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Comparison between inflammation-related markers in peri-implant crevicular fluid and clinical parameters during osseointegration in edentulous jaws

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An Erratum to this article was published on 04 September 2017

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Abstract

Objectives

The aim of this study is to improve the understanding of interleukin mechanisms during osseointegration to enhance the monitoring of implant failure and success. Clinical parameters, implant stability, and cytokine levels in peri-implant crevicular fluid (PICF) during early bone healing after implant placement were investigated.

Material and methods

Sixty narrow implants were placed in mandible anterior region of 30 edentulous patients (67.23 ± 7.66 years). Bone type, insertion torque, and primary stability were registered during surgery. Clinical measurements of peri-implant health and the secondary implant stability quotient (ISQ) were recorded. Samples from the PICF were collected 1, 2, 4, 8, and 12 weeks after surgery and analyzed for IL-1β, IL-6, IL-10, and TNF-α levels using ELISAs.

Results

The gingival index increased significantly during the first week (p = 0.05), while the plaque index increased significantly between 4 to 8 and 8 to 12 weeks (p < 0.05). The probing depth and the ISQ also reduced significantly (p < 0.05) over time. The TNF-α release increased significantly after the 2nd week for non-atrophic patients and 4th week for atrophic patients (p < 0.05). The IL-1β concentrations showed a short-lived peak after 1st week (p = 0.003), specially in atrophic patients and sites with bone type I (p = 0.034; p = 0.007). The IL-6 concentrations peaked during the 1st and 2nd weeks (p < 0.05; p = 0.005) in atrophic patients and in bone type II (p = 0.023; p = 0.003). The IL-10 concentrations increased gradually over time, showing the highest concentrations at the 12th week (p < 0.005). A total of 12 implants failed at different periods.

Conclusion

While the clinical measurements presented differences between the evaluation periods, these were not indicative of early dental implant failure or peri-implant diseases. Smoking, bone atrophy, and bone type can greatly influence the cytokines concentrations during the healing time.

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Change history

  • 04 September 2017

    An erratum to this article has been published.

References

  1. Papaspyridakos P, Chen CJ, Singh M, Weber HP, Gallucci GO (2012) Success criteria in implant dentistry: a systematic review. J Dent Res 91(3):242–248

    Article  PubMed  Google Scholar 

  2. Duarte PM, de Mendonca AC, Maximo MB, Santos VR, Bastos MF, Nociti FH (2009) Effect of anti-infective mechanical therapy on clinical parameters and cytokine levels in human peri-implant diseases. J Periodontol 80(2):234–243

    Article  PubMed  Google Scholar 

  3. Trindade R, Albrektsson T, Tengvall P, Wennerberg A (2016) Foreign body reaction to biomaterials: on mechanisms for buildup and breakdown of osseointegration. Clin Implant Dent Relat Res 18(1):192–203

    Article  PubMed  Google Scholar 

  4. Shanbhag S, Shanbhag V, Stavropoulos A (2015) Genomic analyses of early peri-implant bone healing in humans: a systematic review. Int J Implant Dent 1(1):5

    Article  PubMed  PubMed Central  Google Scholar 

  5. Javed F, Al-Hezaimi K, Salameh Z, Almas K, Romanos GE (2011) Proinflammatory cytokines in the crevicular fluid of patients with peri-implantitis. Cytokine 53(1):8–12

    Article  PubMed  Google Scholar 

  6. Mosmman T, Sad S (1996) The expanding universe of T-cell subset: Th1, Th2 and more. Immunol Today 17(3):138–146

    Article  Google Scholar 

  7. Hall J, Pehrson N-G, Ekestubbe A, Jemt T, Friberg B (2015) A controlled, cross-sectional exploratory study on markers for the plasminogen system and inflammation in crevicular fluid samples from healthy, mucositis and peri-implantitis sites. Eur J Oral Implantol 8(2):153–166

    PubMed  Google Scholar 

  8. Mundy GR (1991) Inflammatory mediators and the destruction of bone. J Periodontal Res 26(3 Pt 2):213–217

    Article  PubMed  Google Scholar 

  9. Li JY, Wang HL (2014) Biomarkers associated with periimplant diseases. Implant Dent 23(5):607–611

    PubMed  Google Scholar 

  10. Boynuegri AD, Yalim M, Nemli SK, Erguder BI, Gokalp P (2012) Effect of different localizations of microgap on clinical parameters and inflammatory cytokines in peri-implant crevicular fluid: a prospective comparative study. Clin Oral Investig 16(2):353–361

