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08.05.2018 | Original Article

The ratios of pro-inflammatory to anti-inflammatory cytokines in the serum of chronic periodontitis patients with and without type 2 diabetes and/or smoking habit

verfasst von: Tamires Szeremeske Miranda, Sílvia Lacerda Heluy, Daniele Ferreira Cruz, Hélio Doyle Pereira da Silva, Magda Feres, Luciene Cristina Figueiredo, Poliana Mendes Duarte

Erschienen in: Clinical Oral Investigations | Ausgabe 2/2019

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Abstract

Objective

This study assessed the impact of chronic periodontitis (CP) and CP associated with type 2 diabetes mellitus (DM) and/or smoking on the serum ratios of pro- to anti-inflammatory cytokines.

Materials and methods

Subjects were assigned into one of the following groups: control (n = 25, non-diabetic non-smokers with no history of periodontitis), CP (n = 26, non-diabetic non-smokers with CP), DMCP (n = 30, non-smokers with DM and CP), SCP (n = 27, non-diabetic smokers with CP), and SDMCP (n = 22, smokers with type 2 DM and CP). Serum levels of 18 cytokines were measured using multiplex immunoassays.

Results

Six ratios of pro-inflammatory to anti-inflammatory cytokines were significantly higher in the CP group than in the control group (p < 0.05). Eleven, seventeen and nine ratios of pro-inflammatory to anti-inflammatory cytokines were significantly higher in the DMCP, SCP and SDMCP groups than in the control group, respectively (p < 0.05). The SCP group presented higher serum ratios of tumor necrosis factor (TNF)-α/interleukin (IL)-4, TNF-α/IL-5, IL-17/IL-13 and IL-6/IL-13 (p < 0.05) than the CP group. Cluster analysis revealed a relevant cluster composed of ten cytokines (IL-17, IL-23, interferon-γ, IL-12, IL-1β, IL-2, IL-21, IL-6, IL-4 and granulocyte-macrophage colony-stimulating factor [GM-CSF]) in the serum of subjects from the DMCP group.

Conclusions

The ratios of pro- to anti-inflammatory cytokines shift to favor a pro-inflammatory status in the serum of patients with CP and even more when CP is associated with one or both risk factors.

Clinical relevance

CP and CP associated with hyperglycemia and/or smoking might contribute to a systemic inflammatory burden and increased risk of systemic complications.

Dinarello CA (2007) Historical insights into cytokines. Eur J Immunol 37(Suppl 1):S34–S45CrossRef

Fietta P, Costa E, Delsante G (2015) Interleukins (ILs), a fascinating family of cytokines. Part II: ILs from IL-20 to IL-38. Theor Biol Forum 108(1–2):19–40PubMed

Monastero RN, Pentyala S (2017) Cytokines as biomarkers and their respective clinical cutoff levels. Int J Inflam; 2017: 4309485. doi: https://doi.org/10.1155/2017/4309485, 1, 11.

Garlet GP (2010) Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J Dent Res 89(12):1349–1363. https://doi.org/10.1177/0022034510376402CrossRefPubMed

Gonzales JR (2015) T- and B-cell subsets in periodontitis. Periodontol 2000; 69(1):181–200. doi: https://doi.org/10.1111/prd.12090.

Stadler AF, Angst PD, Arce RM, Gomes SC, Oppermann RV, Susin C (2016) Gingival crevicular fluid levels of cytokines/chemokines in chronic periodontitis: a meta-analysis. J Clin Periodontol 43(9):727–745. https://doi.org/10.1111/jcpe.12557CrossRefPubMed

Albandar JM (2002) Global risk factors and risk indicators for periodontal diseases. Periodontol 2000; 29:177–206.

Tymkiw KD, Thunell DH, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, Brogden KA, Guthmiller JM (2011) Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 38(3):219–228. https://doi.org/10.1111/j.1600-051X.2010.01684.xCrossRefPubMed

Johannsen A, Susin C, Gustafsson A (2014) Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 2000; 64(1):111–26. doi: https://doi.org/10.1111/j.1600-0757.2012.00456.x.

10.

Sonnenschein SK, Meyle J (2015) Local inflammatory reactions in patients with diabetes and periodontitis. Periodontol 2000; 69(1):221–54. doi: https://doi.org/10.1111/prd.12089.

11.

Knight ET, Liu J, Seymour GJ, Faggion CM Jr, Cullinan MP (2016) Risk factors that may modify the innate and adaptive immune responses in periodontal diseases. Periodontol 2000; 71(1):22–51. doi: https://doi.org/10.1111/prd.12110.

12.

Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U (2000) Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol 71(10):1528–1534CrossRef

13.

