Prognostic value of preoperative highsensitivity modifed Glasgow prognostic score in advanced colon cancer: A retrospective observational study

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Several studies have demonstrated that the preoperative Glasgow prognostic score (GPS) and modifed GPS (mGPS) refected the prognosis in patients undergoing curative surgery for colorectal cancer. However, there are no reports on long-term prognosis prediction using high-sensitivity mGPS (HS-GPS) in colorectal cancer. Therefore, this study aimed to calculate the prognostic value of preoperative HS-GPS in patients with colon cancer.

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Nội dung Text: Prognostic value of preoperative highsensitivity modifed Glasgow prognostic score in advanced colon cancer: A retrospective observational study

Kasahara et al. BMC Cancer (2022) 22:20 https://doi.org/10.1186/s12885-021-09113-8 RESEARCH Open Access Prognostic value of preoperative high- sensitivity modified Glasgow prognostic score in advanced colon cancer: a retrospective observational study Kenta Kasahara, Masanobu Enomoto*, Ryutaro Udo, Tomoya Tago, Junichi Mazaki, Tetsuo Ishizaki, Tesshi Yamada, Yuichi Nagakawa, Kenji Katsumata and Akihiko Tsuchida Abstract Background: Several studies have demonstrated that the preoperative Glasgow prognostic score (GPS) and modi- fied GPS (mGPS) reflected the prognosis in patients undergoing curative surgery for colorectal cancer. However, there are no reports on long-term prognosis prediction using high-sensitivity mGPS (HS-GPS) in colorectal cancer. Therefore, this study aimed to calculate the prognostic value of preoperative HS-GPS in patients with colon cancer. Methods: A cohort of 595 patients with advanced resectable colon cancer managed at our institution was analysed retrospectively. HS-GPS, GPS, and mGPS were evaluated for their ability to predict prognosis based on overall survival (OS) and recurrence-free survival (RFS). Results: In the univariate analysis, HS-GPS was able to predict the prognosis with significant differences in OS but was not superior in assessing RFS. In the multivariate analysis of the HS-GPS model, age, pT, pN, and HS-GPS of 2 compared to HS-GPS of 0 (2 vs 0; hazard ratio [HR], 2.638; 95% confidence interval [CI], 1.046–6.650; P = 0.04) were identified as independent prognostic predictors of OS. In the multivariate analysis of the GPS model, GPS 2 vs 0 (HR, 1.444; 95% CI, 1.018–2.048; P = 0.04) and GPS 2 vs 1 (HR, 2.933; 95% CI, 1.209–7.144; P = 0.017), and in that of the mGPS model, mGPS 2 vs 0 (HR, 1.51; 95% CI, 1.066–2.140; P = 0.02) were independent prognostic predictors of OS. In each classification, GPS outperformed HS-GPS in predicting OS with a significant difference in the area under the receiver operating characteristic curve. In the multivariate analysis of the GPS model, GPS 2 vs 0 (HR, 1.537; 95% CI, 1.190– 1.987; P = 0.002), and in that of the mGPS model, pN, CEA were independent prognostic predictors of RFS. Conclusion: HS-GPS is useful for predicting the prognosis of resectable advanced colon cancer. However, GPS may be more useful than HS-GPS as a prognostic model for advanced colon cancer. Keywords: Glasgow prognostic score, Modified Glasgow prognostic score, High-sensitivity modified Glasgow prognostic score, Colon cancer Background Colorectal cancer (CRC) is the third most commonly diagnosed cancer and the second leading cause of can- cer-related mortality worldwide [1]. CRC prognosis is *Correspondence: enomoto@tokyo-med.ac.jp based on the Union for International Cancer Control Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, 6‑7‑1 Nishi Shinjuku, Shinjuku‑ku, Tokyo 160‑0023, Japan (UICC) tumour node metastasis (TNM) classification; © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativeco mmons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Kasahara et al. BMC Cancer (2022) 22:20 Page 2 of 11 however, differences in outcomes have been reported the Colon and Rectum (JSCCR) guidelines for each age among patients presenting with the same disease stage [2, [6]. Chemotherapy was administered to 10% of stage II 3]. Concurrently, various inflammatory biomarkers have patients and 64% of stage III patients. ADJ included the been suggested as relevant survival predictors in this 5-fluorouracil-based regimen. If CRC recurred, most patient group [4, 5]. patients were treated according to the JSCCR guidelines Several studies have demonstrated that preopera- [6]. Overall survival (OS) was calculated from the date of tive Glasgow prognostic score (GPS) and modified GPS colectomy to the date of death or last follow-up. Recur- (mGPS) reflected the prognosis in patients with CRC or rence-free survival (RFS) was calculated from the date of colon cancer (CC) who were undergoing curative surgery