Immunohistochemical analysis of soft tissue response to polyetheretherketone (PEEK) and titanium healing abutments on dental implants: a randomized pilot clinical study

Iva Milinkovic, Ana Djinic Krasavcevic, Sasha Jankovic, Jelena Sopta, Zoran Aleksic, Iva Milinkovic, Ana Djinic Krasavcevic, Sasha Jankovic, Jelena Sopta, Zoran Aleksic

Abstract

Background: The data on polyetheretherketone (PEEK) influence on the peri-implant soft tissues in clinical settings are deficient. The aims of this pilot study were to analyze and compare soft tissues' response to PEEK and titanium (Ti) healing abutments (HA) by means of histological and immunohistochemical analyses.

Methods: A total of 22 implants with PEEK or Ti HA were placed in 11 patients, applying the "split-mouth" study design. Three months later, soft tissue specimens were harvested from 20 implants for histology in order to qualitatively detect the inflammatory cells' presence, to semi-qualitatively analyze the inflammation intensity and to assess the inflammatory responses type by immunohistochemical analysis using LCA, CD3, CD20 and CD68 antibodies.

Results: Epithelial infiltrate followed by an intensive inflammation in sub-epithelium was observed in 100% around PEEK HA. A number of LCA+ and CD 68+ cells was significantly higher in PEEK comparing to Ti group (p = 0.001 and p = 0.020, respectively), while CD 20+ and CD3+ counted cells were found in a significantly higher amount in Ti than in PEEK group (p = 0.006 and p = 0.010, respectively).

Conclusion: PEEK HA seems to evoke the more intense tissue inflammatory response demonstrated predominantly by histocytes' and plasmacytes' activation, while Ti HA triggers the inflammatory reaction of lower intensity, dominantly mediated by B-cells.

Trial registration: The study registered at ClinicalTrials.gov (NCT04436939).

Keywords: PEEK; Titanium; healing abutment; immunohistochemistry; inflammation.

Conflict of interest statement

The authors declare that they have no competing interests.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Clinical presentation of PEEK and Ti healing abutments placed after the surgery within the split-mouth protocol
Fig. 2
Fig. 2
Hematoxylin-eosin staining, elucidating the presence of the inflammatory cells dominantly in subepithelial tissue (3a,3b). Intraepithelial presence of several inflammatory cells was observed in Fig. 3b, as highlighted by the yellow arrows. HE × 400 magnification
Fig. 3
Fig. 3
Hematoxylin-eosin (HE) staining of the specimens to assess inflammatory reaction. Inflammatory response was classified as „light” (2a), „medium” (2b) or „intensive” (2c). HE × 100 magnification
Fig. 4
Fig. 4
Immunohistochemical analysis of the sections prepared from soft tissues surrounding PEEK and Ti abutments. Comparative presentation of inflammatory cells in specimens appertaining to PEEK group (a, b, c, d) and Ti group (e, f, g, h) showed respectively more pronounced inflammation around PEEK (a, e: LCA; b, f:CD20; c, g: CD3; d, h: CD68). ×400 magnification
Fig. 5
Fig. 5
The number of LCA+, CD20+, CD3+ and CD68+ cells around PEEK and Ti healing abutments. Significant comparisons (p < 0.05) were emphasized on the graph