    Article  PubMed  Google Scholar 

  11. Ataoglu H, Alptekin NO, Haliloglu S, Gursel M, Ataoglu T, Serpek B, Durmus E (2002) Interleukin-Iβ, tumor necrosis factor-α levels and neutrophil elastase activity in peri-implant crevicular fluid: correlation with clinical parameters and effect of smoking. Clin Oral Implants Res 13(5):470–476

    Article  PubMed  Google Scholar 

  12. Duarte PM, Serrao CR, Miranda TS, Zanatta LC, Bastos MF, Faveri M, Figueiredo LC, Feres M (2016) Could cytokine levels in the peri-implant crevicular fluid be used to distinguish between healthy implants and implants with peri-implantitis? A systematic review. J Periodontal Res 51(6):689–698

    Article  PubMed  Google Scholar 

  13. Faot F, Nascimento GG, Bielemann AM, Campao TD, Leite FR, Quirynen M (2015) Can peri-implant crevicular fluid assist in the diagnosis of peri-implantitis? A systematic review and meta-analysis. J Periodontol 86(5):631–645

    Article  PubMed  Google Scholar 

  14. Wu Y, Zhang C, Squarize CH, Zou D (2015) Oral rehabilitation of adult edentulous siblings severely lacking alveolar bone due to ectodermal dysplasia: a report of 2 clinical cases and a literature review. J Oral Maxillofac Surg 73(9):1733):e1–12

    Article  Google Scholar 

  15. Zhang Q, Chen B, Yan F, Guo J, Zhu X, Ma S and Yang W (2014) Interleukin-10 inhibits bone resorption: a potential therapeutic strategy in periodontitis and other bone loss diseases. Biomed Res Int 2014 (284836)

  16. Stow JL, Murray RZ (2013) Intracellular trafficking and secretion of inflammatory cytokines. Cytokine Growth Factor Rev 24(3):227–239

    Article  PubMed  Google Scholar 

  17. Stow JL, Low PC, Offenhauser C, Sangermani D (2009) Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology 214(7):601–612

    Article  PubMed  Google Scholar 

  18. Kishimoto T (2010) IL-6: from its discovery to clinical applications. Int Immunol 22(5):347–352

    Article  PubMed  Google Scholar 

  19. Shrum JP (1996) Cytokines. Clin Dermatol 14:331–336

    Article  PubMed  Google Scholar 

  20. Guncu GN, Akman AC, Gunday S, Yamalik N, Berker E (2012) Effect of inflammation on cytokine levels and bone remodelling markers in peri-implant sulcus fluid: a preliminary report. Cytokine 59(2):313–316

    Article  PubMed  Google Scholar 

  21. Javed F, Ahmed HB, Crespi R, Romanos GE (2013) Role of primary stability for successful osseointegration of dental implants: factors of influence and evaluation. Interv Med Appl Sci 5(4):162–167

    PubMed  PubMed Central  Google Scholar 

  22. Cavallaro J, Greenstein B, Greenstein G (2009) Clinical methodologies for achieving primary dental implant stability. J Am Dent Assoc 140(11):1366–1372

    Article  PubMed  Google Scholar 

  23. Oates TW, Valderrama P, Bischof M, Nedir R, Jones A, Simpson J, Toutenburg H, Cochran DL (2007) Enhanced implant stability with a chemically modified SLA surface a randomized pilot study. Int J Oral Maxillofac Implants 22(5):755–760

    PubMed  Google Scholar 

  24. Xie Q, Wolf J, Ainamo A (1997) Quantitative assessment of vertical heights of maxillary and mandibular bones in panoramic radiographs of elderly dentate and edentulous subjects. Acta Odontol Scand 55(3):155–161

    Article  PubMed  Google Scholar 

  25. Cawood JL, Howell RA (1988) A classification of the edentulous jaws. Int J Oral Maxillofac Surg 17(4):232–236

    Article  PubMed  Google Scholar 

  26. Molly L (2006) Bone density and primary stability in implant therapy. Clin Oral Implants Res 17(Suppl 2):124–135

    Article  PubMed  Google Scholar 

  27. Mombelli A, van Oosten MA, Schurch E Jr, Land NP (1987) The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2(4):145–151