colectomy to the date of either recurrence or death or the [2–4]. It was reported that high-sensitivity mGPS (HS- last follow-up. GPS) was useful for changing the cut-off value of GPS and mGPS in other cancer types and identifying higher number of patients with poor prognosis. However, the Criteria of each GPS related score HS-GPS developed for prediction of prognosis in CRC The HS-mGPS was calculated based on the cut-off val- or CC patients has not been reported in detail [5]. Fur- ues of 0.3 mg/dL for C-reactive protein (CRP) and 3.5 g/ thermore, there are no reports on the value of HS-mGPS dL for albumin levels. Patients with an elevated CRP in predicting long-term prognosis in patients with colo- (> 0.3 mg/dL) and hypoalbuminemia ( 1.0 mg/ Methods dL) and hypoalbuminemia ( 1.0 mg/dL) and hypoal- went surgery at the Tokyo Medical University Hospital buminemia (
Kasahara et al. BMC Cancer (2022) 22:20 Page 3 of 11 Results score significantly correlated with age (P = 0.046), Patient clinicopathological characteristics in association BMI (P = 0.039), tumour location (P = 0.008), surgi- with GPS scores cal approach (P = 0.02), tumour size (P
Kasahara et al. BMC Cancer (2022) 22:20 Page 4 of 11 Table 2 The relarionship between GPS score and clinicopathological characteristics variable GPS 0 GPS 1 GPS 2 P Value (N = 409) (N = 117) (N = 68) Age (years) 0.046
Kasahara et al. BMC Cancer (2022) 22:20 Page 5 of 11 Table 3 The relarionship between mGPS score and clinicopathological characteristics variable mGPS 0 mGPS 1 mGPS 2 P Value (N = 493) (N = 49) (N = 49) Age (years) 0.101
Kasahara et al. BMC Cancer (2022) 22:20 Page 6 of 11 Fig. 1 Overall survival in patients with colorectal cancer according to HS-GPS (a), GPS (b), and mGPS (c). GPS, Glasgow prognostic score; HS-GPS, high-sensitivity mGPS; mGPS, modified Glasgow prognostic score
Kasahara et al. BMC Cancer (2022) 22:20 Page 7 of 11 Table 4 Results of univariate and multivariate analysis of clinicopathological factors affecting OS variable univariate analysis multivariate analysis HS-GPS model GPS model mGPS model p value HR 95%CI p value HR 95%CI p value HR 95%CI p value Age (years) 0.001 2.049 1.195–3.413 0.009 2.052 1.180–3.568 0.11 1.98 1.163–3.371 0.02
Kasahara et al. BMC Cancer (2022) 22:20 Page 8 of 11 (Fig. 2a). For the GPS, the test showed a significant dif- The accuracy of the three inflammation-based prog- ference in GPS 2 vs 0 (P = 0.011) (Fig. 2b). For the mGPS, nostic scoring systems is a frequent topic of discussion. the test showed a significant difference in mGPS 2 vs 0 GPS scores are determined using both CRP and albumin (P = 0.007) (Fig. 2c). values; a score of 0 in both the mGPS and HS-mGPS sys- Table 5 summarises the results of the univariate and tems is determined using CRP alone, regardless of albu- multivariate analyses of the predictive ability of each min levels. Therefore, though hypoalbuminemia is more inflammation-based prognostic score model and other likely to occur secondary to elevated CRP levels, a cru- clinicopathological factors for RFS. Univariate analysis cial difference between the GPS and mGPS or HS-GPS showed that age, pT factor, pN factor, and CEA showed is the inclusion of patients with hypoalbuminemia in the significant differences in RFS prediction. Multivariate absence of elevated CRP levels. Thus, both the inflamma- analysis was performed for the factors that showed sig- tory response and nutritional status must be considered nificant differences (P
Kasahara et al. BMC Cancer (2022) 22:20 Page 9 of 11 Fig. 2 Recurrence-free survival in patients with colorectal cancer according to HS-GPS (a), GPS (b), mGPS (c). GPS, Glasgow prognostic score; HS-GPS, high-sensitivity mGPS; mGPS, modified Glasgow prognostic score
Kasahara et al. BMC Cancer (2022) 22:20 Page 10 of 11 Table 5 Results of univariate and multivariate analysis of clinicopathological factors affecting RFS variable univariate analysis multivariate analysis HS-GPS model GPS model mGPS model p value HR 95%CI p value HR 95%CI p value HR 95%CI p value Age (years) 0.027 1.349 0.897–2.028 0.151 1.281 0.848–1.934 0.24 1.232 0.830–1.830 0.3
