DOI QR코드

DOI QR Code

Prognostic Role of C-reactive Protein in Gastric Cancer: A Meta-analysis

  • Yu, Qing (Department of Oncological Surgery, the First Affiliated Hospital, Zhejiang University) ;
  • Yu, Xiong-Fei (Department of Oncological Surgery, the First Affiliated Hospital, Zhejiang University) ;
  • Zhang, Shou-De (Sir Run Run Shaw Hospital, Zhejiang University) ;
  • Wang, Hao-Hao (Department of Oncological Surgery, the First Affiliated Hospital, Zhejiang University) ;
  • Wang, Hai-Yong (Department of Oncological Surgery, the First Affiliated Hospital, Zhejiang University) ;
  • Teng, Li-Song (Department of Oncological Surgery, the First Affiliated Hospital, Zhejiang University)
  • Published : 2013.10.30

Abstract

Background: A number of studies have investigated the association between increased pretreatment serum C-reactive protein (CRP) levels and the prognosis of gastric cancer. However, due to the inconsistent results, whether the serum CRP level can be a prognostic factor in primary gastric cancer remains controversial. Methods: We searched Medline, PubMed, Embase and the Cochrane Central Register of Controlled Trials for relevant high-quality reports. A meta-analysis was carried out using the included studies to assess the association between pretreatment serum CRP level and overall survival (OS) in patients with gastric cancer. Correlation analyses were conducted to evaluate the relationship between serum CRP and tumor characteristics such as tumor node metastasis (TNM) stage and recurrence. Results: Twelve reports involving 2,597 patients with gastric cancer were included. Primary meta-analysis indicated a significant association between elevated CRP level and poor OS (HR 1.77, 95% CI 1.56-2.00). Subgroup analyses showed no single factor could alter the primary results when we divided the included studies by "number of patients", "max follow-up period", "TNM stage", "treatment" and "cut-off value". Correlation analyses showed that serum CRP level was significantly related to TNM stage (OR 2.96, 95% CI 2.22-3.93) and tumor recurrence (OR 1.81, 95% CI 1.21-2.71). Conclusions: We demonstrated that increased pretreatment serum CRP level (${\geq}10mg/L$) was significantly associated with poor prognosis in gastric cancer patients, either in early or advanced stages.

