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Prognostic value of lymph node distribution after laparoscopic colectomy with Japanese D3 dissection

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Abstract

Purpose

Positive pathologic lymph nodes in colorectal cancer represent an important prognostic indicator. Whether lymph node distribution or the number of metastatic nodes is more strongly associated with survival prediction remains controversial.

Methods

Among 3449 colorectal cancer surgeries performed at Nagasaki University Hospital and five affiliated institutions from April 2016 to March 2022, we investigated 604 patients who underwent laparoscopic radical resection and were diagnosed with pathological stage III cancer. Patients were divided into two groups according to whether they had central vessel metastasis (LND3 group, n=42) or not (LND1/2 group, n=562). After adjusting for background factors using propensity score matching, the LND3 group included 42 patients and the LND1/2 group included 40 patients. Patient background characteristics and prognosis were compared between these two groups.

Results

Before matching, frequencies of right-side colon cancer (64.3% vs 38.1%, p=0.001), multivisceral resection (11.9% vs 4.4%, p=0.039), clinical N2 status (40.5% vs 22.6%, p=0.032), and pathological N2 (73.8% vs 22.6%, p<0.001) were all greater, and the number of lymph nodes retrieved was higher (24 vs 19, p=0.042) in the LND3 group. After matching, no differences in any clinical factors were evident between groups. Five-year RFS (44.8% vs 77.1%, p=0.004) and OS (43.1% vs 83.2%, p<0.001) were worse in the LND3 group. Adjuvant chemotherapy improved RFS (adjuvant chemotherapy (+) vs adjuvant chemotherapy (−): 62.1% vs 27.7%, p=0.047) in the LND3 group.

Conclusion

LND3-positive patients show poorer prognosis than LND1/2 patients and should be treated with an appropriate perioperative treatment strategy.

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Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation--technical notes and outcome. Color Dis 11(4):354–364 discussion 64-5

    Article  CAS  Google Scholar 

  2. West NP, Kobayashi H, Takahashi K, Perrakis A, Weber K, Hohenberger W et al (2012) Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J Clin Oncol 30(15):1763–1769

    Article  PubMed  Google Scholar 

  3. Merrie AE, Phillips LV, Yun K, McCall JL (2001) Skip metastases in colon cancer: assessment by lymph node map** using molecular detection. Surgery. 129(6):684–691

    Article  PubMed  CAS  Google Scholar 

  4. **e D, Yu C, Gao C, Osaiweran H, Hu J, Gong J (2017) An optimal approach for laparoscopic D3 lymphadenectomy plus complete mesocolic excision (D3+CME) for right-sided colon cancer. Ann Surg Oncol 24(5):1312–1313

    Article  PubMed  Google Scholar 

  5. Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ et al (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21(15):2912–2919

    Article  PubMed  Google Scholar 

  6. Tominaga T, Yamaguchi T, Nagasaki T, Akiyoshi T, Nagayama S, Fukunaga Y et al (2021) Improved oncologic outcomes with increase of laparoscopic surgery in modified complete mesocolic excision with D3 lymph node dissection for T3/4a colon cancer: results of 1191 consecutive patients during a 10-year period: a retrospective cohort study. Int J Clin Oncol 26(5):893–902

    Article  PubMed  CAS  Google Scholar 

  7. Hashiguchi Y, Hase K, Ueno H, Mochizuki H, Kajiwara Y, Ichikura T et al (2010) Prognostic significance of the number of lymph nodes examined in colon cancer surgery: clinical application beyond simple measurement. Ann Surg 251(5):872–881

    Article  PubMed  Google Scholar 

  8. Newland RC, Dent OF, Lyttle MN, Chapuis PH, Bokey EL (1994) Pathologic determinants of survival associated with colorectal cancer with lymph node metastases. A multivariate analysis of 579 patients. Cancer. 73(8):2076–2082

    Article  PubMed  CAS  Google Scholar 

  9. Huh JW, Kim CH, Kim HR, Kim YJ (2012) Factors predicting oncologic outcomes in patients with fewer than 12 lymph nodes retrieved after curative resection for colon cancer. J Surg Oncol 105(2):125–129

    Article  PubMed  Google Scholar 

  10. Kim CH, Huh JW, Kim HR, Kim YJ (2014) Prognostic comparison between number and distribution of lymph node metastases in patients with right-sided colon cancer. Ann Surg Oncol 21(4):1361–1368

    Article  PubMed  Google Scholar 

  11. Hashiguchi Y, Muro K, Saito Y, Ito Y, Ajioka Y, Hamaguchi T et al (2020) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 25(1):1–42

    Article  PubMed  Google Scholar 

  12. Kobayashi H, Enomoto M, Higuchi T, Uetake H, Iida S, Ishikawa T et al (2011) Clinical significance of lymph node ratio and location of nodal involvement in patients with right colon cancer. Dig Surg 28(3):190–197

    Article  PubMed  Google Scholar 

  13. Kanemitsu Y, Komori K, Kimura K, Kato T (2013) D3 lymph node dissection in right hemicolectomy with a no-touch isolation technique in patients with colon cancer. Dis Colon Rectum 56(7):815–824

    Article  PubMed  Google Scholar 

  14. Shatari T, Fujita M, Nozawa K, Haku K, Niimi M, Ikeda Y et al (2003) Vascular anatomy for right colon lymphadenectomy. Surg Radiol Anat 25(2):86–88

    Article  PubMed  CAS  Google Scholar 

  15. Garćia-Ruiz A, Milsom JW, Ludwig KA, Marchesa P (1996) Right colonic arterial anatomy. Implications for laparoscopic surgery. Dis Colon Rectum 39(8):906–911