    Article  PubMed  Google Scholar 

  28. Al-Nawas B, Bragger U, Meijer HJ, Naert I, Persson R, Perucchi A, Quirynen M, Raghoebar GM, Reichert TE, Romeo E, Santing HJ, Schimmel M, Storelli S, ten Bruggenkate C, Vandekerckhove B, Wagner W, Wismeijer D, Muller F (2012) A double-blind randomized controlled trial (RCT) of titanium-13Zirconium versus titanium grade IV small-diameter bone level implants in edentulous mandibles—results from a 1-year observation period. Clin Implant Dent Relat Res 14(6):896–904

    Article  PubMed  Google Scholar 

  29. Emecen-Huja P, Eubank TD, Shapiro V, Yildiz V, Tatakis DN, Leblebicioglu B (2013) Peri-implant versus periodontal wound healing. J Clin Periodontol 40(8):816–824

    Article  PubMed  PubMed Central  Google Scholar 

  30. Onuma T, Aquiar K, Duarte PM, Feres M, Giro G, Coelho PG, Cassoni A, Shibli JA (2015) Levels of osteodastogenesis-related factors in the peri-implant crevicular fluid and clinical parameters of immediately loaded implants in patients with osteopenia: a short-term report. Int J Oral Maxillofac Implants 30(6):1431–1436

    Article  PubMed  Google Scholar 

  31. Dogan SB, Kurtis MB, Tuter G, Serdar M, Watanabe K, Karakis S (2015) Evaluation of clinical parameters and levels of proinflammatory cytokines in the crevicular fluid around dental implants in patients with type 2 diabetes mellitus. Int J Oral Maxillofac Implants 30(5):1119–1127

    Article  PubMed  Google Scholar 

  32. Tsoukaki M, Kalpidis CD, Sakellari D, Tsalikis L, Mikrogiorgis G, Konstantinidis A (2013) Clinical, radiographic, microbiological, and immunological outcomes of flapped vs. flapless dental implants: a prospective randomized controlled clinical trial. Clin Oral Implants Res 24(9):969–976

    PubMed  Google Scholar 

  33. Taxel P, Ortiz D, Shafer D, Pendrys D, Reisine S, Rengasamy K, Freilich M (2014) The relationship between implant stability and bone health markers in post-menopausal women with bisphosphonate exposure. Clin Oral Investig 18(1):49–57

    Article  PubMed  Google Scholar 

  34. Güncü GN, Tözüm TF, Güncü MB, Yamalik N (2008) Relationships between implant stability, image-based measures and nitric oxide levels. J Oral Rehabil 35(10):745–753

    Article  PubMed  Google Scholar 

  35. Prati AJ, Casati MZ, Ribeiro FV, Cirano FR, Pastore GP, Pimentel SP, Casarin RCV, Author A, Division of Maxillofacial Surgery P, University SPB, Division of Periodontics PUS, Paulo B, Correspondence A, R.C.V. Casarin DoPPUSP and Brazil. Email cycb (2013) Release of bone markers in immediately loaded and nonloaded dental implants: a randomized clinical trial. J Dental Res 92(12):161S–167S

    Article  Google Scholar 

  36. Basegmez C, Yalcin S, Yalcin F, Ersanli S, Mijiritsky E (2012) Evaluation of periimplant crevicular fluid prostaglandin E2 and matrix metalloproteinase-8 levels from health to periimplant disease status: a prospective study. Implant Dent 21(4):306–310

    Article  PubMed  Google Scholar 

  37. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285(33):25103–25108

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gokmenoglu C, Ozmeric N, Erguder I, Elgun S (2014) The effect of light-emitting diode photobiomodulation on implant stability and biochemical markers in peri-implant crevicular fluid. Photomed Laser Surg 32(3):138–145

    Article  PubMed  Google Scholar 

  39. Slotte C, Lenneras M, Gothberg C, Suska F, Zoric N, Thomsen P, Nannmark U (2012) Gene expression of inflammation and bone healing in peri-implant crevicular fluid after placement and loading of dental implants. A kinetic clinical pilot study using quantitative real-time PCR. Clin Implant Dent Relat Res 14(5):723–736