Keywords

C-reactive protein;gastric carcinoma;prognosis;meta-analysis

References

  1. Aizawa M, Gotohda N, Takahashi S, Konishi M, Kinoshita T (2011). Predictive value of baseline neutrophil/lymphocyte ratio for t4 disease in wall-penetrating gastric cancer. World J Surg, 35, 2717-22. https://doi.org/10.1007/s00268-011-1269-2
  2. Bonner JA, Harari PM, Giralt J, et al (2010). Radiotherapy plus cetuximab for locoregionally advanced head and neck cancer: 5-year survival data from a phase 3 randomised trial, and relation between cetuximab-induced rash and survival. Lancet Oncol, 11, 21-8. https://doi.org/10.1016/S1470-2045(09)70311-0
  3. Balkwill F, Mantovani A (2001). Inflammation and cancer: back to virchow? Lancet, 357, 539-45. https://doi.org/10.1016/S0140-6736(00)04046-0
  4. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50, 1088-101. https://doi.org/10.2307/2533446
  5. Bonner JA, Harari PM, Giralt J, et al (2006). Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med, 354, 567-78. https://doi.org/10.1056/NEJMoa053422
  6. Caruso R, Pallone F, Monteleone G (2007). Emerging role of il-23/il-17 axis in h pylori-associated pathology. World J Gastroenterol, 13, 5547-51. https://doi.org/10.3748/wjg.v13.i42.5547
  7. Catalano V, Labianca R, Beretta GD, et al (2009). Gastric cancer. Crit Rev Oncol Hematol, 71, 127-64. https://doi.org/10.1016/j.critrevonc.2009.01.004
  8. Chang CC, Sun CF, Pai HJ, et al (2010). Preoperative serum c-reactive protein and gastric cancer; Clinical-pathological correlation and prognostic significance. Chang Gung Med J, 33, 301-12.
  9. Chen W, Zheng R, Zhang S, et al (2013). Report of incidence and mortality in china cancer registries, 2009. Chin J Cancer Res, 25, 10-21.
  10. Correa P (1992). Human gastric carcinogenesis: a multistep and multifactorial process--first american cancer society award lecture on cancer epidemiology and prevention. Cancer Res, 52, 6735-40.
  11. Coussens LM, Werb Z (2002). Inflammation and cancer. Nature, 420, 860-7. https://doi.org/10.1038/nature01322
  12. Egger M, Davey SG, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315, 629-34. https://doi.org/10.1136/bmj.315.7109.629
  13. Crumley AB, McMillan DC, McKernan M, McDonald AC, Stuart RC (2006). Evaluation of an inflammation-based prognostic score in patients with inoperable gastro-oesophageal cancer. Br J Cancer, 94, 637-41.
  14. Crumley AB, Stuart RC, McKernan M, McMillan DC (2010). Is hypoalbuminemia an independent prognostic factor in patients with gastric cancer? World J Surg, 34, 2393-8. https://doi.org/10.1007/s00268-010-0641-y
  15. Cunningham D, Allum WH, Stenning SP, et al (2006). Perioperative chemotherapy versus surgery alone for resectable gastroesophageal cancer. N Engl J Med, 355, 11-20. https://doi.org/10.1056/NEJMoa055531
  16. Forman D (2001). Gastric cancer and helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts. Gut, B, 347-53.
  17. Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ (2003). Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer, 89, 1028-30. https://doi.org/10.1038/sj.bjc.6601242
  18. Fujitani K, Yamada M, Hirao M, Kurokawa Y, Tsujinaka T (2011). Optimal indications of surgical palliation for incurable advanced gastric cancer presenting with malignant gastrointestinal obstruction. Gastric Cancer, 14, 353-9. https://doi.org/10.1007/s10120-011-0053-1
  19. Gabay C, Kushner I (1999). Acute-phase proteins and other systemic responses to inflammation. N Engl J Med, 340, 448-54. https://doi.org/10.1056/NEJM199902113400607
  20. Gencer D, Kastle-Larralde N, Pilz LR, et al (2009). Presentation, treatment, and analysis of prognostic factors of terminally ill patients with gastrointestinal tumors. Onkologie, 32, 380-6.
  21. Hurlimann J, Thorbecke GJ, Hochwald GM (1966). The liver as the site of c-reactive protein formation. J Exp Med, 123, 365-78. https://doi.org/10.1084/jem.123.2.365
  22. Hashimoto K, Takashima A, Nagashima K, et al (2010). Progression-free survival in first-line chemotherapy is a prognostic factor in second-line chemotherapy in patients with advanced gastric cancer. J Cancer Res Clin Oncol, 136, 1059-64. https://doi.org/10.1007/s00432-009-0752-8
  23. Heikkila K, Ebrahim S, Lawlor DA (2007). A systematic review of the association between circulating concentrations of c reactive protein and cancer. J Epidemiol Community Health, 61, 824-33. https://doi.org/10.1136/jech.2006.051292
  24. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003). Measuring inconsistency in meta-analyses. BMJ, 327, 557-60. https://doi.org/10.1136/bmj.327.7414.557
  25. Hwang JE, Kim HN, Kim DE, et al (2011). Prognostic significance of a systemic inflammatory response in patients receiving first-line palliative chemotherapy for recurred or metastatic gastric cancer. BMC Cancer, 11, 489. https://doi.org/10.1186/1471-2407-11-489
