International Journal of Clinical Oncology

, Volume 22, Issue 4, pp 758–766

Inflammation-based prognostic scores as indicators to select candidates for primary site resection followed by multimodal therapy among colorectal cancer patients with multiple metastases

  • Tadanobu Shimura
  • Yuji Toiyama
  • Susumu Saigusa
  • Hiroki Imaoka
  • Masato Okigami
  • Hiroyuki Fujikawa
  • Junichiro Hiro
  • Minako Kobayashi
  • Masaki Ohi
  • Toshimitsu Araki
  • Yasuhiro Inoue
  • Keiichi Uchida
  • Yasuhiko Mohri
  • Masato Kusunoki
Original Article

Abstract

Background

Although patients with metastatic colorectal cancer (CRC) are often unable to undergo treatment after resection of primary tumors, identifying such patients before surgery is not easy. In this study, we evaluated the association among clinicopathological findings, survival outcomes, and ability to undergo multimodal therapy after primary tumor resection in patients with Stage IV CRC.

Methods

We collected clinicopathological findings and preoperative laboratory data, including carcinoembryonic antigen (CEA) and systemic inflammatory response markers for 92 patients who were treated for Stage IV CRC between 2005 and 2014. We used multivariate analysis on factors that affect prognosis and ability to undergo postoperative treatment.

Results

Postoperative multimodal therapy improved overall survival (OS) significantly. Among serum markers, elevated CEA, neutrophil-to-lymphocyte ratio, and modified Glasgow prognosis score (mGPS) were significant indicators of shorter OS. In multivariate analysis, low performance status (P = 0.003), undifferentiated histology type (P = 0.019), and elevated mGPS (P = 0.042) were independent predictors of worse prognosis; and older age (P = 0.016), right-sided colon cancer (P = 0.043), and elevated mGPS (P = 0.031) were independent risk factors for difficulty of introducing postoperative multimodal therapy.

Conclusions

Preoperative mGPS is a useful objective indicator for CRC patients with multiple metastases who are able to undergo primary site resection followed by postoperative multimodal therapy.

Keywords

Colorectal cancer Stage IV Primary tumor resection modified Glasgow prognostic score 

Supplementary material

10147_2017_1113_MOESM1_ESM.ppt (194 kb)
Supplemental Figure 1 Modified GPS score against histological differentiation. The mGPS2 group had a significantly higher percentage of poorly differentiated histological type (7/20, 35%) than the mGPS0/1 group (6/72, 8.3%, P = 0.0054). Supplemental Figure 2 Histological differentiation against NLR values. The poor histology group had significantly higher median preoperative NLR (5.53, range 0.96–17.71) than the well/moderate histology group (2.98, range 0.57–30.13; P = 0.0332). Supplemental Figure 3 Patient age in relation to whether or not they underwent postoperative treatment. Median age in the untreated group (75 years; range 59–90 years) was significantly older than in the treated group (63 years, range 31–84 years; P = 0.0002) (PPT 194 kb)
10147_2017_1113_MOESM2_ESM.docx (23 kb)
Supplementary material 2 (DOCX 23 kb)

