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Factors affecting R0 resection of colorectal cancer with synchronous peritoneal metastases: a multicenter prospective observational study by the Japanese Society for Cancer of the Colon and Rectum

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Abstract

Background

In Japan, R0 resection has been recommended for colorectal cancer patients with peritoneal metastases confined to the adjacent peritoneum and those with a few metastases to the distant peritoneum. R0 resection for M1c disease has drawn attention in Western countries and is currently considered an acceptable therapeutic option in the US National Comprehensive Cancer Network guidelines. However, clinical factors that affect the choice of R0 resection are unknown.

Methods

This multicenter, prospective, observational study was conducted by the Japanese Society for Cancer of the Colon and Rectum. Colorectal cancer patients with synchronous peritoneal metastases were enrolled at 28 institutions in Japan from October 2012 to December 2016. To determine factors affecting R0 resection and R1 resection with intended R0 resection, stepwise logistic regression analyses were performed on clinical factors including age, sex, performance status (PS), body mass index, peritoneal cancer index (PCI) score, presence of ascites, presence of distant metastases, and primary tumor site.

Results

R0/R1 resection was performed in 36 (31/5; 25%) of 146 patients. No distant metastases [odds ratio (OR) 52.9; 95% confidence interval (CI) 13.3–210.1; p < 0.0001], low PCI score (1–6) (OR 20.0; 95% CI 4.8–83.4; p < 0.0001), and high PS (0) (OR 2.40; 95% CI 0.66–8.68; p = 0.18) were independent factors affecting R0/R1 resection. PCI score and PS were also independent factors affecting R0/R1 resection in M1c patients without non-peritoneal distant metastases (n = 59).

Conclusion

Distant metastases, PCI score, and PS are three factors which affect R0 resection for M1c disease.

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Abbreviations

AUC:

Area under the curve

CI:

Confidence interval

CRC:

Colorectal cancer

HIPEC:

Hyperthermic intraperitoneal chemotherapy

NCCN:

National Comprehensive Cancer Network

OR:

Odds ratio

OS:

Overall survival

PCI:

Peritoneal cancer index

PS:

Performance status

ROC:

Receiver operating characteristic

TNM classification:

Tumor-node-metastasis classification

References

  1. Franko J, Shi Q, Meyers JP et al (2016) Prognosis of patients with peritoneal metastatic colorectal cancer given systemic therapy: an analysis of individual patient data from prospective randomised trials from the analysis and research in cancers of the digestive system (ARCAD) database. Lancet Oncol 17(12):1709–1719. https://doi.org/10.1016/S1470-2045(16)30500-9

    Article  PubMed  Google Scholar 

  2. UICC (2017) TNM classification of malignant tumours, 8th edn. Wiley, New York

    Google Scholar 

  3. Benson AB 3rd, Venook AP, Bekaii-Saab T et al (2014) Colon cancer, version 3. 2014. J Natl Compr Canc Netw 12(7):1028–1059.  https://doi.org/10.6004/jnccn.2014.0099

    Article  CAS  PubMed  Google Scholar 

  4. Benson AB 3rd, Venook AP, Cederquist L et al (2017) Colon cancer, Version 1.2017, NCCN Clin Pract Guid Oncol. J Natl Compr Canc Netw 15(3):370–398. https://doi.org/10.6004/jnccn.2017.0036

    Article  CAS  PubMed  Google Scholar 

  5. Mulsow J, Merkel S, Agaimy A et al (2011) Outcomes following surgery for colorectal cancer with synchronous peritoneal metastases. Br J Surg 98(12):1785–1791. https://doi.org/10.1002/bjs.7653

    Article  CAS  PubMed  Google Scholar 

  6. Sugarbaker PH, Ryan DP (2012) Cytoreductive surgery plus hyperthermic perioperative chemotherapy to treat peritoneal metastases from colorectal cancer: standard of care or an experimental approach? Lancet Oncol 13(8):e362–369. https://doi.org/10.1016/S1470-2045(12)70210-3

    Article  PubMed  Google Scholar 

  7. Benson AB, Venook AP, Al-Hawary MM et al (2018) NCCN guidelines insights: colon cancer, Version 2.2018. J Natl Compr Canc Netw 16(4):359–369. https://doi.org/10.6004/jnccn.2018.0021

    Article  PubMed  Google Scholar 

  8. Watanabe T, Muro K, Ajioka Y, Japanese Society for Cancer of the C, Rectum et al (2018) Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 23(1):1–34. https://doi.org/10.1007/s10147-017-1101-6

    Article  PubMed  Google Scholar 

  9. Hashiguchi Y, Muro K, Saito Y, Japanese Society for Cancer of the C, Rectum et al (2019) Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. https://doi.org/10.1007/s10147-019-01485-z

