Clinicopathological features and prognosis of primary small bowel adenocarcinoma: a large multicenter analysis of the JSCCR database in Japan

doi:10.1007/s00535-024-02081-3

Multicenter Study

. 2024 May;59(5):376-388.

doi: 10.1007/s00535-024-02081-3. Epub 2024 Feb 27.

Clinicopathological features and prognosis of primary small bowel adenocarcinoma: a large multicenter analysis of the JSCCR database in Japan

Ken Yamashita¹, Shiro Oka², Takeshi Yamada³, Keigo Mitsui⁴, Hironori Yamamoto⁵, Keiichi Takahashi⁶, Akio Shiomi⁷, Kinichi Hotta⁸, Yoji Takeuchi⁹, Toshio Kuwai¹⁰, Fumio Ishida¹¹, Shin-Ei Kudo¹¹, Shoichi Saito¹², Masashi Ueno¹³, Eiji Sunami¹⁴, Tomoki Yamano¹⁵, Michio Itabashi¹⁶, Kazuo Ohtsuka¹⁷, Yusuke Kinugasa¹⁸, Takayuki Matsumoto¹⁹, Tamotsu Sugai²⁰, Toshio Uraoka²¹, Koichi Kurahara²², Shigeki Yamaguchi²³, Tomohiro Kato²⁴, Masazumi Okajima²⁵, Hiroshi Kashida²⁶, Yoshito Akagi²⁷, Hiroaki Ikematsu²⁸, Masaaki Ito²⁹, Motohiro Esaki³⁰, Masaya Kawai³¹, Takashi Yao³², Madoka Hamada³³, Takahiro Horimatsu³⁴, Keiji Koda³⁵, Yasumori Fukai³⁶, Koji Komori³⁷, Yusuke Saitoh³⁸, Yukihide Kanemitsu³⁹, Hiroyuki Takamaru⁴⁰, Kazutaka Yamada⁴¹, Hiroaki Nozawa⁴², Tetsuji Takayama⁴³, Kazutomo Togashi⁴⁴, Eiji Shinto⁴⁵, Takehiro Torisu⁴⁶, Akira Toyoshima⁴⁷, Naoki Ohmiya⁴⁸, Takeshi Kato⁴⁹, Eigo Otsuji⁵⁰, Shinji Nagata⁵¹, Yojiro Hashiguchi⁵², Kenichi Sugihara⁵³, Yoichi Ajioka⁵⁴, Shinji Tanaka¹

