Skip to main content
Top
Published in: International Journal of Colorectal Disease 1/2021

01-01-2021 | Lymphadenectomy | Original Article

Proposal for a post-operative surveillance strategy for stage I colorectal cancer patients based on a novel recurrence risk stratification: a multicenter retrospective study

Authors: Tsuyoshi Ozawa, Yojiro Hashiguchi, Soichiro Ishihara, Tamuro Hayama, Takeshi Tsuchiya, Keijiro Nozawa, Shinichi Yamauchi, Kenichi Sugihara, Keiji Matsuda

Published in: International Journal of Colorectal Disease | Issue 1/2021

Login to get access

Abstract

Background

The recurrent risk of stage I colorectal cancer (CRC) is not clear, and the data regarding appropriate post-operative surveillance schedules in stage I CRC are scarce.

Objectives

We aimed to stratify stage I CRC based on the recurrence risk and evaluate optimal post-operative surveillance durations based on this stratification.

Methods

We retrospectively analyzed the cases of 6607 stage I CRC patients from 24 institutions. To assess the patients’ clinicopathological factors that impact recurrence-free survival (RFS), we performed univariate and multivariate analyses using Cox proportional hazards models. We divided the patients into classes based on their numbers of factors that were associated with poor RFI in the multivariate analysis.

Results

Recurrence occurred in 3.9% patients. The multivariate analysis revealed the independent factors for poor RFS: rectal cancer, T2 depth, presence of lymphatic invasion, high level of pre-operative carcinoembryonic antigen, and absence of D2–3 lymphadenectomy. We also divided the patients into three classes based on their numbers of these risk factors; the 3-year and 5-year RFS rates were 99.3% and 99.1% in the no-risk patients, 97.4% and 96.5% in the patients with 1–2 risks, and 92.1% and 90.0% in the patients with 3–5 risks, respectively. In the patients with no risk and in the patients with 1–2 risks after 3 years post-surgery, ≤ 1% recurrence occurred. Thus, post-operative surveillance may be omitted in these populations.

