38_Epithelial Attachment and Downgrowth on Dental Implant

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  • Epithelial Attachment and Downgrowth on Dental ImplantAbutmentsA Comprehensive ReviewGERHARD IGLHAUT, DDS*, FRANK SCHWARZ, DDS, PhD, ROBERT R. WINTER, DDS, ILJA MIHATOVIC, DDS,

    MICHAEL STIMMELMAYR, DDS, HENNING SCHLIEPHAKE, DDS, MD, PhD

    ABSTRACT

    The soft tissues around dental implants are enlarged compared with the gingiva because of the longer junctionalepithelium and the hemidesmosonal attachments are fewer, suggestive of a poorer quality attachment. Inflammatoryinfiltrates caused by bacterial colonization of the implant-abutment interface are thought to be one ofthe factors causing epithelial downgrowth and subsequent peri-implant bone loss. Gold alloys and dental ceramicsas well as the contamination of the implant surface with amino alcohols, appear to promote epithelialdowngrowth. Physical manipulaton of the abutment surfaces, including concave abutment designs, platform switching,and microgrooved surfaces are believed to inhibit epithelial downgrowth and minimizes bone loss at the implantshoulder. This paper reviews the factors that are believed to influence the migration of epithelial attachmentthe dental implant and abutment surfaces. Exploration of innovative computer-aided design/computer-aidedmanufacturing-based concepts such as one abutmentone time and their effect on epithelial downgrowth arediscussed.

    CLINICAL SIGNIFICANCE

    Based on the review of current literature, the authors recommend inserting definitive abutments at the time ofsurgical uncovering.To implement this concept, registration of the implant position should to be taken at the time ofsurgical implant placement.

    (J Esthet Restor Dent 26:324331, 2014)

    INTRODUCTION

    Clinical observations of patients without inammatoryconditions over several years showed that substantialperi-implant tissue loss may occur within no more than2 to 5 years post-prosthodontic rehabilitation and causeconsiderable esthetic compromise. Immediate implantplacement and prosthodontic rehabilitation oftenappear to be associated with esthetic problems.1 Thishas prompted a search for the factors of peri-implant

    tissue recession apparently unrelated to inammatoryprocesses and the conditions required to ensure stablelong-term results.

    The three-dimensional position of the implant appearsto be a critical factor for an acceptable estheticoutcome.2 Based on studies of the sagittal dimension,Evans and Chen3 recommend implant placement in amore palatal position. Implants oriented in a buccalposition were associated with three times more

    *Director, Oral Surgery Office, Bahnhofstrasse 20, 87700 Memmingen, GermanyAssociate Professor, Department of Oral Surgery, Heinrich-Heine University, Moorenstrasse 5, 40225 Dsseldorf, GermanyProsthodontist, Private Office, 9942 E Chiricahua Pass, Scottsdale, AZ 85262, USAOral Surgeon, Oral Surgery Office, Josef-Heiligbrunnerstrasse 2, 93413 Cham, GermanyHead, Department of Oral and Maxillofacial Surgery, George-Augusta-University Gttingen, Robert-Koch-Strasse 40, 37075 Gttingen, Germany

    REVIEWARTICLE

    DOI 10.1111/jerd.12097 2014 Wiley Periodicals, Inc.Vol 26 No 5 324331 2014 Journal of Esthetic and Restorative Dentistry324

  • soft-tissue recession than implants oriented in a palatalaspect (1.8 versus 0.6 mm). In the horizontal dimension,a distance of 1.5 to 2 mm from the roots of theneighboring teeth has been recommended.4 Thevertical position of the implant shoulder should beoriented to the buccal bone level of the neighboringteeth.5 The attachment levels associated withtwo-piece implants and standard abutment connectionscan be distinguished from abutment connections withplatform switching. This may be related to unfavorableeects of the microgap between the implant shoulderand the abutment.6 Thin soft-tissue structuresmay, however, lead to unpleasant grayish-lividdiscolorations.7

    What anatomical tissue dimensions are requiredfor an acceptable long-term esthetic outcome? Onestudy8 demonstrated that with a baseline bonethickness of 1.8 mm or more at the level of theimplant shoulder, there was no loss of bone afterhealing, and in some cases, there was a gain in bone.Comparing bone thickness of 1 and 2 mm at implantneck, Baone and colleagues9 failed in recent animalexperiments to detect any dierences in bone volumeafter a healing time of 3 months. Grunder andcolleagues2 claimed that the vestibular and approximalbone volume should be sucient to guarantee a circularbone thickness of 2 mm at the implant shoulder. Heconcluded that the proper implant diameter in theanterior region is normally limited to 4 mmor less.

