Skip to main content

Advertisement

SpringerLink
Log in

Less intensive surveillance after radical surgery for stage I–III colorectal cancer by focusing on the doubling time of recurrence

  • Original Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

Purpose

To propose a new and improved surveillance schedule for colorectal cancer (CRC) patients by focusing on the recurrence rate, resectability, and especially, the tumor doubling time (DT) of recurrent tumors.

Methods

The subjects of this retrospective review were 1774 consecutive patients who underwent radical surgery for stage I–III CRC between January, 2004 and December, 2015. We calculated the DT by measuring the tumor diameter using computed tomography (CT).

Results

The median DT for recurrences in the liver, lung, peritoneum, and other locations were 35, 72, 85, and 36 days, respectively, (p < 0.001) and tumor growth rates differed according to the organs where recurrence developed. Multiple linear regression analysis showed that the DT was strongly associated with the relapse-free interval from primary surgery (p < 0.001), and that the DT in patients with recurrence detected ≥ 3 years after primary surgery was longer by 151.1 days than that in patients with recurrence detected within 1 year after primary surgery. We proposed a less intensive surveillance, which achieved an average cost reduction of 32.5% compared with conventional surveillance in Japan.

Conclusion

We propose a new and more cost-efficient surveillance schedule for CRC surgery patients in the clinical setting.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424. https://doi.org/10.3322/caac.21492.

    Article  Google Scholar 

  2. Sadahiro S, Suzuki T, Ishikawa K, Nakamura T, Tanaka Y, Masuda T, et al. Recurrence patterns after curative resection of colorectal cancer in patients followed for a minimum of ten years. Hepatogastroenterology. 2003;50:1362–6.

    PubMed  Google Scholar 

  3. Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg. 2004;239:818–25. https://doi.org/10.1097/01.sla.0000128305.90650.71.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ike H, Shimada H, Ohki S, Togo S, Yamaguchi S, Ichikawa Y. Results of aggressive resection of lung metastases from colorectal carcinoma detected by intensive follow-up. Dis Colon Rectum. 2002;45:468–73. https://doi.org/10.1007/s10350-004-6222-0.

    Article  PubMed  Google Scholar 

  5. Shah SA, Haddad R, Al-Sukhni W, Kim RD, Greig PD, Grant DR, et al. Surgical resection of hepatic and pulmonary metastases from colorectal carcinoma. J Am Coll Surg. 2006;202:468–75. https://doi.org/10.1016/j.jamcollsurg.2005.11.008.

    Article  PubMed  Google Scholar 

  6. Jeffery GM, Hickey BE, Hider P. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev. 2002;1:002200. https://doi.org/10.1002/14651858.CD002200.

    Article  Google Scholar 

  7. Figueredo A, Rumble RB, Maroun J, Earle CC, Cummings B, McLeod R, et al. Follow-up of patients with curatively resected colorectal cancer: a practice guideline. BMC Cancer. 2003;3:26. https://doi.org/10.1186/1471-2407-3-26.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Tjandra JJ, Chan MK. Follow-up after curative resection of colorectal cancer: a meta-analysis. Dis Colon Rectum. 2007;50:1783–99. https://doi.org/10.1007/s10350-007-9030-5.

    Article  PubMed  Google Scholar 

  9. Renehan AG, Egger M, Saunders MP, O'Dwyer ST. Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials. BMJ. 2002;324:813. https://doi.org/10.1136/bmj.324.7341.813.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wille-Jorgensen P, Syk I, Smedh K, Laurberg S, Nielsen DT, Petersen SH, et al. Effect of more vs. less frequent follow-up testing on overall and colorectal cancer-specific mortality in patients with stage ii or iii colorectal cancer: the COLOFOL randomized clinical trial. JAMA. 2018;319:2095–103. https://doi.org/10.1001/jama.2018.5623.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Jeffery M, Hickey BE, Hider PN, See AM. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev. 2016;11:002200. https://doi.org/10.1002/14651858.CD002200.pub3.

    Article  Google Scholar 

  12. Primrose JN, Perera R, Gray A, Rose P, Fuller A, Corkhill A, et al. 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. 2014;311:263–70. https://doi.org/10.1001/jama.2013.285718.

    Article  CAS  PubMed  Google Scholar 

  13. Mant D, Gray A, Pugh S, Campbell H, George S, Fuller A, et al. A randomised controlled trial to assess the cost-effectiveness of intensive versus no scheduled follow-up in patients who have undergone resection for colorectal cancer with curative intent. Health Technol Assess. 2017;21:1–86. https://doi.org/10.3310/hta21320.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Rosati G, Ambrosini G, Barni S, Andreoni B, Corradini G, Luchena G, et al. A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma. Ann Oncol. 2016;27:274–80. https://doi.org/10.1093/annonc/mdv541.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  16. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology-colon cancer, version 2. 2019. https://www.nccn.org/professionals/physician_gls/pdf/colon.pdf. Accessed 13 Dec 2019.

