Association of the IL-10 polymorphisms and periodontitis: a meta-analysis

Abstract

No clear consensus has been reached regarding the association of IL-10 polymorphisms and periodontitis. Therefore, we performed a meta-analysis of case–control studies and a systemic review in an effort to systematically summarize the existing knowledge. Studies were identified by searching PubMed database until December 2011. IL-10 −1082 (−1087) A>G, −819 (−824) C>T and −592 (−597) C>A polymorphisms were included in the present meta-analysis. We calculated the specific odds ratios along with their 95 % confidence intervals to compare the distribution of alleles and genotypes between cases and controls. An additive “per-allele” model (major allele vs. minor allele) was performed, and dominant and recessive models were also considered. The random-effects model was applied for the analysis. Cumulative analysis was also performed. Heterogeneity and publication bias were assessed. Nine case–control studies involving 841 periodontitis cases (644 chronic periodontitis and 197 aggressive periodontitis cases) and 748 controls were included. We found statistically significant association of IL-10 −819 (−824) C>T and IL-10 −592 (−597) C>A polymorphisms in Caucasians. The IL-10 −819 (−824) T and −592 (−597) A alleles may confer a relative increase in the risk for chronic periodontitis in Caucasians. Future studies may be important to reinforce these findings.

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

Fig. 1

References

  1. 1.

    Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820

    PubMed  Article  Google Scholar 

  2. 2.

    Papapanou RN, Lindhe J (2003) Epidemiology of periodontal diseases. In: Lindhe J, Karring T, Lang NP (eds) Clinical periodontology and implant dentistry, 4th edn. Blackwell, Oxford, pp 50–80

    Google Scholar 

  3. 3.

    Kinane DF, Hart TC (2003) Gene and gene polymorphisms associated with periodontal disease. Crit Rev Oral Biol Med 14:430–449

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    Van Dyke TE, Dave S (2005) Risk factors for periodontitis. J Int Acad Periodontol 7:3–7

    PubMed  Google Scholar 

  5. 5.

    Michalowicz BS, Diehl SR, Gunsolley JC, Sparks BS, Brooks CN, Koertge TE, Califano JV, Burmeister JA, Schenkein HA (2000) Evidence of a substantial genetic basis for risk of adult periodontitis. J Periodontol 71:1699–1707

    PubMed  Article  CAS  Google Scholar 

  6. 6.

    American Academy of Periodontology (1999) The pathogenesis of periodontal diseases (position paper). J Periodontol 70:457–470

    Article  Google Scholar 

  7. 7.

    Preshaw PM, Taylor JJ (2011) How has research into cytokine interactions and their role in driving immune responses impacted our understanding of periodontitis? J Clin Periodontol 38(Suppl 11):60–84

    PubMed  Article  Google Scholar 

  8. 8.

    Kinane DF, Shiba H, Hart TC (2005) The genetic basis of periodontitis. Periodontol 2000 39:91–117

    PubMed  Article  Google Scholar 

  9. 9.

    Tatakis DN, Kumar PS (2005) Etiology and pathogenesis of periodontal disease. Dent Clin North Am 49:491–516

    PubMed  Article  Google Scholar 

  10. 10.

    Kinane DF, Preshaw PM, Loos BG (2011) Host-response: understanding the cellular and molecular mechanisms of host-microbial interactions—consensus of the seventh European workshop of periodontology. J Clin Periodontol 38(Suppl 11):44–48

    PubMed  Article  Google Scholar 

  11. 11.

    Smith AJP, Humphries SE (2009) Cytokine and cytokine receptor gene polymorphisms and their functionality. Cytokine Growth Factor Rev 20:43–59

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Stabholz A, Soskolne WA, Shapira L (2010) Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000 53:138–153

    PubMed  Article  Google Scholar 

  13. 13.

    Yoshie H, Kobayashi T, Tai H, Galicia JC (2007) The role of genetic polymorphisms in periodontitis. Periodontology 2000 43:102–132

    PubMed  Article  Google Scholar 

  14. 14.

    Brett PM, Zygogianni P, Griffiths GS, Tomaz M, Parkar M, D’Aiuto F, Tonetti M (2005) Functional gene polymorphisms in aggressive and chronic periodontitis. J Dent Res 84:1149–1153

    PubMed  Article  CAS  Google Scholar 

  15. 15.

    Babel N, Cherepnev G, Babel D, Tropmann A, Hammer M, Volk H-D, Reinke P (2006) Analysis of tumor necrosis factor-α, transforming growth factor-β, interleukin-10, IL-6, and interferon-γ gene polymorphisms in patients with chronic periodontitis. J Periodontol 77:1978–1983

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Berglundh T, Donati M, Mahn-Zorii M, Hanson L-A, Padyukov L (2003) Association of the −1087 IL 10 gene polymorphism with severe chronic periodontitis in Swedish Caucasians. J Clin Periodontol 30:249–254

    PubMed  Article  Google Scholar 

  17. 17.

    Sumer AP, Kara N, Keles GC, Gunes S, Koprulu H, Bagci H (2007) Association of interleukin-10 gene polymorphisms with severe generalized chronic periodontitis. J Periodontol 78:493–497

    PubMed  Article  CAS  Google Scholar 

  18. 18.