References

    1. Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants. 1986;1(1):11–25.
    1. Mombelli A, Muller N, Cionca N. The epidemiology of peri-implantitis. Clin Oral Implants Res. 2012;23:67–76. doi: 10.1111/j.1600-0501.2012.02541.x.
    1. Atieh MA, Alsabeeha NHM, Faggion CM, Duncan WJ. The frequency of peri-implant diseases: a systematic review and meta-analysis. J Periodontol. 2013;84(11):1586–1598.
    1. Derks J, Håkansson J, Wennström JL, Klinge B, Berglundh T. Patient-reported outcomes of dental implant therapy in a large randomly selected sample. Clin Oral Implants Res. 2015;26(5):586–591. doi: 10.1111/clr.12464.
    1. Hahnel S, Wieser A, Lang R, Rosentritt M. Biofilm formation on the surface of modern implant abutment materials. Clin Oral Implants Res. 2015;26(11):1297–1301. doi: 10.1111/clr.12454.
    1. Berglundh T, Abrahamsson I, Welander M, Lang NP, Lindhe J. Morphogenesis of the peri-implant mucosa: an experimental study in dogs. Clin Oral Implants Res. 2007;18(1):1–8. doi: 10.1111/j.1600-0501.2006.01380.x.
    1. Welander M, Abrahamsson I, Berglundh T. The mucosal barrier at implant abutments of different materials. Clin Oral Implants Res. 2008;19(7):635–641.
    1. Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg B, Thomsen P. The soft tissue barrier at implants and teeth. Clin Oral Implants Res. 1991;2(2):81–90. doi: 10.1034/j.1600-0501.1991.020206.x.
    1. Abdallah MN, Badran Z, Ciobanu O, Hamdan N, Tamimi F. Strategies for optimizing the soft tissue seal around osseointegrated implants. Adv Healthc Mater. 2017;6(20):1700549.
    1. Toth JM, Wang M, Estes BT, Scifert JL, Seim HB, Turner AS. Polyetheretherketone as a biomaterial for spinal applications. Biomaterials. 2006;27(3):324–334. doi: 10.1016/j.biomaterials.2005.07.011.
    1. Skinner HB. Composite technology for total hip arthroplasty. Clin Orthop Relat Res. 1988;235:224–236. doi: 10.1097/00003086-198810000-00022.
    1. Kern M, Lehmann F. Influence of surface conditioning on bonding to polyetheretherketon (PEEK) Dent Mater. 2012;28(12):1280–1283. doi: 10.1016/j.dental.2012.09.010.
    1. Rabiei A, Sandukas S. Processing and evaluation of bioactive coatings on polymeric implants. J Biomed Mater Res A. 2013;101(9):2621–2629. doi: 10.1002/jbm.a.34557.
    1. Utzschneider S, Becker F, Grupp TM, Sievers B, Paulus A, Gottschalk O, et al. Inflammatory response against different carbon fiber-reinforced PEEK wear particles compared with UHMWPE in vivo. Acta Biomater. 2010;6(11):4296–4304. doi: 10.1016/j.actbio.2010.06.002.
    1. Najeeb S, Zafar MS, Khurshid Z, Siddiqui F. Applications of polyetheretherketone (PEEK) in oral implantology and prosthodontics. J Prosthodont Res. 2016;60(1):12–19. doi: 10.1016/j.jpor.2015.10.001.
    1. Papathanasiou I, Kamposiora P, Papavasiliou G, Ferrari M. The use of PEEK in digital prosthodontics: a narrative review. BMC Oral Health. 2020;20(1):217. doi: 10.1186/s12903-020-01202-7.
    1. Barkarmo S, Longhorn D, Leer K, Johansson CB, Stenport V, Franco-Tabares S, et al. Biofilm formation on polyetheretherketone and titanium surfaces. Clin Exp Dent Res. 2019;5(4):427–437. doi: 10.1002/cre2.205.
    1. Barkarmo S, Östberg A-K, Johansson CB, Franco-Tabares S, Johansson PH, Dahlgren U, et al. Inflammatory cytokine release from human peripheral blood mononuclear cells exposed to polyetheretherketone and titanium-6 aluminum-4 vanadium in vitro. J Biomater Appl. 2018;33(2):245–258. doi: 10.1177/0885328218786005.
    1. Caballé-Serrano J, Chappuis V, Monje A, Buser D, Bosshardt DD. Soft tissue response to dental implant closure caps made of either polyetheretherketone (PEEK) or titanium. Clin Oral Implants Res. 2019;30(8):808–816. doi: 10.1111/clr.13487.
    1. van Brakel R, Meijer GJ, Verhoeven JW, Jansen J, de Putter C, Cune MS. Soft tissue response to zirconia and titanium implant abutments: an in vivo within-subject comparison. J Clin Periodontol. 2012;39(10):995–1001. doi: 10.1111/j.1600-051X.2012.01931.x.
