Abstract
Background
The pre-operative systemic inflammatory response (SIR) measured using an acute-phase-protein-based score (modified Glasgow Prognostic Score (mGPS)) or the differential white cell count (neutrophil–lymphocyte ratio (NLR)) demonstrates prognostic significance following curative resection of colon cancer. We investigate the complementary use of both measures to better stratify outcomes.
Methods
The effect on survival of mGPS and NLR was examined using uni/multivariate analysis (UVA/MVA) in patients undergoing curative surgery for colon cancer. The synergistic effect of these scores in predicting OS/CSS was examined using a Systemic Inflammatory Grade (SIG).
Results
One thousand seven hundred and eight patients with TNM-I–III colon cancer were included. On MVA both mGPS and NLR were significant for OS (HR 1.16/1.21, respectively). Three-year survival stratified by mGPS was 83–58%(TNM-I–III), 87–65%(TNM-II) and 75–49%(TNM-III), and by NLR was 84–62%(TNM-I–III), 88–69%(TNM-II) and 77-49%(TNM-III). When mGPS and NLR were combined to form an overall SIG 0/1/2/3/4, this stratified 3-year OS 88%/84%/76%/65%/60% and CSS 93%/90%/82%/73%/70%, respectively (both p < 0.001). SIG stratified OS 93–68%/82–48% and CSS 97–80%/86–58% in TNM Stage II/III disease, respectively (all p < 0.001).
Conclusions
The present study shows that the pre-operative SIR in patients undergoing curative surgery for colon cancer is best measured using a SIG utilising mGPS and NLR.
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References
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A. & Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394–424 (2018).
Cancer Research UK. Bowel cancer incidence statistics. https://www.cancerresearchuk.org./health-professional/cancer-statistics/statistics-by-cancer-type/bowel-cancer/incidence. Accessed Nov 2020.
Dolan, R. D., McSorley, S. T., Park, J. H., Watt, D. G., Roxburgh, C. S., Horgan, P. G. et al. The prognostic value of systemic inflammation in patients undergoing surgery for colon cancer: comparison of composite ratios and cumulative scores. Br. J. Cancer 119, 40–51 (2018).
Park, J. H., Ishizuka, M., McSorley, S. T., Kubota, K., Roxburgh, C. S. D., Nagata, H. et al. Staging the tumor and staging the host: a two centre, two country comparison of systemic inflammatory responses of patients undergoing resection of primary operable colorectal cancer. Am. J. Surg. 216, 458–464 (2018).
Dolan, R. D., Lim, J., McSorley, S. T., Horgan, P. G. & McMillan, D. C. The role of the systemic inflammatory response in predicting outcomes in patients with operable cancer: systematic review and meta-analysis. Sci. Rep. 7, 16717 (2017).
Park, J. H., Watt, D. G., Roxburgh, C. S., Horgan, P. G. & McMillan, D. C. Colorectal cancer, systemic inflammation, and outcome: staging the tumor and staging the host. Ann. Surg. 263, 326–336 (2016).
Park, J. H., Fuglestad, A. J., Kostner, A. H., Oliwa, A., Graham, J., Horgan, P. G. et al. Systemic inflammation and outcome in 2295 patients with stage I-III colorectal cancer from Scotland and Norway: first results from the ScotScan Colorectal Cancer Group. Ann. Surg. Oncol. 27, 2784–2794 (2020).
McAllister, S. S. & Weinberg, R. A. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat. Cell Biol. 16, 717–727 (2014).
McMillan, D. C. The systemic inflammation-based Glasgow Prognostic Score: a decade of experience in patients with cancer. Cancer Treat. Rev. 39, 534–540 (2013).
Dolan, R. D., Laird, B. J. A., Horgan, P. G. & McMillan, D. C. The prognostic value of the systemic inflammatory response in randomised clinical trials in cancer: a systematic review. Crit. Rev. Oncol. Hematol. 132, 130–137 (2018).
Inamoto, S., Kawada, K., Okamura, R., Hida, K. & Sakai, Y. Prognostic impact of the combination of neutrophil-to-lymphocyte ratio and Glasgow prognostic score in colorectal cancer: a retrospective cohort study. Int. J. Colorectal Dis. 34, 1303–1315 (2019).
Brewster, D., Muir, C. & Crichton, J. Registration of colorectal cancer in Scotland: an assessment of data accuracy based on review of medical records. Public Health 109, 285–292 (1995).
Brewster, D. H., Stockton, D., Harvey, J. & Mackay, M. Reliability of cancer registration data in Scotland, 1997. Eur. J. Cancer 38, 414–417 (2002).
ScotPHO. Classification of deaths—Public Health Information for Scotland. https://www.scotpho.org.uk/publications/overview-of-key-data-sources/scottish-national-data-schemes/deaths. (2020)
Dolan, R. D., McSorley, S. T., Horgan, P. G., Laird, B. & McMillan, D. C. The role of the systemic inflammatory response in predicting outcomes in patients with advanced inoperable cancer: systematic review and meta-analysis. Crit. Rev. Oncol. Hematol. 116, 134–146 (2017).
McSorley, S. T., Lau, H. Y. N., McIntosh, D., Forshaw, M. J., McMillan, D. C. & Crumley, A. B. Staging the tumor and staging the host: pretreatment combined neutrophil lymphocyte ratio and modified Glasgow Prognostic Score is associated with overall survival in patients with esophagogastric cancers undergoing treatment with curative intent. Ann. Surg. Oncol. 28, 722–731 (2021).
Diakos, C. I., Charles, K. A., McMillan, D. C. & Clarke, S. J. Cancer-related inflammation and treatment effectiveness. Lancet Oncol. 15, e493–e503 (2014).
Mansouri, D., McMillan, D. C., Crearie, C., Morrison, D. S., Crighton, E. M. & Horgan, P. G. Temporal trends in mode, site and stage of presentation with the introduction of colorectal cancer screening: a decade of experience from the West of Scotland. Br. J. Cancer 113, 556–561 (2015).
Kannarkatt, J., Joseph, J., Kurniali, P. C., Al-Janadi, A. & Hrinczenko, B. Adjuvant chemotherapy for stage II colon cancer: a clinical dilemma. J. Oncol. Pract. 13, 233–241 (2017).
Quasar Collaborative, G., Gray, R., Barnwell, J., McConkey, C., Hills, R. K., Williams, N. S. et al. Adjuvant chemotherapy versus observation in patients with colorectal cancer: a randomised study. Lancet 370, 2020–2029 (2007).
Ter Veer, E., van Rijssen, L. B., Besselink, M. G., Mali, R. M. A., Berlin, J. D., Boeck, S. et al. Consensus statement on mandatory measurements in pancreatic cancer trials (COMM-PACT) for systemic treatment of unresectable disease. Lancet Oncol. 19, e151–e160 (2018).
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A.G.—designing the work, acquiring data, data interpretation and drafting the manuscript. D.C.M.M.—conceiving and designing the work, interpreting the results and revising the manuscript. J-.P.—interpreting the results and revising the manuscript. D.M.—interpreting the results and revising the manuscript. P.H.—interpreting the results and revising the manuscript. C.R.—interpreting the results and revising the manuscript. All authors have approved the final version of this work and agree to be accountable for all aspects of this work.
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Golder, A.M., McMillan, D.C., Park, J.H. et al. The prognostic value of combined measures of the systemic inflammatory response in patients with colon cancer: an analysis of 1700 patients. Br J Cancer 124, 1828–1835 (2021). https://doi.org/10.1038/s41416-021-01308-x
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DOI: https://doi.org/10.1038/s41416-021-01308-x
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