    Article  PubMed  Google Scholar 

  16. Nagasaki T, Akiyoshi T, Fujimoto Y, Konishi T, Nagayama S, Fukunaga Y et al (2015) Prognostic impact of distribution of lymph node metastases in stage III colon cancer. World J Surg 39(12):3008–3015

    Article  PubMed  Google Scholar 

  17. Watanabe T, Itabashi M, Shimada Y, Tanaka S, Ito Y, Ajioka Y 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

    Article  PubMed  PubMed Central  Google Scholar 

  18. Balciscueta Z, Balciscueta I, Uribe N, Pellino G, Frasson M, Garcia-Granero E et al (2021) D3-lymphadenectomy enhances oncological clearance in patients with right colon cancer. Result of a meta-analysis. Eur J Surg Oncol 47(7):1541–1551

    Article  PubMed  Google Scholar 

  19. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD et al (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196

    Article  PubMed  Google Scholar 

  20. West NP, Morris EJ, Rotimi O, Cairns A, Finan PJ, Quirke P (2008) Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study. Lancet Oncol 9(9):857–865

    Article  PubMed  Google Scholar 

  21. Zurleni T, Cassiano A, Gjoni E, Ballabio A, Serio G, Marzoli L et al (2018) Surgical and oncological outcomes after complete mesocolic excision in right-sided colon cancer compared with conventional surgery: a retrospective, single-institution study. Int J Color Dis 33(1):1–8

    Article  Google Scholar 

  22. Benson AB 3rd, Venook AP, Cederquist L, Chan E, Chen YJ, Cooper HS et al (2017) Colon Cancer, Version 1.2017, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 15(3):370–398

    Article  PubMed  CAS  Google Scholar 

  23. Weber K, Merkel S, Perrakis A, Hohenberger W (2013) Is there a disadvantage to radical lymph node dissection in colon cancer? Int J Color Dis 28(2):217–226

    Article  CAS  Google Scholar 

  24. Cho MS, Baek SJ, Hur H, Soh Min B, Baik SH, Kyu KN (2015) Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg 261(4):708–715

    Article  PubMed  Google Scholar 

  25. Kim JC, Lee KH, Yu CS, Kim HC, Kim JR, Chang HM et al (2004) The clinicopathological significance of inferior mesenteric lymph node metastasis in colorectal cancer. Eur J Surg Oncol 30(3):271–279

    Article  PubMed  CAS  Google Scholar 

  26. Bertelsen CA, Kirkegaard-Klitbo A, Nielsen M, Leotta SM, Daisuke F, Gögenur I (2016) Pattern of colon cancer lymph node metastases in patients undergoing central mesocolic lymph node excision: a systematic review. Dis Colon Rectum 59(12):1209–1221

    Article  PubMed  Google Scholar 

  27. Kataoka K, Beppu N, Shiozawa M, Ikeda M, Tomita N, Kobayashi H et al (2020) Colorectal cancer treated by resection and extended lymphadenectomy: patterns of spread in left- and right-sided tumours. Br J Surg 107(8):1070–1078

    Article  PubMed  CAS  Google Scholar 

  28. Sehgal R, Coffey JC (2014) Historical development of mesenteric anatomy provides a universally applicable anatomic paradigm for complete/total mesocolic excision. Gastroenterol Rep (Oxf) 2(4):245–250

    Article  PubMed  Google Scholar 

  29. Cheong CK, Nistala KRY, Ng CH, Syn N, Chang HSY, Sundar R et al (2020) Neoadjuvant therapy in locally advanced colon cancer: a meta-analysis and systematic review. J Gastrointest Oncol 11(5):847–857

    Article  PubMed  PubMed Central  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Surgical Oncology, Nagasaki University Graduate School of Biomedical Science, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan

    Keisuke Noda, Tetsuro Tominaga, Takashi Nonaka, Rika Ono, Kaido Oishi, Yuma Takamura & Takeshi Nagayasu

  2. Department of Surgery, Isahaya General Hospital, 24-1 Isahaya, Nagasaki, 854-8501, Japan

    Keisuke Noda & Mitsutoshi Ishii

  3. Department of Surgery, Sasebo City General Hospital, 9-3 Hirasemachi, Nagasaki, 857-8511, Japan

    Makoto Hisanaga

  4. Department of Surgery, National Hospital Organization Nagasaki Medical Center, 1-1001-1 Omura, Nagasaki, 856-8562, Japan

    Hiroaki Takeshita

  5. Department of Surgery, Ureshino Medical Center, 4279-3 Ureshino, Saga, 843-0393, Japan

    Shosaburo Oyma

  6. Department of Surgery, Saiseikai Nagasaki Hospital, 2-5-1 Katafuchi, Nagasaki, 850-0003, Japan

    Kazuhide Ishimaru

Authors
  1. Keisuke Noda
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  2. Tetsuro Tominaga
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  12. Takeshi Nagayasu
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Contributions

KN and TT mainly designed the study and analyzed the data. TN, RO, KO, YT, MI, MH, HT, SO, and KI performed surgery and provided patient care. TN supervised this study.

Corresponding author

Correspondence to Tetsuro Tominaga.

Ethics declarations

Ethics approval

This research study was conducted retrospectively using data obtained for clinical purposes, and was reviewed and approved by the Clinical Research Review Board of Nagasaki University Hospital (approval no. 16062715-5).

Consent to participate

Informed consent was obtained as part of routine care from all individual participants included in the study.

Competing interests

The authors declare no competing interests.

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Noda, K., Tominaga, T., Nonaka, T. et al. Prognostic value of lymph node distribution after laparoscopic colectomy with Japanese D3 dissection. Langenbecks Arch Surg 409, 28 (2024). https://doi.org/10.1007/s00423-023-03222-7

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