International Journal of Colorectal Disease

, Volume 34, Issue 4, pp 621–628 | Cite as

D3 lymph node dissection reduces recurrence after primary resection for elderly patients with colon cancer

  • Masakatsu NumataEmail author
  • Sho Sawazaki
  • Toru Aoyama
  • Hiroshi Tamagawa
  • Tsutomu Sato
  • Hiroyuki Saeki
  • Yusuke Saigusa
  • Masataka Taguri
  • Hiroyuki Mushiake
  • Takashi Oshima
  • Norio Yukawa
  • Manabu Shiozawa
  • Yasushi Rino
  • Munetaka Masuda
Original Article



The favorable oncological impact of D3 lymph node dissection after colon cancer surgery has been described previously. However, D3 lymph node dissection is potentially more invasive than conventional D2 lymph node dissection. The oncological merit of D3 lymph node dissection in elderly patients with colon cancer remains unclear. This study aimed to clarify the oncological outcome after D3 lymph node dissection in patients with colon cancer aged > 75 years.


This is a retrospective cohort analysis using propensity matching method. The study was conducted at a university hospital and two community teaching hospitals in a large urban city. A total of 378 consecutive patients with pathological stage II and stage III colon cancer who underwent primary resection with either D2 or D3 lymph node dissection were retrospectively identified on a prospective database between 2000 and 2015. The primary and secondary outcomes of interests were recurrence-free survival and postoperative complication rate, respectively.


After propensity matching, 232 patients were analyzed. The long-term findings showed that the elderly who underwent D3 lymph node dissection had significantly better recurrence-free survival than those who underwent D2 lymph node dissection (p = 0.01). The incidence of postoperative complication was almost similar between the two groups.


D3 lymph node dissection provides better recurrence-free survival than D2 lymph node dissection after primary resection for elderly patients with pathological stage II and stage III colon cancer.


Lymph node dissection Colon cancer Elderly Oncological outcome 


Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Research involving human participants

All study protocols were approved by the Yokohama City University Institutional Review Board (Approval No. 170700003).

Informed consent

Informed consent was waived owing to the retrospective nature of the study. The details of the study protocol were provided to patients through a notice board in the hospital and were also published on the hospital websites.


