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Clinical features and oncological outcomes of intestinal cancers associated with ulcerative colitis and Crohn’s disease

  • Original Article—Alimentary Tract
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Abstract

Background

Patients with longstanding inflammatory bowel disease are at high risk of developing intestinal cancers. In this study, we aimed to elucidate the differences between intestinal cancers associated with ulcerative colitis and Crohn’s disease.

Methods

Intestinal cancers in ulcerative colitis and Crohn’s disease patients treated between 1983 and 2020 at 43 Japanese institutions were retrospectively analyzed..

Results

A total of 1505 intestinal cancers in 1189 ulcerative colitis and 316 Crohn’s disease patients were studied. Almost all of ulcerative colitis-associated cancers (99%) were in the colon and rectum, whereas half of Crohn’s disease-associated cancers (44%) were in the anus, with 11% in the small intestine. Ulcerative colitis-associated cancers were diagnosed more frequently by surveillance (67% vs. 25%, P < 0.0001) and at earlier stages (stages 0–1, 71% vs. 27%, P < 0.0001) compared with Crohn’s disease-associated cancers. Colorectal cancers associated with Crohn’s disease showed a significantly worse 5-year overall survival rate than those associated with ulcerative colitis (stage 2, 76% vs. 89%, P = 0.01, stage 3, 18% vs. 68%, P = 0.0009, and stage 4, 0% vs. 13%, P = 0.04). Surveillance correlated with earlier diagnoses for ulcerative colitis- and Crohn’s disease-associated intestinal cancers, whereas shorter intervals between endoscopic examinations correlated with an earlier cancer diagnosis in ulcerative colitis patients but not in Crohn’s disease patients.

Conclusions

The clinical and oncological features of ulcerative colitis- and Crohn’s disease-associated cancers were very different. Crohn’s disease-associated cancers were diagnosed at more advanced stages and were detected less frequently by surveillance. Additionally, they showed a significantly poorer prognosis.

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Data accessibility statement

The data underlying this article will be shared after all the analyses are completed on reasonable request to the corresponding author.

Abbreviations

JSCCR:

Japanese Society for Cancer of the Colon and Rectum

ACG:

American College of Gastroenterology

IBD:

Inflammatory bowel disease

UC:

Ulcerative colitis

CD:

Chrohn’s disease

References

  1. Kaplan GG, Ng SC. Understanding and preventing the global increase of inflammatory bowel disease. Gastroenterology. 2017;152:313-21.e2.

    Article  Google Scholar 

  2. Ekbom A, Helmick C, Zack M, et al. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med. 1990;323:1228–33.

    Article  CAS  Google Scholar 

  3. Ekbom A, Helmick C, Zack M, et al. Increased risk of large-bowel cancer in Crohn’s disease with colonic involvement. Lancet (London, England). 1990;336:357–9.

    Article  CAS  Google Scholar 

  4. Uchino M, Ikeuchi H, Hata K, et al. Changes in the rate of and trends in colectomy for ulcerative colitis during the era of biologics and calcineurin inhibitors based on a Japanese nationwide cohort study. Surg Today. 2019;49:1066–73.

    Article  CAS  Google Scholar 

  5. Watanabe T, Ajioka Y, Mitsuyama K, et al. Comparison of targeted vs random biopsies for surveillance of ulcerative colitis-associated colorectal cancer. Gastroenterology. 2016;151:1122–30.

    Article  Google Scholar 

  6. 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;113:1801–9.

    Article  Google Scholar 

  7. Magro F, Gionchetti P, Eliakim R, et al. Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. J Crohn's Colitis. 2017;11:649–670.

  8. Rubin DT, Ananthakrishnan AN, Siegel CA, et al. ACG clinical guideline: ulcerative colitis in adults. Am J Gastroenterol. 2019;114:384–413.

    Article  Google Scholar 

  9. Farraye FA, Odze RD, Eaden J, et al. AGA technical review on the diagnosis and management of colorectal neoplasia in inflammatory bowel disease. Gastroenterology. 2010;138:746–74, 774 e1–4; quiz e12–3.

  10. Cairns SR, Scholefield JH, Steele RJ, et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut. 2010;59:666–89.

    Article  Google Scholar 

  11. Cole EB, Shah Y, McLean LP, et al. Frequency of surveillance and impact of surveillance colonoscopies in patients with ulcerative colitis who developed colorectal cancer. Clin Colorectal Cancer. 2018;17:e289–92.

    Article  Google Scholar 

  12. Ananthakrishnan AN, Cagan A, Cai T, et al. Colonoscopy is associated with a reduced risk for colon cancer and mortality in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol. 2015;13:322-329.e1.

    Article  Google Scholar 

  13. Jess T, Loftus EV Jr, Velayos FS, et al. Risk of intestinal cancer in inflammatory bowel disease: a population-based study from olmsted county. Minnesota Gastroenterol. 2006;130:1039–46.