    The soft-tissue volume also appears to be a factoraecting peri-implant tissue stability.10 Periodontal softtissues are considered as thin biotype if they are lessthan 1 mm, and thick biotype if they show a tissuethickness of 1.0 to 1.3 mm.11 Thin biotype tissue tendsto be associated with substantially more pronouncedrecession. This suggests the use of soft-tissue grafts12,13or combined soft-tissue/onlay grafts to gain tissuethickness.1416 The width of the attached gingiva isthought to be yet another factor determining tissuestability. Therefore, the maintenance or establishmentof a keratinized peri-implant mucosa to a width of3 mm or more has been recommended in severalstudies.1719

    SOFT-TISSUE INTERFACE AROUNDORAL IMPLANTS

    Gargiulo and colleagues20 showed in a human histologicstudy the average apicocoronal soft-tissue dimensionaround teeth, and consequently the soft-tissue cuabove the bone level, to have a mean width of 2.73 mm,with a mean epithelium portion of 1.66 mm, and amean connective tissue portion of 1.06 mm. In total theconnective tissue attachment and the epithelialattachment showed an average mean width of 2.04 mmand was described as biologic width. Vacek andcolleagues21 found similar dimensions of dentogingivaljunction. Thus, the epithelium is about 1 mm indistance to the alveolar bone. The attachment to theroot cementum possibly acts as a seal and may help toexclude microorganisms. The junctional epithelium ismechanically attached to the tooth surface (enamel androot cementum) by hemidesmosomes,22 whereas theconnective tissue is mechanically and chemicallyattached to the root cementum by perpendicularlyoriented collagen bers described as Sharpeys bers.23Measuring clinically the soft-tissue width between thebone margin and the gingival margin, Kois24 subdividedit in three biotypes: Based on clinical probing, hedescribed a buccal probing depth of approximately3 mm as normal crest type (85% of subjects), a probingdepth of 3.5 to 4 mm as low crest type (13% ofsubjects), and a probing depth of 2 to 2.5 mm as highcrest type (2% of subjects).

    In animal experiments,25 the peri-implant soft-tissuedimension was slightly enlarged (33.5 mm). A barrierepithelium facing the abutment surface showed a heightabout 2 mm followed by a connective tissue portion of1 to 1.5 mm above the alveolar bone crest, apparently indirect contact to the TiO2 layer of the implant. Acomparison of dierent implant systems did not showany variations.26 The barrier epithelium seems to beattached to titanium surfaces by hemidesmosomes23and provide a mucosal attachment. As there is no rootcement, connective tissue attachment to implantsdiers from that to natural teeth: Unlike comparednatural teeth, the collagen ber bundles are notperpendicularly arranged, but rather parallel to theimplant surface.25 Mechanical and chemical

    EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

    2014 Wiley Periodicals, Inc. DOI 10.1111/jerd.12097 Journal of Esthetic and Restorative Dentistry Vol 26 No 5 324331 2014 325

  • attachment to the titanium surface is absent.Instead, a proteoglycane layer the thickness of 20 mcould be shown. The connective tissue composition alsoshows dierences: Around natural teeth tissue iscomprised of approximately 60% collagen bers and 5to 15% broblasts, compared with 85% collagenbers and 1 to 3% broblasts around titanium implants.Thus, mucosal connective tissue resembles scar tissue.Blood vessels were shown less abundant in peri-implantsoft tissue. The vasculary blood supply to gingivalstructures is provided by large supraperiosteal bloodvessels and by the vascular plexus of the periodontalligament. The vascular system of the peri-implant softtissue is limited to the large supraperiosteal bloodvessel. Due to the lack of periodontal ligament, avascular plexus is missing at the interface of crestalbone and implant surface. This nding was supportedby Moon and colleagues.27 In a zone of 40 m close tothe titanium surface, the number of blood vessels wasextremely low (0.3%). As a result, immune responsesaround oral implants may be reduced.28 Schwarzand colleagues29 showed in a dog study, thatwell-vascularized subepithelial connective tissue coulddevelop around chemically modied, acid-etched aswell as chemically modied grit-blasted andacid-etched titanium surfaces. After 14 days of openhealing, collagen bers radial oriented to the implantsurface were histologically proved. Highly hydrophilicsurfaces appear to promote proper soft-tissueintegration.

