New insights on collagen structural organization and spatial distribution around dental implants: a comparison between machined and laser-treated surfaces.

Collagen Dental implants Fourier Transform InfraRed Imaging spectroscopy Healing abutments Implant surface Synthegra Transmucosal surface

Journal

Journal of translational medicine
ISSN: 1479-5876
Titre abrégé: J Transl Med
Pays: England
ID NLM: 101190741

Informations de publication

Date de publication:
31 Jan 2024
Historique:
received: 23 06 2023
accepted: 18 01 2024
medline: 1 2 2024
pubmed: 1 2 2024
entrez: 31 1 2024
Statut: epublish

Résumé

One of the main factors for the osseointegration of dental implants is the development of an adequate soft tissue barrier, mainly composed by collagen, which protects the implant from bacterial development. The structural features of the peri-implant collagen are influenced by the implant components and, in particular, by the type of the surface. In the clinical practice, healing abutments are characterized by smooth surfaces, named machined. Recently, a new laser technique, Synthegra, has been developed to obtain a topography-controlled surface with micrometric regular pores that seems reducing the risk of peri-implantitis. Based on this background, this study aims investigating the structural organization and spatial distribution of collagen surrounding healing abutments characterized by laser-treated and machined surfaces. Gingiva portions surrounding custom-made healing abutments (HA), characterized by alternated laser-treated and machined surfaces, were collected and analyzed by combining Fourier Transform InfraRed Imaging (FTIRI) spectroscopy, a non-invasive and high-resolution bidimensional analytical technique, with histological and multivariate analyses. Masson's trichrome staining, specific for collagen, highlighted a massive presence of collagen in all the analyzed samples, evidencing a surface-related spatial distribution. The nature of collagen, investigated by the FTIRI spectroscopy, appeared more abundant close to the laser-treated surface, with a perpendicular disposition of the bundles respect to the HA; conversely, a parallel distribution was observed around the machined surface. A different secondary structure was also found, with a higher amount of triple helices and a lower quantity of random coils in collagen close to the laser treated surfaces. FTIRI spectroscopy demonstrates that the use of a laser treated transmucosal surface can improve the morphological organization of the peri-implant collagen, which presents a distribution more similar to that of natural teeth. This trial is registered with ClinicalTrials.gov Identifier: (Registration Number: NCT05754970). Registered 06/03/2023, retrospectively registered, https://clinicaltrials.gov/show/NCT05754970 .

Sections du résumé

BACKGROUND BACKGROUND
One of the main factors for the osseointegration of dental implants is the development of an adequate soft tissue barrier, mainly composed by collagen, which protects the implant from bacterial development. The structural features of the peri-implant collagen are influenced by the implant components and, in particular, by the type of the surface. In the clinical practice, healing abutments are characterized by smooth surfaces, named machined. Recently, a new laser technique, Synthegra, has been developed to obtain a topography-controlled surface with micrometric regular pores that seems reducing the risk of peri-implantitis. Based on this background, this study aims investigating the structural organization and spatial distribution of collagen surrounding healing abutments characterized by laser-treated and machined surfaces.
METHODS METHODS
Gingiva portions surrounding custom-made healing abutments (HA), characterized by alternated laser-treated and machined surfaces, were collected and analyzed by combining Fourier Transform InfraRed Imaging (FTIRI) spectroscopy, a non-invasive and high-resolution bidimensional analytical technique, with histological and multivariate analyses.
RESULTS RESULTS
Masson's trichrome staining, specific for collagen, highlighted a massive presence of collagen in all the analyzed samples, evidencing a surface-related spatial distribution. The nature of collagen, investigated by the FTIRI spectroscopy, appeared more abundant close to the laser-treated surface, with a perpendicular disposition of the bundles respect to the HA; conversely, a parallel distribution was observed around the machined surface. A different secondary structure was also found, with a higher amount of triple helices and a lower quantity of random coils in collagen close to the laser treated surfaces.
CONCLUSIONS CONCLUSIONS
FTIRI spectroscopy demonstrates that the use of a laser treated transmucosal surface can improve the morphological organization of the peri-implant collagen, which presents a distribution more similar to that of natural teeth.
TRIAL REGISTRATION BACKGROUND
This trial is registered with ClinicalTrials.gov Identifier: (Registration Number: NCT05754970). Registered 06/03/2023, retrospectively registered, https://clinicaltrials.gov/show/NCT05754970 .

