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Evaluation of adipokines and inflammatory mediator expression levels in patients with periodontitis and peri-implantitis: a cross-sectional study

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Abstract

Objectives

The aim of this study was to analyze the mRNA and protein expression of adiponectin, leptin, visfatin, tumor necrosis factor (TNF)-α, and interleukin (IL)-6 levels in periodontitis and peri-implantitis sites in systemically healthy individuals and to investigate the influence of the presence of current periodontitis on their expression levels in peri-implantitis sites.

Materials and methods

Soft tissue biopsy samples were collected from 60 systemically healthy patients [15 periodontally healthy patients (group I), 16 patients with periodontitis (group II), 15 patients with peri-implantitis (group III), and 14 patients with peri-implantitis and periodontitis (group IV)]; mRNA expression levels of adiponectin, leptin, visfatin, TNF-α, and IL-6 were measured by quantitative real-time PCR; and their protein levels were assessed by immunohistochemistry.

Results

The mRNA expression levels of all biomarkers were significantly higher for group II compared to group I, while significantly higher levels of leptin, TNF-α, and IL-6 were observed in group III in comparison with group I. Group II exhibited significantly higher mRNA expression of adiponectin and TNF-α than group III. Group IV showed significantly higher expression levels of adiponectin, leptin, TNF-α, and IL-6 compared to group III. Regarding the expression of protein levels, which was estimated through quantification of the histoscore, both groups II and III presented higher H-scores than group I for all biomarkers except leptin.

Conclusions

The presence of current periodontitis may enhance expression levels of adiponectin, leptin, TNF-α, and IL-6 in peri-implant soft tissue.

Clinical relevance

The presence of periodontitis is an important risk factor for the severity of peri-implant inflammation as well as the onset of peri-implantitis.

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References

  1. Papapanou PN, Sanz M, Buduneli N et al (2018) Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 89:173–182

    Google Scholar 

  2. Berglundh T, Armitage G, Araujo MG et al (2018) Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 45:286–291

    Google Scholar 

  3. Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C (1992) Experimental breakdown of peri-implant and periodontal tissues: a study in the beagle dog. Clin Oral Implants Res 3:9–16

    PubMed  Google Scholar 

  4. Heitz-Mayfield LJ, Lang NP (2010) Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontol 2000 53:167–181

    PubMed  Google Scholar 

  5. Carcuac O, Berglundh T (2014) Composition of human peri-implantitis and periodontitis lesions. J Dent Res 93:1083–1088

    PubMed  PubMed Central  Google Scholar 

  6. Becker ST, Beck-Broichsitter BE, Graetz C, Dörfer CE, Wiltfang J, Häsler R (2014) Peri-implantitis versus periodontitis: functional differences indicated by transcriptome profiling. Clin Implant Dent Relat Res 16:401–411

    PubMed  Google Scholar 

  7. Salvi GE, Cosgarea R, Sculean A (2017) Prevalence and mechanisms of peri-implant diseases. J Dent Res 96:31–37

    PubMed  Google Scholar 

  8. Takamori Y, Atsuta I, Nakamura H, Sawase T, Koyano K, Hara Y (2017) Histopathological comparison of the onset of peri-implantitis and periodontitis in rats. Clin Oral Implants Res 28:163–170

    PubMed  Google Scholar 

  9. Yu X, Hu Y, Freire M, Yu P, Kawai T, Han X (2018) Role of toll-like receptor 2 in inflammation and alveolar bone loss in experimental peri-implantitis versus periodontitis. J Periodontal Res 53:98–106

    PubMed  Google Scholar 

  10. Berglundh T, Zitzmann NU, Donati M (2011) Are peri-implantitis lesions different from periodontitis lesions? J Clin Periodontol 38:188–202

    PubMed  Google Scholar 

  11. Cho-Yan Lee J, Mattheos N, Nixon KC, Ivanovski S (2012) Residual periodontal pockets are a risk indicator for peri-implantitis in patients treated for periodontitis. Clin Oral Implants Res 23:325–333

    PubMed  Google Scholar 

  12. Sgolastra F, Petrucci A, Severino M, Gatto R, Monaco A (2015) Periodontitis, implant loss and peri-implantitis. A meta-analysis. Clin Oral Implants Res 26:e8–e16