Conclusions

Our new classification properly stratified the recurrence risks of stage I CRC patients, and may help reduce unnecessary post-operative surveillance.
Appendix
Available only for authorised users
Literature
1.
go back to reference Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, Jemal A (2017) Colorectal cancer statistics, 2017. CA Cancer J Clin 67(3):177–193CrossRef Siegel RL, Miller KD, Fedewa SA, Ahnen DJ, Meester RGS, Barzi A, Jemal A (2017) Colorectal cancer statistics, 2017. CA Cancer J Clin 67(3):177–193CrossRef
2.
go back to reference Kattan MW, Hess KR, Amin MB, Lu Y, Moons KG, Gershenwald JE, Gimotty PA, Guinney JH, Halabi S, Lazar AJ, Mahar AL, Patel T, Sargent DJ, Weiser MR, Compton C, members of the AJCC Precision Medicine Core (2016) American Joint Committee on Cancer acceptance criteria for inclusion of risk models for individualized prognosis in the practice of precision medicine. CA Cancer J Clin 66(5):370–374CrossRef Kattan MW, Hess KR, Amin MB, Lu Y, Moons KG, Gershenwald JE, Gimotty PA, Guinney JH, Halabi S, Lazar AJ, Mahar AL, Patel T, Sargent DJ, Weiser MR, Compton C, members of the AJCC Precision Medicine Core (2016) American Joint Committee on Cancer acceptance criteria for inclusion of risk models for individualized prognosis in the practice of precision medicine. CA Cancer J Clin 66(5):370–374CrossRef
3.
go back to reference Hashiguchi Y, Muro K, Saito Y 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. 25(1):1–42 Hashiguchi Y, Muro K, Saito Y 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. 25(1):1–42
4.
go back to reference Kim C, Kim WR, Kim KY, Chon HJ, Beom SH, Kim H, Jung M, Shin SJ, Kim NK, Ahn JB (2018) Predictive nomogram for recurrence of stage I colorectal cancer after curative resection. Clin Colorectal Cancer 17(3):e513–e518CrossRef Kim C, Kim WR, Kim KY, Chon HJ, Beom SH, Kim H, Jung M, Shin SJ, Kim NK, Ahn JB (2018) Predictive nomogram for recurrence of stage I colorectal cancer after curative resection. Clin Colorectal Cancer 17(3):e513–e518CrossRef
5.
go back to reference Blumberg D, Paty PB, Picon AI et al (1998) Stage I rectal cancer: identification of high-risk patients. J Am Coll Surg 186(5):574–579 discussion 579-80CrossRef Blumberg D, Paty PB, Picon AI et al (1998) Stage I rectal cancer: identification of high-risk patients. J Am Coll Surg 186(5):574–579 discussion 579-80CrossRef
6.
go back to reference Costas-Chavarri A, Nandakumar G, Temin S, Lopes G, Cervantes A, Cruz Correa M, Engineer R, Hamashima C, Ho GF, Huitzil FD, Malekzadeh Moghani M, Sharara AI, Stern MC, Teh C, Vázquez Manjarrez SE, Verjee A, Yantiss R, Shah MA (2019) Treatment of patients with early-stage colorectal cancer: ASCO resource-stratified guideline. J Glob Oncol 5:1–19CrossRef Costas-Chavarri A, Nandakumar G, Temin S, Lopes G, Cervantes A, Cruz Correa M, Engineer R, Hamashima C, Ho GF, Huitzil FD, Malekzadeh Moghani M, Sharara AI, Stern MC, Teh C, Vázquez Manjarrez SE, Verjee A, Yantiss R, Shah MA (2019) Treatment of patients with early-stage colorectal cancer: ASCO resource-stratified guideline. J Glob Oncol 5:1–19CrossRef
7.
go back to reference Rodriguez-Moranta F, Salo J, Arcusa A et al (2006) Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial. J Clin Oncol 24(3):386–393CrossRef Rodriguez-Moranta F, Salo J, Arcusa A et al (2006) Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial. J Clin Oncol 24(3):386–393CrossRef
8.
go back to reference van der Stok EP, Spaander MCW, Grunhagen DJ et al (2017) Surveillance after curative treatment for colorectal cancer. Nat Rev Clin Oncol 14(5):297–315CrossRef van der Stok EP, Spaander MCW, Grunhagen DJ et al (2017) Surveillance after curative treatment for colorectal cancer. Nat Rev Clin Oncol 14(5):297–315CrossRef
9.