  26. Iwasa S, Nakajima TE, Nakamura K, et al (2011). Systemic chemotherapy for peritoneal disseminated gastric cancer with inadequate oral intake: a retrospective study. Int J Clin Oncol, 16, 57-62. https://doi.org/10.1007/s10147-010-0135-9
  27. Jemal A, Bray F, Center MM, et al (2011). Global cancer statistics. CA Cancer J Clin, 61, 69-90. https://doi.org/10.3322/caac.20107
  28. Jeong JH, Lim SM, Yun JY, et al (2012). Comparison of two inflammation-based prognostic scores in patients with unresectable advanced gastric cancer. Oncology, 83, 292-9. https://doi.org/10.1159/000342376
  29. Kao SC, Pavlakis N, Harvie R, et al (2010). High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy. Clin Cancer Res, 16, 5805-13. https://doi.org/10.1158/1078-0432.CCR-10-2245
  30. Mantovani A, Allavena P, Sica A, Balkwill F (2008). Cancer-related inflammation. Nature, 454, 436-44. https://doi.org/10.1038/nature07205
  31. Karakiewicz PI, Hutterer GC, Trinh QD, et al (2007). C-reactive protein is an informative predictor of renal cell carcinoma-specific mortality: a european study of 313 patients. Cancer, 110, 1241-7. https://doi.org/10.1002/cncr.22896
  32. Kwon HC, Kim SH, Oh SY, et al (2012). Clinicopathologic significance of expression of nuclear factor-kappab rela and its target gene products in gastric cancer patients. World J Gastroenterol, 18, 4744-50. https://doi.org/10.3748/wjg.v18.i34.4744
  33. Macdonald JS, Smalley SR, Benedetti J, et al (2001). Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction. N Engl J Med, 345, 725-30. https://doi.org/10.1056/NEJMoa010187
  34. Mohri Y, Tanaka K, Ohi M, et al (2010). Prognostic significance of host- and tumor-related factors in patients with gastric cancer. World J Surg, 34, 285-90. https://doi.org/10.1007/s00268-009-0302-1
  35. Nozoe T, Iguchi T, Adachi E, Matsukuma A, Ezaki T (2011). Preoperative elevation of serum c-reactive protein as an independent prognostic indicator for gastric cancer. Surg Today, 41, 510-3. https://doi.org/10.1007/s00595-009-4297-x
  36. Parmar MK, Torri V, Stewart L (1998). Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med, 17, 2815-34. https://doi.org/10.1002/(SICI)1097-0258(19981230)17:24<2815::AID-SIM110>3.0.CO;2-8
  37. Parsonnet J, Friedman GD, Vandersteen DP, et al (1991). Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med, 325, 1127-31. https://doi.org/10.1056/NEJM199110173251603
  38. Pine JK, Fusai KG, Young R, et al (2009). Serum c-reactive protein concentration and the prognosis of ductal adenocarcinoma of the head of pancreas. Eur J Surg Oncol, 35, 605-10. https://doi.org/10.1016/j.ejso.2008.12.002
  39. Talmadge J E, Fidler I J (2010). Aacr centennial series: the biology of cancer metastasis: historical perspective. Cancer Res, 70, 5649-69. https://doi.org/10.1158/0008-5472.CAN-10-1040
  40. Proctor MJ, Morrison DS, Talwar D, et al (2011). An inflammation-based prognostic score (mgps) predicts cancer survival independent of tumour site: a glasgow inflammation outcome study. Br J Cancer, 104, 726-34. https://doi.org/10.1038/sj.bjc.6606087
  41. Sakuramoto S, Sasako M, Yamaguchi T, et al (2007). Adjuvant chemotherapy for gastric cancer with s-1, an oral fluoropyrimidine. N Engl J Med, 357, 1810-20. https://doi.org/10.1056/NEJMoa072252
  42. Shimura T, Kitagawa M, Yamada T, et al (2012). C-reactive protein is a potential prognostic factor for metastatic gastric cancer. Anticancer Res, 32, 491-6.
  43. Tillett W S, Francis T (1930). Serological reactions in pneumonia with a non-protein somatic fraction of pneumococcus. J Exp Med, 52, 561-71. https://doi.org/10.1084/jem.52.4.561
  44. Ulich TR, Del CJ, Guo K, Souza L (1989). The hematologic effects of chronic administration of the monokines tumor necrosis factor, interleukin-1, and granulocyte-colony stimulating factor on bone marrow and circulation. Am J Pathol, 134, 149-59.
  45. Ulich TR, Del CJ, Keys M, Granger GA, Ni RX (1987). Kinetics and mechanisms of recombinant human interleukin 1 and tumor necrosis factor-alpha-induced changes in circulating numbers of neutrophils and lymphocytes. J Immunol, 139, 3406-15.
  46. Wang DS, Ren C, Qiu MZ, et al (2012). Comparison of the prognostic value of various preoperative inflammation-based factors in patients with stage iii gastric cancer. Tumour Biol, 33, 749-56. https://doi.org/10.1007/s13277-011-0285-z
  47. Wells GA, Shea B, O'Connell D, et al (2008). The newcastle-ottawa scale (nos) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm, Accessed 1 January 2008,
  48. Woo Y, Hyung WJ, Obama K, et al (2012). Elevated high-sensitivity c-reactive protein, a marker of advanced stage gastric cancer and postgastrectomy disease recurrence. J Surg Oncol, 105, 405-9. https://doi.org/10.1002/jso.22129
  49. Zheng ZX, Zheng RS, Chen WQ (2013). An analysis of incidence and mortality of stomach cancer in china, 2009. China Cancer, 327-32.