    PubMed  Google Scholar 

  13. Wang R, Zhao W, Tang ZH, Jin LJ, Cao CF (2014) Peri-implant conditions and their relationship with periodontal conditions in Chinese patients: a cross-sectional study. Clin Oral Implants Res 25:372–377

    PubMed  Google Scholar 

  14. Ferreira SD, Martins CC, Amaral SA, Vieira TR, Albuquerque BN, Cota LOM, Esteves Lima RP, Costa FO (2018) Periodontitis as a risk factor for peri-implantitis: systematic review and meta-analysis of observational studies. J Dent 79:1–10

    PubMed  Google Scholar 

  15. Isler SC, Uraz A, Kaymaz O, Cetiner D (2019) An evaluation of the relationship between peri-implant soft tissue biotype and the severity of peri-implantitis: a cross-sectional study. Int J Oral Maxillofac Implants 34:187–196

    PubMed  Google Scholar 

  16. Arunyanak SP, Sophon N, Tangsathian T, Supanimitkul K, Suwanwichit T, Kungsadalpipob K (2019) The effect of factors related to periodontal status toward peri-implantitis. Clin Oral Implants Res 30:791–799

    PubMed  Google Scholar 

  17. Teixeira MK, Lira-Junior R, Lourenço EJV et al (2020) The modulation of the TREM-1/PGLYRP1/MMP-8 axis in peri-implant diseases. Clin Oral Investig 24:1837–1844

    PubMed  Google Scholar 

  18. Zhu J, Guo B, Gan X, Zhang L, He Y, Liu B, Chen X, Zhang S, Yu H (2017) Association of circulating leptin and adiponectin with periodontitis: a systematic review and meta-analysis. BMC Oral Health 17:104

    PubMed  PubMed Central  Google Scholar 

  19. Su Y, Wang D, Xuan D, Ni J, Luo S, Xie B, Zhang J (2013) Periodontitis as a novel contributor of adipose tissue inflammation promotes insulin resistance in a rat model. J Periodontol 84:1617–1626

    PubMed  Google Scholar 

  20. Özcan E, Saygun NI, Ilıkçı R, Karslıoğlu Y, Muşabak U, Yeşillik S (2018) Evaluation of chemerin and its receptors, ChemR23 and CCRL2, in gingival tissues with healthy and periodontitis. Odontology 106:29–36

    PubMed  Google Scholar 

  21. Ghallab NA, Amr EM, Shaker OG (2015) Expression of leptin and visfatin in gingival tissues of chronic periodontitis with and without type 2 diabetes mellitus: a study using enzyme-linked immunosorbent assay and real-time polymerase chain reaction. J Periodontol 86:882–889

    PubMed  Google Scholar 

  22. Özcan E, Saygun NI, Ilıkçı R, Karslıoğlu Y, Muşabak U, Yeşillik S (2017) Increased visfatin expression is associated with nuclear factor-kappa B and phosphatidylinositol 3-kinase in periodontal inflammation. Clin Oral Investig 21:1113–1121

    PubMed  Google Scholar 

  23. Kanoriya D, Pradeep AR, Mallika A, Singhal S, Garg V (2017) Correlation of crevicular fluid and serum levels of retinol-binding protein 4 and leptin in chronic periodontitis and obesity. Clin Oral Investig 21:2319–2325

    PubMed  Google Scholar 

  24. Thanakun S, Izumi Y (2016) Effect of periodontitis on adiponectin, C-reactive protein, and immunoglobulin G against Porphyromonas gingivalis in Thai people with overweight or obese status. J Periodontol 87:566–576

    PubMed  Google Scholar 

  25. Recker EN, Avila-Ortiz G, Fischer CL, Pagan-Rivera K, Brogden KA, Dawson DV, Elangovan S (2015) A cross-sectional assessment of biomarker levels around implants versus natural teeth in periodontal maintenance patients. J Periodontol 86:264–272

    PubMed  Google Scholar 

  26. Teles FR, Teles RP, Martin L, Socransky SS, Haffajee AD (2012) Relationships among interleukin-6, tumor necrosis factor-α, adipokines, vitamin D, and chronic periodontitis. J Periodontol 83:1183–1191