    FACTORS AFFECTING EPITHELIALDOWNGROWTH

    Epithelial downgrowth on titanium surfaces isattributable to coronalapical proliferation andmigration of epithelial cells derived from the mucosasurrounding the wound surface forming a junctionalepithelium of a thickness of about 2 mm.30 Thepresence of granulation tissue in contact with thetransmucosal titanium surfaces is thought to be aprimary factor limiting apical epithelial migration.31Animal experiments conrmed the important roleconnective tissue plays in preventing epithelialdowngrowth.32,33 The location of the junctional

    epithelium appears to be determined by the initialphases of wound healing.34

    Results of animal studies demonstrate the inuence ofthe physical design of the implant systems on the heightof the junctional epithelium, i.e., two-part bone-levelversus single-part tissue-level implants, have variedwidely. Hermann and colleagues6 found signicantlymore apical epithelial migration around bone-levelimplants and postulated that the transmucosalabutmentimplant interface (microgap) was anegative factor explaining peri-implant bone loss. Thiscontrasts with several other studies documentingsoft-tissue adaptation at the abutment level.25,26,30,35However, inammatory cell inltrates were seen onlyaround bone-level implants; they were absent aroundtissue-level implants.35 The inltrates appear to becaused by bacterial colonization translocated from theoral cavity to the abutmentimplant interface.3639Harder and colleagues40,41 conrmed that endotoxinmicroleakage also occurred at conicalabutmentimplant connections and detectedlipopolysaccharide-mediated proinammatory cytokinegene expression. Endotoxins of gram-negative bacteriamay induce alveolar bone resorption via theosteoclast-activating pathway.42 These small moleculecomplexes of lipopolysaccharides and proteins canpenetrate small gaps and are known to play a major rolein bone destruction processes.

    Material properties appear to be another factoraecting epithelial downgrowth. Animal experimentsshowed a peri-implant cu of about 3.5 mm in width tobe present around abutments of pure titanium andAl2O3 ceramics. Around abutments of gold and goldalloys fused with dental ceramics, the soft-tissueattachment migrated toward the implant neck andassociated bone loss was noted.43 Kohal and colleagues44reported favorable soft-tissue formation on bothtitanium and ZrO2 surfaces. In a further animal study,the soft-tissue dimension at Ti and ZrO2 abutmentsremained stable after 5 months of healing. However, atgold/platinum alloys abutment sites, an apical shift ofthe barrier epithelium and marginal bone lostoccurred.45 In a 4-year prospective clinical study, Vigoloand colleagues46 evaluated abutments of titanium versus

    EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

    DOI 10.1111/jerd.12097 2014 Wiley Periodicals, Inc.Vol 26 No 5 324331 2014 Journal of Esthetic and Restorative Dentistry326

  • gold alloy when used with cemented single implantcrowns. Statistical analysis revealed no signicantdierences regarding peri-implant bone loss andsoft-tissue level. In a systematic review, Linkevicius andcolleagues47 evaluated available evidence for dierencesrelated to peri-implant tissue stability around titaniumabutments versus gold alloy, zirconium oxide, oraluminum oxide. The included studies failed to giveevidence that titanium abutments maintain a higherbone level in comparison with other materials.

    The negative eect of abutment surface contaminationand eective cleaning has also been discussed.48 In thiscontext, the removal of rmly adherent amino alcoholsappears to be a problem factor.49 Amino-alcoholsolution was supplied in vitro on machined titaniumsurfaces and four dierent methods were used toremove the adsorbed alcohol. Rinsing in water, salinesolution, and 5% H2O2 solution failed to remove theamino-alcohol; however, ozone exposure resulted incomplete removal of the alcohol from the titaniumsurface. Using an ultrasonic cleaning (Clemsonbioengineering cleaning [CBC]) protocol on bothtitanium and aluminum oxide surfaces removed anaverage 99.96% of contaminants.50 A further studyevaluated the eect of multiple sterilization on in vitrocell attachment on pure titanium surfaces.51 Ultravioletsterilized surfaces showed no changes related to cellattachment levels. In contrast, both ethylene oxide andsteam autoclave sterilization altered the titaniumsurface and decreased levels of cell attachment. In ananimal study, contaminated titanium abutments werecleaned ultrasonically in butanol and ethanol or onlyrinsed in saline solution, before being implanted in theabdominal wall of rats.52 New uncontaminated titaniumabutments were inserted as a control group.Irrespective of cleaning procedure, all contaminatedcomponents induced an altered tissue responsecompared to controls.

    Animal experiments and clinical studies conrmed theeect of the abutment design on epithelial downgrowth.Becker and colleagues53 showed the junctionalepithelium to end at the mismatch of the implantshoulder of tapered implants (platform switching,mismatch 0.30.5 mm). In another animal experiment,

    Farronato and colleagues54 found signicantly lessepithelial attachment and less peri-implant bone lossfor implants with platform switching than for thosewith standard abutmentimplant connections.Connective tissue adaptation by contrast, was of similarwidth. In a systematic review and meta-analysis,55implants with a mismatch of 0.4 mm were found to beassociated with less bone loss (mean 0.37 mm). Despitethe maintenance of the soft-tissue level, the clinicalrelevance appears in question.