    Article  PubMed  PubMed Central  Google Scholar 

  10. Watanabe T, Itabashi M, Shimada Y, Japanese Society for Cancer of the C, Rectum et al (2012) Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol 17(1):1–29. https://doi.org/10.1007/s10147-011-0315-2

    Article  PubMed  Google Scholar 

  11. Watanabe T, Itabashi M, Shimada Y, Japanese Society for Cancer of the C, Rectum et al (2015) Japanese Society for Cancer of the Colon and Rectum (JSCCR) Guidelines 2014 for treatment of colorectal cancer. Int J Clin Oncol 20(2):207–239. https://doi.org/10.1007/s10147-015-0801-z

    Article  PubMed  PubMed Central  Google Scholar 

  12. Noura S, Ohue M, Ito Y et al (2016) New staging system for colorectal cancer patients with synchronous peritoneal metastasis in accordance with the japanese classification of colorectal carcinoma: a multi-institutional study. Dig Surg 33(1):66–73. https://doi.org/10.1159/000442027

    Article  PubMed  Google Scholar 

  13. Kobayashi H, Kotake K, Sugihara K (2014) Outcomes of surgery without HIPEC for synchronous peritoneal metastasis from colorectal cancer: data from a multi-center registry. Int J Clin Oncol 19(1):98–105. https://doi.org/10.1007/s10147-012-0505-6

    Article  PubMed  Google Scholar 

  14. Sato H, Maeda K, Kotake K et al (2016) Factors affecting recurrence and prognosis after R0 resection for colorectal cancer with peritoneal metastasis. J Gastroenterol 51(5):465–472. https://doi.org/10.1007/s00535-015-1122-8

    Article  CAS  PubMed  Google Scholar 

  15. Shida D, Tsukamoto S, Ochiai H et al (2018) Long-term outcomes after R0 resection of synchronous peritoneal metastasis from colorectal cancer without cytoreductive surgery or hyperthermic intraperitoneal chemotherapy. Ann Surg Oncol 25(1):173–178. https://doi.org/10.1245/s10434-017-6133-7

    Article  PubMed  Google Scholar 

  16. Shida D, Tanabe T, Boku N et al (2019) Prognostic value of primary tumor sidedness for unresectable stage IV colorectal cancer: a retrospective study. Ann Surg Oncol 26(5):1358–1365. https://doi.org/10.1245/s10434-019-07209-x

    Article  PubMed  Google Scholar 

  17. Wittekind C, Compton CC, Greene FL et al (2002) TNM residual tumor classification revisited. Cancer 94(9):2511–2516. https://doi.org/10.1002/cncr.10492

    Article  PubMed  Google Scholar 

  18. JSCCR (2018) Japanese classification of colorectal, appendiceal, and anal carcinoma, 9th edn. Kanehara & Co., Ltd, Tokyo

    Google Scholar 

  19. Shida D, Yoshida T, Tanabe T et al (2018) Prognostic impact of R0 resection and targeted therapy for colorectal cancer with synchronous peritoneal metastasis. Ann Surg Oncol 25(6):1646–1653. https://doi.org/10.1245/s10434-018-6436-3

    Article  PubMed  Google Scholar 

  20. Bushati M, Rovers KP, Sommariva A et al (2018) The current practice of cytoreductive surgery and HIPEC for colorectal peritoneal metastases: results of a worldwide web-based survey of the peritoneal surface oncology group international (PSOGI). Eur J Surg Oncol 44(12):1942–1948. https://doi.org/10.1016/j.ejso.2018.07.003

    Article  CAS  PubMed  Google Scholar 

  21. Vallicelli C, Cavaliere D, Catena F et al (2014) Management of peritoneal carcinomatosis from colorectal cancer: review of the literature. Int J Colorectal Dis 29(8):895–898. https://doi.org/10.1007/s00384-014-1907-x

    Article  PubMed  Google Scholar 

  22. Stillwell AP, Ho YH, Veitch C (2011) Systematic review of prognostic factors related to overall survival in patients with stage IV colorectal cancer and unresectable metastases. World J Surg 35(3):684–692. https://doi.org/10.1007/s00268-010-0891-8

    Article  PubMed  Google Scholar 

  23. Arnold D, Lueza B, Douillard JY et al (2017) Prognostic and predictive value of primary tumour side in patients with RAS wild-type metastatic colorectal cancer treated with chemotherapy and EGFR directed antibodies in six randomized trials. Ann Oncol 28(8):1713–1729. https://doi.org/10.1093/annonc/mdx175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kobayashi H, Kotake K, Funahashi K, Study Group for Peritoneal Metastasis from Colorectal Cancer by the Japanese Society for Cancer of the C, Rectum et al (2014) Clinical benefit of surgery for stage IV colorectal cancer with synchronous peritoneal metastasis. J Gastroenterol 49(4):646–654. https://doi.org/10.1007/s00535-013-0820-3