Affiliations

¹ Department of Gastroenterology, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-Ku, Hiroshima, 734-8551, Japan.
² Department of Gastroenterology, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-Ku, Hiroshima, 734-8551, Japan. oka4683@hiroshima-u.ac.jp.
³ Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, Tokyo, Japan.
⁴ Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, Tokyo, Japan.
⁵ Department of Medicine, Division of Gastroenterology, Jichi Medical University, Tochigi, Japan.
⁶ Department of Colorectal Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan.
⁷ Division of Colon and Rectal Surgery, Shizuoka Cancer Center, Shizuoka, Japan.
⁸ Division of Endoscopy, Shizuoka Cancer Center, Shizuoka, Japan.
⁹ Department of Gastrointestinal Oncology, Osaka International Cancer Institute, Osaka, Japan.
¹⁰ Department of Gastroenterology, National Hospital Organization Kure Medical Center and Chugoku Cancer Center, Hiroshima, Japan.
¹¹ Digestive Disease Center, Showa University Northern Yokohama Hospital, Kanagawa, Japan.
¹² Department of Lower Gastrointestinal Medicine, Cancer Institute Hospital of the Japanese Foundation for Cancer Research, Tokyo, Japan.
¹³ Department of Gastroenterological Surgery, Toranomon Hospital, Tokyo, Japan.
¹⁴ Department of Surgery, Kyorin University School of Medicine, Tokyo, Japan.
¹⁵ Division of Lower Gastrointestinal Surgery, Department of Surgery, Hyogo College of Medicine, Hyogo, Japan.
¹⁶ Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University, Tokyo, Japan.
¹⁷ Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.
¹⁸ Department of Gastrointestinal Surgery, Tokyo Medical and Dental University, Tokyo, Japan.
¹⁹ Division of Gastroenterology, Department of Internal Medicine, Iwate Medical University, Iwate, Japan.
²⁰ Department of Diagnostic Pathology, Iwate Medical University, Iwate, Japan.
²¹ Department of Gastroenterology and Hepatology, Gunma University Graduate School of Medicine, Gunma, Japan.
²² Division of Gastroenterology, Matsuyama Red Cross Hospital, Ehime, Japan.
²³ Department of Gastroenterological Surgery, Saitama Medical University International Medical Center, Saitama, Japan.
²⁴ Division of Gastroenterology and Hepatology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan.
²⁵ Department of Surgery, Hiroshima City Hiroshima Citizens Hospital, Hiroshima, Japan.
²⁶ Department of Gastroenterology and Hepatology, Kindai University Faculty of Medicine, Osaka, Japan.
²⁷ Department of Surgery, Kurume University School of Medicine, Fukuoka, Japan.
²⁸ Department of Gastroenterology and Endoscopy, National Cancer Center Hospital East, Chiba, Japan.
²⁹ Department of Colorectal Surgery, National Cancer Center Hospital East, Chiba, Japan.
³⁰ Division of Gastroenterology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga, Japan.
³¹ Department of Coloproctological Surgery, Faculty of Medicine, Juntendo University, Tokyo, Japan.
³² Department of Human Pathology, Juntendo University Graduate School of Medicine, Tokyo, Japan.
³³ Department of Gastrointestinal Surgery, Kansai Medical University Hospital, Osaka, Japan.
³⁴ Department of Clinical Oncology, Kyoto University Hospital, Kyoto, Japan.
³⁵ Department of Surgery, Teikyo University Chiba Medical Center, Chiba, Japan.
³⁶ Department of Gastroenterology, Maebashi Red Cross Hospital, Gunma, Japan.
³⁷ Department of Gastroenterological Surgery, Aichi Cancer Center Hospital, Aichi, Japan.
³⁸ Department of Gastroenterology, Asahikawa City Hospital, Asahikawa, Hokkaido, Japan.
³⁹ Department of Colorectal Surgery, National Cancer Center Hospital, Tokyo, Japan.
⁴⁰ Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan.
⁴¹ Department of Surgery, Coloproctology Center Takano Hospital, Kumamoto, Japan.
⁴² Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan.
⁴³ Department of Gastroenterology and Oncology, Tokushima University Graduate School of Biomedical Sciences, Tokushima, Japan.
⁴⁴ Department of Coloproctology, Aizu Medical Center, Fukushima Medical University, Fukushima, Japan.
⁴⁵ Department of Surgery, National Defense Medical College, Tokorozawa, Saitama, Japan.
⁴⁶ Department of Medicine and Clinical Science, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
⁴⁷ Department of Colorectal Surgery, Japanese Red Cross Medical Center, Tokyo, Japan.
⁴⁸ Department of Advanced Endoscopy, Fujita Health University School of Medicine, Aichi, Japan.
⁴⁹ Department of Surgery, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁵⁰ Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, Kyoto, Japan.
⁵¹ Department of Gastroenterology, Hiroshima City North Medical Center Asa Citizens Hospital, Hiroshima, Japan.
⁵² Department of Surgery, Japanese Red Cross Omori Hospital, Tokyo, Japan.
⁵³ Tokyo Medical and Dental University, Tokyo, Japan.
⁵⁴ Division of Molecular and Diagnostic Pathology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

PMID: 38411920
PMCID: PMC11033235
DOI: 10.1007/s00535-024-02081-3

Multicenter Study

Clinicopathological features and prognosis of primary small bowel adenocarcinoma: a large multicenter analysis of the JSCCR database in Japan

Ken Yamashita et al. J Gastroenterol. 2024 May.