Górska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madaliński K (2003) Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol 30(12):1046–1052CrossRef

14.

Nakajima T, Honda T, Domon H, Okui T, Kajita K, Ito H, Takahashi N, Maekawa T, Tabeta K, Yamazaki K (2010) Periodontitis-associated up-regulation of systemic inflammatory mediator level may increase the risk of coronary heart disease. J Periodontal Res 45(1):116–122. https://doi.org/10.1111/j.1600-0765.2009.01209.xCrossRefPubMed

15.

Duarte PM, da Rocha M, Sampaio E, Mestnik MJ, Feres M, Figueiredo LC, Bastos MF, Faveri M (2010) Serum levels of cytokines in subjects with generalized chronic and aggressive periodontitis before and after non-surgical periodontal therapy: a pilot study. J Periodontol 81(7):1056–1063. https://doi.org/10.1902/jop.2010.090732CrossRefPubMed

16.

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. https://doi.org/10.1111/j.1600-051X.2010.01602.xCrossRefPubMed

17.

Li G, Yue Y, Tian Y, Li JL, Wang M, Liang H, Liao P, Loo WT, Cheung MN, Chow LW (2012) Association of matrix metalloproteinase (MMP)-1, 3, 9, interleukin (IL)-2, 8 and cyclooxygenase (COX)-2 gene polymorphisms with chronic periodontitis in a Chinese population. Cytokine 60(2):552–560. https://doi.org/10.1016/j.cyto.2012.06.239CrossRefPubMed

18.

Gokul K, Faizuddin M, Pradeep AR (2012) Estimation of the level of tumor necrosis factor- α in gingival crevicular fluid and serum in periodontal health & disease: a biochemical study. Indian J Dent Res 23(3):348–352. https://doi.org/10.4103/0970-9290.102221CrossRefPubMed

19.

Gümüş P, Nizam N, Lappin DF, Buduneli N (2014) Saliva and serum levels of B-cell activating factors and tumor necrosis factor-α in patients with periodontitis. J Periodontol 85(2):270–280. https://doi.org/10.1902/jop.2013.130117CrossRefPubMed

20.

Napimoga MH, Nametala C, da Silva FL, Miranda TS, Bossonaro JP, Demasi AP, Duarte PM (2014) Involvement of the Wnt-β-catenin signalling antagonists, sclerostin and dickkopf-related protein 1, in chronic periodontitis. J Clin Periodontol 41(6):550–557. https://doi.org/10.1111/jcpe.12245CrossRefPubMed

21.

Keles ZP, Keles GC, Avci B, Cetinkaya BO, Emingil G (2014) Analysis of YKL-40 acute-phase protein and interleukin-6 levels in periodontal disease. J Periodontol 85(9):1240–1246. https://doi.org/10.1902/jop.2014.130631CrossRefPubMed

22.

Chen XT, Tan JY, Lei LH, Chen LL (2015) Cytokine levels in plasma and gingival crevicular fluid in chronic periodontitis. Am J Dent 28(1):9–12PubMed

23.

Ikezawa-Suzuki I, Shimada Y, Tai H, Komatsu Y, Tanaka A, Yoshie H (2008) Effects of treatment on soluble tumour necrosis factor receptor type 1 and 2 in chronic periodontitis. J Clin Periodontol 35(11):961–968. https://doi.org/10.1111/j.1600-051X.2008.01317.xCrossRefPubMed

24.

Dağ A, Firat ET, Arikan S, Kadiroğlu AK, Kaplan A (2009) The effect of periodontal therapy on serum TNF-alpha and HbA1c levels in type 2 diabetic patients. Aust Dent J 54(1):17–22. https://doi.org/10.1111/j.1834-7819.2008.01083.xCrossRefPubMed

25.

Longo PL, Artese HP, Rabelo MS, Kawamoto D, Foz AM, Romito GA, Dib SA, Mayer MP (2014) Serum levels of inflammatory markers in type 2 diabetes patients with chronic periodontitis. J Appl Oral Sci 22(2):103–108CrossRef

26.

Acharya AB, Thakur S, Muddapur MV (2015) Evaluation of serum interleukin-10 levels as a predictor of glycemic alteration in chronic periodontitis and type 2 diabetes mellitus. J Indian Soc Periodontol 19(4):388–392. https://doi.org/10.4103/0972-124X.150876CrossRefPubMedPubMedCentral

27.

Acharya AB, Thakur S, Muddapur MV, Kulkarni RD (2017) Cytokine ratios in chronic periodontitis and type 2 diabetes mellitus. Diabetes Metab Syndr 11(4):277–278. https://doi.org/10.1016/j.dsx.2016.12.007CrossRefPubMed

28.