    Google Scholar 

  17. Steele SR, Chang GJ, Hendren S, Weiser M, Irani J, Buie WD, et al. Practice guideline for the surveillance of patients after curative treatment of colon and rectal cancer. Dis Colon Rectum. 2015;58:713–25. https://doi.org/10.1097/DCR.0000000000000410.

    Article  PubMed  Google Scholar 

  18. Labianca R, Nordlinger B, Beretta GD, Mosconi S, Mandala M, Cervantes A, et al. Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2013;24(Suppl 6):vi64–72. https://doi.org/10.1093/annonc/mdt354.

    Article  PubMed  Google Scholar 

  19. Shida D, Yoshida T, Tanabe T, Tsukamoto S, Ochiai H, Kanemitsu Y. Prognostic Impact of R0 resection and targeted therapy for colorectal cancer with synchronous peritoneal metastasis. Ann Surg Oncol. 2018;25:1646–53. https://doi.org/10.1245/s10434-018-6436-3.

    Article  PubMed  Google Scholar 

  20. Collins VP, Loeffler RK, Tivey H. Observations on growth rates of human tumors. Am J Roentgenol Radium Ther Nucl Med. 1956;76:988–1000.

    CAS  PubMed  Google Scholar 

  21. Collins VP. Time of occurrence of pulmonary metastasis from carcinoma of colon and rectum. Cancer. 1962;15:387–95.

    Article  CAS  Google Scholar 

  22. Miyake H, Murono K, Nagata H, Nozawa H, Kawai K, Hata K, et al. Prognostic significance of doubling time in patients undergoing radical surgery for metachronous peritoneal metastases of colorectal cancer. Int J Colorectal Dis. 2019;34:801–9. https://doi.org/10.1007/s00384-019-03259-5.

    Article  PubMed  Google Scholar 

  23. Tanaka K, Shimada H, Miura M, Fujii Y, Yamaguchi S, Endo I, et al. Metastatic tumor doubling time: most important prehepatectomy predictor of survival and nonrecurrence of hepatic colorectal cancer metastasis. World J Surg. 2004;28:263–70. https://doi.org/10.1007/s00268-003-7088-3.

    Article  PubMed  Google Scholar 

  24. Tanaka K, Shimada H, Fujii Y, Endo I, Sekido H, Togo S, et al. Pre-hepatectomy prognostic staging to determine treatment strategy for colorectal cancer metastases to the liver. Langenbecks Arch Surg. 2004;389:371–9. https://doi.org/10.1007/s00423-004-0490-y.

    Article  PubMed  Google Scholar 

  25. Tanaka K, Shimada H, Ueda M, Matsuo K, Endo I, Togo S. Long-term characteristics of 5-year survivors after liver resection for colorectal metastases. Ann Surg Oncol. 2007;14:1336–46. https://doi.org/10.1245/s10434-006-9071-3.

    Article  PubMed  Google Scholar 

  26. Kawaguchi K, Uehara K, Nakayama G, Fukui T, Fukumoto K, Nakamura S, et al. Growth rate of chemotherapy-naive lung metastasis from colorectal cancer could be a predictor of early relapse after lung resection. Int J Clin Oncol. 2016;21:329–34. https://doi.org/10.1007/s10147-015-0889-1.

    Article  CAS  PubMed  Google Scholar 

  27. Tomimaru Y, Noura S, Ohue M, Okami J, Oda K, Higashiyama M, et al. Metastatic tumor doubling time is an independent predictor of intrapulmonary recurrence after pulmonary resection of solitary pulmonary metastasis from colorectal cancer. Dig Surg. 2008;25:220–5. https://doi.org/10.1159/000140693.

    Article  PubMed  Google Scholar 

  28. Cucchetti A, Russolillo N, Johnson P, Tarchi P, Ferrero A, Cucchi M, et al. Impact of primary cancer features on behaviour of colorectal liver metastases and survival after hepatectomy. BJS Open. 2019;3:186–94. https://doi.org/10.1002/bjs5.100.

    Article  CAS  PubMed  Google Scholar 

  29. Hermanek P, Hutter RV, Sobin LH, Wittekind C. International Union Against Cancer. Classification of isolated tumor cells and micrometastasis. Cancer. 1999;86:2668–73.

    Article  CAS  Google Scholar 

  30. Mohajeri G, Hejab K, Sheikhbahaei S, Mohajeri M, Niknam N, Mohammadi A. Micrometastasis in colorectal cancer: does it affect staging? ANZ J Surg. 2018;88:E237–E241241. https://doi.org/10.1111/ans.13809.

    Article  PubMed  Google Scholar 

  31. Alsaggar M, Yao Q, Cai H, Liu D. Differential growth and responsiveness to cancer therapy of tumor cells in different environments. Clin Exp Meta. 2016;33:115–24. https://doi.org/10.1007/s10585-015-9761-y.

