Skip to main content

Advertisement

Log in

Effects of the interleukin-1β-511 C/T gene polymorphism on the risk of gastric cancer in the context of the relationship between race and H. pylori infection: a meta-analysis of 20,000 subjects

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The interleukin (IL)-1β-511 C/T polymorphism has been shown to be functional and to contribute to the risk of gastric cancer. However, the relationship between the IL-1β-511 C/T polymorphism and gastric carcinogenesis remains inconclusive. A systematical electronic search was conducted of the MEDLINE, EMBASE, and CENTRAL databases. A random and a fixed effects model were exploited to estimate summary odds ratios and 95 % confidence intervals. Subgroup and sensitivity analyses were carried out with respect to ethnicity, quality assessment scores, control sources, genotyping methods, cancer histopathology and location, and Helicobacter pylori (H. pylori) infection. A total of 45 studies containing 9,066 cases of gastric cancer and 11,192 control subjects satisfied the inclusion criteria. The IL-1β-511 C/T polymorphism was found to enhance the risk of stomach cancer for overall and HWE-satisfying studies. Asians showed a positive relationship in both the overall and HWE-satisfying groups, whereas Caucasians did not. Based on subgroup analysis, H. pylori infection and genotype analysis using PCR–RFLP methods increase the association between IL-1β-511 T allele carrier and risk of stomach cancer. A positive relationship was found between the IL-1β-511 C/T SNP and stomach carcinoma susceptibility, and the results suggest that Asian ethnicity, H. pylori infection and methodologically, PCR–RFLP genotyping strengthen this relationship. Reflecting on prevalence of H. pylori in Asian countries, additional studies on the IL-1β-511 C/T SNP in the context of ethnicity and H. pylori infection may provide key insights into the mechanism underlying gastric cancer carcinogenesis. It was found PCR–RFLP is the most reliable genotyping method, and thus, it is recommendable to adopt it to determine the presence of the IL-1β-511 C/T SNP.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Rozengurt E, Walsh JH (2001) Gastrin, CCK, signaling, and cancer. Annu Rev Physiol 63:49–76

    Article  CAS  PubMed  Google Scholar 

  2. Ambs S, Merriam WG, Ogunfusika MO, Bennett WP, Ishibe N et al (1998) p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat Med 4:1371–1376

    Article  CAS  PubMed  Google Scholar 

  3. Oger P, Dessaux Y, Petit A, Gardan L, Manceau C et al (1998) Validity, sensitivity and resolution limit of the PCR–RFLP analysis of the rrs (16S rRNA gene) as a tool to identify soil-borne and plant-associated bacterial populations. Genet Sel Evol 30:1–22

    Article  Google Scholar 

  4. Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G et al (1995) Long-term sequelae of Helicobacter pylori gastritis. Lancet 345:1525–1528

    Article  CAS  PubMed  Google Scholar 

  5. Shin A, Kim J, Park S (2011) Gastric cancer epidemiology in Korea. J Gastric Cancer 11:135–140

    Article  PubMed Central  PubMed  Google Scholar 

  6. Logan RPH, Walker MM (2001) Epidemiology and diagnosis of Helicobacter pylori infection. BMJ 323:920–922

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Thakkinstian A, McEvoy M, Minelli C, Gibson P, Hancox B et al (2005) Systematic review and meta-analysis of the association between {beta}2-adrenoceptor polymorphisms and asthma: a HuGE review. Am J Epidemiol 162:201–211

    Article  PubMed  Google Scholar 

  8. El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH et al (2000) Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 404:398–402

    Article  CAS  PubMed  Google Scholar 

  9. Cox A, Camp NJ, Nicklin MJ, di Giovine FS, Duff GW (1998) An analysis of linkage disequilibrium in the interleukin-1 gene cluster, using a novel grouping method for multiallelic markers. Am J Hum Genet 62:1180–1188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Vincenzi B, Patti G, Galluzzo S, Pantano F, Venditti O et al (2008) Interleukin 1beta-511 T gene (IL1beta) polymorphism is correlated with gastric cancer in the Caucasian population: results from a meta-analysis. Oncol Rep 20:1213–1220