References

  1. 1.
    Ferlay J, Soerjomataram I, Dikshit R et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386CrossRefPubMedGoogle Scholar
  2. 2.
    Siegel R, Naishadham D, Jemal A (2012) Cancer statistics, 2012. CA Cancer J Clin 62:10–29CrossRefPubMedGoogle Scholar
  3. 3.
    Cook AD, Single R, McCahill LE (2005) Surgical resection of primary tumors in patients who present with stage IV colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000. Ann Surg Oncol 12:637–645CrossRefPubMedGoogle Scholar
  4. 4.
    van der Pool AE, Damhuis RA, Ijzermans JN et al (2012) Trends in incidence, treatment and survival of patients with stage IV colorectal cancer: a population-based series. Colorectal Dis 14:56–61CrossRefPubMedGoogle Scholar
  5. 5.
    van der Geest LG, Lam-Boer J, Koopman M et al (2015) Nationwide trends in incidence, treatment and survival of colorectal cancer patients with synchronous metastases. Clin Exp Metastasis 32:457–465CrossRefPubMedGoogle Scholar
  6. 6.
    Cirocchi R, Trastulli S, Abraha I et al (2012) Non-resection versus resection for an asymptomatic primary tumour in patients with unresectable stage IV colorectal cancer. Cochrane Database Syst Rev 8(8):CD008997. doi:10.1002/14651858.CD008997.pub2 Google Scholar
  7. 7.
    Rahbari NN, Lordick F, Fink C et al (2012) Resection of the primary tumour versus no resection prior to systemic therapy in patients with colon cancer and synchronous unresectable metastases (UICC stage IV): SYNCHRONOUS–a randomised controlled multicentre trial (ISRCTN30964555). BMC Cancer 12:142–151CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Lam-Boer JT, Van der Geest LG, Verhoef C et al (2016) Palliative resection of the primary tumor is associated with improved overall survival in incurable stage IV colorectal cancer: a nationwide population-based propensity-score adjusted study in the Netherlands. Int J Cancer 139:2082–2094CrossRefPubMedGoogle Scholar
  9. 9.
    Faron M, Pignon JP, Malka D et al (2015) Is primary tumour resection associated with survival improvement in patients with colorectal cancer and unresectable synchronous metastases? A pooled analysis of individual data from four randomised trials. Eur J Cancer 51:166–176CrossRefPubMedGoogle Scholar
  10. 10.
    Ahmed S, Leis A, Chandra-Kanthan S et al (2016) Surgical management of the primary tumor in stage iv colorectal cancer: a confirmatory retrospective cohort study. J Cancer 7:837–845CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Ahmed S, Leis A, Fields A et al (2014) Survival impact of surgical resection of primary tumor in patients with stage IV colorectal cancer: results from a large population-based cohort study. Cancer 120:683–691CrossRefPubMedGoogle Scholar
  12. 12.
    Wilkinson KJ, Chua W, Ng W et al (2010) Management of asymptomatic primary tumours in stage IV colorectal cancer: review of outcomes. World J Gastrointest Oncol 7:513–523Google Scholar
  13. 13.
    Stillwell AP, Buettner PG, Ho YH (2010) Meta-analysis of survival of patients with stage IV colorectal cancer managed with surgical resection versus chemotherapy alone. World J Surg 34:797–807CrossRefPubMedGoogle Scholar
  14. 14.
    Watanabe T, Itabashi M, Shimada 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 20:207–239CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Uratani R, Toiyama Y, Shimura T et al (2015) Preoperative lower body mass index correlates with poorer prognosis in patients undergoing curative laparoscopic surgery for colorectal cancer. Anticancer Res 35:5639–5648PubMedGoogle Scholar
  16. 16.
    Toiyama Y, Hiro J, Shimura T et al (2016) The impact of body mass index on oncological outcomes in colorectal cancer patients with curative intent. Int J Clin Oncol 21(6):1102–1110CrossRefPubMedGoogle Scholar
  17. 17.
    Toiyama Y, Inoue Y, Kawamura M et al (2015) Elevated platelet count as predictor of recurrence in rectal cancer patients undergoing preoperative chemoradiotherapy followed by surgery. Int Surg 100:199–207CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Mori K, Toiyama Y, Saigusa S et al (2015) Systemic analysis of predictive biomarkers for recurrence in colorectal cancer patients treated with curative surgery. Dig Dis Sci 60:2477–2487CrossRefPubMedGoogle Scholar
