Analysis of clinicopathological features and oncological outcomes of ulcerative colitis-associated colorectal cancer based on macroscopic classification

Ayano Saito; Yuichiro Yokoyama; Motoi Uchino; Hiroki Ikeuchi; Koji Okabayashi; Shiro Oka; Daijiro Higashi; Shimpei Ogawa; Kazuhiro Watanabe; Masatsune Shibutani; Yoshiki Okita; Toshifumi Wakai; Yusuke Mizuuchi; Kinya Okamoto; Kazutaka Yamada; Yu Sato; Takayuki Ogino; Hideaki Kimura; Kenichi Takahashi; Koya Hida; Yusuke Kinugasa; Fumio Ishida; Junji Okuda; Koji Daito; Takayuki Yamamoto; Seiichiro Yamamoto; Fumikazu Koyama; Tsunekazu Hanai; Koji Komori; Dai Shida; Junya Arakaki; Fumihiko Fujita; Shigeki Yamaguchi; Hideki Ueno; Keiji Matsuda; Atsuo Maemoto; Riichiro Nezu; Shin Sasaki; Eiji Sunami; Tatsuki Noguchi; Kenichi Sugihara; Yoichi Ajioka; Soichiro Ishihara; Study Group for Inflammatory Bowel Disease Associated Intestinal Cancers by the Japanese Society for Cancer of the Colon, Rectum

doi:10.1007/s00384-025-05001-w

Analysis of clinicopathological features and oncological outcomes of ulcerative colitis-associated colorectal cancer based on macroscopic classification

Int J Colorectal Dis. 2025 Oct 29;40(1):223. doi: 10.1007/s00384-025-05001-w.

Authors

Ayano Saito¹, Yuichiro Yokoyama², Motoi Uchino³, Hiroki Ikeuchi³, Koji Okabayashi⁴, Shiro Oka⁵, Daijiro Higashi⁶, Shimpei Ogawa⁷, Kazuhiro Watanabe⁸, Masatsune Shibutani⁹, Yoshiki Okita¹⁰, Toshifumi Wakai¹¹, Yusuke Mizuuchi¹², Kinya Okamoto¹³, Kazutaka Yamada¹⁴, Yu Sato¹⁵, Takayuki Ogino¹⁶, Hideaki Kimura¹⁷, Kenichi Takahashi¹⁸, Koya Hida¹⁹, Yusuke Kinugasa²⁰, Fumio Ishida²¹, Junji Okuda²², Koji Daito²³, Takayuki Yamamoto²⁴, Seiichiro Yamamoto²⁵, Fumikazu Koyama²⁶, Tsunekazu Hanai²⁷, Koji Komori²⁸, Dai Shida²⁹, Junya Arakaki³⁰, Fumihiko Fujita³¹, Shigeki Yamaguchi³², Hideki Ueno³³, Keiji Matsuda³⁴, Atsuo Maemoto³⁵, Riichiro Nezu³⁶, Shin Sasaki³⁷, Eiji Sunami³⁸, Tatsuki Noguchi², Kenichi Sugihara³⁹, Yoichi Ajioka⁴⁰, Soichiro Ishihara²; Study Group for Inflammatory Bowel Disease Associated Intestinal Cancers by the Japanese Society for Cancer of the Colon, Rectum