    PubMed  Google Scholar 

  11. Wang P, Xia HH, Zhang JY, Dai LP, Xu XQ et al (2007) Association of interleukin-1 gene polymorphisms with gastric cancer: a meta-analysis. Int J Cancer 120:552–562

    Article  CAS  PubMed  Google Scholar 

  12. Camargo MC, Mera R, Correa P, Peek RM Jr, Fontham ET et al (2006) Interleukin-1beta and interleukin-1 receptor antagonist gene polymorphisms and gastric cancer: a meta-analysis. Cancer Epidemiol Biomark Prev 15:1674–1687

    Article  CAS  Google Scholar 

  13. Xue H, Lin B, Ni P, Xu H, Huang G (2010) Interleukin-1B and interleukin-1 RN polymorphisms and gastric carcinoma risk: a meta-analysis. J Gastroenterol Hepatol 25:1604–1617

    Article  PubMed  Google Scholar 

  14. Song H, Peng JS, Yang ZL, Xiang J (2010) Association of interleukin-1 gene polymorphisms with susceptibility of gastric cancer: a meta-analysis of chinese population. Chinese Journal of Cancer Prevention and Treatment 17:1705–1710

    CAS  Google Scholar 

  15. Kamangar F, Cheng C, Abnet CC, Rabkin CS (2006) Interleukin-1B polymorphisms and gastric cancer risk—a meta-analysis. Cancer Epidemiol Biomark Prev 15:1920–1928

    Article  CAS  Google Scholar 

  16. Tiret L, Cambien F (1995) Departure from Hardy-Weinberg equilibrium should be systematically tested in studies of association between genetic markers and disease. Circulation 92:3364–3365

    CAS  PubMed  Google Scholar 

  17. Thompson SG, Pocock SJ (1991) Can meta-analyses be trusted? Lancet 338:1127–1130

    Article  CAS  PubMed  Google Scholar 

  18. Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22:719–748

    CAS  PubMed  Google Scholar 

  19. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  CAS  PubMed  Google Scholar 

  20. Gyorffy B, Kocsis I, Vasarhelyi B (2004) Biallelic genotype distributions in papers published in Gut between 1998 and 2003: altered conclusions after recalculating the Hardy–Weinberg equilibrium. Gut 53: 614–615; author reply 615-616

  21. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  CAS  PubMed  Google Scholar 

  22. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Zeng ZR, Hu PJ, Hu S, Pang RP, Chen MH et al (2003) Association of interleukin 1B gene polymorphism and gastric cancers in high and low prevalence regions in China. Gut 52:1684–1689

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Perri F, Piepoli A, Bonvicini C, Gentile A, Quitadamo M et al (2005) Cytokine gene polymorphisms in gastric cancer patients from two Italian areas at high and low cancer prevalence. Cytokine 30:293–302

    Article  CAS  PubMed  Google Scholar 

  25. Persson C, Engstrand L, Nyren O, Hansson LE, Enroth H et al (2009) Interleukin 1-beta gene polymorphisms and risk of gastric cancer in Sweden. Scand J Gastroenterol 44:339–345

    Article  CAS  PubMed  Google Scholar 

  26. Zhao JD, Geng PL, Li ZQ, Cui S, Zhao JH et al (2012) Associations between interleukin-1 polymorphisms and gastric cancers among three ethnicities. World J Gastroenterol 18:7093–7099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Burada F, Angelescu C, Mitrut P, Ciurea T, Cruce M et al (2012) Interleukin-4 receptor −3223T → C polymorphism is associated with increased gastric adenocarcinoma risk. Can J Gastroenterol 26:532–536

    PubMed Central  PubMed  Google Scholar 

  28. He BS, Pan YQ, Xu YF, Zhu C, Qu LL et al (2011) Polymorphisms in interleukin-1B (IL-1B) and interleukin 1 receptor antagonist (IL-1RN) genes associate with gastric cancer risk in the Chinese population. Dig Dis Sci 56:2017–2023