. 2024 May;59(5):376-388.

doi: 10.1007/s00535-024-02081-3. Epub 2024 Feb 27.

Authors

Affiliations

¹ Department of Gastroenterology, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-Ku, Hiroshima, 734-8551, Japan.
² Department of Gastroenterology, Hiroshima University Hospital, 1-2-3, Kasumi, Minami-Ku, Hiroshima, 734-8551, Japan. oka4683@hiroshima-u.ac.jp.
³ Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, Tokyo, Japan.
⁴ Department of Gastroenterology, Nippon Medical School, Graduate School of Medicine, Tokyo, Japan.
⁵ Department of Medicine, Division of Gastroenterology, Jichi Medical University, Tochigi, Japan.
⁶ Department of Colorectal Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan.
⁷ Division of Colon and Rectal Surgery, Shizuoka Cancer Center, Shizuoka, Japan.
⁸ Division of Endoscopy, Shizuoka Cancer Center, Shizuoka, Japan.
⁹ Department of Gastrointestinal Oncology, Osaka International Cancer Institute, Osaka, Japan.
¹⁰ Department of Gastroenterology, National Hospital Organization Kure Medical Center and Chugoku Cancer Center, Hiroshima, Japan.
¹¹ Digestive Disease Center, Showa University Northern Yokohama Hospital, Kanagawa, Japan.
¹² Department of Lower Gastrointestinal Medicine, Cancer Institute Hospital of the Japanese Foundation for Cancer Research, Tokyo, Japan.
¹³ Department of Gastroenterological Surgery, Toranomon Hospital, Tokyo, Japan.
¹⁴ Department of Surgery, Kyorin University School of Medicine, Tokyo, Japan.
¹⁵ Division of Lower Gastrointestinal Surgery, Department of Surgery, Hyogo College of Medicine, Hyogo, Japan.
¹⁶ Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University, Tokyo, Japan.
¹⁷ Department of Gastroenterology and Hepatology, Tokyo Medical and Dental University, Tokyo, Japan.
¹⁸ Department of Gastrointestinal Surgery, Tokyo Medical and Dental University, Tokyo, Japan.
¹⁹ Division of Gastroenterology, Department of Internal Medicine, Iwate Medical University, Iwate, Japan.
²⁰ Department of Diagnostic Pathology, Iwate Medical University, Iwate, Japan.
²¹ Department of Gastroenterology and Hepatology, Gunma University Graduate School of Medicine, Gunma, Japan.
²² Division of Gastroenterology, Matsuyama Red Cross Hospital, Ehime, Japan.
²³ Department of Gastroenterological Surgery, Saitama Medical University International Medical Center, Saitama, Japan.
²⁴ Division of Gastroenterology and Hepatology, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan.
²⁵ Department of Surgery, Hiroshima City Hiroshima Citizens Hospital, Hiroshima, Japan.
²⁶ Department of Gastroenterology and Hepatology, Kindai University Faculty of Medicine, Osaka, Japan.
²⁷ Department of Surgery, Kurume University School of Medicine, Fukuoka, Japan.
²⁸ Department of Gastroenterology and Endoscopy, National Cancer Center Hospital East, Chiba, Japan.
²⁹ Department of Colorectal Surgery, National Cancer Center Hospital East, Chiba, Japan.
³⁰ Division of Gastroenterology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga, Japan.
³¹ Department of Coloproctological Surgery, Faculty of Medicine, Juntendo University, Tokyo, Japan.
³² Department of Human Pathology, Juntendo University Graduate School of Medicine, Tokyo, Japan.
³³ Department of Gastrointestinal Surgery, Kansai Medical University Hospital, Osaka, Japan.
³⁴ Department of Clinical Oncology, Kyoto University Hospital, Kyoto, Japan.
³⁵ Department of Surgery, Teikyo University Chiba Medical Center, Chiba, Japan.
³⁶ Department of Gastroenterology, Maebashi Red Cross Hospital, Gunma, Japan.
³⁷ Department of Gastroenterological Surgery, Aichi Cancer Center Hospital, Aichi, Japan.
³⁸ Department of Gastroenterology, Asahikawa City Hospital, Asahikawa, Hokkaido, Japan.
³⁹ Department of Colorectal Surgery, National Cancer Center Hospital, Tokyo, Japan.
⁴⁰ Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan.
⁴¹ Department of Surgery, Coloproctology Center Takano Hospital, Kumamoto, Japan.
⁴² Department of Surgical Oncology, The University of Tokyo, Tokyo, Japan.
⁴³ Department of Gastroenterology and Oncology, Tokushima University Graduate School of Biomedical Sciences, Tokushima, Japan.
⁴⁴ Department of Coloproctology, Aizu Medical Center, Fukushima Medical University, Fukushima, Japan.
⁴⁵ Department of Surgery, National Defense Medical College, Tokorozawa, Saitama, Japan.
⁴⁶ Department of Medicine and Clinical Science, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan.
⁴⁷ Department of Colorectal Surgery, Japanese Red Cross Medical Center, Tokyo, Japan.
⁴⁸ Department of Advanced Endoscopy, Fujita Health University School of Medicine, Aichi, Japan.
⁴⁹ Department of Surgery, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁵⁰ Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, Kyoto, Japan.
⁵¹ Department of Gastroenterology, Hiroshima City North Medical Center Asa Citizens Hospital, Hiroshima, Japan.
⁵² Department of Surgery, Japanese Red Cross Omori Hospital, Tokyo, Japan.
⁵³ Tokyo Medical and Dental University, Tokyo, Japan.
⁵⁴ Division of Molecular and Diagnostic Pathology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