    Article  Google Scholar 

  14. Gillen CD, Andrews HA, Prior P, et al. Crohn’s disease and colorectal cancer. Gut. 1994;35:651–5.

    Article  CAS  Google Scholar 

  15. Dossett LA, White LM, Welch DC, et al. Small bowel adenocarcinoma complicating Crohn’s disease: case series and review of the literature. Am Surg. 2007;73:1181–7.

    Article  Google Scholar 

  16. Watanabe T, Konishi T, Kishimoto J, et al. Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study. Inflamm Bowel Dis. 2011;17:802–8.

    Article  Google Scholar 

  17. Olén O, Erichsen R, Sachs MC, et al. Colorectal cancer in ulcerative colitis: a Scandinavian population-based cohort study. The Lancet. 2020;395:123–31.

    Article  Google Scholar 

  18. Sasaki H, Ikeuchi H, Bando T, et al. Clinicopathological characteristics of cancer associated with Crohn’s disease. Surg Today. 2017;47:35–41.

    Article  CAS  Google Scholar 

  19. Olén O, Erichsen R, Sachs MC, et al. Colorectal cancer in Crohn’s disease: a Scandinavian population-based cohort study. Lancet Gastroenterol Hepatol. 2020;5:475–84.

    Article  Google Scholar 

  20. Choi PM, Zelig MP. Similarity of colorectal cancer in Crohn’s disease and ulcerative colitis: implications for carcinogenesis and prevention. Gut. 1994;35:950–4.

    Article  CAS  Google Scholar 

  21. Arhi C, Askari A, Nachiappan S, et al. Stage at diagnosis and survival of colorectal cancer with or without underlying inflammatory bowel disease: a population-based study. J Crohns Colitis. 2021;15:375–82.

    Article  Google Scholar 

  22. Japan Society for Cancer of the Colon and Rectum. Multi-institutional registry of large bowel cancer in Japan Vol. 33 Cases treated in 2007. 2018; Available from: http://www.jsccr.jp/registration/pdf/Vol_33.pdf.

  23. Lutgens MW, Oldenburg B, Siersema PD, et al. Colonoscopic surveillance improves survival after colorectal cancer diagnosis in inflammatory bowel disease. Br J Cancer. 2009;101:1671–5.

    Article  CAS  Google Scholar 

  24. Hata K, Anzai H, Ikeuchi H, et al. Surveillance colonoscopy for ulcerative colitis-associated colorectal cancer offers better overall survival in real-world surgically resected cases. Am J Gastroenterol. 2019;114:483–9.

    Article  Google Scholar 

  25. Hata K, Ishihara S, Watanabe T. Successful surveillance colonoscopy for patients with ulcerative colitis after ileorectal anastomosis. J Crohns Colitis. 2015;9:937–8.

    Article  Google Scholar 

  26. 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;36:3761–6.

    Google Scholar 

  27. Lakatos PL, David G, Pandur T, et al. Risk of colorectal cancer and small bowel adenocarcinoma in Crohn’s disease: a population-based study from western Hungary 1977–2008. J Crohns Colitis. 2011;5:122–8.

    Article  Google Scholar 

  28. Hata K, Ishihara S, Ajioka Y, et al. Long-term follow-up of targeted biopsy yield (LOFTY Study) in ulcerative colitis surveillance colonoscopy. J Clin Med. 2020;9:2286.

    Article  Google Scholar 

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Acknowledgements

We thank all the involved doctors in the following institutions: Department of Inflammatory Bowel Disease Surgery, Hyogo College of Medicine; Department of Surgery, Keio University; Department of Surgery, Fukuoka University Chikushi Hospital; Department of Surgical Oncology, The University of Tokyo Hiroshima University Hospital; Department of Surgical Oncology, Osaka City University Graduate School of Medicine; Department of Surgery, Tohoku University Graduate School of Medicine; Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University; Department of Coloproctology, Tokyo Yamate Medical Center; Department of Gastrointestinal and Pediatric Surgery, Institute of Life Sciences, Mie University Graduate School of Medicine; Department of Gastroenterological Surgery, Graduate School of Medical, Osaka University; Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University; Department of Surgery, Coloproctology Center Takano Hospital; Division of Digestive and General Surgery, Graduate School of Medical and Dental Sciences, Niigata University; Department of Surgery, Toho University Sakura Medical Center; Inflammatory Bowel Disease Centre, Yokohama City University Medical Centre; Department of Colorectal Surgery, Tohoku Rosai Hospital; Department of Surgery, Kyoto University Hospital; Department of Gastrointestinal Surgery, Tokyo Medical and Dental University; Department of General and Gastroenterological Surgery, Osaka Medical and Pharmaceutical University; Department of Surgery, Kindai University, Faculty of Medicine; Department of Surgery, Nara Medical University; Department of Surgery, National Defense Medical College; Inflammatory Bowel Disease Center, Yokkaichi Hazu Medical Center; Department of Surgery, Fujita Health University, School of Medicine; Inflammatory Bowel Disease Center, Sapporo Higashi Tokushukai Hospital; Center for Gastroenterology, Department of Surgery, Urasoe General Hospital; Department of Gastroenterological Surgery, Aichi Cancer Center Hospital; Department of Surgery, Kurume University Hospital; Department of Surgery, IMSUT Hospital, The Institute of Medical Science, The University of Tokyo; Department of Gastroenterological Surgery, Saitama Medical University International Medical Center; Department of Surgery, Teikyo University School of Medicine; Department of Gastroenterological Surgery, Osaka City General Hospital; Kurume Coloproctology Center; Department of Surgery, Nishinomiya Municipal Central Hospital; Department of Coloproctological Surgery, Japanese Red Cross Medical Center; Department of Surgery, Osaka Rosai Hospital; Department of Surgery, Kyorin University; Department of Colorectal Surgery, National Cancer Center Hospital; Department of Surgery, Tokyo Medical University Hospital; Department of Gastroenterological Surgery, Nagoya University Hospital; Department of Surgery, National Center for Global Health and Medicine; Department of Surgery, Yamagata Prefectural Central Hospital; Division of Gastroenterological Surgery, Saitama Cancer Center; Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School; Departments of Surgery, Faculty of Medical Sciences, University of Fukui; Department of Gastroenterological Surgery Tokai University School of Medicine. We also wish to thank Keisuke Hata for his advice on the study designs and analysis of the data.