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

29.

Araujo MW, Hovey KM, Benedek JR, Grossi SG, Dorn J, Wactawski-Wende J, Genco RJ, Trevisan M (2003) Reproducibility of probing depth measurement using a constant-force electronic probe: analysis of inter- and intraexaminer variability. J Periodontol 74:1736–1740CrossRef

30.

Paludan SR (1998) Interleukin-4 and interferon-gamma: the quintessence of a mutual antagonistic relationship. Scand J Immunol 48(5):459–468CrossRef

31.

Ikezawa I, Tai H, Shimada Y, Komatsu Y, Galicia JC, Yoshie H (2005) Imbalance between soluble tumour necrosis factor receptors type 1 and 2 in chronic periodontitis. J Clin Periodontol 32(10):1047–1054CrossRef

32.

Yamazaki K, Honda T, Oda T, Ueki-Maruyama K, Nakajima T, Yoshie H, Seymour GJ (2005) Effect of periodontal treatment on the C-reactive protein and proinflammatory cytokine levels in Japanese periodontitis patients. J Periodontal Res 40(1):53–58CrossRef

33.

Shimada Y, Komatsu Y, Ikezawa-Suzuki I, Tai H, Sugita N, Yoshie H (2010) The effect of periodontal treatment on serum leptin, interleukin-6, and C-reactive protein. J Periodontol 81(8):1118–1123. https://doi.org/10.1902/jop.2010.090741CrossRefPubMed

34.

Ozçaka O, Nalbantsoy A, Buduneli N (2011) Interleukin-17 and interleukin-18 levels in saliva and plasma of patients with chronic periodontitis. J Periodontal Res 46(5):592–598. https://doi.org/10.1111/j.1600-0765.2011.01377.x.CrossRefPubMed

35.

Becerik S, Öztürk VÖ, Atmaca H, Atilla G, Emingil G (2012) Gingival crevicular fluid and plasma acute-phase cytokine levels in different periodontal diseases. J Periodontol 83(10):1304–1313CrossRef

36.

Zimmermann GS, Bastos MF, Dias Gonçalves TE, Chambrone L, Duarte PM (2013) Local and circulating levels of adipocytokines in obese and normal weight individuals with chronic periodontitis. J Periodontol 84(5):624–633. https://doi.org/10.1902/jop.2012.120254CrossRefPubMed

37.

Cetinkaya B, Guzeldemir E, Ogus E, Bulut S (2013) Proinflammatory and anti-inflammatory cytokines in gingival crevicular fluid and serum of patients with rheumatoid arthritis and patients with chronic periodontitis. J Periodontol 84(1):84–93. https://doi.org/10.1902/jop.2012.110467CrossRefPubMed

38.

Boström EA, Kindstedt E, Sulniute R, Palmqvist P, Majster M, Holm CK, Zwicker S, Clark R, Önell S, Johansson I, Lerner UH, Lundberg P (2015) Increased eotaxin and MCP-1 levels in serum from individuals with periodontitis and in human gingival fibroblasts exposed to pro-inflammatory cytokines. PLoS One 10(8):e0134608. https://doi.org/10.1371/journal.pone.0134608CrossRefPubMedPubMedCentral

39.

Al-Shukaili A, Al-Ghafri S, Al-Marhoobi S, Al-Abri S, Al-Lawati J, Al-Maskari M (2013) Analysis of inflammatory mediators in type 2 diabetes patients. Int J Endocrinol 2013:976810. doi: https://doi.org/10.1155/2013/976810, 1, 7.

40.

Zhang C, Xiao C, Wang P, Xu W, Zhang A, Li Q, Xu X (2014) The alteration of Th1/Th2/Th17/Treg paradigm in patients with type 2 diabetes mellitus: relationship with diabetic nephropathy. Hum Immunol 75(4):289–296. https://doi.org/10.1016/j.humimm.2014.02.007CrossRefPubMed

41.

Madhumitha H, Mohan V, Deepa M, Babu S, Aravindhan V (2014) Increased Th1 and suppressed Th2 serum cytokine levels in subjects with diabetic coronary artery disease. Cardiovasc Diabetol 13(1):1. https://doi.org/10.1186/1475-2840-13-1CrossRefPubMedPubMedCentral

42.

Roohi A, Tabrizi M, Abbasi F, Ataie-Jafari A, Nikbin B, Larijani B, Qorbani M, Meysamie A, Asgarian-Omran H, Nikmanesh B, Bajouri A, Shafiey N, Maleki A (2014) Serum IL-17, IL-23, and TGF-β levels in type 1 and type 2 diabetic patients and age-matched healthy controls. Biomed Res Int 2014:718946. doi: https://doi.org/10.1155/2014/718946, 1, 7.