    Article  CAS  PubMed  Google Scholar 

  29. Wex T, Leodolter A, Bornschein J, Kuester D, Kahne T et al (2010) Interleukin 1 beta (IL1B) gene polymorphisms are not associated with gastric carcinogenesis in Germany. Anticancer Res 30:505–511

    CAS  PubMed  Google Scholar 

  30. Yu J, Zeng Z, Wang S, Tian L, Wu J et al (2010) IL-1β-511 polymorphism is associated with increased risk of certain subtypes of gastric cancer in Chinese: a case-control study. Am J Gastroenterol 105:557–564

    Article  CAS  PubMed  Google Scholar 

  31. Melo Barbosa HP, Martins LC, Dos Santos SE, Demachki S, Assumpcao MB et al (2009) Interleukin-1 and TNF-alpha polymorphisms and Helicobacter pylori in a Brazilian Amazon population. World J Gastroenterol 15:1465–1471

    Article  PubMed Central  PubMed  Google Scholar 

  32. Kumar S, Kumar A, Dixit VK (2009) Evidences showing association of interleukin-1B polymorphisms with increased risk of gastric cancer in an Indian population. Biochem Biophys Res Commun 387:456–460

    Article  CAS  PubMed  Google Scholar 

  33. Feng Y, Zhang J, Dai L, Zhang J, Wang P et al (2008) Inflammatory cytokine gene polymorphisms in gastric cancer cases’ and controls’ family members from Chinese areas at high cancer prevalence. Cancer Lett 270:250–259

    Article  CAS  PubMed  Google Scholar 

  34. Shin WG, Jang JS, Kim HS, Kim SJ, Kim KH et al (2008) Polymorphisms of interleukin-1 and interleukin-2 genes in patients with gastric cancer in Korea. J Gastroenterol Hepatol 23:1567–1573

    Article  CAS  PubMed  Google Scholar 

  35. Garcia-Gonzalez MA, Lanas A, Quintero E, Nicolas D, Parra-Blanco A et al (2007) Gastric cancer susceptibility is not linked to pro-and anti-inflammatory cytokine gene polymorphisms in whites: a Nationwide Multicenter Study in Spain. Am J Gastroenterol 102:1878–1892

    Article  CAS  PubMed  Google Scholar 

  36. Sun H, Wang Y, Ma X, Pei F, Sun H et al (2007) A method of oligochip for single nucleotide polymorphism genotyping in the promoter region of the interleukin-1 beta gene and its clinical application. Oligonucleotides 17:336–344

    Article  CAS  PubMed  Google Scholar 

  37. Sugimoto M, Furuta T, Shirai N, Nakamura A, Xiao F et al (2007) Different effects of polymorphisms of tumor necrosis factor-alpha and interleukin-1 beta on development of peptic ulcer and gastric cancer. J Gastroenterol Hepatol 22:51–59

    Article  CAS  PubMed  Google Scholar 

  38. Li C, Xia HH, Xie W, Hu Z, Ye M et al (2007) Association between interleukin-1 gene polymorphisms and Helicobacter pylori infection in gastric carcinogenesis in a Chinese population. J Gastroenterol Hepatol 22:234–239

    Article  CAS  PubMed  Google Scholar 

  39. Ito H, Kaneko K, Makino R, Konishi K, Kurahashi T et al (2007) Interleukin-1beta gene in esophageal, gastric and colorectal carcinomas. Oncol Rep 18:473–481

    CAS  PubMed  Google Scholar 

  40. Zhang D, Zheng H, Zhou Y, Tang X, Yu B et al (2007) Association of IL-1beta gene polymorphism with cachexia from locally advanced gastric cancer. BMC Cancer 7:45

    Article  PubMed Central  PubMed  Google Scholar 

  41. Kamangar F, Abnet CC, Hutchinson AA, Newschaffer CJ, Helzlsouer K et al (2006) Polymorphisms in inflammation-related genes and risk of gastric cancer (Finland). Cancer Causes Control 17:117–125

    Article  PubMed  Google Scholar 

  42. Kim N, Cho SI, Yim JY, Kim JM, Lee DH et al (2006) The effects of genetic polymorphisms of IL-1 and TNF-A on Helicobacter pylori-induced gastroduodenal diseases in Korea. Helicobacter 11:105–112