Kasahara et al. BMC Cancer (2022) 22:20 Page 11 of 11 unknown. Further improvement in the prognosis of CRC 6. Hashiguchi Y, Muro K, Saito Y, Ito Y, Ajioka Y, Hamaguchi T, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines:1–42. may not be possible with a single marker. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guide- lines:1–42. Japanese Society for Cancer of the Colon and Rectum (JSCCR) Conclusion guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol. 2020;25:1–42. HS-GPS was useful for predicting the OS prognosis of 7. Deshmukh SK, Srivastava SK, Poosarla T, Dyess DL, Holliday NP, Singh AP, resectable advanced CC. Long-term prediction of RFS et al. Inflammation, immunosuppressive microenvironment and breast only showed a dominant tendency. HS-GPS may be less cancer: opportunities for cancer prevention and therapy. Ann Transl Med. 2019;7:593. effective as a prognostic score for CC than GPS. 8. Benson AB 3rd, Venook AP, Cederquist L, Chan E, Chen YJ, Cooper HS, et al. Colon Cancer, Version 1.2017, NCCN Clinical Practice Guidelines in Acknowledgements Oncology. J Natl Compr Canc Netw. 2017;15:370–98. Not applicable. 9. Benson AB, Venook AP, Al-Hawary MM, Cederquist L, Chen YJ, Ciombor KK, et al. NCCN Guidelines Insights: Colon Cancer, Version 2.2018. J Natl Authors’ contributions Compr Canc Netw. 2018;16:359–69. KK contributed to the concept and design of the study, collection and inter- 10. Mazaki J, Katsumata K, Kasahara K, Tago T, Wada T, Kuwabara H, et al. pretation of data, writing of the manuscript, and revision of the manuscript. Neutrophil-to-lymphocyte ratio is a prognostic factor for colon cancer: a ME and KK contributed to the concept and design of the study, interpreta- propensity score analysis. BMC Cancer. 2020;20:922. tion of data, and revision of the manuscript. RU, TI, JM, TT, TY, YN, and AT 11. Chan JC, Chan DL, Diakos CI, Engel A, Pavlakis N, Gill A, et al. The contributed to the collection and interpretation of data and revision of the lymphocyte-to-monocyte ratio is a superior predictor of overall survival manuscript. All the authors approved the final version of the manuscript. in comparison to established biomarkers of resectable colorectal cancer. Ann Surg. 2017;265:539–46. Funding 12. Rossi S, Basso M, Strippoli A, Schinzari G, D’Argento E, Larocca M, et al. Are The authors declare that they have received no grants/funds from any institu- markers of systemic inflammation good prognostic indicators in colorec- tion/organization/person for the purpose of this study. tal cancer? Clin Colorectal Cancer. 2017;16:264–74. 13. Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ. Evalua- Availability of data and materials tion of cumulative prognostic scores based on the systemic inflamma- The datasets during and/or analysed during the current study are available tory response in patients with inoperable non-small-cell lung cancer. Br J from the corresponding author upon reasonable request. Cancer. 2003;89:1028–30. 14. McMillan DC, Crozier JE, Canna K, Angerson WJ, McArdle CS. Evaluation Declarations of an inflammation-based prognostic score (GPS) in patients undergoing resection for colon and rectal cancer. Int J Color Dis. 2007;22:881–6. Ethics approval and consent to participate 15. Dolan RD, Lim J, McSorley ST, Horgan PG, McMillan DC. The role of the This study adhered to the principles of the Declaration of Helsinki and was systemic inflammatory response in predicting outcomes in patients approved by the Ethics Committee of Tokyo Medical University Hospital with operable cancer: systematic review and meta-analysis. Sci Rep. (T2019–0054). Informed consent was obtained from all patients. 2017;7:16717. 16. Liu Y, He X, Pan J, Chen S, Wang L. Prognostic role of Glasgow prognostic Consent for publication score in patients with colorectal cancer: evidence from population stud- Not applicable. ies. Sci Rep. 2017;7:6144. 17. Hirahara N, Matsubara T, Kaji S, Kawabata Y, Hyakudomi R, Yamamoto T, Competing interests et al. Glasgow prognostic score is a better predictor of the long-term sur- The authors have no conflicts of interest directly relevant to the content of this vival in patients with gastric cancer, compared to the modified Glasgow article. prognostic score or high-sensitivity modified Glasgow prognostic score. Oncotarget. 2020;11:4169–77. Received: 3 April 2021 Accepted: 10 December 2021 Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. References 1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49. https://doi.org/10.3322/caac.21660. 2. Lu X, Guo W, Xu W, Zhang X, Shi Z, Zheng L, et al. Prognostic value of the Glasgow prognostic score in colorectal cancer: a meta-analysis of 9,839 Ready to submit your research ? Choose BMC and benefit from: patients. Cancer Manag Res. 2019;11:229–49. 3. Roxburgh CS, McMillan DC. Role of systemic inflammatory response • fast, convenient online submission in predicting survival in patients with primary operable cancer. Future • thorough peer review by experienced researchers in your field Oncol. 2010;6:149–63. 4. Son W, Shin SJ, Park SH, Lee SK, Park EJ, Baik SH, et al. Clinical impact of • rapid publication on acceptance combined modified Glasgow prognostic score and C-reactive protein/ • support for research data, including large and complex data types albumin ratio in patients with colorectal cancer. Diagnostics (Basel). • gold Open Access which fosters wider collaboration and increased citations 2020;10:859. 5. 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