go back to reference Sargent D, Sobrero A, Grothey A, O’Connell MJ, Buyse M, Andre T, Zheng Y, Green E, Labianca R, O’Callaghan C, Seitz JF, Francini G, Haller D, Yothers G, Goldberg R, de Gramont A (2009) Evidence for cure by adjuvant therapy in colon cancer: observations based on individual patient data from 20,898 patients on 18 randomized trials. J Clin Oncol 27(6):872–877CrossRef Sargent D, Sobrero A, Grothey A, O’Connell MJ, Buyse M, Andre T, Zheng Y, Green E, Labianca R, O’Callaghan C, Seitz JF, Francini G, Haller D, Yothers G, Goldberg R, de Gramont A (2009) Evidence for cure by adjuvant therapy in colon cancer: observations based on individual patient data from 20,898 patients on 18 randomized trials. J Clin Oncol 27(6):872–877CrossRef
10.
go back to reference Hashiguchi Y, Hase K, Ueno H, Mochizuki H, Shinto E, Yamamoto J (2011) Optimal margins and lymphadenectomy in colonic cancer surgery. Br J Surg 98(8):1171–1178CrossRef Hashiguchi Y, Hase K, Ueno H, Mochizuki H, Shinto E, Yamamoto J (2011) Optimal margins and lymphadenectomy in colonic cancer surgery. Br J Surg 98(8):1171–1178CrossRef
11.
go back to reference Benson AB 3rd, Schrag D, Somerfield MR et al (2004) American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol 22(16):3408–3419CrossRef Benson AB 3rd, Schrag D, Somerfield MR et al (2004) American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage II colon cancer. J Clin Oncol 22(16):3408–3419CrossRef
12.
go back to reference Grothey A, Sobrero AF, Shields AF, Yoshino T, Paul J, Taieb J, Souglakos J, Shi Q, Kerr R, Labianca R, Meyerhardt JA, Vernerey D, Yamanaka T, Boukovinas I, Meyers JP, Renfro LA, Niedzwiecki D, Watanabe T, Torri V, Saunders M, Sargent DJ, Andre T, Iveson T (2018) Duration of adjuvant chemotherapy for stage III colon cancer. N Engl J Med 378(13):1177–1188CrossRef Grothey A, Sobrero AF, Shields AF, Yoshino T, Paul J, Taieb J, Souglakos J, Shi Q, Kerr R, Labianca R, Meyerhardt JA, Vernerey D, Yamanaka T, Boukovinas I, Meyers JP, Renfro LA, Niedzwiecki D, Watanabe T, Torri V, Saunders M, Sargent DJ, Andre T, Iveson T (2018) Duration of adjuvant chemotherapy for stage III colon cancer. N Engl J Med 378(13):1177–1188CrossRef
13.
go back to reference Salazar R, Roepman P, Capella G, Moreno V, Simon I, Dreezen C, Lopez-Doriga A, Santos C, Marijnen C, Westerga J, Bruin S, Kerr D, Kuppen P, van de Velde C, Morreau H, van Velthuysen L, Glas AM, van’t Veer LJ, Tollenaar R (2011) Gene expression signature to improve prognosis prediction of stage II and III colorectal cancer. J Clin Oncol 29(1):17–24CrossRef Salazar R, Roepman P, Capella G, Moreno V, Simon I, Dreezen C, Lopez-Doriga A, Santos C, Marijnen C, Westerga J, Bruin S, Kerr D, Kuppen P, van de Velde C, Morreau H, van Velthuysen L, Glas AM, van’t Veer LJ, Tollenaar R (2011) Gene expression signature to improve prognosis prediction of stage II and III colorectal cancer. J Clin Oncol 29(1):17–24CrossRef
14.
go back to reference Sinicrope FA, Shi Q, Smyrk TC, Thibodeau SN, Dienstmann R, Guinney J, Bot BM, Tejpar S, Delorenzi M, Goldberg RM, Mahoney M, Sargent DJ, Alberts SR (2015) Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes. Gastroenterology 148(1):88–99CrossRef Sinicrope FA, Shi Q, Smyrk TC, Thibodeau SN, Dienstmann R, Guinney J, Bot BM, Tejpar S, Delorenzi M, Goldberg RM, Mahoney M, Sargent DJ, Alberts SR (2015) Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes. Gastroenterology 148(1):88–99CrossRef
15.
go back to reference Teloken PE, Ransom D, Faragher I, Jones I, Gibbs P, Platell C (2016) Recurrence in patients with stage I colorectal cancer. ANZ J Surg 86(1–2):49–53CrossRef Teloken PE, Ransom D, Faragher I, Jones I, Gibbs P, Platell C (2016) Recurrence in patients with stage I colorectal cancer. ANZ J Surg 86(1–2):49–53CrossRef
16.
go back to reference Chok KS, Law WL (2007) Prognostic factors affecting survival and recurrence of patients with pT1 and pT2 colorectal cancer. World J Surg 31(7):1485–1490CrossRef Chok KS, Law WL (2007) Prognostic factors affecting survival and recurrence of patients with pT1 and pT2 colorectal cancer. World J Surg 31(7):1485–1490CrossRef