    Article  CAS  Google Scholar 

  32. Algire GH, Legallais FY, Anderson BF. Vascular reactions of normal and malignant tissues in Vivo. VI. The role of hypotension in the action of components of podophyllin on transplanted sarcomas. J Natl Cancer Inst. 1954;14:879–93.

    CAS  PubMed  Google Scholar 

  33. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285:1182–6. https://doi.org/10.1056/NEJM197111182852108.

    Article  CAS  PubMed  Google Scholar 

  34. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature. 2001;411:375–9. https://doi.org/10.1038/35077241.

    Article  CAS  PubMed  Google Scholar 

  35. Coccolini F, Gheza F, Lotti M, Virzi S, Iusco D, Ghermandi C, et al. Peritoneal carcinomatosis. World J Gastroenterol. 2013;19:6979–94. https://doi.org/10.3748/wjg.v19.i41.6979.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Tempero MA, Williams CA, Anderson JC. The value of hepatic ultrasound and biochemical liver tests in screening for liver metastases. J Clin Oncol. 1986;4:1074–8. https://doi.org/10.1200/JCO.1986.4.7.1074.

    Article  CAS  PubMed  Google Scholar 

  37. Schneider J, Koullouros M, Mackay C, Ramsay G, Parnaby C, Stevenson L. Is Liver ultrasound useful as part of the surveillance strategy following potentially curative colorectal cancer resection? Dig Dis. 2019;37:234–8. https://doi.org/10.1159/000495114.

    Article  PubMed  Google Scholar 

  38. Floriani I, Torri V, Rulli E, Garavaglia D, Compagnoni A, Salvolini L, et al. Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging. 2010;31:19–311. https://doi.org/10.1002/jmri.22010.

    Article  PubMed  Google Scholar 

  39. Seo SI, Lim SB, Yoon YS, Kim CW, Yu CS, Kim TW, et al. Comparison of recurrence patterns between </=5 years and >5 years after curative operations in colorectal cancer patients. J Surg Oncol. 2013;108:9–13. https://doi.org/10.1002/jso.23349.

    Article  PubMed  Google Scholar 

  40. Wicherts DA, Miller R, de Haas RJ, Bitsakou G, Vibert E, Veilhan LA, et al. Long-term results of two-stage hepatectomy for irresectable colorectal cancer liver metastases. Ann Surg. 2008;248:994–1005. https://doi.org/10.1097/SLA.0b013e3181907fd9.

    Article  PubMed  Google Scholar 

  41. Dorr NM, Bartels M, Morgul MH. Current treatment of colorectal liver metastasis as a chronic disease. Anticancer Res. 2020;40:1–7. https://doi.org/10.21873/anticanres.13921.

    Article  PubMed  Google Scholar 

  42. Goere D, Souadka A, Faron M, Cloutier AS, Viana B, Honore C, et al. Extent of colorectal peritoneal carcinomatosis: attempt to define a threshold above which HIPEC does not offer survival benefit: a comparative study. Ann Surg Oncol. 2015;22:2958–64. https://doi.org/10.1245/s10434-015-4387-5.

    Article  PubMed  Google Scholar 

  43. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med. 1995;1:149–53. https://doi.org/10.1038/nm0295-149.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was supported by the Project for Cancer Research and Therapeutic Evolution from the Japan Agency for Medical Research and Development (grant number: JP19cm0106502) and by Grants-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (grant numbers: 17K10620, 17K10621, 17K10623, 18K07194, 19K09114 and 19K09115).

Author information

Authors and Affiliations

  1. Department of Surgical Oncology, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan

    Hiroaki Miyake, Kazushige Kawai, Hiroaki Nozawa, Kazuhito Sasaki, Manabu Kaneko, Koji Murono, Shigenobu Emoto, Hiroaki Ishii, Hirofumi Sonoda & Soichiro Ishihara

Authors
  1. Hiroaki Miyake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazushige Kawai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroaki Nozawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuhito Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manabu Kaneko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Koji Murono
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shigenobu Emoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hiroaki Ishii
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hirofumi Sonoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Soichiro Ishihara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroaki Miyake.

Ethics declarations

Conflict of interest

Soichiro Ishihara receives lecture fees from EA Pharma, Alfresa, Otsuka, KAKEN, Yakult, Johnson and Johnson, TAIHO, Takeda, CHUGAI, Nippon Kayaku, Pfizer, Merck, Janssen, and research funding from TAIHO, Takeda, Mitsubishi Tanabe, CHUGAI, TSUMURA, Eli Lilly, Pfizer, MIYARISAN, Merck, MOCHIDA. The other authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miyake, H., Kawai, K., Nozawa, H. et al. Less intensive surveillance after radical surgery for stage I–III colorectal cancer by focusing on the doubling time of recurrence. Surg Today 51, 550–560 (2021). https://doi.org/10.1007/s00595-020-02135-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-020-02135-y

Keywords

Search

Navigation