    In an animal study, Schwarz and colleagues29demonstrated evidence that 14 days after soft-tissuehealing, perpendicularly oriented collagen bers couldbe promoted to high hydrophilic titanium surface.In a following study,56 however, the resistance toprobing was quite poor. Clinical probing more than twotimes increased mean-probing depth and markedlydisrupted the epithelial and connective tissueattachment. Nevins and colleagues57 examined theattachment of soft tissues to titanium surfacesmicrogrooved with a pulsed laser histologically andmicroscopically by polarized light and scanning electronmicroscopy. They showed evidence that after 6 monthsof healing, the soft tissue in humans was attachedmechanically by perpendicular collagen ber bundleson a microgrooved surface. In a clinical study up to

    FIGURE 1. Histologic specimen showing peri-implant softand hard tissues around a titanium abutment with a lasermicrogrooved surface.

    EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

    2014 Wiley Periodicals, Inc. DOI 10.1111/jerd.12097 Journal of Esthetic and Restorative Dentistry Vol 26 No 5 324331 2014 327

  • 37 months, Pecora and colleagues58 found a positiveeect on probing depth and maintenance ofperi-implant bone around implants with amicrostructured shoulder surface in contrast toimplants with machined surface. The high mechanicalstability of this attachment suggests the formation of asoft-tissue seal above the crestal bone.

    Kim and colleagues59 compared the eects of abutmentshapes relative with bone levels. They comparedconcave microgrooved transmucosal proles, convex

    machined proles, and straight anodically oxidizedproles of bone-level implants. Around convexmachined proles, the junctional epithelium was foundlonger, around concave microgrooved prolesconnective tissue attachment was more extended andthe bone-level stable. Two animal studies60,61 apparentlysupport positive eects of concave microgroovedabutment surfaces related to the maintenance ofperi-implant soft- and hard-tissue structures. In arecent animal study, Iglhaut and colleagues61 comparedsoft- and hard-tissue stability around abutments withmachined versus 0.8 mm microgrooved versus 2.8 mmmicrogrooved titanium surface. The author concludedthat the width of microgrooved abutment surfaces wasnegatively correlated to the extent of epithelialdowngrowth (Figures 1 and 2), and was positivelycorrelated to the extent of connective tissue attachmentand crestal bone level (Figure 3).

    Abutment dis/reconnection seems to have an importanteect on tissue-level maintenance adjacent to dentalimplants. In an animal study, Abrahamsson andcolleagues62 demonstrated apical epithelial downgrowthand peri-implant bone loss when abutments weredis/reconnection with alcohol disinfection ve times atmonthly intervals. Iglhaut and colleagues61 observed anegative eect even after two abutmentdis/reconnections (Figure 4). In contrast, Hermann andcolleagues63 found in a dog study no negative eect on

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    FIGURE 2. Comparative histomorphometric data of thejunctional epithelium around machined (M) and lasermicrogrooved surfaces with a width of 0.7 mm (LaserLokpartial [LP]) and 2.9 mm (LaserLok complete [LC]).

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    FIGURE 4. Soft-tissue attachment in percent to machined(M) and laser microgrooved surfaces with a width of 0.7 mm(LP) and 2.9 mm (LC) after two abutment reconnections.

    EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

    DOI 10.1111/jerd.12097 2014 Wiley Periodicals, Inc.Vol 26 No 5 324331 2014 Journal of Esthetic and Restorative Dentistry328

  • the peri-implant tissue after ve abutmentdis/reconnections without alcohol disinfection. In afurther animal study, Hermann and colleagues64described unfavorable eects of micromobile abutmentsindependent of the width of the microgap. Based onthese studies, tissue loss was hypothesized to beminimized by one-stage insertion of denitiveabutments and immediate prosthodontic rehabilitation(one abutmentone time concept). Clinical studies6365conrmed that this procedure seems to have a positiveeect on the maintenance of peri-implant soft and hardtissue. However, Canullo and colleagues66 mentionedthat the dierence of 0.2 mm might have a poor clinicaleect.

    Based on the review of current literature, the authorsrecommend inserting denitive abutments at the timeof surgical uncovering. To implement this concept,registration of the implant position should to be takenat the time of surgical implant placement.

    DISCLOSURE

    The authors have no nancial interest in any of thecompanies whose products were mentioned in thispaper.

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    Reprint requests: Gerhard Iglhaut, DDS, Oral Surgery Office,

    Bahnhofstrasse 20, 87700 Memmingen, Germany;Tel.: +498331-2864;Fax: +498331-44528; email: [email protected]

    EPITHELIAL ATTACHMENT AND DOWNGROWTH ON DENTAL IMPLANT ABUTMENTS Iglhaut et al.

    2014 Wiley Periodicals, Inc. DOI 10.1111/jerd.12097 Journal of Esthetic and Restorative Dentistry Vol 26 No 5 324331 2014 331

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