Funding

This work was supported by the Japanese Society of Cancer of the Colon and Rectum.

Author information

Authors and Affiliations

  1. Department of Surgical Oncology, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan

    Tatsuki Noguchi & Soichiro Ishihara

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

    Motoi Uchino & Hiroki Ikeuchi

  3. Department of Surgery, Keio University School of Medicine, Tokyo, Japan

    Koji Okabayashi

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

    Kitaro Futami

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

    Shinji Tanaka

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

    Hiroki Ohge

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

    Hisashi Nagahara

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

    Kazuhiro Watanabe

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

    Michio Itabashi

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

    Kinya Okamoto

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

    Yoshiki Okita

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

    Tsunekazu Mizushima

  13. Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan

    Yusuke Mizuuchi

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

    Kazutaka Yamada

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

    Yoshifumi Shimada

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

    Yu Sato

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

    Hideaki Kimura

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

    Kenichi Takahashi

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

    Koya Hida

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

    Yusuke Kinugasa

  21. Department of General and Gastroenterological Surgery, Osaka Medical and Pharmaceutical University, Takatsuki, Japan

    Junji Okuda

  22. Department of Surgery, Faculty of Medicine, Kindai University, Osaka, Japan

    Koji Daito

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

    Fumikazu Koyama

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

    Hideki Ueno

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

    Takayuki Yamamoto

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

    Tsunekazu Hanai

  27. Inflammatory Bowel Disease Center, Sapporo Higashi Tokushukai Hospital, Sapporo, Japan

    Atsuo Maemoto

  28. Department of Biostatistics, School of Public Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan

    Koji Oba

  29. Interfaculty Initiative in Information Studies, Graduate School of Interdisciplinary Information Studies, The University of Tokyo, Tokyo, Japan

    Koji Oba

  30. Division of Molecular and Diagnostic Pathology, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan

    Yoichi Ajioka

  31. Tokyo Medical and Dental University, Tokyo, Japan

    Kenichi Sugihara

Authors
  1. Tatsuki Noguchi
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  32. Kenichi Sugihara
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Consortia

for the Study Group for Inflammatory Bowel Disease Associated Intestinal Cancers by the Japanese Society for Cancer of the Colon, Rectum

Contributions

SI is the chief investigator of this study group and the corresponding author; contributed to the design of the work, the analysis, and interpretation of data for the work; and revised the manuscript critically for important intellectual content. TN is the first author and contributed to the acquisition of data for the work, and drafted the work. KS and YA contributed to the conception of the work, and revised the work critically for important intellectual content. MU, HI, KO, KF, ST, HO, HN, KW, MI, KO, YT, TM, MN, KY, TW, YS, HK, KT, KH, YK, JO, KD, FK, HU, TY, TH, AM, and JA contributed to the acquisition of the data for the work, and revised the work critically for important intellectual content. KW, KH, JO, FK, HU, and AM contributed to the analysis of the data for the work, and revised the work critically for important intellectual content. HI, KF, ST, HO, KW, MI, YT, TM, MN, TW, KT, KH, YK, JO, KD, and KO contributed to the interpretation of the data for the work, and revised the work critically for important intellectual content. All the authors approved the final version to be published, and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The funding source had no role in study design, data collection, data analysis and interpretation, preparation of the manuscript, or decision to publish.

Corresponding author

Correspondence to Soichiro Ishihara.

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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 58, 14–24 (2023). https://doi.org/10.1007/s00535-022-01927-y

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