    PubMed  Google Scholar 

  27. Consultation WHOE (2004) Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363:157–163

    Google Scholar 

  28. Silness J, Löe H (1964) Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135

    PubMed  Google Scholar 

  29. Löe H, Silness J (1963) Periodontal disease in pregnancy I. Prevalence and severity. Acta Odontol Scand 21:533–551

    PubMed  Google Scholar 

  30. Monje A, Wang HL, Nart J (2017) Association of preventive maintenance therapy compliance and peri-implant diseases: a cross-sectional study. J Periodontol 88:1030–1041

    PubMed  Google Scholar 

  31. Mardegan GP, Shibli JA, Roth LA, Faveri M, Giro G, Bastos MF (2017) Transforming growth factor-β, interleukin-17, and IL-23 gene expression profiles associated with human peri-implantitis. Clin Oral Implants Res 28:e10–e15

    PubMed  Google Scholar 

  32. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45

    PubMed  PubMed Central  Google Scholar 

  33. Hamzaoui K, Houman H, Ben Dhifallah I, Kamoun M, Hamzaoui A (2008) Serum BAFF levels and skin mRNA expression in patients with Behçet’s disease. Clin Exp Rheumatol 26:S64–S71

    PubMed  Google Scholar 

  34. Qi S, Zhao X, Li M, Zhang X, Lu Z, Yang C, Zhang C, Zhang H, Zhang N (2015) Aberrant expression of Notch1/numb/snail signaling, an epithelial mesenchymal transition related pathway, in adenomyosis. Reprod Biol Endocrinol 13:96

    PubMed  PubMed Central  Google Scholar 

  35. Tian W, Zhu Y, Wang Y, Teng F, Zhang H, Liu G, Ma X, Sun D, Rohan T, Xue F (2013) Visfatin, a potential biomarker and prognostic factor for endometrial cancer. Gynecol Oncol 129:505–512

    PubMed  Google Scholar 

  36. Pradeep AR, Raghavendra NM, Prasad MR, Kathariya R, Patel SP, Sharma A (2011) Gingival crevicular fluid and serum visfatin concentration: their relationship in periodontal health and disease. J Periodontol 82:1314–1319

    PubMed  Google Scholar 

  37. Özcan E, Saygun NI, Serdar MA, Kurt N (2015) Evaluation of the salivary levels of visfatin, chemerin, and progranulin in periodontal inflammation. Clin Oral Investig 19:921–928

    PubMed  Google Scholar 

  38. Le Sage F, Meilhac O, Gonthier MP (2017) Porphyromonas gingivalis lipopolysaccharide induces pro-inflammatory adipokine secretion and oxidative stress by regulating Toll-like receptor-mediated signaling pathways and redox enzymes in adipocytes. Mol Cell Endocrinol 446:102–110

    PubMed  Google Scholar 

  39. Nogueira AV, Nokhbehsaim M, Eick S et al (2014) Regulation of visfatin by microbial and biomechanical signals in PDL cells. Clin Oral Investig 18:171–178

    PubMed  Google Scholar 

  40. Yamaguchi N, Kukita T, Li YJ, Martinez Argueta JG, Saito T, Hanazawa S, Yamashita Y (2007) Adiponectin inhibits osteoclast formation stimulated by lipopolysaccharide from Actinobacillus actinomycetemcomitans. FEMS Immunol Med Microbiol 49:28–34

    PubMed  Google Scholar 

  41. Furugen R, Hayashida H, Yamaguchi N, Yoshihara A, Ogawa H, Miyazaki H, Saito T (2008) The relationship between periodontal condition and serum levels of resistin and adiponectin in elderly Japanese. J Periodontal Res 43:556–562

    PubMed  Google Scholar 

  42. Wohlfahrt JC, Aass AM, Granfeldt F, Lyngstadaas SP, Reseland JE (2014) Sulcus fluid bone marker levels and the outcome of surgical treatment of peri-implantitis. J Clin Periodontol 41:424–431

    PubMed  Google Scholar 

  43. Chen X, Lu J, Bao J, Guo J, Shi J, Wang Y (2013) Adiponectin: a biomarker for rheumatoid arthritis? Cytokine Growth Factor Rev 24:83–89