Identifiants

pubmed: 38297308
doi: 10.1186/s12967-024-04906-4
pii: 10.1186/s12967-024-04906-4
doi:

Banques de données

ClinicalTrials.gov
['NCT05754970']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

120

Subventions

Organisme : Ministero dell'Istruzione, dell'Università e della Ricerca
ID : ex 60% 2022 B.S.

Informations de copyright

© 2024. The Author(s).

Références

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;1:11–25.
pubmed: 3527955
Do TA, Le HS, Shen Y-W, Huang H-L, Fuh L-J. Risk factors related to late failure of dental implant-a systematic review of recent studies. Int J Environ Res Public Health. 2020;17:3931. https://doi.org/10.3390/ijerph17113931 .
doi: 10.3390/ijerph17113931 pubmed: 32498256 pmcid: 7312800
Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (I). Success criteria and epidemiology. Eur J Oral Sci. 1998;106:527–51. https://doi.org/10.1046/j.0909-8836.t01-2-.x .
doi: 10.1046/j.0909-8836.t01-2-.x pubmed: 9527353
Tonetti MS, Schmid J. Pathogenesis of implant failures. Periodontol. 1994;2000(4):127–38. https://doi.org/10.1111/j.1600-0757.1994.tb00013.x .
doi: 10.1111/j.1600-0757.1994.tb00013.x
Ericsson I, Berglundh T, Marinello C, Liljenberg B, Lindhe J. Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res. 1992;3:99–103. https://doi.org/10.1034/j.1600-0501.1992.030301.x .
doi: 10.1034/j.1600-0501.1992.030301.x pubmed: 1290796
Lang N, Berglundh T, Lang NP, Berglundh T. Working Group 4 of Seventh European Workshop on Periodontology. Periimplant diseases: Where are we now?—Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38(Suppl 11):178–81. https://doi.org/10.1111/j.1600-051X.2010.01674.x .
doi: 10.1111/j.1600-051X.2010.01674.x pubmed: 21323713
Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res. 1994;5:254–9.
doi: 10.1034/j.1600-0501.1994.050409.x pubmed: 7640340
Roos-Jansåker A-M, Renvert H, Lindahl C, Renvert S. Nine- to fourteen-year follow-up of implant treatment. Part III: factors associated with peri-implant lesions. J Clin Periodontol. 2006;33:296–301. https://doi.org/10.1111/j.1600-051X.2006.00908.x .
doi: 10.1111/j.1600-051X.2006.00908.x pubmed: 16553639
Quirynen M, De Soete M, van Steenberghe D. Infectious risks for oral implants: a review of the literature. Clin Oral Implants Res. 2002;13:1–19. https://doi.org/10.1034/j.1600-0501.2002.130101.x .
doi: 10.1034/j.1600-0501.2002.130101.x pubmed: 12005139
Mombelli A. In vitro models of biological responses to implant microbiological models. Adv Dent Res. 1999;13:67–72. https://doi.org/10.1177/08959374990130011701 .
doi: 10.1177/08959374990130011701 pubmed: 11276749
Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B. Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res. 1992;3:1–8. https://doi.org/10.1034/j.1600-0501.1992.030101.x .
doi: 10.1034/j.1600-0501.1992.030101.x pubmed: 1420721
Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C. Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res. 1992;3:9–16. https://doi.org/10.1034/j.1600-0501.1992.030102.x .
doi: 10.1034/j.1600-0501.1992.030102.x pubmed: 1420727
Tete S, Mastrangelo F, Bianchi A, Zizzari V, Scarano A. Collagen fiber orientation around machined titanium and zirconia dental implant necks: an animal study. Int J Oral Maxillofac Implants. 2009;24:52–8.
pubmed: 19344025
Querido W, Kandel S, Pleshko N. Applications of vibrational spectroscopy for analysis of connective tissues. Molecules. 2021;26:922. https://doi.org/10.3390/molecules26040922 .
doi: 10.3390/molecules26040922 pubmed: 33572384 pmcid: 7916244
Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010;123:4195–200. https://doi.org/10.1242/jcs.023820 .
doi: 10.1242/jcs.023820 pubmed: 21123617 pmcid: 2995612
Leppert PC, Baginski T, Prupas C, Catherino WH, Pletcher S, Segars JH. Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium. Fertil Steril. 2004;82:1182–7. https://doi.org/10.1016/j.fertnstert.2004.04.030 .
doi: 10.1016/j.fertnstert.2004.04.030 pubmed: 15474093 pmcid: 4137471
Belloni A, Furlani M, Greco S, Notarstefano V, Pro C, Randazzo B, Pellegrino P, Zannotti A, Carpini GD, Ciavattini A, Di Lillo F, Giorgini E, Giuliani A, Cinti S, Ciarmela P. Uterine leiomyoma as useful model to unveil morphometric and macromolecular collagen state and impairment in fibrotic diseases: an ex-vivo human study. Biochim Biophys Acta Mol Basis Dis. 2022;1868: 166494. https://doi.org/10.1016/j.bbadis.2022.166494 .
doi: 10.1016/j.bbadis.2022.166494 pubmed: 35850176
Gargiulo AW, Wentz FM, Orban B. Dimensions and relations of the dentogingival junction in humans. J Periodontol. 1961;32:261–7. https://doi.org/10.1902/jop.1961.32.3.261 .
doi: 10.1902/jop.1961.32.3.261
Watts T. Clinical periodontology and implant dentistry, 4th edition. Br Dent J. 2003;195:722–722. https://doi.org/10.1038/sj.bdj.4810851 .
doi: 10.1038/sj.bdj.4810851
Berglundh T, Lindhe J. Dimension of the periimplant mucosa. Biological width revisited. J Clin Periodontol. 1996;23:971–3.
doi: 10.1111/j.1600-051X.1996.tb00520.x pubmed: 8915028
Chavrier C, Couble ML, Hartmann DJ. Qualitative study of collagenous and noncollagenous glycoproteins of the human healthy keratinized mucosa surrounding implants. Clin Oral Implants Res. 1994;5:117–24. https://doi.org/10.1034/j.1600-0501.1994.050301.x .
doi: 10.1034/j.1600-0501.1994.050301.x pubmed: 7827225
Schwarz F, Derks J, Monje A, Wang H-L. Peri-implantitis. J Periodontol. 2018;89(Suppl 1):S267–90. https://doi.org/10.1002/JPER.16-0350 .
doi: 10.1002/JPER.16-0350 pubmed: 29926957
Ericsson I, Lindhe J. Probing depth at implants and teeth. An experimental study in the dog. J Clin Periodontol. 1993;20:623–7. https://doi.org/10.1111/j.1600-051x.1993.tb00706.x .
doi: 10.1111/j.1600-051x.1993.tb00706.x pubmed: 8227448
Fujii N, Kusakari H, Maeda T. A histological study on tissue responses to titanium implantation in rat maxilla: the process of epithelial regeneration and bone reaction. J Periodontol. 1998;69:485–95. https://doi.org/10.1902/jop.1998.69.4.485 .
doi: 10.1902/jop.1998.69.4.485 pubmed: 9609380
Iglhaut G, Schwarz F, Winter RR, Mihatovic I, Stimmelmayr M, Schliephake H. Epithelial attachment and downgrowth on dental implant abutments—a comprehensive review. J Esthet Restor Dent. 2014;26:324–31. https://doi.org/10.1111/jerd.12097 .
doi: 10.1111/jerd.12097 pubmed: 24612047
Gittens RA, Scheideler L, Rupp F, Hyzy SL, Geis-Gerstorfer J, Schwartz Z, Boyan BD. A review on the wettability of dental implant surfaces II: biological and clinical aspects. Acta Biomater. 2014;10:2907–18. https://doi.org/10.1016/j.actbio.2014.03.032 .
doi: 10.1016/j.actbio.2014.03.032 pubmed: 24709541 pmcid: 4103435
Ma Q, Wang W, Chu PK, Mei S, Ji K, Jin L, Zhang Y. Concentration- and time-dependent response of human gingival fibroblasts to fibroblast growth factor 2 immobilized on titanium dental implants. Int J Nanomed. 2012;7:1965–76. https://doi.org/10.2147/IJN.S29538 .
doi: 10.2147/IJN.S29538
Sugawara S, Maeno M, Lee C, Nagai S, Kim DM, Da Silva J, Nagai M, Kondo H. Establishment of epithelial attachment on titanium surface coated with platelet activating peptide. PLoS ONE. 2016;11: e0164693. https://doi.org/10.1371/journal.pone.0164693 .