    Article  PubMed  Google Scholar 

  25. Shida D (2018) ASO author reflections: long-term outcomes After R0 resection of colorectal peritoneal metastasis. Ann Surg Oncol 25(Suppl 3):832–833. https://doi.org/10.1245/s10434-018-6782-1

    Article  PubMed  Google Scholar 

  26. Shida D (2018) ASO author reflections: R0 resection and targeted therapy for colorectal peritoneal metastasis. Ann Surg Oncol 25(Suppl 3):842–843. https://doi.org/10.1245/s10434-018-6890-y

    Article  PubMed  Google Scholar 

  27. Kobayashi H, Kotake K, Study Group for Peritoneal Metastasis from Colorectal Cancer by the Japanese Society for Cancer of the C, Rectum (2014) Enhancing the objectivity of the Japanese classification of peritoneal metastases from colorectal cancer. Jpn J Clin Oncol 44(10):898–902. https://doi.org/10.1093/jjco/hyu114

    Article  PubMed  Google Scholar 

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Acknowledgements

This study is based on data collected from 28 hospitals participating in a multicenter, prospective, observational study of CRC with synchronous peritoneal metastases conducted by the JSCCR. We thank all the participating patients and their families, as well as investigators and operation staff members. We also thank Masamichi Yasuno (Tokyo Medical and Dental University), Masayuki Ohue (Osaka International Cancer Institute), Hideo Yano (National Center for Global Health and Medicine), Soichiro Ishihara (University of Tokyo), Keiji Koda (Teikyo University Chiba Medical Center), Hirotoshi Kobayashi (Tokyo Metropolitan Hiroo Hospital), Fumio Baba (Kumamoto University), Yoshiharu Sakai (Kyoto University), Yojiro Hashiguchi (Teikyo University), Akio Yamaguchi (University of Fukui), Masato Kusunoki (Mie University), Naohiro Tomita (Hyogo College of Medicine), Tadahiko Masaki (Kyorin University), Yoshito Akagi (Kurume University), Mitsuyoshi Ota (Yokohama City University Medical Center), Kenichi Hakamada (Hirosaki University), and Yasuhiro Kodera (Nagoya University).

Funding

None to report.

Author information

Authors and Affiliations

  1. Department of Colorectal Surgery, National Cancer Center Hospital, 5-1-1 Tsukiji, Chuo-ku, Tokyo, 1040045, Japan

    Dai Shida & Yukihide Kanemitsu

  2. Department of Surgery, Teikyo University Mizonokuchi Hospital, Kawasaki, Japan

    Hirotoshi Kobayashi

  3. Department of Surgery, Bell Land General Hospital, Sakai, Japan

    Masao Kameyama

  4. National Defense Medical College, Tokorozawa, Japan

    Kazuo Hase

  5. International Medical Center, Fujita Health University Hospital, Toyoake, Japan

    Kotaro Maeda

  6. Department of Gastroenterological Surgery, Yamagata Prefectural Central Hospital, Yamagata, Japan

    Takeshi Suto

  7. Department of Surgery, Institute of Gastroenterology, Tokyo Women’s Medical University, Tokyo, Japan

    Michio Itabashi

  8. Department of General and Gastroenterological Surgery, Toho University Omori Medical Center, Tokyo, Japan

    Kimihiko Funahashi

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

    Fumikazu Koyama

  10. Department of Surgery, Tochigi Cancer Center, Utsunomiya, Japan

    Heita Ozawa

  11. Department of Surgery, Osaka Rosai Hospital, Sakai, Japan

    Shingo Noura

  12. Department of Digestive Tract and General Surgery, Saitama Medical Center, Saitama Medical University, Kawagoe, Japan

    Hideyuki Ishida

  13. Department of Gastroenterology and Surgery, Sano City Hospital, Sano, Japan

    Kenjiro Kotake

  14. Tokyo Medical and Dental University, Tokyo, Japan

    Kenichi Sugihara

Authors
  1. Dai Shida
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  2. Hirotoshi Kobayashi
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  4. Kazuo Hase
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  14. Kenjiro Kotake
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  15. Kenichi Sugihara
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Corresponding author

Correspondence to Dai Shida.

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All authors: Study Group for Peritoneal Metastasis from Colorectal Cancer by the Japanese Society for Cancer of the Colon and Rectum.

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Shida, D., Kobayashi, H., Kameyama, M. et al. Factors affecting R0 resection of colorectal cancer with synchronous peritoneal metastases: a multicenter prospective observational study by the Japanese Society for Cancer of the Colon and Rectum. Int J Clin Oncol 25, 330–337 (2020). https://doi.org/10.1007/s10147-019-01562-3

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  • DOI: https://doi.org/10.1007/s10147-019-01562-3

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