, Matsui T, Hirai F, et al. Cancer risk in Japanese Crohn's disease patients: Investigation of the standardized incidence ratio. J Gastroenterol Hepatol 2013;28(8):1300–5.
Jess T, Gamborg M, Matzen P, et al. Increased risk of intestinal cancer in Crohn's disease: A meta-analysis of population-based cohort studies. Am J Gastroenterol 2005;100(12):2724–9.
Jess T, Horváth-Puhó E, Fallingborg J, et al. Cancer risk in inflammatory bowel disease according to patient phenotype and treatment: A Danish population-based cohort study. Am J Gastroenterol 2013;108(12):1869–76.
Olén O, Erichsen R, Sachs MC, et al. Colorectal cancer in Crohn's disease: A Scandinavian population-based cohort study. Lancet Gastroenterol Hepatol 2020;5(5):475–84.
Uchino M, Ikeuchi H, Hata K, et al. Intestinal cancer in patients with Crohn's disease: A systematic review and meta-analysis. J Gastroenterol Hepatol 2021;36(2):329–36.
Zisman TL, Rubin DT. Colorectal cancer and dysplasia in inflammatory bowel disease. World J Gastroenterol 2008;14(17):2662–9.
Ekbom A, Adami HO, Helmick C, et al. Increased risk of large-bowel cancer in Crohn's disease with colonic involvement. Lancet 1990;336(8711):357–9.
Askling J, Dickman PW, Ekbom A, et al. Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology 2001;120(6):1356–62.
Gillen CD, Walmsley RS, Prior P, et al. Ulcerative colitis and Crohn's disease: A comparison of the colorectal cancer risk in extensive colitis. Gut 1994;35(11):1590–2.
Ji SG, Juran BD, Mucha S, et al. Genome-wide association study of primary sclerosing cholangitis identifies new risk loci and quantifies the genetic relationship with inflammatory bowel disease. Nat Genet 2017;49(2):269–73.
Vitali F, Wein A, Rath T, et al. The outcome of patients with inflammatory bowel disease-associated colorectal cancer is not worse than that of patients with sporadic colorectal cancer-a matched-pair analysis of survival. Int J Colorectal Dis 2022;37(2):381–91.
Lu C, Schardey J, Zhang T, et al. Survival outcomes and clinicopathological features in inflammatory bowel disease-associated colorectal cancer: A systematic review and meta-analysis. Ann Surg 2022;276(5):e319–e330.
Stahl TJ, Schoetz DJ Jr, Roberts PL, et al. Crohn's disease and carcinoma: Increasing justification for surveillance? Dis Colon Rectum 1992;35(9):850–6.
Connell WR, Sheffield JP, Kamm MA, et al. Lower gastrointestinal malignancy in Crohn's disease. Gut 1994;35(3):347–52.
Kiran RP, Khoury W, Church JM, et al. Colorectal cancer complicating inflammatory bowel disease: Similarities and differences between Crohn's and ulcerative colitis based on three decades of experience. Ann Surg 2010;252:330–5.
Mizushima T, Ohno Y, Nakajima K, et al. Malignancy in Crohn's disease: Incidence and clinical characteristics in Japan. Digestion 2010;81(4):265–70.
Sasaki H, Ikeuchi H, Bando T, et al. Clinicopathological characteristics of cancer associated with Crohn's disease. Surg Today 2017;47(1):35–41.
Kim J, Lee HS, Park SH, et al. Pathologic features of colorectal carcinomas associated with Crohn's disease in Korean population. Pathol Res Pract 2017;213(3):250–5.
Hirsch D, Wangsa D, Zhu YJ, et al. Dynamics of genome alterations in Crohn's disease-associated colorectal carcinogenesis. Clin Cancer Res 2018;24(20):4997–5011.
Noguchi T, Ishihara S, Uchino M, et al. Clinical features and oncological outcomes of intestinal cancers associated with ulcerative colitis and Crohn's disease. J Gastroenterol 2022;58(1):14–24.
Proposed guidelines for the management of patients with Crohn's disease. Annual reports of Research Group of Intractable Inflammatory Bowel Disease subsidized by the Ministry of Health, Labor and Welfare of Japan. 2008. (in Japanese).