doi: 10.1371/journal.pone.0164693 pubmed: 27741287 pmcid: 5065151
van Dijk IA, Beker AF, Jellema W, Nazmi K, Wu G, Wismeijer D, Krawczyk PM, Bolscher JGM, Veerman ECI, Stap J. Histatin 1 enhances cell adhesion to titanium in an implant integration model. J Dent Res. 2017;96:430–6. https://doi.org/10.1177/0022034516681761 .
doi: 10.1177/0022034516681761 pubmed: 27941125
Di Baldassarre A, Cimetta E, Bollini S, Gaggi G, Ghinassi B. Human-induced pluripotent stem cell technology and cardiomyocyte generation: progress and clinical applications. Cells. 2018;7:48. https://doi.org/10.3390/cells7060048 .
doi: 10.3390/cells7060048 pubmed: 29799480 pmcid: 6025241
Mangano C, Mangano FG, Shibli JA, Roth LA, D’Addazio G, Piattelli A, Iezzi G. Immunohistochemical evaluation of peri-implant soft tissues around machined and direct metal laser sintered (DMLS) healing abutments in humans. Int J Environ Res Public Health. 2018;15:1611. https://doi.org/10.3390/ijerph15081611 .
doi: 10.3390/ijerph15081611 pubmed: 30061523 pmcid: 6121298
Bächle M, Kohal RJ. A systematic review of the influence of different titanium surfaces on proliferation, differentiation and protein synthesis of osteoblast-like MG63 cells. Clin Oral Implants Res. 2004;15:683–92. https://doi.org/10.1111/j.1600-0501.2004.01054.x .
doi: 10.1111/j.1600-0501.2004.01054.x pubmed: 15533129
Di Giulio M, Traini T, Sinjari B, Nostro A, Caputi S, Cellini L. Porphyromonas gingivalis biofilm formation in different titanium surfaces, an in vitro study. Clin Oral Implants Res. 2016;27:918–25. https://doi.org/10.1111/clr.12659 .
doi: 10.1111/clr.12659 pubmed: 26249670
Sinjari B, Guarnieri S, Diomede F, Merciaro I, Mariggio MA, Caputi S, Trubiani O. Influence of titanium laser surface geometry on proliferation and on morphological features of human mandibular primary osteoblasts. J Biol Regul Homeost Agents. 2012;26:505–13.
pubmed: 23034270
Ghinassi B, Di Baldassarre A, D’Addazio G, Traini T, Andrisani M, Di Vincenzo G, Gaggi G, Piattelli M, Caputi S, Sinjari B. Gingival response to dental implant: comparison study on the effects of new nanopored laser-treated vs. traditional healing abutments. Int J Mol Sci. 2020;21:6056. https://doi.org/10.3390/ijms21176056 .
doi: 10.3390/ijms21176056 pubmed: 32842709 pmcid: 7504205
Ghinassi B, D’Addazio G, Di Baldassarre A, Femminella B, Di Vincenzo G, Piattelli M, Gaggi G, Sinjari B. Immunohistochemical results of soft tissues around a new implant healing-abutment surface: a human study. J Clin Med. 2020;9:1009. https://doi.org/10.3390/jcm9041009 .
doi: 10.3390/jcm9041009 pubmed: 32252463 pmcid: 7230724
Paraskevaidi M, Matthew BJ, Holly BJ, Hugh BJ, Thulya CPV, Loren C, StJohn C, Peter G, Callum G, Sergei KG, Kamila K, Maria K, Kássio LMG, Pierre M-HL, Evangelos P, Savithri P, John AA, Alexandra S, Marfran S, Josep S-S, Gunjan T, Michael W, Bayden W. Clinical applications of infrared and Raman spectroscopy in the fields of cancer and infectious diseases. Appl Spectrosc Rev. 2021;56:804–68. https://doi.org/10.1080/05704928.2021.1946076 .
doi: 10.1080/05704928.2021.1946076
Belloni A, Montanari E, Sagrati A, Lorenzi T, Balloni A, Busardò FP, Notarstefano V, Fabri M, Giorgini E. Novel insights from Fourier-transform infraRed imaging on the morpho-chemical profile of human corpus callosum. Appl Sci. 2023;13:3954. https://doi.org/10.3390/app13063954 .
doi: 10.3390/app13063954
Licini C, Notarstefano V, Marchi S, Cerqueni G, Ciapetti G, Vitale-Brovarone C, Giorgini E, Mattioli-Belmonte M. Altered type I collagen networking in osteoporotic human femoral head revealed by histomorphometric and Fourier transform infrared imaging correlated analyses. BioFactors Oxf Engl. 2022;48:1089–110. https://doi.org/10.1002/biof.1870 .
