Skip to main content

Advertisement

Log in

Evaluation of Two Inflammation-Based Prognostic Scores in Patients with Resectable Gallbladder Carcinoma

  • Hepatobiliary Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Survival after surgery for gallbladder cancer is generally poor. A number of inflammation-based prognostic scores have been established to help predict survival after surgery for several types of cancer. The objective of this study was to analyze and compare the utility of two inflammation-based prognostic scores, the Glasgow prognostic score (GPS) and the neutrophil-to-lymphocyte ratio (NLR), for predicting survival in patients with gallbladder cancer after surgery with curative intent.

Methods

We retrospectively reviewed the medical records of 85 patients with histologically confirmed, resectable gallbladder carcinoma (GBC), who were to receive curative surgery in our department. Univariate and multivariate analyses were performed to evaluate the relationship between the variables to overall survival (OS).

Results

A significant difference was detected in OS in patients with low and high GPS and NLR scores. Univariate analyses using clinicopathological characteristics revealed that tumor differentiation; tumor invasion; lymph node metastasis; tumor, node, metastasis classification system stage; positive margin status; combined common bile duct resection; serum levels of C-reactive protein, albumin, carbohydrate antigen 19-9 (CA19-9), carcinoembryonic antigen, and CA125; white blood cell count; and GPS and NLR were all associated with OS. Among these characteristics, multivariate analysis demonstrated that a high GPS was independently associated with poorer OS, together with tumor invasion, lymph node metastasis, and positive margin status.

Conclusions

GPS is superior to NLR with respect to its prognostic value for patients with GBC after surgery with curative intent. GPS is not only associated with tumor progression but is also an independent marker of poor prognosis.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Cobourn N, Cleary S, Tan J, et al. Surgery for gallbladder cancer: a population-based analysis. J Am Coll Surg. 2008;207:371–82.

    Article  Google Scholar 

  2. Wang JW, Peng SY, Li JT, et al. Identification of metastasis-associated proteins involved in gallbladder carcinoma metastasis by proteomic analysis and functional exploration of chloride intracellular channel 1. Cancer Lett. 2009;281:71–81.

    Article  CAS  PubMed  Google Scholar 

  3. Liu YB, He XW, Wang JW, et al. Establishment of liver metastasis model of human gallbladder cancer and isolation of the subpopulation with high metastatic potential. Zhonghua Yi Xue Za Zhi. 2006;86:2117–21.

    PubMed  Google Scholar 

  4. Quan Z, Gu J, Dong P, et al. Reactive oxygen species-mediated endoplasmic reticulum stress and mitochondrial dysfunction contribute to cirsimaritin-induced apoptosis in human gallbladder carcinoma GBC-SD cells. Cancer Lett. 2010;295:252–9.

    Article  CAS  PubMed  Google Scholar 

  5. Dong P, Zhang Y, Gu J, et al. Wogonin, an active ingredient of Chinese herb medicine Scutellaria baicalensis, inhibits the mobility and invasion of human gallbladder carcinoma GBC-SD cells by inducing the expression of maspin. J Ethnopharmacol. 2011;137:1373–80.

    Article  CAS  PubMed  Google Scholar 

  6. Dong P, He XW, Gu J, et al. Vimentin significantly promoted gallbladder carcinoma metastasis. Chin Med J (Engl). 2011;124:4236–44.

    CAS  PubMed  Google Scholar 

  7. Zhang Z, Wang X, Wu W, et al. Effects of matrine on proliferation and apoptosis in gallbladder carcinoma cells (GBC-SD). Phytother Res. 2012;26:932–7.

    Article  CAS  PubMed  Google Scholar 

  8. Tan Z, Li M, Wu W, et al. NLK is a key regulator of proliferation and migration in gallbladder carcinoma cells. Mol Cell Biochem. 2012;369:27–33.

    Article  CAS  PubMed  Google Scholar 

  9. He XW, Cao HQ, Xu LP, et al. Establishment and characterization of serial subpopulations with highly metastatic potential via different metastatic routes. Zhonghua Yi Xue Za Zhi. 2011;91:1852–5.

    CAS  PubMed  Google Scholar 

  10. Batra Y, Pal S, Dutta U, et al. Gallbladder cancer in India: a dismal picture. J Gastroenterol Hepatol. 2005;20:309–14.

    Article  PubMed  Google Scholar 

  11. Bartlett DL, Fong Y, Fortner JG, et al. Long-term results after resection for gallbladder cancer. Implications for staging and management. Ann Surg. 1996;224:639–46.