    Article  CAS  PubMed  Google Scholar 

  43. Shirai K, Ohmiya N, Taguchi A, Mabuchi N, Yatsuya H et al (2006) Interleukin-8 gene polymorphism associated with susceptibility to non-cardia gastric carcinoma with microsatellite instability. J Gastroenterol Hepatol 21:1129–1135

    Article  CAS  PubMed  Google Scholar 

  44. Ikehara SK, Ikehara Y, Matsuo K, Hirose K, Niwa T et al (2006) A polymorphism of C-to-T substitution at -31 IL1B is associated with the risk of advanced gastric adenocarcinoma in a Japanese population. J Hum Genet 51:927–933

    Article  CAS  PubMed  Google Scholar 

  45. Morgan DR, Dominguez RL, Keku TO, Heidt PE, Martin CF et al (2006) Gastric cancer and the high combination prevalence of host cytokine genotypes and Helicobacter pylori in Honduras. Clin Gastroenterol Hepatol 4:1103–1111

    Article  CAS  PubMed  Google Scholar 

  46. Alpizar-Alpizar W, Perez-Perez GI, Une C, Cuenca P, Sierra R (2005) Association of interleukin-1B and interleukin-1RN polymorphisms with gastric cancer in a high-risk population of Costa Rica. Clin Exp Med 5:169–176

    Article  CAS  PubMed  Google Scholar 

  47. Lu W, Pan K, Zhang L, Lin D, Miao X et al (2005) Genetic polymorphisms of interleukin (IL)-1B, IL-1RN, IL-8, IL-10 and tumor necrosis factor alpha and risk of gastric cancer in a Chinese population. Carcinogenesis 26:631–636

    Article  CAS  PubMed  Google Scholar 

  48. Taguchi A, Ohmiya N, Shirai K, Mabuchi N, Itoh A et al (2005) Interleukin-8 promoter polymorphism increases the risk of atrophic gastritis and gastric cancer in Japan. Cancer Epidemiol Biomark Prev 14:2487–2493

    Article  CAS  Google Scholar 

  49. Muramatsu A, Azuma T, Okuda T, Satomi S, Ohtani M et al (2005) Association between interleukin-1beta-511 C/T polymorphism and reflux esophagitis in Japan. J Gastroenterol 40:873–877

    Article  CAS  PubMed  Google Scholar 

  50. Sakuma K, Uozaki H, Chong JM, Hironaka M, Sudo M et al (2005) Cancer risk to the gastric corpus in Japanese, its correlation with interleukin-1beta gene polymorphism (+3953*T) and Epstein-Barr virus infection. Int J Cancer 115:93–97

    Article  CAS  PubMed  Google Scholar 

  51. Chang YW, Jang JY, Kim NH, Lee JW, Lee HJ et al (2005) Interleukin-1B (IL-1B) polymorphisms and gastric mucosal levels of IL-1beta cytokine in Korean patients with gastric cancer. Int J Cancer 114:465–471

    Article  CAS  PubMed  Google Scholar 

  52. Ruzzo A, Graziano F, Pizzagalli F, Santini D, Battistelli V et al (2005) Interleukin 1B gene (IL-1B) and interleukin 1 receptor antagonist gene (IL-1RN) polymorphisms in Helicobacter pylori-negative gastric cancer of intestinal and diffuse histotype. Ann Oncol 16:887–892

    Article  CAS  PubMed  Google Scholar 

  53. Zhang WH, Wang XL, Zhou J, An LZ, Xie XD (2005) Association of interleukin-1B (IL-1B) gene polymorphisms with risk of gastric cancer in Chinese population. Cytokine 30:378–381

    Article  CAS  PubMed  Google Scholar 

  54. Yang J, Hu Z, Xu Y, Shen J, Niu J et al (2004) Interleukin-1B gene promoter variants are associated with an increased risk of gastric cancer in a Chinese population. Cancer Lett 215:191–198