doi: 10.1002/biof.1870
Femminella B, Iaconi MC, Di Tullio M, Romano L, Sinjari B, D’Arcangelo C, De Ninis P, Paolantonio M. Clinical comparison of platelet-rich fibrin and a gelatin sponge in the management of palatal wounds after epithelialized free gingival graft harvest: a randomized clinical trial. J Periodontol. 2016;87:103–13. https://doi.org/10.1902/jop.2015.150198 .
doi: 10.1902/jop.2015.150198 pubmed: 26313017
Balan V, Mihai C-T, Cojocaru F-D, Uritu C-M, Dodi G, Botezat D, Gardikiotis I. Vibrational spectroscopy fingerprinting in medicine: from molecular to clinical practice. Materials. 2019;12:2884. https://doi.org/10.3390/ma12182884 .
doi: 10.3390/ma12182884 pubmed: 31489927 pmcid: 6766044
Belbachir K, Noreen R, Gouspillou G, Petibois C. Collagen types analysis and differentiation by FTIR spectroscopy. Anal Bioanal Chem. 2009;395:829–37. https://doi.org/10.1007/s00216-009-3019-y .
doi: 10.1007/s00216-009-3019-y pubmed: 19685340
Barnas E, Skret-Magierlo J, Skret A, Kaznowska E, Depciuch J, Szmuc K, Łach K, Krawczyk-Marć I, Cebulski J. Simultaneous FTIR and Raman spectroscopy in endometrial atypical hyperplasia and cancer. Int J Mol Sci. 2020;21:4828. https://doi.org/10.3390/ijms21144828 .
doi: 10.3390/ijms21144828 pubmed: 32650484 pmcid: 7402178
Stani C, Vaccari L, Mitri E, Birarda G. FTIR investigation of the secondary structure of type I collagen: new insight into the amide III band. Spectrochim Acta A Mol Biomol Spectrosc. 2020;229: 118006. https://doi.org/10.1016/j.saa.2019.118006 .
doi: 10.1016/j.saa.2019.118006 pubmed: 31927236
Covani U, Giammarinaro E, Di Pietro N, Boncompagni S, Rastelli G, Romasco T, Velasco-Ortega E, Jimenez-Guerra A, Iezzi G, Piattelli A, Marconcini S. Electron microscopy (EM) analysis of collagen fibers in the peri-implant soft tissues around two different abutments. J Funct Biomater. 2023;14:445. https://doi.org/10.3390/jfb14090445 .
doi: 10.3390/jfb14090445 pubmed: 37754859 pmcid: 10532031
Noreen R, Moenner M, Hwu Y, Petibois C. FTIR spectro-imaging of collagens for characterization and grading of gliomas. Biotechnol Adv. 2012;30:1432–46. https://doi.org/10.1016/j.biotechadv.2012.03.009 .
doi: 10.1016/j.biotechadv.2012.03.009 pubmed: 22484050
Talari ACS, Martinez MAG, Movasaghi Z, Rehman S, Rehman IU. Advances in Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl Spectrosc Rev. 2017;52:456–506. https://doi.org/10.1080/05704928.2016.1230863 .
doi: 10.1080/05704928.2016.1230863
Byler DM, Susi H. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers. 1986;25:469–87. https://doi.org/10.1002/bip.360250307 .
doi: 10.1002/bip.360250307 pubmed: 3697478
Cai S, Singh BR. Identification of beta-turn and random coil amide III infrared bands for secondary structure estimation of proteins. Biophys Chem. 1999;80:7–20. https://doi.org/10.1016/s0301-4622(99)00060-5 .
doi: 10.1016/s0301-4622(99)00060-5 pubmed: 10457593
Singh BR, DeOliveira D, Fu F-N, Fuller M. Fourier transform infrared analysis of amide III bands of proteins for the secondary structure estimation, SPIE 1890 (1993). https://doi.org/10.1117/12.145242 .
Comut AA, Weber HP, Shortkroff S, Cui FZ, Spector M. Connective tissue orientation around dental implants in a canine model. Clin Oral Implants Res. 2001;12:433–40. https://doi.org/10.1034/j.1600-0501.2001.120502.x .
doi: 10.1034/j.1600-0501.2001.120502.x pubmed: 11564102