    Article  PubMed  Google Scholar 

  40. Güncü MB, Aslan Y, Tümer C, Güncü GN, Uysal S (2008) In-patient comparison of immediate and conventional loaded implants in mandibular molar sites within 12 months. Clin Oral Implants Res 19(4):335–341

    Article  PubMed  Google Scholar 

  41. Tozum TF, Turkyilmaz I, Yamalik N, Tumer C, Kilinc A, Kilinc K, Karabulut E, Eratalay K (2005) Analysis of thte possible impact of inflammation severity and early and delayed loading on nitric oxide metabolism around dental implants. Int J Oral Maxillofac Implants 20(4):547–556

    PubMed  Google Scholar 

  42. Gruber R, Nadir J, Haas R (2010) Neutrophil elastase activity and concentrations of interleukin 1-beta in crevicular fluid after immediate replacement and immediate loading of implants. Br J Oral Maxillofac Surg 48(3):228–231

    Article  PubMed  Google Scholar 

  43. Khoury SB, Thomas L, Walters JD, Sheridan JF, Leblebicioglu B (2008) Early wound healing following one-stage dental implant placement with and without antibiotic prophylaxis: a pilot study. J Periodontol 79(10):1904–1912

    Article  PubMed  PubMed Central  Google Scholar 

  44. Nogueira-Filho G, Pesun I, Isaak-Ploegman C, Wijegunasinghe M, Wierzbicki T, McCulloch CA (2014) Longitudinal comparison of cytokines in peri-implant fluid and gingival crevicular fluid in healthy mouths. J Periodontol 85(11):1582–1588

    Article  PubMed  Google Scholar 

  45. Nowzari H, Botero JE, DeGiacomo M, Villacres MC, Rich SK (2008) Microbiology and cytokine levels around healthy dental implants and teeth. Clin Implant Dent Relat Res 10(3):166–173

    Article  PubMed  Google Scholar 

  46. Gurol C, Kazazoglu E, Dabakoglu B, Korachi M (2011) A comparative study of the role of cytokine polymorphisms interleukin-10 and tumor necrosis factor alpha in susceptibility to implant failure and chronic periodontitis. Int J Oral Maxillofac Implants 26(5):955–960

    PubMed  Google Scholar 

  47. Dimitriou R, Tsiridis E, Giannoudis PV (2005) Current concepts of molecular aspects of bone healing. Injury 36(12):1392–1404

    Article  PubMed  Google Scholar 

  48. Wei L, Sun Y, Kong XF, Zhang C, Yue T, Zhu Q, He DY, Jiang LD (2016) The effects of dopamine receptor 2 expression on B cells on bone metabolism and TNF-alpha levels in rheumatoid arthritis. BMC Musculoskelet Disord 19(17):352

    Article  Google Scholar 

  49. Lim HS, Park YH, Kim SK (2016) Relationship between serum inflammatory marker and bone mineral density in healthy adults. J Bone Metab 23(1):27–33

    Article  PubMed  PubMed Central  Google Scholar 

  50. Lang NP, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Bosshardt DD (2011) Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clin Oral Implants Res 22(4):349–356

    Article  PubMed  Google Scholar 

  51. Graves DT, Nooh N, Gillen T, Davey M, Patel S, Cottrell D, Amar S (2001) IL-1 plays a critical role in oral, but not dermal, wound healing. J Immunol 167(9):5316–5320

    Article  PubMed  Google Scholar 

  52. Carta S, Tassi S, Semino C, Fossati G, Mascagni P, Dinarello CA, Rubartelli A (2006) Histone deacetylase inhibitors prevent exocytosis of interleukin-1beta-containing secretory lysosomes: role of microtubules. Blood 108(5):1618–1626

    Article  PubMed  PubMed Central  Google Scholar 

  53. Petkovic AB, Matic SM, Stamatovic NV, Vojvodic DV, Todorovic TM, Lazic ZR, Kozomara RJ (2010) Proinflammatory cytokines (IL-1beta and TNF-alpha) and chemokines (IL-8 and MIP-1alpha) as markers of peri-implant tissue condition. Int J Oral Maxillofac Surg 39(5):478–485