    Article  CAS  PubMed  Google Scholar 

  55. Lee KA, Ki CS, Kim HJ, Sohn KM, Kim JW et al (2004) Novel interleukin 1beta polymorphism increased the risk of gastric cancer in a Korean population. J Gastroenterol 39:429–433

    Article  CAS  PubMed  Google Scholar 

  56. Glas J, Torok HP, Schneider A, Brunnler G, Kopp R et al (2004) Allele 2 of the interleukin-1 receptor antagonist gene is associated with early gastric cancer. J Clin Oncol 22:4746–4752

    Article  CAS  PubMed  Google Scholar 

  57. Chen A, Li CN, Hsu PI, Lai KH, Tseng HH et al (2004) Risks of interleukin-1 genetic polymorphisms and Helicobacter pylori infection in the development of gastric cancer. Aliment Pharmacol Ther 20:203–211

    Article  PubMed  Google Scholar 

  58. Kang WK, Park WS, Chin HM, Park CH (2004) The role of interleukin-1beta gene polymorphism in the gastric carcinogenesis. Korean J Gastroenterol 44:25–33

    CAS  PubMed  Google Scholar 

  59. Hartland S, Newton JL, Griffin SM, Donaldson PT (2004) A functional polymorphism in the interleukin-1 receptor-1 gene is associated with increased risk of Helicobacter pylori infection but not with gastric cancer. Dig Dis Sci 49:1545–1550

    Article  CAS  PubMed  Google Scholar 

  60. Gatti LL, Burbano RR, de Assumpcao PP, Smith Mde A, Payao SL (2004) Interleukin-1beta polymorphisms, Helicobacter pylori infection in individuals from Northern Brazil with gastric adenocarcinoma. Clin Exp Med 4:93–98

    Article  PubMed  Google Scholar 

  61. Wu MS, Chen LT, Shun CT, Huang SP, Chiu HM et al (2004) Promoter polymorphisms of tumor necrosis factor-alpha are associated with risk of gastric mucosa-associated lymphoid tissue lymphoma. Int J Cancer 110:695–700

    Article  CAS  PubMed  Google Scholar 

  62. Machado JC, Figueiredo C, Canedo P, Pharoah P, Carvalho R et al (2003) A proinflammatory genetic profile increases the risk for chronic atrophic gastritis and gastric carcinoma. Gastroenterology 125:364–371

    Article  CAS  PubMed  Google Scholar 

  63. El-Omar EM, Rabkin CS, Gammon MD, Vaughan TL, Risch HA et al (2003) Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124:1193–1201

    Article  CAS  PubMed  Google Scholar 

  64. Wu MS, Wu CY, Chen CJ, Lin MT, Shun CT et al (2003) Interleukin-10 genotypes associate with the risk of gastric carcinoma in Taiwanese Chinese. Int J Cancer 104:617–623

    Article  CAS  PubMed  Google Scholar 

  65. zur Hausen A, Crusius JB, Murillo LS, Alizadeh BZ, Morre SA et al (2003) IL-1B promoter polymorphism and Epstein-Barr virus in Dutch patients with gastric carcinoma. Int J Cancer 107:866–867

    Article  CAS  PubMed  Google Scholar 

  66. Machado JC, Pharoah P, Sousa S, Carvalho R, Oliveira C et al (2001) Interleukin 1B and interleukin 1RN polymorphisms are associated with increased risk of gastric carcinoma. Gastroenterology 121:823–829

    Article  CAS  PubMed  Google Scholar 

  67. Johnson LR, Guthrie PD (1976) Stimulation of DNA synthesis by big and little gastrin (G-34 and G-17). Gastroenterology 71:599–602

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sungsoo Park.

Additional information

Min-Jeong Park and Myung-Han Hyun contributed equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, MJ., Hyun, MH., Yang, JP. et al. Effects of the interleukin-1β-511 C/T gene polymorphism on the risk of gastric cancer in the context of the relationship between race and H. pylori infection: a meta-analysis of 20,000 subjects. Mol Biol Rep 42, 119–134 (2015). https://doi.org/10.1007/s11033-014-3748-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-014-3748-7

Keywords

Navigation