Japanese Society for Cancer of the Colon and Rectum: Japanese Classification of Colorectal Carcinoma. 3rd English Edition. Kanehara: Tokyo, Japan, 2019.
Vetter LE, Merkel S, Bénard A, et al. Colorectal cancer in Crohn's colitis is associated with advanced tumor invasion and a poorer survival compared with ulcerative colitis: A retrospective dual-center study. Int J Colorectal Dis 2021;36(1):141–50.
Bye WA, Ma C, Nguyen TM, et al. Strategies for detecting colorectal cancer in patients with inflammatory bowel disease: A Cochrane systematic review and meta-analysis. Am J Gastroenterol 2018;113(12):1801–9.
Palmieri C, Müller G, Kroesen AJ, et al. Perianal fistula-associated carcinoma in Crohn's disease: A multicentre retrospective case control study. J Crohns Colitis 2021;15(10):1686–93.
Birch RJ, Burr N, Subramanian V, et al. Inflammatory bowel disease-associated colorectal cancer epidemiology and outcomes: An English population-based study. Am J Gastroenterol 2022;117(11):1858–70.
Matsuno H, Mizushima T, Nezu R, et al. Detection of anorectal cancer among patients with Crohn's disease undergoing surveillance with various biopsy methods. Digestion 2016;94(1):24–9.
Higashi D, Katsuno H, Kimura H, et al. Current state of and problems related to cancer of the intestinal tract associated with Crohn's disease in Japan. Anticancer Res 2016;36(7):3761–6.
Shwaartz C, Munger JA, Deliz JR, et al. Fistula-associated anorectal cancer in the setting of Crohn's disease. Dis Colon Rectum 2016;59(12):1168–73.
Beaugerie L, Carrat F, Nahon S, et al. High risk of anal and rectal cancer in patients with anal and/or perianal Crohn's disease. Clin Gastroenterol Hepatol 2018;16(6):892–9.e2.
Galata C, Hirsch D, Reindl W, et al. Clinical and histopathologic features of colorectal adenocarcinoma in Crohn's disease. J Clin Gastroenterol 2018;52(7):635–40.
Nitsche U, Zimmermann A, Späth C, et al. Mucinous and signet-ring cell colorectal cancers differ from classical adenocarcinomas in tumor biology and prognosis. Ann Surg 2013;258(5):775–83.
National Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology. Anal Carcinoma. Version 2. NCCN: Plymouth Meeting, PA, 2017.
Herrinton LJ, Liu L, Levin TR, et al. Incidence and mortality of colorectal adenocarcinoma in persons with inflammatory bowel disease from 1998 to 2010. Gastroenterology 2012;143(2):382–9.
Te Groen M, Derks M, den Broeder N, et al. Quality of surveillance impacts the colitis-associated advanced neoplasia risk: A multicenter case-control study. Clin Gastroenterol Hepatol 2022:S1542-3565(22)01177-6. doi: 10.1016/j.cgh.2022.12.010.
doi: 10.1016/j.cgh.2022.12.010
Wang YR, Cangemi JR, Loftus EV Jr, et al. Rate of early/missed colorectal cancers after colonoscopy in older patients with or without inflammatory bowel disease in the United States. Am J Gastroenterol 2013;108(3):444–9.
Delbeke D, Martin WH. PET and PET-CT for evaluation of colorectal carcinoma. Semin Nucl Med 2004;34:209–23.
Hirano Y, Futami K, Higashi D, et al. Anorectal cancer surveillance in Crohn's disease. J Anus Rectum Colon 2018;2(4):145–54.
Bosch SL, van Rooijen SJ, Bokkerink GM, et al. Acute toxicity and surgical complications after preoperative (chemo)radiation therapy for rectal cancer in patients with inflammatory bowel disease. Radiother Oncol 2017;123(1):147–53.
Iesalnieks I, Gaertner WB, Gla H, et al. Fistula-associated anal adenocarcinoma in Crohn's disease. Inflamm Bowel Dis 2010;16(10):1643–8.
Alsughayer A, Grass F, McKenna NP, et al. Does IBD portend worse outcomes in patients with rectal cancer? A case-matched analysis. Dis Colon Rectum 2020;63(9):1265–75.