    Article  CAS  PubMed  Google Scholar 

  12. Butte JM, Matsuo K, Gönen M, et al. Gallbladder cancer: differences in presentation, surgical treatment, and survival in patients treated at centers in three countries. J Am Coll Surg. 2011;212:50–61.

    Article  PubMed  Google Scholar 

  13. Cziupka K, Partecke LI, Mirow L, et al. Outcomes and prognostic factors in gallbladder cancer: a single-centre experience. Langenbecks Arch Surg. 2012;397:899–907.

    Article  PubMed  Google Scholar 

  14. Kobayashi A, Oda T, Fukunaga K, et al. Invasion of the hepatic artery is a crucial predictor of poor outcomes in gallbladder carcinoma. World J Surg. 2012;36:645–50.

    Article  PubMed  Google Scholar 

  15. Lee HJ, Lee K, Lee DG, et al. Chemokine (C–X–C motif) ligand 12 is associated with gallbladder carcinoma progression and is a novel independent poor prognostic factor. Clin Cancer Res. 2012;18:3270–80.

    Article  CAS  PubMed  Google Scholar 

  16. Yang XW, Yang J, Li L, et al. Analysis of the relationships between clinicopathologic factors and survival in gallbladder cancer following surgical resection with curative intent. PLoS One. 2012;7:e51513. doi:10.1371/journal.pone.0051513.

  17. Lim H, Seo DW, Park DH, et al. Prognostic factors in patients with gallbladder cancer after surgical resection: analysis of 279 operated patients. J Clin Gastroenterol. 2013;47:443–8.

    Google Scholar 

  18. Nevin JE, Moran TJ, Kay S, et al. Carcinoma of the gallbladder: staging, treatment, and prognosis. Cancer. 1976;37:141–8.

    Article  CAS  PubMed  Google Scholar 

  19. Edge SB; American Joint Committee on Cancer; American Cancer Society. AJCC cancer staging handbook: from the AJCC cancer staging manual. 7th ed. New York: Springer; 2010.

    Google Scholar 

  20. La Torre M, Nigri G, Cavallini M, et al. The Glasgow prognostic score as a predictor of survival in patients with potentially resectable pancreatic adenocarcinoma. Ann Surg Oncol. 2012;19:2917–23.

    Article  PubMed  Google Scholar 

  21. Kubota T, Hiki N, Nunobe S, et al. Significance of the inflammation-based Glasgow prognostic score for short- and long-term outcomes after curative resection of gastric cancer. J Gastrointest Surg. 2012;16:2037–44.

    Article  PubMed  Google Scholar 

  22. Ishizuka M, Nagata H, Takagi K, et al. Inflammation-based prognostic system predicts survival after surgery for stage IV colorectal cancer. Am J Surg. 2013;205:22–8.

    Article  PubMed  Google Scholar 

  23. Jeong JH, Lim SM, Yun JY, et al. Comparison of two inflammation-based prognostic scores in patients with unresectable advanced gastric cancer. Oncology. 2012;83:292–9.

    Article  PubMed  Google Scholar 

  24. He W, Yin C, Guo G, Jiang C, et al. Initial neutrophil lymphocyte ratio is superior to platelet lymphocyte ratio as an adverse prognostic and predictive factor in metastatic colorectal cancer. Med Oncol. 2013;30:439. doi:10.1007/s12032-012-0439-x.

  25. Azab B, Shah N, Radbel J, et al. Pretreatment neutrophil/lymphocyte ratio is superior to platelet/lymphocyte ratio as a predictor of long-term mortality in breast cancer patients. Med Oncol. 2013;30:432. doi:10.1007/s12032-012-0432-4.

    Google Scholar 

  26. Forrest LM, McMillan DC, McArdle CS, et al. Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable nonsmall-cell lung cancer. Br J Cancer. 2003;89:1028–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Lien YC, Hsieh CC, Wu YC, et al. Preoperative serum albumin level is a prognostic indicator for adenocarcinoma of the gastric cardia. J Gastrointest Surg. 2004;8:1041–8.

    Article  PubMed  Google Scholar 

  28. Crumley AB, McMillan DC, McKernan M, et al. Evaluation of an inflammation-based prognostic score in patients with inoperable gastrooesophageal cancer. Br J Cancer. 2006;94:637–41.