PMID: 38411920
PMCID: PMC11033235
DOI: 10.1007/s00535-024-02081-3

Abstract

Background: The clinicopathological features and prognosis of primary small bowel adenocarcinoma (PSBA), excluding duodenal cancer, remain undetermined due to its rarity in Japan.

Methods: We analyzed 354 patients with 358 PSBAs, between January 2008 and December 2017, at 44 institutions affiliated with the Japanese Society for Cancer of the Colon and Rectum.

Results: The median age was 67 years (218 males, 61.6%). The average tumor size was 49.9 (7-100) mm. PSBA sites consisted of jejunum (66.2%) and ileum (30.4%). A total of 219 patients (61.9%) underwent diagnostic small bowel endoscopy, including single-balloon endoscopy, double-balloon endoscopy, and capsule endoscopy before treatment. Nineteen patients (5.4%) had Lynch syndrome, and 272 patients (76.8%) had symptoms at the initial diagnosis. The rates for stages 0, I, II, III, and IV were 5.4%, 2.5%, 27.1%, 26.0%, and 35.6%, respectively. The 5-year overall survival rates at each stage were 92.3%, 60.0%, 75.9%, 61.4%, and 25.5%, respectively, and the 5-year disease-specific survival (DSS) rates were 100%, 75.0%, 84.1%, 59.3%, and 25.6%, respectively. Patients with the PSBA located in the jejunum, with symptoms at the initial diagnosis or advanced clinical stage had a worse prognosis. However, multivariate analysis using Cox-hazard model revealed that clinical stage was the only significant predictor of DSS for patients with PSBA.

Conclusions: Of the patients with PSBA, 76.8% had symptoms at the initial diagnosis, which were often detected at an advanced stage. Detection during the early stages of PSBA is important to ensure a good prognosis.