    1. Su-Mingxhsu O, Raine I, Fawger H. Use of avidin biotin peroxidase complex (ABC) in immunoperoxidase technique: a comparison between ABC and unlabeled antibodies (PAP) procedures. J Histochem Cytochem. 1981;29:577. doi: 10.1177/29.4.6166661.
    1. Gualini F, Berglundh T. Immunohistochemical characteristics of inflammatory lesions at implants. J Clin Periodontol. 2003;30(1):14–18. doi: 10.1034/j.1600-051X.2003.300103.x.
    1. Serichetaphongse P, Chengprapakorn W, Thongmeearkom S, Pimkhaokham A. Immunohistochemical assessment of the peri-implant soft tissue around different abutment materials: A human study. Clin Implant Dent Relat Res. 2020;22(5):638–646. doi: 10.1111/cid.12942.
    1. Calame KL. Plasma cells: finding new light at the end of B cell development. Nat Immunol. 2001;2(12):1103–1108. doi: 10.1038/ni1201-1103.
    1. Esposito M, Thomsen P, Mölne J, Gretzer C, Ericson LE, Lekholm U. Immunohistochemistry of soft tissues surrounding late failures of Brånemark implants. Clin Oral Implants Res. 1997;8(5):352–366. doi: 10.1034/j.1600-0501.1997.080502.x.
    1. Galarraga-Vinueza ME, Obreja K, Ramanauskaite A, Magini R, Begic A, Sader R, et al. Macrophage polarization in peri-implantitis lesions. Clin Oral Investig. 2021;25(4):2335–2344. doi: 10.1007/s00784-020-03556-2.
    1. Streuli M, Morimoto C, Schrieber M, Schlossman SF, Saito H. Characterization of CD45 and CD45R monoclonal antibodies using transfected mouse cell lines that express individual human leukocyte common antigens. J Immunol. 1988;141(11):3910–3914.
    1. Wang H, Xu M, Zhang W, Kwok DTK, Jiang J, Wu Z, et al. Mechanical and biological characteristics of diamond-like carbon coated poly aryl-ether-ether-ketone. Biomaterials. 2010;31(32):8181–8187. doi: 10.1016/j.biomaterials.2010.07.054.
    1. Nieminen T, Kallela I, Wuolijoki E, Kainulainen H, Hiidenheimo I, Rantala I. Amorphous and crystalline polyetheretherketone: Mechanical properties and tissue reactions during a 3-year follow-up. J Biomed Mater Res A. 2008;84(2):377–383. doi: 10.1002/jbm.a.31310.
    1. Rea M, Ricci S, Ghensi P, Lang NP, Botticelli D, Soldini C. Marginal healing using Polyetheretherketone as healing abutments: an experimental study indogs. Clin Oral Implants Res. 2017;28(7):e46–e50. doi: 10.1111/clr.12854.
    1. Tonetti MS, Imboden M, Gerber L, Lang NP. Compartmentalization of inflammatory cell phenotypes in normal gingiva and peri-implant keratinized mucosa. J Clin Periodontol. 1995;22(10):735–742. doi: 10.1111/j.1600-051X.1995.tb00255.x.
    1. Obădan F, Crăiţoiu Ş, Manolea HO, Hincu M-C, Iacov-Crăiţoiu MM. The evaluation of the morphological evolution of the tissue integration of dental implants through conventional histology and immunohistochemistry techniques. Romanian J Morphol Embryol. 2018;59(3):851–859.
    1. Chehroudi B, Ghrebi S, Murakami H, Waterfield JD, Owen G, Brunette DM. Bone formation on rough, but not polished, subcutaneously implanted Ti surfaces is preceded by macrophage accumulation. J J Biomed Mater Res A. 2010;93(2):724–737.
    1. Miron RJ, Bosshardt DD. Multinucleated giant cells: good guys or bad guys? Tissue Eng Part B Rev. 2018;24(1):53–65. doi: 10.1089/ten.teb.2017.0242.
    1. Lang NP, Berglundh T. Working Group 4 of the Seventh European Workshop on P. Periimplant diseases: where are we now?–Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38:178–181. doi: 10.1111/j.1600-051X.2010.01674.x.
    1. Volpe S, Verrocchi D, Andersson P, Gottlow J, Sennerby L. Comparison of early bacterial colonization of PEEK and titanium healing abutments using real-time PCR. Appl Osseoint Res. 2008;6(2):54–56.
    1. Seymour GJ, Gemmell E, Lenz LJ, Henry P, Bower R, Yamazaki K. Immunohistologic analysis of the inflammatory infiltrates associated with osseointegrated implants. Int J Oral Maxillofac Implants. 1989;4(3):191–8.
    1. Bambini F, Santarelli A, Marzo G, Rubini C, Orsini G, Di Iorio D, et al. CD3 and CD20 expression in titanium vs zirconia peri-implant soft tissues: a human study. Eur J Inflamm. 2013;11(1):305–310. doi: 10.1177/1721727X1301100133.

Source: PubMed

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