    Article  PubMed  Google Scholar 

  54. Jawa RS, Anillo S, Huntoon K, Baumann H, Kulaylat M (2011) Analytic review: interleukin-6 in surgery, trauma, and critical care: part I: basic science. J Intensive Care Med 26(1):3–12

    Article  PubMed  Google Scholar 

  55. Jawa RS, Anillo S, Huntoon K, Baumann H, Kulaylat M (2011) Interleukin-6 in surgery, trauma, and critical care part II: clinical implications. J Intensive Care Med 26(2):73–87

    Article  PubMed  Google Scholar 

  56. Tatli U, Damlar I, Erdogan O, Esen E (2013) Effects of smoking on periimplant health status and IL-1beta, TNF-alpha, and PGE2 levels in periimplant crevicular fluid: a cross-sectional study on well-maintained implant recall patients. Implant Dent 22(5):519–524

    Article  PubMed  Google Scholar 

  57. Rioux N, Castonguay A (2001) 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone modulation of cytokine release in U937 human macrophages. Cancer Immunol Immunother 49(12):663–670

    Article  PubMed  Google Scholar 

  58. Takanashi S, Hasegawa Y, Kanehira Y, Yamamoto K, Fujimoto K, Satoh K, Okamura K (1999) Interleukin-10 level in sputum is reduced in bronchial asthma, COPD and in smokers. Eur Respir J 4:309–314

    Article  Google Scholar 

  59. Zweers J, van Doornik A, Hogendorf EA, Quirynen M, Van der Weijden GA (2015) Clinical and radiographic evaluation of narrow- vs. regular-diameter dental implants: a 3-year follow-up. A retrospective study. Clin Oral Implants Res 26(2):149–156

    Article  PubMed  Google Scholar 

  60. Preoteasa E, Imre M, Preoteasa CT (2014) A 3-year follow-up study of overdentures retained by mini-dental implants. Int J Oral Maxillofac Implants 29(5):1170–1176

    Article  PubMed  Google Scholar 

  61. de Souza RF, Ribeiro AB, Della Vecchia MP, Costa L, Cunha TR, Reis AC, Albuquerque RF Jr (2015) Mini vs. standard implants for mandibular overdentures: a randomized trial. J Dental Res 94(10):1376–1384

    Article  Google Scholar 

  62. Catalan A, Martinez A, Marchesani F, Gonzalez U (2016) Mandibular overdentures retained by two mini-implants: a seven-year retention and satisfaction study. J Prosthodont 25(5):364–370

    Article  PubMed  Google Scholar 

  63. Emami E, Cerutti-Kopplin D, Menassa M, Audy N, Kodama N, Durand R, Rompre P, de Grandmont P (2016) Does immediate loading affect clinical and patient-centered outcomes of mandibular 2-unsplinted-implant overdenture? A 2-year within-case analysis. J Dent 50:30–36

    Article  PubMed  Google Scholar 

  64. Gomes FI, Aragao MG, de Paulo Teixeira Pinto V, Gondim DV, Barroso FC, Silva AA, Bezerra MM, Chaves HV (2015) Effects of nonsteroidal anti-inflammatory drugs on osseointegration: a review. J Oral Implantol 41(2):219–230

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Neodent for supplying the dental implants used in the study. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Correspondence to Fernanda Faot.

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The authors declare that they have no conflict of interest.

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There was no grant support or funding for this study.

Ethical approval

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. The research protocol was approved by the Ethics Committee of School of Dentistry (Number 1.267.086/2015), Federal University of Pelotas. Patients and their families or legal representatives provided signed written informed consent.

Informed consent

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

Additional information

The original version of this article was revised: the results of the cytokine analyses (page 5 and Table 3) should be referred to as “median” instead of “means”. In addition, the significant differences between the categorized groups in the Figs. 1–4 were indicated by asterisks, but these asterisks disappeared during the conversion of the figures’ source files.

An erratum to this article is available at https://doi.org/10.1007/s00784-017-2191-2.

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Bielemann, A.M., Marcello-Machado, R.M., Leite, F.R.M. et al. Comparison between inflammation-related markers in peri-implant crevicular fluid and clinical parameters during osseointegration in edentulous jaws. Clin Oral Invest 22, 531–543 (2018). https://doi.org/10.1007/s00784-017-2169-0

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