Nothdurft FP, Fontana D, Ruppenthal S, May A, Aktas C, Mehraein Y, Lipp P, Kaestner L. Differential behavior of fibroblasts and epithelial cells on structured implant abutment materials: a comparison of materials and surface topographies. Clin Implant Dent Relat Res. 2015;17:1237–49. https://doi.org/10.1111/cid.12253 .
doi: 10.1111/cid.12253 pubmed: 25066589
Guarnieri R, Miccoli G, Reda R, Mazzoni A, Di Nardo D, Testarelli L. Laser microgrooved vs. machined healing abutment disconnection/reconnection: a comparative clinical, radiographical and biochemical study with split-mouth design. Int J Implant Dent. 2021;7:19. https://doi.org/10.1186/s40729-021-00301-6 .
doi: 10.1186/s40729-021-00301-6 pubmed: 33728493 pmcid: 7966690
Gulati K, Moon H-J, Kumar PTS, Han P, Ivanovski S. Anodized anisotropic titanium surfaces for enhanced guidance of gingival fibroblasts. Mater Sci Eng C Mater Biol Appl. 2020;112: 110860. https://doi.org/10.1016/j.msec.2020.110860 .
doi: 10.1016/j.msec.2020.110860 pubmed: 32409032
Myshin HL, Wiens JP. Factors affecting soft tissue around dental implants: a review of the literature. J Prosthet Dent. 2005;94:440–4. https://doi.org/10.1016/j.prosdent.2005.08.021 .
doi: 10.1016/j.prosdent.2005.08.021 pubmed: 16275304
Stern IB. Current concepts of the dentogingival junction: the epithelial and connective tissue attachments to the tooth. J Periodontol. 1981;52:465–76. https://doi.org/10.1902/jop.1981.52.9.465 .
doi: 10.1902/jop.1981.52.9.465 pubmed: 7026753
Linden GJ, Mullally BH, Freeman R. Stress and the progression of periodontal disease. J Clin Periodontol. 1996;23:675–80. https://doi.org/10.1111/j.1600-051x.1996.tb00593.x .
doi: 10.1111/j.1600-051x.1996.tb00593.x pubmed: 8841901
Lindhe J, Meyle J, on behalf of G.D. of the E.W. on Periodontology. Peri-implant diseases: consensus Report of the Sixth European Workshop on Periodontology. J Clin Periodontol. 2008;35:282–5. https://doi.org/10.1111/j.1600-051X.2008.01283.x .
doi: 10.1111/j.1600-051X.2008.01283.x pubmed: 18724855
Ivanovski S, Lee R. Comparison of peri-implant and periodontal marginal soft tissues in health and disease. Periodontol. 2018;2000(76):116–30. https://doi.org/10.1111/prd.12150 .
doi: 10.1111/prd.12150
Heitz-Mayfield LJA, Lang NP. Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontol. 2010;53:167–81. https://doi.org/10.1111/j.1600-0757.2010.00348.x .
doi: 10.1111/j.1600-0757.2010.00348.x
Chai WL, Moharamzadeh K, Brook IM, Van Noort R. A review of histomorphometric analysis techniques for assessing implant-soft tissue interface. Biotech Histochem. 2011;86:242–54. https://doi.org/10.3109/10520291003707916 .
doi: 10.3109/10520291003707916 pubmed: 20392135
Abrahamsson I, Zitzmann NU, Berglundh T, Linder E, Wennerberg A, Lindhe J. The mucosal attachment to titanium implants with different surface characteristics: an experimental study in dogs. J Clin Periodontol. 2002;29:448–55. https://doi.org/10.1034/j.1600-051x.2002.290510.x .
doi: 10.1034/j.1600-051x.2002.290510.x pubmed: 12060428
Kloss FR, Steinmüller-Nethl D, Stigler RG, Ennemoser T, Rasse M, Hächl O. In vivo investigation on connective tissue healing to polished surfaces with different surface wettability. Clin Oral Implants Res. 2011;22:699–705. https://doi.org/10.1111/j.1600-0501.2010.02038.x .
doi: 10.1111/j.1600-0501.2010.02038.x pubmed: 21087321
Albrektsson T, Canullo L, Cochran D, De Bruyn H. “Peri-Implantitis”: a complication of a foreign body or a man-made “disease”. Facts and fiction. Clin Implant Dent Relat Res. 2016;18:840–9. https://doi.org/10.1111/cid.12427 .
doi: 10.1111/cid.12427 pubmed: 27238274