43.

Gupta S, Maratha A, Siednienko J, Natarajan A, Gajanayake T, Hoashi S, Miggin S (2017) Analysis of inflammatory cytokine and TLR expression levels in type 2 diabetes with complications. Sci Rep 7(1):7633. https://doi.org/10.1038/s41598-017-07230-8CrossRefPubMedPubMedCentral

44.

Daloee MH, Avan A, Mirhafez SR, Kavousi E, Hasanian-Mehr M, Darroudi S, Tajfard M, Tayefi M, Qazizade H, Mohammadi A, Ferydouni N, Ebrahimi M, Ghayour-Mobarhan M (2017) Impact of cigarette smoking on serum pro- and anti-inflammatory cytokines and growth factors. Am J Mens Health 11(4):1169–1173. https://doi.org/10.1177/1557988315601724CrossRefPubMed

45.

Petrescu F, Voican SC, Silosi I (2010) Tumor necrosis factor-alpha serum levels in healthy smokers and nonsmokers. Int J Chron Obstruct Pulmon Dis 5:217–222PubMedPubMedCentral

46.

Nadeem A, Javaid K, Sami W, Zafar A, Jahan S, Zaman S, Nagi A (2013) Inverse relationship of serum IL-17 with type-II diabetes retinopathy. Clin Lab 59(11–12):1311–1317PubMed

47.

Maddur MS, Miossec P, Kaveri SV, Bayry J (2012) Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 181(1):8–18. https://doi.org/10.1016/j.ajpath.2012.03.044CrossRefPubMed

48.

Tahmasebinia F, Pourgholaminejad A (2017) The role of Th17 cells in auto-inflammatory neurological disorders. Prog Neuropsychopharmacol Biol Psychiatry 79(Pt B):408–416. https://doi.org/10.1016/j.pnpbp.2017.07.023CrossRefPubMed

49.

Barin JG, Talor MV, Schaub JA, Diny NL, Hou X, Hoyer M, Archer NK, Gebremariam ES, Davis MF, Miller LS, Rose NR, Čiháková D (2016) Collaborative interferon-γ and Interleukin-17 signaling protects the oral mucosa from Staphylococcus aureus. Am J Pathol 186(9):2337–2352. https://doi.org/10.1016/j.ajpath.2016.07.001CrossRefPubMedPubMedCentral

50.

Veldhoen M (2017) Interleukin 17 is a chief orchestrator of immunity. Nat Immunol 18(6):612–621. https://doi.org/10.1038/ni.3742CrossRefPubMed

51.

Mills KH (2008) Induction, function and regulation of IL-17-producing T cells. Eur J Immunol 38(10):2636–2649. https://doi.org/10.1002/eji.200838535CrossRefPubMed

52.

Liao W, Lin JX, Leonard WJ (2011) IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr Opin Immunol 23(5):598–604. https://doi.org/10.1016/j.coi.2011.08.003CrossRefPubMedPubMedCentral

53.

Liao W, Lin JX, Leonard WJ (2013) Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 38(1):13–25. https://doi.org/10.1016/j.immuni.2013.01.004CrossRefPubMedPubMedCentral

54.

Churchman SM, Geiler J, Parmar R, Horner EA, Church LD, Emery P, Buch MH, McDermott MF, Ponchel F (2012) Multiplexing immunoassays for cytokine detection in the serum of patients with rheumatoid arthritis: lack of sensitivity and interferenceby rheumatoid factor. Clin Exp Rheumatol 30(4):534–542PubMed

Titel: The ratios of pro-inflammatory to anti-inflammatory cytokines in the serum of chronic periodontitis patients with and without type 2 diabetes and/or smoking habit
verfasst von: Tamires Szeremeske Miranda
Sílvia Lacerda Heluy
Daniele Ferreira Cruz
Hélio Doyle Pereira da Silva
Magda Feres
Luciene Cristina Figueiredo
Poliana Mendes Duarte
Publikationsdatum: 08.05.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Clinical Oral Investigations / Ausgabe 2/2019
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-018-2471-5

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The ratios of pro-inflammatory to anti-inflammatory cytokines in the serum of chronic periodontitis patients with and without type 2 diabetes and/or smoking habit

Abstract

Objective

Materials and methods

Results

Conclusions

Clinical relevance

Neu im Fachgebiet Zahnmedizin

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Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

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Abstract

Objective

Materials and methods

Results

Conclusions

Clinical relevance

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