Affiliations

¹ Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan. saitoa-psu@h.u-tokyo.ac.jp.
² Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan.
³ Department of Inflammatory Bowel Disease Surgery, Hyogo Medical University, Nishinomiya, Japan.
⁴ Department of Surgery, Keio University School of Medicine, Tokyo, Japan.
⁵ Department of Gastroenterology, Graduate School of Biomedical and Health Sciences, Hiroshima University, Hiroshima, Japan.
⁶ Department of Surgery, Fukuoka University Chikushi Hospital, Chikushino, Japan.
⁷ Department of Surgery, Division of Inflammatory Bowel Disease Surgery, Tokyo Women's Medical University, Tokyo, Japan.
⁸ Department of Surgery, Tohoku University Graduate School of Medicine, Sendai, Japan.
⁹ Department of Gastroenterological Surgery, Osaka Metropolitan University Graduate School of Medicine, Osaka, Japan.
¹⁰ Department of Gastrointestinal and Pediatric Surgery, Institute of Life Sciences, Mie University Graduate School of Medicine, Tsu, Japan.
¹¹ Division of Digestive and General Surgery, Graduate School of Medical and Dental Sciences, Niigata University, Niigata, Japan.
¹² Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
¹³ Department of Coloproctology, Tokyo Yamate Medical Center, Tokyo, Japan.
¹⁴ Department of Surgery, Coloproctology Center, Takano Hospital, Kumamoto, Japan.
¹⁵ Department of Surgery, Toho University Sakura Medical Center, Chiba, Japan.
¹⁶ Department of Gastroenterological Surgery, Graduate School of Medical, Osaka University, Osaka, Japan.
¹⁷ Inflammatory Bowel Disease Center, Yokohama City University Medical Center, Yokohama, Japan.
¹⁸ Department of Colorectal Surgery, Tohoku Rosai Hospital, Sendai, Japan.
¹⁹ Department of Surgery, Kyoto University Hospital, Kyoto, Japan.
²⁰ Department of Gastrointestinal Surgery, Institute of Science Tokyo, Tokyo, Japan.
²¹ Digestive Disease Center, Showa University Northern Yokohama Hospital, Kanagawa, Japan.
²² Department of General and Gastroenterological Surgery, Osaka Medical and Pharmaceutical University, Takatsuki, Japan.
²³ Department of Surgery, Faculty of Medicine, Kindai University, Osaka, Japan.
²⁴ Inflammatory Bowel Disease Center, Yokkaichi Hazu Medical Center, Yokkaichi, Japan.
²⁵ Department of Gastroenterological Surgery, Tokai University School of Medicine, Tokyo, Japan.
²⁶ Department of Surgery, Nara Medical University, Nara, Japan.
²⁷ Department of Surgery, School of Medicine, Fujita Health University, Aichi, Japan.
²⁸ Department of Gastroenterological Surgery, Aichi Cancer Center Hospital, Aichi, Japan.
²⁹ Department of Surgery, IMSUT Hospital, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
³⁰ Center for Gastroenterology, Department of Surgery, Urasoe General Hospital, Okinawa, Japan.
³¹ Department of Surgery, Kurume University Hospital, Kurume, Japan.
³² Department of Gastroenterological Surgery, Saitama Medical University International Medical Center, Saitama, Japan.
³³ Department of Surgery, National Defense Medical College, Tokorozawa, Japan.
³⁴ Department of Surgery, Teikyo University School of Medicine, Tokyo, Japan.
³⁵ Inflammatory Bowel Disease Center, Sapporo-Higashi Tokushukai Hospital, Sapporo, Japan.
³⁶ Department of Surgery, Nishinomiya Municipal Central Hospital, Nishinomiya, Japan.
³⁷ Department of Coloproctological Surgery, Japanese Red Cross Medical Center, Tokyo, Japan.
³⁸ Department of Surgery, Kyorin University, Tokyo, Japan.
³⁹ Institute of Science Tokyo, Tokyo, Japan.
⁴⁰ Department of Pathology, Niigata University, Niigata, Japan.

Abstract

Purpose: Few studies have reported the association of macroscopic classification with clinicopathological characteristics and prognosis of ulcerative colitis-associated colorectal cancer (UC-CRC), unlike sporadic CRC. In this study, we aimed to clarify the clinical significance of macroscopic classification of UC-CRC.

Methods: The cohort included 480 patients with UC-CRC with invasion beyond the muscularis propria treated at 43 Japanese institutions between 1983 and 2023. The patients were divided into six groups based on the macroscopic type (types 0-5), and clinicopathological features and prognoses were compared.

Results: Among 480 patients, 66 (13.8%), 75 (15.6%), 116 (24.2%), 63 (13.1%), 68 (14.2%), and 92 (19.2%) had type 0-5 tumors, respectively. There were significant differences in the clinicopathological characteristics with a younger age in type 4 or 5 tumors than in type 2 tumors (p < 0.01) and a higher frequency of undifferentiated carcinomas (p < 0.01) and lymph node metastasis (p < 0.01) and more advanced depth of invasion (p < 0.01) in type 4 tumors than in type 1 or 2 tumors. Type 4 and 5 were independent risk factors for 5-year recurrence-free survival (p = 0.02; type 4 [HR: 6.35], type 5 [HR: 5.25]) and type 0, 4, and 5 for overall survival (p = 0.02; type 0 [HR: 4.51], type 4 [HR: 5.70], type 5 [HR: 4.02]).

Conclusions: Type 0, 4, and 5 tumors were characteristic macroscopic types of UC-CRC and correlated with worse prognosis. Therefore, endoscopic diagnosis of the macroscopic type of UC-CRC might be helpful in determining tumor aggressiveness.

Keywords: Macroscopic classification; Prognosis; Ulcerative colitis; Ulcerative colitis associated cancer.

MeSH terms

Adult
Aged
Colitis, Ulcerative* / complications
Colitis, Ulcerative* / pathology
Colitis-Associated Neoplasms* / classification
Colitis-Associated Neoplasms* / pathology
Colorectal Neoplasms* / classification
Colorectal Neoplasms* / complications
Colorectal Neoplasms* / pathology
Disease-Free Survival
Female
Humans
Lymphatic Metastasis
Male
Middle Aged
Neoplasm Invasiveness
Prognosis
Risk Factors
Treatment Outcome