  19. 19.
    Inoue Y, Iwata T, Okugawa Y et al (2013) Prognostic significance of a systemic inflammatory response in patients undergoing multimodality therapy for advanced colorectal cancer. Oncology 84:100–107CrossRefPubMedGoogle Scholar
  20. 20.
    Toiyama Y, Miki C, Inoue Y et al (2011) Evaluation of an inflammation-based prognostic score for the identification of patients requiring postoperative adjuvant chemotherapy for stage II colorectal cancer. Exp Ther Med 2:95–101PubMedGoogle Scholar
  21. 21.
    Hu H, Krasinskas A, Willis J (2011) Perspectives on current tumor-node-metastasis (TNM) staging of cancers of the colon and rectum. Semin Oncol 38:500–510CrossRefPubMedGoogle Scholar
  22. 22.
    Oken MM, Creech RH, Tormey DC et al (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649–655CrossRefPubMedGoogle Scholar
  23. 23.
    McMillan DC (2009) Systemic inflammation, nutritional status and survival in patients with cancer. Curr Opin Clin Nutr Metab Care 12:223–226CrossRefPubMedGoogle Scholar
  24. 24.
    Chiang SF, Hung HY, Tang R et al (2012) Can neutrophil-to-lymphocyte ratio predict the survival of colorectal cancer patients who have received curative surgery electively? Int J Colorectal Dis 27:1347–1357CrossRefPubMedGoogle Scholar
  25. 25.
    Kwon HC, Kim SH, Oh SY et al (2012) Clinical significance of preoperative neutrophil-lymphocyte versus platelet-lymphocyte ratio in patients with operable colorectal cancer. Biomarkers 17:216–222CrossRefPubMedGoogle Scholar
  26. 26.
    Ishizuka M, Nagata H, Takagi K et al (2012) Preoperative thrombocytosis is associated with survival after surgery for colorectal cancer. J Surg Oncol 106:887–891CrossRefPubMedGoogle Scholar
  27. 27.
    Damjanov N, Weiss J, Haller DG (2009) Resection of the primary colorectal cancer is not necessary in nonobstructed patients with metastatic disease. Oncologist 14:963–969CrossRefPubMedGoogle Scholar
  28. 28.
    McMillan DC (2013) The systemic inflammation-based Glasgow Prognostic Score: a decade of experience in patients with cancer. Cancer Treat Rev 39:534–540CrossRefPubMedGoogle Scholar
  29. 29.
    Proctor MJ, Morrison DS, Talwar D et al (2011) A comparison of inflammation-based prognostic scores in patients with cancer. A Glasgow Inflammation Outcome Study. Eur J Cancer 47:2633–2641CrossRefPubMedGoogle Scholar
  30. 30.
    Canna K, McArdle PA, McMillan DC et al (2005) The relationship between tumour T-lymphocyte infiltration, the systemic inflammatory response and survival in patients undergoing curative resection for colorectal cancer. Br J Cancer 92:651–654CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    McMillan DC, Canna K, McArdle CS (2003) Systemic inflammatory response predicts survival following curative resection of colorectal cancer. Br J Surg 90:215–219CrossRefPubMedGoogle Scholar
  32. 32.
    Miki C, Konishi N, Ojima E et al (2004) C-reactive protein as a prognostic variable that reflects uncontrolled up-regulation of the IL-1-IL-6 network system in colorectal carcinoma. Dig Dis Sci 49:970–976CrossRefPubMedGoogle Scholar
  33. 33.
    Delmore G (1997) Assessment of nutritional status in cancer patients: widely neglected? Support Care Cancer 5:376–380CrossRefPubMedGoogle Scholar
  34. 34.
    McMillan DC, Scott HR, Watson WS et al (1998) Longitudinal study of body cell mass depletion and the inflammatory response in cancer patients. Nutr Cancer 31:101–105CrossRefPubMedGoogle Scholar
  35. 35.
    McMillan DC, Watson WS, O’Gorman P et al (2001) Albumin concentrations are primarily determined by the body cell mass and the systemic inflammatory response in cancer patients with weight loss. Nutr Cancer 39:210–213CrossRefPubMedGoogle Scholar
  36. 36.
    McMillan DC (2008) An inflammation-based prognostic score and its role in the nutrition-based management of patients with cancer. Proc Nutr Soc 67:257–262CrossRefPubMedGoogle Scholar