Keywords: Capsule endoscopy; Double-balloon endoscopy; Lynch syndrome; Primary small bowel adenocarcinoma; Prognosis.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no conflicts of interest.

Figures

**Fig. 1**
Flowchart for enrolled tumors and patients in this study

**Fig. 2**
Prognosis of 354 patients with primary small bowel adenocarcinoma according to the clinical stage

**Fig. 3**
Prognosis of 342 patients with primary small bowel adenocarcinoma according to the tumor site

**Fig. 4**
Prognosis of 335 patients with primary small bowel adenocarcinoma according to the presence or absence of symptoms

See this image and copyright information in PMC

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References

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[1] Bilimoria KY, Bentrem DJ, Wayne JD, et al. Small bowel cancer in the United States: changes in epidemiology, treatment, and survival over the last 20 years. Ann Surg. 2009;249:63–71. doi: 10.1097/SLA.0b013e31818e4641. - DOI - PubMed

[2] Bilimoria KY, Bentrem DJ, Wayne JD, et al. Small bowel cancer in the United States: changes in epidemiology, treatment, and survival over the last 20 years. Ann Surg. 2009;249:63–71. doi: 10.1097/SLA.0b013e31818e4641. - DOI - PubMed

[3] Wilhelm A, Galata C, Beutner U, et al. Duodenal localization is a negative predictor of survival after small bowel adenocarcinoma resection: a population-based, propensity score-matched analysis. J Surg Oncol. 2018;117:397–408. doi: 10.1002/jso.24877. - DOI - PubMed

[4] Wilhelm A, Galata C, Beutner U, et al. Duodenal localization is a negative predictor of survival after small bowel adenocarcinoma resection: a population-based, propensity score-matched analysis. J Surg Oncol. 2018;117:397–408. doi: 10.1002/jso.24877. - DOI - PubMed

[5] Overman MJ, Hu C-Y, Kopetz S, et al. A population-based comparison of adenocarcinoma of the large and small intestine: insights into a rare disease. Ann Surg Oncol. 2012;19:1439–1445. doi: 10.1245/s10434-011-2173-6. - DOI - PMC - PubMed

[6] Overman MJ, Hu C-Y, Kopetz S, et al. A population-based comparison of adenocarcinoma of the large and small intestine: insights into a rare disease. Ann Surg Oncol. 2012;19:1439–1445. doi: 10.1245/s10434-011-2173-6. - DOI - PMC - PubMed

[7] Legué LM, Bernards N, Gerritse SL, et al. Trends in incidence, treatment and survival of small bowel adenocarcinomas between 1999 and 2013: a population-based study in the Netherlands. Acta Oncol. 2016;55:1183–1189. doi: 10.1080/0284186X.2016.1182211. - DOI - PubMed

[8] Legué LM, Bernards N, Gerritse SL, et al. Trends in incidence, treatment and survival of small bowel adenocarcinomas between 1999 and 2013: a population-based study in the Netherlands. Acta Oncol. 2016;55:1183–1189. doi: 10.1080/0284186X.2016.1182211. - DOI - PubMed

[9] Schottenfeld D, Beebe-Dimmer JL, Vigneau FD. The epidemiology and pathogenesis of neoplasia in the small intestine. Ann Epidemiol. 2009;19:58–69. doi: 10.1016/j.annepidem.2008.10.004. - DOI - PMC - PubMed

[10] Schottenfeld D, Beebe-Dimmer JL, Vigneau FD. The epidemiology and pathogenesis of neoplasia in the small intestine. Ann Epidemiol. 2009;19:58–69. doi: 10.1016/j.annepidem.2008.10.004. - DOI - PMC - PubMed

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Clinicopathological features and prognosis of primary small bowel adenocarcinoma: a large multicenter analysis of the JSCCR database in Japan

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Clinicopathological features and prognosis of primary small bowel adenocarcinoma: a large multicenter analysis of the JSCCR database in Japan

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Conflict of interest statement

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