    Scarel-Caminaga RM, Trevilatto PC, Souza AP, Brito RB, Camargo LEA, Line SRP (2004) Interleukin-10 gene promoter polymorphisms are associated with chronic periodontitis. J Clin Periodontol 31:443–448

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    Zhang K, Hei P, Deng L, Lin J (2007) Interleukin-10 gene promoter polymorphisms and their protein production in peritoneal fluid in patients with endometriosis. Mol Hum Reprod 13:135–140

    PubMed  Article  CAS  Google Scholar 

  20. 20.

    Ma SL, Tang NL, Lam LC, Chiu HF (2005) The association between promoter polymorphism of the interleukin-10 gene and Alzheimer’s disease. Neurobiol Aging 26:1005–1010

    PubMed  Article  CAS  Google Scholar 

  21. 21.

    Gaudreault N, Ducharme V, Lamontagne M, Guauque-Olarte S, Mathieu P, Pibarot P, Bossé Y (2011) Replication of genetic association studies in aortic stenosis in adults. Am J Cardiol 108(9):1305–1310

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Fowler EV, Eri R, Hume G, Johnstone S, Pandeya N, Lincoln D, Templeton D, Radford-Smith GL (2005) TNF alpha and IL10 SNPs act together to predict disease behavior in Crohn’s disease. J Med Genet 42:523–528

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Liu N, Lu H, Tao F, Guo T, Liu C, Cui B, Ning G (2011) An association of interleukin-10 gene polymorphisms with Graves’ disease in two Chinese populations. Endocrine 40(1):90–94

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Stanilova SA, Miteva LD, Karakolev ZT, Stefanov CS (2006) Interleukin-10-1082 promoter polymorphism in association with cytokine production and sepsis susceptibility. Intensive Care Med 32:260–266

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Trikalinos TA, Salanti G, Zintzaras E, Ioannidis JP (2008) Meta-analysis methods. Adv Genet 60:311–334

    PubMed  Article  Google Scholar 

  26. 26.

    Lohmueller KE, Pearce CL, Pike M, Lander ES, Hirschhorn JN (2003) Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat Genet 33(2):177–182

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    Nikolopoulos GK, Dimou NL, Hamodrakas SJ, Bagos PG (2008) Cytokine gene polymorphisms in periodontal disease: a meta-analysis of 53 studies including 4178 cases and 4590 controls. J Clin Periodontol 35:754–767

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Ozturk A, Vieira AR (2009) TLR4 as a risk factor for periodontal disease: a reappraisal. J Clin Periodontol 36:279–286

    PubMed  Article  CAS  Google Scholar 

  29. 29.

    Shao M, Huang P, Cheng R, Hu T (2009) Interleukin-6 polymorphisms modify the risk of periodontitis: a systematic review and meta-analysis. J Zhejiang Univ Sci B 10(12):920–927

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    Thakkinstian A, McElduff P, D’Este C, Duffy D, Attia J (2005) A method for meta-analysis of molecular association studies. Stat Med 24(9):1291–1306

    PubMed  Article  Google Scholar 

  31. 31.

    Cochran W (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129

    Article  Google Scholar 

  32. 32.

    Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analysis. BMJ 327(7414):557–560

    PubMed  Article  Google Scholar 

  33. 33.

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

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    PubMed  Article  CAS  Google Scholar 

  35. 35.

    Mellati E, Arab HR, Tavakkol-Afshari J, Ebadian AR, Radvar M (2007) Analysis of −1082 IL-10 gene polymorphism in Iranian patients with generalized aggressive periodontitis. Med Sci Monit 13(11):CR510–CR514

    PubMed  CAS  Google Scholar 

  36. 36.

    Claudino M, Trombone APF, Cardoso CR, Ferreira SB Jr, Martins W Jr, Assis GF, Santos CF, Trevilatto PC, Campanelli AP, Silva JS, Garlet GP (2008) The broad effects of the functional IL-10 promoter −592 polymorphism: modulation of IL-10, TIMP-3, and OPG expression and their association with periodontal disease outcome. J Leukoc Biol 84:1565–1573

    PubMed  Article  CAS  Google Scholar 

  37. 37.

    Reichert S, Machulla HKG, Klapproth J, Zimmermann U, Reichert Y, Gläser CH, Schaller HG, Stein J, Schulz S (2008) The interleukin-10 promoter haplotype ATA is a putative risk factor for aggressive periodontitis. J Periodontal Res 43:40–47

    PubMed  CAS  Google Scholar 

  38. 38.