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Scott HR, McMillan DC, Forrest LM, et al. The systemic inflammatory response, weight loss, performance status and survival in patients with inoperable non-small cell lung cancer. Br J Cancer. 2002;87:264–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Azab B, Bhatt V, Phookhan J, et al. Usefulness of the neutrophil-to-lymphocyte ratio in predicting short- and long-term mortality in breast cancer patients. Ann Surg Oncol. 2012;19:217–24.

    Article  PubMed  Google Scholar 

  31. Regimbeau JM, Fuks D, Bachellier P, et al. Prognostic value of jaundice in patients with gallbladder cancer by the AFC-GBC-2009 study group. Eur J Surg Oncol. 2011;37:505–12.

    Article  CAS  PubMed  Google Scholar 

  32. Kao SC, Pavlakis N, Harvie R, et al. High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy. Clin Cancer Res. 2010;16:5805–13.

    Article  CAS  PubMed  Google Scholar 

  33. Wenguang W, Xuefeng W, Zhiping Z, et al. Three-step method for lymphadenectomy in gastric cancer surgery: a single institution experience of 120 patients. J Am Coll Surg. 2011;212:200–8.

    Article  PubMed  Google Scholar 

  34. Kinoshita A, Onoda H, Imai N, et al. The Glasgow Prognostic Score, an inflammation based prognostic score, predicts survival in patients with hepatocellular carcinoma. BMC Cancer. 2013;13:52. doi:10.1186/1471-2407-13-52.

  35. Qian BZ, Li J, Zhang H, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Tan W, Zhang W, Strasner A, et al. Tumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signalling. Nature. 2011;470:548–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Mantovani A. Cancer: inflaming metastasis. Nature. 2009;457:36–7.

    Article  CAS  PubMed  Google Scholar 

  39. Roxburgh CS, McMillan DC. Role of systemic inflammatory response in predicting survival in patients with primary operable cancer. Future Oncol. 2010;6:149–63.

    Article  CAS  PubMed  Google Scholar 

  40. Koike Y, Miki C, Okugawa Y, et al. Preoperative C-reactive protein as a prognostic and therapeutic marker for colorectal cancer. J Surg Oncol. 2008;98:540–4.

    Article  CAS  PubMed  Google Scholar 

  41. Jagdev SP, Gregory W, Vasudev NS, et al. Improving the accuracy of preoperative survival prediction in renal cell carcinoma with C-reactive protein. Br J Cancer. 2010;103:1649–56.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Kobayashi T, Teruya M, Kishiki T, et al. Inflammation-based prognostic score, prior to neoadjuvant chemoradiotherapy, predicts postoperative outcome in patients with esophageal squamous cell carcinoma. Surgery. 2008;144:729–35.

    Article  PubMed  Google Scholar 

  43. McMillan DC, Elahi MM, Sattar N, et al. Measurement of the systemic inflammatory response predicts cancer specific and non-cancer survival in patients with cancer. Nutr Cancer. 2001;41:64–9.

    CAS  PubMed  Google Scholar 

  44. Gregory AD, Houghton AM. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res. 2011;71:2411–6.

    Article  CAS  PubMed  Google Scholar 

  45. Zhao JJ, Pan K, Wang W, et al. The prognostic value of tumor-infiltrating neutrophils in gastric adenocarcinoma after resection. PLoS One. 2012;7:e33655. doi:10.1371/journal.pone.0033655.

  46. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21:137–48.

    Article  CAS  PubMed  Google Scholar 

  47. Morgan RA, Dudley ME, Wunderlich JR, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 2006;314:126–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Kinoshita A, Onoda H, Imai N, et al. Comparison of the prognostic value of inflammation-based prognostic scores in patients with hepatocellular carcinoma. Br J Cancer. 2012;107:988–93.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgment

This study was supported by National Natural Science Foundation of China (81272402 and 81172029), Foundation of Shanghai Outstanding Academic Leaders (11XD1403800), National High Technology Research and Development Program (863 Program; 2012AA022606), Shanghai Science And Technology Commission Medical-Guiding Project (12401905800), Foundation for Interdisciplinary Research of Shanghai Jiao Tong University (YG2011ZD07) and Chang Jiang Scholars Program.

Disclosures

The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ying-Bin Liu MD, PhD.

Additional information

Xiang-Song Wu and Liu-Bin Shi have contributed equally to this article, and both should be considered first author.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, XS., Shi, LB., Li, ML. et al. Evaluation of Two Inflammation-Based Prognostic Scores in Patients with Resectable Gallbladder Carcinoma. Ann Surg Oncol 21, 449–457 (2014). https://doi.org/10.1245/s10434-013-3292-z

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-013-3292-z

Keywords

Navigation