    PubMed  Google Scholar 

  44. Deschner J, Eick S, Damanaki A, Nokhbehsaim M (2014) The role of adipokines in periodontal infection and healing. Mol Oral Microbiol 29:258–269

    PubMed  Google Scholar 

  45. Ay ZY, Kırzıoğlu FY, Tonguç MÖ, Sütçü R, Kapucuoğlu N (2012) The gingiva contains leptin and leptin receptor in health and disease. Odontology 100:222–231

    PubMed  Google Scholar 

  46. Damanaki A, Nokhbehsaim M, Eick S et al (2014) Regulation of NAMPT in human gingival fibroblasts and biopsies. Mediat Inflamm 2014:912821

    Google Scholar 

  47. Ghassib I, Chen Z, Zhu J, Wang HL (2019) Use of IL-1 β, IL-6, TNF-α, and MMP-8 biomarkers to distinguish peri-implant diseases: a systematic review and meta-analysis. Clin Implant Dent Relat Res 21:190–207

    PubMed  Google Scholar 

  48. Venza I, Visalli M, Cucinotta M, De Grazia G, Teti D, Venza M (2010) Proinflammatory gene expression at chronic periodontitis and peri-implantitis sites in patients with or without type 2 diabetes. J Periodontol 81:99–108

    PubMed  Google Scholar 

  49. Maier T, Güell M, Serrano L (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett 583:3966–3973

    PubMed  Google Scholar 

  50. Koussounadis A, Langdon SP, Um IH, Harrison DJ, Smith VA (2015) Relationship between differentially expressed mRNA and mRNA-protein correlations in a xenograft model system. Sci Rep 5:10775

    PubMed  PubMed Central  Google Scholar 

  51. Costa FO, Takenaka-Martinez S, Cota LOM, Ferreira SD, Silva GLM, Costa JE (2012) Peri-implant disease in subjects with and without preventive maintenance: a 5-year follow-up. J Clin Periodontol 39:173–181

    PubMed  Google Scholar 

  52. Acharya A, Koh ML, Kheur S, Watt RM, Jin L, Mattheos N (2016) Salivary IL-1β and red complex bacteria as predictors of the inflammatory status in sub-peri-implant niches of subjects with peri-implant mucositis. Clin Oral Implants Res 27:662–667

    PubMed  Google Scholar 

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Funding

This study was funded by Gazi University Projects of Scientific Investigation, with project number 03/2017-16.

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Authors and Affiliations

  1. Department of Periodontology, Faculty of Dentistry, Gazi University, Biskek caddesi 1.sokak 06500 Emek, Ankara, Turkey

    Sila Cagri Isler, Fatma Soysal & F. Berrin Unsal

  2. Department of Periodontology, Gulhane Faculty of Dental Medicine, Health Sciences University, Ankara, Turkey

    Erkan Ozcan & N. Isıl Saygun

  3. Department of Oral Pathology, Faculty of Dentistry, Gazi University, Ankara, Turkey

    Emre Baris

  4. Department of Medical Biology, School of Medicine, Usak University, Usak, Turkey

    Rahsan Ilikci

Authors
  1. Sila Cagri Isler
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  2. Fatma Soysal
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  3. Erkan Ozcan
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  4. N. Isıl Saygun
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  5. F. Berrin Unsal
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  7. Rahsan Ilikci
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Contributions

All authors have made substantial contributions to the conception and design of the study. SCI contributed to data acquisition and interpretation and drafted and critically revised the manuscript. FS has been involved in the data collection and data analysis. EO, NIS, and FBU contributed to the design and data interpretation, critically revised the manuscript, and have given final approval of the version to be published. EB and RI contributed to the data acquisition and interpretation and critically revised the manuscript.

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Correspondence to Sila Cagri Isler.

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The authors declare that they have no conflicts of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Isler, S.C., Soysal, F., Ozcan, E. et al. Evaluation of adipokines and inflammatory mediator expression levels in patients with periodontitis and peri-implantitis: a cross-sectional study. Clin Oral Invest 25, 3555–3565 (2021). https://doi.org/10.1007/s00784-020-03678-7

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  • DOI: https://doi.org/10.1007/s00784-020-03678-7

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