    Hu K-F, Huang K-C, Ho Y-P, Lin Y-C, Ho K-Y, Wu Y-M, Yang Y-H, Tsai C-C (2009) Interleukin-10 (−592 C/A) and interleukin-12B (+16974 A/C) gene polymorphisms and the interleukin-10 ATA haplotype are associated with periodontitis in a Taiwanese population. J Periodontal Res 44:378–385

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Kinane DF, Hodge P, Eskdale J, Ellis R, Gallagher G (1999) Analysis of genetic polymorphisms at the interleukin-10 and tumour necrosis factor loci in early-onset periodontitis. J Periodontal Res 34(7):379–386

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Yamazaki K, Tabeta K, Nakajima T, Ohsawa Y, Ueki K, Itoh H, Yoshie H (2001) Interleukin-10 gene promoter polymorphism in Japanese patients with adult and early-onset periodontitis. J Clin Periodontol 28:828–832

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Gonzales JR, Michel J, Diete A, Herrmann JM, Bödeker RH, Meyle J (2002) Analysis of genetic polymorphisms at the interleukin-10 loci in aggressive and chronic periodontitis. J Clin Periodontol 29:816–822

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Loos BG, John RP, Laine ML (2005) Identification of genetic risk factors for periodontitis and possible mechanisms of action. J Clin Periodontol 32(Suppl. 6):159–179

    PubMed  Article  CAS  Google Scholar 

  43. 43.

    de Sá AR, Moreira PR, Xavier GM, Sampaio I, Kalapothakis E, Dutra WO, Gomez RS (2007) Association of CD14, IL1B, IL6, IL10 and TNFA functional gene polymorphisms with symptomatic dental abscesses. Int Endod J 40:563–572

    PubMed  Article  Google Scholar 

  44. 44.

    Savarrio L, Donati M, Carr C, Kinane DF, Berglundh T (2007) Interleukin-24, RANTES and CCR5 gene polymorphisms are not associated with chronic adult periodontitis. J Periodontal Res 42:152–158

    PubMed  Article  CAS  Google Scholar 

  45. 45.

    Cullinan MP, Westerman B, Hamlet SM, Palmer JE, Faddy MJ, Seymour GJ, Middleton PG, Taylor JJ (2008) Progression of periodontal disease and interleukin-10 gene polymorphism. J Periodontal Res 43:328–333

    PubMed  Article  CAS  Google Scholar 

  46. 46.

    Donati M, Liljenberg B, Padyukov L, Berglundh T (2008) Local expression of interleukin-10 and mCD14 in relation to the −1087 IL-10 and −159 CD14 gene polymorphisms in chronic periodontitis. J Periodontol 79:517–524

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    Erciyas K, Pehlivan S, Sever T, Igci M, Arslan A, Orbak R (2010) Association between TNF-α, TGF-β1, IL-10, IL-6 and IFN-γ gene polymorphisms and generalized aggressive periodontitis. Clin Invest Med 33(2):E85–E91

    PubMed  CAS  Google Scholar 

  48. 48.

    Haverkamp MH, Lindeboom JA, de Visser AW, Kremer D, Kuijpers TW, van de Vosse E, van Dissel JT (2010) Nontuberculous mycobacterial cervicofacial lymphadenitis in children from the multicenter, randomized, controlled trial in The Netherlands: relevance of polymorphisms in candidate host immunity genes. Int J Pediatr Otorhinolaryngol 74(7):752–754

    PubMed  Article  Google Scholar 

  49. 49.

    Passoja A, Puijola I, Knuuttila M, Niemelä O, Karttunen R, Raunio T, Tervonen T (2010) Serum levels of interleukin-10 and tumour necrosis factor-α in chronic periodontitis. J Clin Periodontol 37(10):881–887

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    Larsson L, Thorbert-Mros S, Rymo L, Berglungh T (2011) Interleukin-10 (Il-10) genotypes of the −1087 single nucleotide polymorphism influence Sp1 expression in periodontitis lesions. J Periodontol. doi:10.1902/jop.2011.100623

  51. 51.

    Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4(1):1–6

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Crawley E, Kay R, Sillibourne J, Patel P, Hutchinson I, Woo P (1999) Polymorphic haplotypes of the interleukin-10 5′ flanking region determine variable interleukin-10 transcription and are associated with particular phenotypes of juvenile rheumatoid arthritis. Arthritis Rheum 42:1101–1108

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    Hirose M, Ishihara K, Saito A, Nakagawa T, Yamada S, Okuda K (2001) Expression of cytokines and inducible nitric oxide synthase in inflamed gingival tissue. J Periodontol 72(5):590–597

    PubMed  Article  CAS  Google Scholar 

  54. 54.

    Suárez LJ, Ocampo AM, Dueñas RE, Rodríguez A (2004) Relative proportions of T-cell subpopulations and cytokines that mediate and regulate the adaptative immune response in patients with aggressive periodontitis. J Periodontol 75(9):1209–1215

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

This work was partially supported by the PhD grant SFRH/BD/44490/2008 of the Science and Technology Foundation (FCT) from Portugal.

Author information

Affiliations

Authors

Corresponding author

Correspondence to C. M. Albuquerque.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Albuquerque, C.M., Cortinhas, A.J., Morinha, F.J. et al. Association of the IL-10 polymorphisms and periodontitis: a meta-analysis. Mol Biol Rep 39, 9319–9329 (2012). https://doi.org/10.1007/s11033-012-1738-1

Download citation

Keywords

  • Interleukin-10
  • Meta-analysis
  • Periodontitis
  • Polymorphism