17.
go back to reference Mroczkowski P, Schmidt U, Sahm M, Gastinger I, Lippert H, Kube R (2012) Prognostic factors assessed for 15,096 patients with colon cancer in stages I and II. World J Surg 36(7):1693–1698CrossRef Mroczkowski P, Schmidt U, Sahm M, Gastinger I, Lippert H, Kube R (2012) Prognostic factors assessed for 15,096 patients with colon cancer in stages I and II. World J Surg 36(7):1693–1698CrossRef
18.
go back to reference Kang SI, Kim DW, Kwak Y, Lee HS, Kim MH, Kim MJ, Oh HK, Kang SB (2018) The prognostic implications of primary tumor location on recurrence in early-stage colorectal cancer with no associated risk factors. Int J Color Dis 33(6):719–726CrossRef Kang SI, Kim DW, Kwak Y, Lee HS, Kim MH, Kim MJ, Oh HK, Kang SB (2018) The prognostic implications of primary tumor location on recurrence in early-stage colorectal cancer with no associated risk factors. Int J Color Dis 33(6):719–726CrossRef
19.
go back to reference Bertelsen CA, Neuenschwander AU, Jansen JE, Tenma JR, Wilhelmsen M, Kirkegaard-Klitbo A, Iversen ER, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Born PW, Kristensen B, Kleif J (2019) 5-year outcome after complete mesocolic excision for right-sided colon cancer: a population-based cohort study. Lancet Oncol 20(11):1556–1565CrossRef Bertelsen CA, Neuenschwander AU, Jansen JE, Tenma JR, Wilhelmsen M, Kirkegaard-Klitbo A, Iversen ER, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Born PW, Kristensen B, Kleif J (2019) 5-year outcome after complete mesocolic excision for right-sided colon cancer: a population-based cohort study. Lancet Oncol 20(11):1556–1565CrossRef
20.
go back to reference Primrose JN, Perera R, Gray A, Rose P, Fuller A, Corkhill A, George S, Mant D, FACS Trial Investigators (2014) Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA 311(3):263–270CrossRef Primrose JN, Perera R, Gray A, Rose P, Fuller A, Corkhill A, George S, Mant D, FACS Trial Investigators (2014) Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA 311(3):263–270CrossRef
21.
go back to reference Snyder RA, Hu CY, Cuddy A, Francescatti AB, Schumacher JR, van Loon K, You YN, Kozower BD, Greenberg CC, Schrag D, Venook A, McKellar D, Winchester DP, Chang GJ, for the Alliance for Clinical Trials in Oncology Network Cancer Surveillance Optimization Working Group (2018) Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer. JAMA 319(20):2104–2115CrossRef Snyder RA, Hu CY, Cuddy A, Francescatti AB, Schumacher JR, van Loon K, You YN, Kozower BD, Greenberg CC, Schrag D, Venook A, McKellar D, Winchester DP, Chang GJ, for the Alliance for Clinical Trials in Oncology Network Cancer Surveillance Optimization Working Group (2018) Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer. JAMA 319(20):2104–2115CrossRef
22.
go back to reference Benson AB, Venook AP, Al-Hawary MM et al (2018) NCCN guidelines insights: colon cancer, version 2.2018. J Natl Compr Cancer Netw 16(4):359–369CrossRef Benson AB, Venook AP, Al-Hawary MM et al (2018) NCCN guidelines insights: colon cancer, version 2.2018. J Natl Compr Cancer Netw 16(4):359–369CrossRef
23.
go back to reference Steele SR, Chang GJ, Hendren S, Weiser M, Irani J, Buie WD, Rafferty JF (2015) Practice guideline for the surveillance of patients after curative treatment of colon and rectal cancer. Dis Colon Rectum 58(8):713–725CrossRef Steele SR, Chang GJ, Hendren S, Weiser M, Irani J, Buie WD, Rafferty JF (2015) Practice guideline for the surveillance of patients after curative treatment of colon and rectal cancer. Dis Colon Rectum 58(8):713–725CrossRef
24.
go back to reference Schmoll HJ, Van Cutsem E, Stein A et al (2012) ESMO consensus guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol 23(10):2479–2516CrossRef Schmoll HJ, Van Cutsem E, Stein A et al (2012) ESMO consensus guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann Oncol 23(10):2479–2516CrossRef
25.
