Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Clinical Oral Investigations
Published in: Clinical Oral Investigations 1/2018

01-01-2018 | Original Article

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

Authors: Amália M Bielemann, Raissa M Marcello-Machado, Fábio Renato Manzolli Leite, Frederico Canato Martinho, Otacílio Luiz Chagas-Júnior, Altair Antoninha Del Bel Cury, Fernanda Faot

Published in: Clinical Oral Investigations | Issue 1/2018

Login to get access

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.
Appendix
Available only for authorised users
Literature
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):242–248CrossRefPubMed
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):234–243CrossRefPubMed
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):192–203CrossRefPubMed
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):5CrossRefPubMedPubMedCentral
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):8–12CrossRefPubMed
6.
Mosmman T, Sad S (1996) The expanding universe of T-cell subset: Th1, Th2 and more. Immunol Today 17(3):138–146CrossRef
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):153–166PubMed
8.
Mundy GR (1991) Inflammatory mediators and the destruction of bone. J Periodontal Res 26(3 Pt 2):213–217CrossRefPubMed
9.
Li JY, Wang HL (2014) Biomarkers associated with periimplant diseases. Implant Dent 23(5):607–611PubMed
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):353–361CrossRefPubMed
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):470–476CrossRefPubMed
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):689–698CrossRefPubMed
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):631–645CrossRefPubMed
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):e1–12CrossRef
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):227–239CrossRefPubMed
17.
Stow JL, Low PC, Offenhauser C, Sangermani D (2009) Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology 214(7):601–612CrossRefPubMed
18.
19.
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):313–316CrossRefPubMed
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):162–167PubMedPubMedCentral
22.
Cavallaro J, Greenstein B, Greenstein G (2009) Clinical methodologies for achieving primary dental implant stability. J Am Dent Assoc 140(11):1366–1372CrossRefPubMed
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):755–760PubMed
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):155–161CrossRefPubMed
25.
Cawood JL, Howell RA (1988) A classification of the edentulous jaws. Int J Oral Maxillofac Surg 17(4):232–236CrossRefPubMed
26.
Molly L (2006) Bone density and primary stability in implant therapy. Clin Oral Implants Res 17(Suppl 2):124–135CrossRefPubMed
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):145–151CrossRefPubMed
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):896–904CrossRefPubMed
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):816–824CrossRefPubMedPubMedCentral
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):1431–1436CrossRefPubMed
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):1119–1127CrossRefPubMed
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):969–976PubMed
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):49–57CrossRefPubMed
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):745–753CrossRefPubMed
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–167SCrossRef
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):306–310CrossRefPubMed
37.
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):138–145CrossRefPubMed
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):723–736CrossRefPubMed
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):335–341CrossRefPubMed
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):547–556PubMed
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):228–231CrossRefPubMed
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):1904–1912CrossRefPubMedPubMedCentral
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):1582–1588CrossRefPubMed
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):166–173CrossRefPubMed
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):955–960PubMed
47.
Dimitriou R, Tsiridis E, Giannoudis PV (2005) Current concepts of molecular aspects of bone healing. Injury 36(12):1392–1404CrossRefPubMed
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):352CrossRef
49.
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):349–356CrossRefPubMed
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):5316–5320CrossRefPubMed
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):1618–1626CrossRefPubMedPubMedCentral
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):478–485CrossRefPubMed
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):3–12CrossRefPubMed
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):73–87CrossRefPubMed
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):519–524CrossRefPubMed
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):663–670CrossRefPubMed
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 4:309–314CrossRef
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):149–156CrossRefPubMed
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):1170–1176CrossRefPubMed
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):1376–1384CrossRef
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):364–370CrossRefPubMed
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 50:30–36CrossRefPubMed
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):219–230CrossRefPubMed
Metadata
Title
Comparison between inflammation-related markers in peri-implant crevicular fluid and clinical parameters during osseointegration in edentulous jaws
Authors
Amália M Bielemann
Raissa M Marcello-Machado
Fábio Renato Manzolli Leite
Frederico Canato Martinho
Otacílio Luiz Chagas-Júnior
Altair Antoninha Del Bel Cury
Fernanda Faot
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 1/2018
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-017-2169-0

Other articles of this Issue 1/2018

Clinical Oral Investigations 1/2018 Go to the issue

Review

Oral hygiene and oral health in older people with dementia: a comprehensive review with focus on oral soft tissues

Original Article

Topical application of morphine for wound healing and analgesia in patients with oral lichen planus: a randomized, double-blind, placebo-controlled study

Original Article

Biological predictors of radiosensitivity in head and neck squamous cell carcinoma

Original Article

Significance of genetic variations in developmental enamel defects of primary dentition in Polish children

Review

Oral pregabalin for acute pain relief after cervicofacial surgery: a systematic review

Original Article

Regenerative properties of collagenated porcine bone grafts in human maxilla: demonstrative study of the kinetics by synchrotron radiation microtomography and light microscopy