Cited by

  1. Prognostic Significance of the Peripheral Blood Absolute Monocyte Count in Patients with Locally Advanced or Metastatic Hepatocellular Carcinoma Receiving Systemic Chemotherapy vol.15, pp.15, 2014, https://doi.org/10.7314/APJCP.2014.15.15.6387
  2. Prognostic Value of C-Reactive Protein in Esophageal Cancer: a Meta-analysis vol.15, pp.19, 2014, https://doi.org/10.7314/APJCP.2014.15.19.8075
  3. Goseki Grade and Tumour Location Influence Survival of Patients with Gastric Cancer vol.15, pp.3, 2014, https://doi.org/10.7314/APJCP.2014.15.3.1429
  4. Prognostic Significance of C-reactive Protein in Urological Cancers: a Systematic Review and Meta-analysis vol.15, pp.8, 2014, https://doi.org/10.7314/APJCP.2014.15.8.3369
  5. Meta-Analysis of the Prognostic Value of Smad4 Immunohistochemistry in Various Cancers vol.9, pp.10, 2014, https://doi.org/10.1371/journal.pone.0110182
  6. Effect of Intraoperative Glucose Fluctuation and Postoperative IL-6, TNF-α, CRP Levels on the Short-term Prognosis of Patients with Intracranial Supratentorial Neoplasms vol.15, pp.24, 2015, https://doi.org/10.7314/APJCP.2014.15.24.10879
  7. Evaluation of Inflammation Parameters in Philadelphia Negative Chronic Myeloproliferative Neoplasia Patients vol.16, pp.13, 2015, https://doi.org/10.7314/APJCP.2015.16.13.5159
  8. Nutrition support can bring survival benefit to high nutrition risk gastric cancer patients who received chemotherapy vol.23, pp.7, 2015, https://doi.org/10.1007/s00520-014-2523-6
  9. FokI Polymorphism of the Vitamin D Receptor Gene Is Associated with Susceptibility to Gastric Cancer: A Case-Control Study vol.236, pp.3, 2015, https://doi.org/10.1620/tjem.236.219
  10. Preoperative C-reactive protein as a prognostic predictor for upper tract urothelial carcinoma: A systematic review and meta-analysis vol.3, pp.4, 2015, https://doi.org/10.3892/mco.2015.553
  11. Serum C-reactive protein and overall survival of patients with osteosarcoma vol.36, pp.7, 2015, https://doi.org/10.1007/s13277-015-3240-6
  12. Association between the inflammatory biomarker, C-reactive protein, and the response to radiochemotherapy in patients with esophageal cancer vol.4, pp.4, 2016, https://doi.org/10.3892/mco.2016.753
  13. Relationship between red blood cell distribution width, bilirubin, and clinical characteristics of patients with gastric cancer vol.39, pp.5, 2017, https://doi.org/10.1111/ijlh.12675
  14. Prognostic Significance of the Preoperative Ratio of C-Reactive Protein to Albumin and Neutrophil–Lymphocyte Ratio in Gastric Cancer Patients pp.1432-2323, 2017, https://doi.org/10.1007/s00268-017-4400-1
  15. Prognostic Significance of Platelet-Based Inflammatory Indicators in Patients with Gastric Cancer vol.42, pp.8, 2018, https://doi.org/10.1007/s00268-018-4527-8
  16. Comparison of body condition score and other minimally invasive biomarkers between dogs with gastric carcinoma and dogs with chronic gastritis vol.254, pp.2, 2019, https://doi.org/10.2460/javma.254.2.226