  37. 37.
    McMillan DC, Crozier JE, Canna K et al (2007) Evaluation of an inflammation-based prognostic score (GPS) in patients undergoing resection for colon and rectal cancer. Int J Colorectal Dis 22:881–886CrossRefPubMedGoogle Scholar
  38. 38.
    Ishizuka M, Nagata H, Takagi K et al (2007) Inflammation-based prognostic score is a novel predictor of postoperative outcome in patients with colorectal cancer. Ann Surg 246:1047–1051CrossRefPubMedGoogle Scholar
  39. 39.
    Ishizuka M, Nagata H, Takagi K et al (2013) Inflammation-based prognostic system predicts survival after surgery for stage IV colorectal cancer. Am J Surg 205:22–28CrossRefPubMedGoogle Scholar
  40. 40.
    Kishiki T, Masaki T, Matsuoka H et al (2013) Modified Glasgow prognostic score in patients with incurable stage IV colorectal cancer. Am J Surg 206:234–240CrossRefPubMedGoogle Scholar
  41. 41.
    Maeda K, Shibutani M, Otani H et al (2013) Prognostic value of preoperative inflammation-based prognostic scores in patients with stage IV colorectal cancer who undergo palliative resection of asymptomatic primary tumors. Anticancer Res 33:5567–5573PubMedGoogle Scholar
  42. 42.
    Adachi T, Hinoi T, Hattori M et al (2015) The modified Glasgow prognostic score for early mortality in patients with synchronous peritoneal carcinomatosis from colorectal cancer. Surg Today 45:1396–1403CrossRefPubMedGoogle Scholar
  43. 43.
    Kobayashi S, Karube Y, Nishihira M et al (2016) Usefulness of inflammation-based prognostic score in patients undergoing lung metastasectomy for colorectal carcinoma. World J Surg 40:1632–1637CrossRefPubMedGoogle Scholar
  44. 44.
    Shibutani M, Maeda K, Nagahara H et al (2015) Significance of markers of systemic inflammation for predicting survival and chemotherapeutic outcomes and monitoring tumor progression in patients with unresectable metastatic colorectal cancer. Anticancer Res 35:5037–5046PubMedGoogle Scholar
  45. 45.
    Kuijpers CC, Sluijter CE, von der Thusen JH et al (2016) Interlaboratory variability in the histologic grading of colorectal adenocarcinomas in a nationwide cohort. Am J Surg Pathol 40:1100–1108CrossRefPubMedGoogle Scholar
  46. 46.
    Petrelli F, Tomasello G, Borgonovo K et al (2016) Prognostic survival associated with left-sided vs right-sided colon cancer: a systematic review and meta-analysis. JAMA Oncol. doi:10.1001/jamaoncol.2016.4227 Google Scholar
  47. 47.
    Yahagi M, Okabayashi K, Hasegawa H et al (2016) The worse prognosis of right-sided compared with left-sided colon cancers: a systematic review and meta-analysis. J Gastrointest Surg 20:648–655CrossRefPubMedGoogle Scholar
  48. 48.
    Nitsche U, Stogbauer F, Spath C et al (2016) Right sided colon cancer as a distinct histopathological subtype with reduced prognosis. Dig Surg 33:157–163CrossRefPubMedGoogle Scholar
  49. 49.
    Ishihara S, Nishikawa T, Tanaka T et al (2014) Prognostic impact of tumor location in stage IV colon cancer: a propensity score analysis in a multicenter study. Int J Surg 12:925–930CrossRefPubMedGoogle Scholar
  50. 50.
    Chan M, Hugh-Yeun K, Gresham G et al (2016) Population-based patterns and factors associated with underuse of palliative systemic therapy in elderly patients with metastatic colon cancer. Clin Colorectal Cancer. doi:10.1016/j.clcc.2016.08.004 PubMedGoogle Scholar

Copyright information

© Japan Society of Clinical Oncology 2017

Authors and Affiliations

  • Tadanobu Shimura
    • 1
  • Yuji Toiyama
    • 1
  • Susumu Saigusa
    • 1
  • Hiroki Imaoka
    • 1
  • Masato Okigami
    • 1
  • Hiroyuki Fujikawa
    • 1
  • Junichiro Hiro
    • 1
  • Minako Kobayashi
    • 1
  • Masaki Ohi
    • 1
  • Toshimitsu Araki
    • 1
  • Yasuhiro Inoue
    • 1
  • Keiichi Uchida
    • 1
  • Yasuhiko Mohri
    • 1
  • Masato Kusunoki
    • 1
  1. 1.Department of Gastrointestinal and Pediatric Surgery, Division of Reparative Medicine, Institute of Life Sciences, Graduate School of MedicineMie UniversityMieJapan

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