Corvino E, Pesce P, Mura R, Marcano E, Canullo L. Influence of modified titanium abutment surface on peri-implant soft tissue behavior: a systematic review of in vitro studies. Int J Oral Maxillofac Implants. 2020;35:503–19. https://doi.org/10.11607/jomi.8110 .
doi: 10.11607/jomi.8110 pubmed: 32406646
Buehler MJ. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc Natl Acad Sci USA. 2006;103:12285–90. https://doi.org/10.1073/pnas.0603216103 .
doi: 10.1073/pnas.0603216103 pubmed: 16895989 pmcid: 1567872
Schierano G, Ramieri G, Cortese M, Aimetti M, Preti G. Organization of the connective tissue barrier around long-term loaded implant abutments in man. Clin Oral Implants Res. 2002;13:460–4. https://doi.org/10.1034/j.1600-0501.2002.130503.x .
doi: 10.1034/j.1600-0501.2002.130503.x pubmed: 12453121
Ruggeri A, Franchi M, Marini N, Trisi P, Piatelli A. Supracrestal circular collagen fiber network around osseointegrated nonsubmerged titanium implants. Clin Oral Implants Res. 1992;3:169–75. https://doi.org/10.1034/j.1600-0501.1992.030403.x .
doi: 10.1034/j.1600-0501.1992.030403.x pubmed: 1298431
Nevins M, Nevins ML, Camelo M, Boyesen JL, Kim DM. Human histologic evidence of a connective tissue attachment to a dental implant. Int J Periodontics Restorative Dent. 2008;28:111–21.
pubmed: 18546807
Geurs NC, Vassilopoulos PJ, Reddy MS. Histologic evidence of connective tissue integration on laser microgrooved abutments in humans. Clin Adv Periodontics. 2011;1:29–33. https://doi.org/10.1902/cap.2011.100005 .
doi: 10.1902/cap.2011.100005
Liu M, Zhou J, Yang Y, Zheng M, Yang J, Tan J. Surface modification of zirconia with polydopamine to enhance fibroblast response and decrease bacterial activity in vitro: a potential technique for soft tissue engineering applications. Colloids Surf B Biointerfaces. 2015;136:74–83. https://doi.org/10.1016/j.colsurfb.2015.06.047 .
doi: 10.1016/j.colsurfb.2015.06.047 pubmed: 26363269
Lindhe J, Berglundh T. The interface between the mucosa and the implant. Periodontol. 1998;2000(17):47–54. https://doi.org/10.1111/j.1600-0757.1998.tb00122.x .
doi: 10.1111/j.1600-0757.1998.tb00122.x
DeAngelo SJ, Kumar PS, Beck FM, Tatakis DN, Leblebicioglu B. Early soft tissue healing around one-stage dental implants: clinical and microbiologic parameters. J Periodontol. 2007;78:1878–86. https://doi.org/10.1902/jop.2007.070122 .
doi: 10.1902/jop.2007.070122 pubmed: 18062110

Auteurs

Alessia Belloni (A)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Giulio Argentieri (G)

Electron Microscopy Laboratory, Department of Innovative Technologies in Medicine and Dentistry, University "G. d'Annunzio" Chieti-Pescara, Chieti, Italy.

Giulia Orilisi (G)

Department of Clinical Sciences and Stomatology, Polytechnic University of Marche, Ancona, Italy.

Valentina Notarstefano (V)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Elisabetta Giorgini (E)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Gianmaria D'Addazio (G)

Electron Microscopy Laboratory, Department of Innovative Technologies in Medicine and Dentistry, University "G. d'Annunzio" Chieti-Pescara, Chieti, Italy.

Giovanna Orsini (G)

Department of Clinical Sciences and Stomatology, Polytechnic University of Marche, Ancona, Italy. g.orsini@staff.univpm.it.

Sergio Caputi (S)

Electron Microscopy Laboratory, Department of Innovative Technologies in Medicine and Dentistry, University "G. d'Annunzio" Chieti-Pescara, Chieti, Italy.

Bruna Sinjari (B)

Electron Microscopy Laboratory, Department of Innovative Technologies in Medicine and Dentistry, University "G. d'Annunzio" Chieti-Pescara, Chieti, Italy.

Classifications MeSH