  1. 1.
    Kotake K, Honjo S, Sugihara K, Hashiguchi Y, Kato T, Kodaira S, Muto T, Koyama Y (2012) Number of lymph nodes retrieved is an important determinant of survival of patients with stage II and stage III colorectal cancer. Jpn J Clin Oncol 42(1):29–35. CrossRefGoogle Scholar
  2. 2.
    Swanson RS, Compton CC, Stewart AK, Bland KI (2003) The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 10(1):65–71CrossRefGoogle Scholar
  3. 3.
    Watanabe T, Itabashi M, Shimada Y 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. CrossRefGoogle Scholar
  4. 4.
    Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Iversen ER, Kristensen B, Gögenur I (2015) Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 16(2):161–168. CrossRefGoogle Scholar
  5. 5.
    Vermillion SA, Hsu FC, Dorrell RD, Shen P, Clark CJ (2017) Modified frailty index predicts postoperative outcomes in older gastrointestinal cancer patients. J Surg Oncol 115(8):997–1003. CrossRefGoogle Scholar
  6. 6.
    Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA (2001) Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56(3):M146–M156CrossRefGoogle Scholar
  7. 7.
    Makary MA, Segev DL, Pronovost PJ, Syin D, Bandeen-Roche K, Patel P, Takenaga R, Devgan L, Holzmueller CG, Tian J, Fried LP (2010) Frailty as a predictor of surgical outcomes in older patients. J Am Coll Surg 210(6):901–908. CrossRefGoogle Scholar
  8. 8.
    Saxton A, Velanovich V (2011) Preoperative frailty and quality of life as predictors of postoperative complications. Ann Surg 253(6):1223–1229. CrossRefGoogle Scholar
  9. 9.
    Handforth C, Clegg A, Young C, Simpkins S, Seymour MT, Selby PJ, Young J (2015) The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann Oncol 26(6):1091–1101. CrossRefGoogle Scholar
  10. 10.
    Japanese Society for Cancer of the Colon and Rectum (2009) Japanese classification of colorectal carcinoma, 2nd English edn. Kanehara & Co., JapanGoogle Scholar
  11. 11.
    West NP, Kobayashi H, Takahashi K, Perrakis A, Weber K, Hohenberger W, Sugihara K, Quirke P (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. CrossRefGoogle Scholar
  12. 12.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213CrossRefGoogle Scholar
  13. 13.
    Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48(3):452–458. CrossRefGoogle Scholar
  14. 14.
    Kotake K, Mizuguchi T, Moritani K et al (2014) Impact of D3 lymph node dissection on survival for patients with T3 and T4 colon cancer. Int J Color Dis 29(7):847–852. CrossRefGoogle Scholar
  15. 15.
    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. CrossRefGoogle Scholar
  16. 16.
    Ouchi A, Komori K, Kimura K, Kinoshita T, Shimizu Y, Nagino M (2018) Survival benefit of Japanese extended lymphadenectomy for clinically node-negative and node-positive colorectal cancers. Dis Colon Rectum 61(2):162–171. CrossRefGoogle Scholar
  17. 17.
    Bertelsen CA, Kirkegaard-Klitbo A, Nielsen M, Leotta SM, Daisuke F, Gogenur 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):1209–1221CrossRefGoogle Scholar
  18. 18.
    Sirop S, Kanaan M, Korant A, Wiese D, Eilender D, Nagpal S, Arora M, Singh T, Saha S (2011) Detection and prognostic impact of micrometastasis in colorectal cancer. J Surg Oncol 103(6):534–537. CrossRefGoogle Scholar
  19. 19.
    Rahbari NN, Bork U, Motschall E, Thorlund K, Büchler MW, Koch M, Weitz J (2012) Molecular detection of tumor cells in regional lymph nodes is associated with disease recurrence and poor survival in node-negative colorectal cancer: a systematic review and meta-analysis. J Clin Oncol 30(1):60–70. CrossRefGoogle Scholar
  20. 20.
    Coller FA, Kay EB, Macintyre RS (1941) Regional lymphatic metastases of carcinoma of the colon. Ann Surg 114(1):56–67CrossRefGoogle Scholar
  21. 21.
    Emmanuel A, Haji A (2016) Complete mesocolic excision and extended (D3) lymphadenectomy for colonic cancer: is it worth that extra effort? A review of the literature. Int J Color Dis 31(4):797–804. CrossRefGoogle Scholar
  22. 22.
    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 364365. CrossRefGoogle Scholar
  23. 23.
    West NP, Hohenberger W, Weber K, Perrakis A, Finan PJ, Quirke P (2010) Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 28(2):272–278. CrossRefGoogle Scholar
  24. 24.
    Bertelsen CA, Neuenschwander AU, Jansen JE, Kirkegaard-Klitbo A, Tenma JR, Wilhelmsen M, Rasmussen LA, Jepsen LV, Kristensen B, Gögenur I, the Copenhagen Complete Mesocolic Excision Study (COMES), the Danish Colorectal Cancer Group (DCCG) (2016) Short-term outcomes after complete mesocolic excision compared with ‘conventional’ colonic cancer surgery. Br J Surg 103(5):581–589. CrossRefGoogle Scholar
  25. 25.
    Matsuoka H, Maeda K, Hanai T, Sato H, Masumori K, Koide Y, Katsuno H, Endo T, Shiota M, Sugihara K (2018) Surgical management of colorectal cancer for the aging population—a survey by the Japanese Society for Cancer of Colon and Rectum. Asian J Surg 41(2):192–196. CrossRefGoogle Scholar
  26. 26.
    Shiga M, Maeda H, Oba K, Okamoto K, Namikawa T, Fujisawa K, Yokota K, Kobayashi M, Hanazaki K (2017) Safety of laparoscopic surgery for colorectal cancer in patients over 80 years old: a propensity score matching study. Surg Today 47(8):951–958. CrossRefGoogle Scholar
  27. 27.
    Aquina CT, Mohile SG, Tejani MA, Becerra AZ, Xu Z, Hensley BJ, Arsalani-Zadeh R, Boscoe FP, Schymura MJ, Noyes K, Monson JRT, Fleming FJ (2017) The impact of age on complications, survival, and cause of death following colon cancer surgery. Br J Cancer 116(3):389–397CrossRefGoogle Scholar
  28. 28.
    Kvasnovsky CL, Adams K, Sideris M, Laycock J, Haji AK, Haq A, Nunoo-Mensah J, Papagrigoriadis S (2016) Elderly patients have more infectious complications following laparoscopic colorectal cancer surgery. Color Dis 18(1):94–100CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Masakatsu Numata
    • 1
    Email author
  • Sho Sawazaki
    • 1
  • Toru Aoyama
    • 1
  • Hiroshi Tamagawa
    • 1
  • Tsutomu Sato
    • 1
  • Hiroyuki Saeki
    • 2
  • Yusuke Saigusa
    • 3
  • Masataka Taguri
    • 3
  • Hiroyuki Mushiake
    • 1
  • Takashi Oshima
    • 4
  • Norio Yukawa
    • 1
  • Manabu Shiozawa
    • 4
  • Yasushi Rino
    • 1
  • Munetaka Masuda
    • 1
  1. 1.Department of SurgeryYokohama City UniversityYokohamaJapan
  2. 2.Department of SurgeryYokohama Minami Kyosai HospitalYokohamaJapan
  3. 3.Department of BiostatisticsYokohama City UniversityYokohamaJapan
  4. 4.Department of Gastroenterological SurgeryKanagawa Cancer HospitalYokohamaJapan

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