go back to reference Labianca R, Nordlinger B, Beretta GD et al (2013) Early colon cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi64–vi72CrossRef Labianca R, Nordlinger B, Beretta GD et al (2013) Early colon cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 24(Suppl 6):vi64–vi72CrossRef
26.
go back to reference Tsikitis VL, Malireddy K, Green EA, Christensen B, Whelan R, Hyder J, Marcello P, Larach S, Lauter D, Sargent DJ, Nelson H (2009) Postoperative surveillance recommendations for early stage colon cancer based on results from the clinical outcomes of surgical therapy trial. J Clin Oncol 27(22):3671–3676CrossRef Tsikitis VL, Malireddy K, Green EA, Christensen B, Whelan R, Hyder J, Marcello P, Larach S, Lauter D, Sargent DJ, Nelson H (2009) Postoperative surveillance recommendations for early stage colon cancer based on results from the clinical outcomes of surgical therapy trial. J Clin Oncol 27(22):3671–3676CrossRef
27.
go back to reference Okamura R, Hida K, Nishizaki D, Sugihara K, Sakai Y (2018) Proposal of a stage-specific surveillance strategy for colorectal cancer patients: a retrospective analysis of Japanese large cohort. Eur J Surg Oncol 44(4):449–455CrossRef Okamura R, Hida K, Nishizaki D, Sugihara K, Sakai Y (2018) Proposal of a stage-specific surveillance strategy for colorectal cancer patients: a retrospective analysis of Japanese large cohort. Eur J Surg Oncol 44(4):449–455CrossRef
28.
go back to reference Hutchins G, Southward K, Handley K, Magill L, Beaumont C, Stahlschmidt J, Richman S, Chambers P, Seymour M, Kerr D, Gray R, Quirke P (2011) Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J Clin Oncol 29(10):1261–1270CrossRef Hutchins G, Southward K, Handley K, Magill L, Beaumont C, Stahlschmidt J, Richman S, Chambers P, Seymour M, Kerr D, Gray R, Quirke P (2011) Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J Clin Oncol 29(10):1261–1270CrossRef
29.
go back to reference Taieb J, Le Malicot K, Shi Q et al (2017) Prognostic value of BRAF and KRAS mutations in MSI and MSS stage III colon cancer. J Natl Cancer Inst 109(5):djw272 Taieb J, Le Malicot K, Shi Q et al (2017) Prognostic value of BRAF and KRAS mutations in MSI and MSS stage III colon cancer. J Natl Cancer Inst 109(5):djw272
30.
go back to reference Petrelli F, Tomasello G, Borgonovo K, Ghidini M, Turati L, Dallera P, Passalacqua R, Sgroi G, Barni S (2017) Prognostic survival associated with left-sided vs right-sided colon cancer: a systematic review and meta-analysis. JAMA Oncol 3(2):211–219CrossRef Petrelli F, Tomasello G, Borgonovo K, Ghidini M, Turati L, Dallera P, Passalacqua R, Sgroi G, Barni S (2017) Prognostic survival associated with left-sided vs right-sided colon cancer: a systematic review and meta-analysis. JAMA Oncol 3(2):211–219CrossRef
31.
go back to reference Mou S, Soetikno R, Shimoda T, Rouse R, Kaltenbach T (2013) Pathologic predictive factors for lymph node metastasis in submucosal invasive (T1) colorectal cancer: a systematic review and meta-analysis. Surg Endosc 27(8):2692–2703CrossRef Mou S, Soetikno R, Shimoda T, Rouse R, Kaltenbach T (2013) Pathologic predictive factors for lymph node metastasis in submucosal invasive (T1) colorectal cancer: a systematic review and meta-analysis. Surg Endosc 27(8):2692–2703CrossRef
Metadata
Title
Proposal for a post-operative surveillance strategy for stage I colorectal cancer patients based on a novel recurrence risk stratification: a multicenter retrospective study
Authors
Tsuyoshi Ozawa
Yojiro Hashiguchi
Soichiro Ishihara
Tamuro Hayama
Takeshi Tsuchiya
Keijiro Nozawa
Shinichi Yamauchi
Kenichi Sugihara
Keiji Matsuda
Publication date
01-01-2021
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Colorectal Disease / Issue 1/2021
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI
https://doi.org/10.1007/s00384-020-03737-1

Other articles of this Issue 1/2021

International Journal of Colorectal Disease 1/2021 Go to the issue