Auteurs

Takayuki Ogino (T)

Department of Gastroenterological Surgery, Graduate School of Medical, Osaka University, Osaka, Japan.
Department of Therapeutics for Inflammatory Bowel Diseases, Graduate School of Medical, Osaka University, Osaka, Japan.

Tsunekazu Mizushima (T)

Department of Therapeutics for Inflammatory Bowel Diseases, Graduate School of Medical, Osaka University, Osaka, Japan.

Makoto Fujii (M)

Division of Health Sciences, Graduate School of Medical, Osaka University, Osaka, Japan.

Yuki Sekido (Y)

Department of Gastroenterological Surgery, Graduate School of Medical, Osaka University, Osaka, Japan.

Hidetoshi Eguchi (H)

Department of Gastroenterological Surgery, Graduate School of Medical, Osaka University, Osaka, Japan.

Riichiro Nezu (R)

Department of Surgery, Osaka Central Hospital, Osaka, Japan.

Hiroki Ikeuchi (H)

Department of Inflammatory Bowel Disease Surgery, Hyogo College of Medicine, Nishinomiya, Japan.

Uchino Motoi (U)

Department of Inflammatory Bowel Disease Surgery, Hyogo College of Medicine, Nishinomiya, Japan.

Kitaro Futami (K)

Department of Surgery, Fukuoka University Chikushi Hospital, Chikushino, Japan.

Kinya Okamoto (K)

Department of Coloproctology, Tokyo Yamate Medical Center, Tokyo, Japan.

Hisashi Nagahara (H)

Department of Surgery, Osaka City University, Graduate School of Medicine, Osaka, Japan.

Kazuhiro Watanabe (K)

Department of Surgery, Tohoku University Graduate School of Medicine, Sendai, Japan.

Koji Okabayashi (K)

Department of Surgery, Keio University, Tokyo, Japan.

Kazutaka Yamada (K)

Department of Surgery, Coloproctology Center Takano Hospital, Kumamoto, Japan.

Hiroki Ohge (H)

Department of Infectious Diseases, Hiroshima University Hospital, Hiroshima, Japan.

Shinji Tanaka (S)

Department of Endoscopy, Hiroshima University Hospital, Hiroshima, Japan.

Yusuke Mizuuchi (Y)

Department of Surgery and Oncology, Kyusyu University, Fukuoka, Japan.

Yoshiki Ohkita (Y)

Department of Gastrointestinal and Pediatric Surgery, Institute of Life Sciences, Mie University Graduate School of Medicine, Tsu, Japan.

Yu Sato (Y)

Department of Surgery, Toho University Sakura Medical Center, Chiba, Japan.

Hideki Ueno (H)

Department of Surgery, National Defense Medical College, Tokorozawa, Japan.

Toru Kono (T)

Advanced Surgery Center, Sapporo Higashi Tokushukai Hospital, Sapporo, Japan.

Michio Itabashi (M)

Department of Surgery, Division of Inflammatory Bowel Disease Surgery, Tokyo Women's Medical University, Tokyo, Japan.

Hideaki Kimura (H)

Inflammatory Bowel Disease Center, Yokohama City University Medical Centre, Yokohama, Japan.

Koya Hida (K)

Department of Surgery, Kyoto University Hospital, Kyoto, Japan.

Yusuke Kinugasa (Y)

Department of Gastrointestinal Surgery, Tokyo Medical and Dental University, Tokyo, Japan.

Kenichi Takahashi (K)

Department of Colorectal Surgery, Tohoku Rosai Hospital, Sendai, Japan.

Fumikazu Koyama (F)

Department of Surgery, Nara Medical University, Kashihara, Japan.

Tsunekazu Hanai (T)

Department of Surgery, Fujita Health University, School of Medicine, Toyoake, Japan.

Kiyoshi Maeda (K)

Department of Gastroenterological Surgery, Osaka City General Hospital, Osaka, Japan.

Toshihiro Noake (T)

Kurume Coloproctology Center, Kurume, Japan.

Yoshifumi Shimada (Y)

Division of Digestive and General Surgery, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan.

Takayuki Yamamoto (T)

Inflammatory Bowel Disease Center, Yokkaichi Hazu Medical Center, Yokkaichi, Japan.

Junya Arakaki (J)

Center for Gastroenterology, Department of Surgery, Urasoe General Hospital, Urasoe, Japan.

Keiji Mastuda (K)

Department of Surgery, Teikyo University School of Medicine, Tokyo, Japan.

Junji Okuda (J)

Department of General and Gastroenterological Surgery, Osaka Medical College, Takatsuki, Japan.

Eiji Sunami (E)

Department of Surgery, Kyorin University, Tokyo, Japan.

Yoshito Akagi (Y)

Department of Surgery, Kurume University Hospital, Kurume, Japan.

Kenji Kastumata (K)

Department of Surgery, Tokyo Medical University Hospital, Tokyo, Japan.

Kay Uehara (K)

Department of Gastroenterological Surgery, Nagoya University Hospital, Nagoya, Japan.

Takeshi Yamada (T)

Department of Digestive Surgery, Nippon Medical School, Tokyo, Japan.

Shin Sasaki (S)

Department of Coloproctological Surgery, Japanese Red Cross Medical Center, Tokyo, Japan.

Soichiro Ishihara (S)

Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan.

Yoichi Ajioka (Y)

Department of Pathology, Niigata University, Niigata, Japan.

Kenichi Sugihara (K)

Tokyo Medical and Dental University, Tokyo, Japan.

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