Nicola BALDINI Fabio VIGNOLETTI Biological width around implants · thÓ (Gargiulo etal. , 1961)....

Journal de Parodontologie & d’Implantologie Orale - Vol. 29 N°4

RÉSUMÉ

Les relations entre les tissus mous et la surface implantairereprésentent un défi considérable pour les fabricants d’im-plants si l’on considère les différents types de connexions,de cols implantaires et de plateformes qui existent. La pré-sence assez constante d’une hauteur d’attache conjonctivesur les implants dentaires, qui est semblable sous bien desaspects à la jonction dento-gingivale, a été bien documen-tée dans des études histologiques réalisées sur des modèlesanimaux. En se fondant sur des études histologiques simi-laires, on a pu évaluer l’influence de différentes variables,telles que la technique chirurgicale, le protocole chirurgical,la mise en charge de l’implant, la structure de l’implant, lessurfaces en titane et les matériaux composant les piliers, surl’espace biologique péri-implantaire. Le but de cette étudeest de faire le point sur ces questions.

MOTS CLÉSEspace biologique, implant, cicatrisation des tissus mous,épithélium de jonction, tissu conjonctif.

Biological width aroundimplantsHistological evidence: a reviewon animal studies

Espace biologiquepéri-implantaire

Preuves histologiques :revue d’études animales

ABSTRACT

Soft tissue relationship to implant surface is one of the mostchallenging area for implant manufacturers as it is evidentby different kind of connections, implant shoulders and plat-forms. The presence of a quite constant dimension of softtissue attachment to dental implants, similar for many fea-tures to dentogingival junction, has been well documentedin histological studies on animal models. Based on similarhistological studies, the influence of different variables, likethe surgical technique, the surgical protocol, implant loa-ding, implant structure, titanium surfaces and abutmentmaterials on peri-implant biological width has been evalua-ted. The aim of this study is to produce a review on thesetopics.

KEY WORDS

Biologic width, implant, soft tissues healing, junctional epi-thelium, connective tissue.

Massimo DE SANCTIS1

Nicola BALDINI2

Fabio VIGNOLETTI3

1- PhD, Department of odonto-stomatological sciences, Sienna University,Italy

2- DDS, Department of odonto-stomatological sciences, Sienna University,Italy

3- Madrid Complutense University, Spain

Accepted for publication:30 April 2010


Biological width around implants. Histological evidence: a review on animal studies

dentogingival junction, but there arealso obvious anatomical differenceslike the lack of periodontal ligamentand a different vascular distribution(Berglundh et al., 1991). Peri-implantbiological width has been studiedand measured in both histologicalanimal studies and clinical humanstudies.The aim of the present study is toproduce a review on the dimensionsof the peri-implant biological widthand to analyze the factors that maydetermine variations on biologicalwidth values.

Structureand biologicaldimensions

In the first animal studies ofBerglundh et al. in 1991, it was de-monstrated that the peri-implant mu-cosa established a cuff-like barrierwhich adhered to the surface of thetitanium abutment (Berghlund et al.,1991). The peri-implant tissue is ascar tissue that repairs the injury ofthe implant insertion: the soft tis-sues of the edentulous crest, oncerepositioned and sutured, participa-te to the formation of a “new” tissuethat protects the exposed bone andseals the emergence of the implant.As the gingiva, the peri-implant mu-cosa has a well-keratinized oral epi-thelium which is continuous with ajunctional epithelium that faces thetitanium surface.The structure of junctional epithe-lium is still matter of debate: a junc-tional epithelium similar to the junc-tional epithelium on teeth has beendocumented in a number of studiesfrom different authors (Abrahamssonet al., 1996, 1999, 2002; Berglundh

et al., 1991, 2007; Moon, 1999). Ina work on rats (Ikeda et al., 2000),the presence of a basal lamina andhemidesmosomes in peri-implantjunctional epithelium was confirmedalthough it was stated that the fin-ding of a basal lamina was less evi-dent than on the control tooth sites,and it was well detectable only inthe lower part of junctional epithe-lium.Results from a recent article byShioya et al. differ greatly by the workof Ikeda (Shioya et al., 2009): oneweek after implant insertion, peri-implant epithelium was observed,8 weeks after implant insertion, theperi-implant epithelium receded, andthe implant interface appeared to besealed by aligned special cells withsurrounding elongated fibroblastsand bundles of collagen fibers. Nohemidesmoses and no basal lami-na were found in this tissue. This fin-ding is in contrast with the previousscientific literature and opens newphases for further research.The most important difference bet-ween the two tissues is representedby the collagen fibers departing fromthe bone crest that are not insertedon the titanium surface and run pa-rallel to implant surface, following theimplant orientation (fig. 1 and 2). Fur-thermore according to Berglundhet al., experimental model, the col-lagen content of the peri-implant mu-cosa is higher, while the fibroblastdensity is much lower when compa-red to the gingival tissue (Berglundhet al., 1991).Another important observation wasthat all gingival and peri-implant unitsexamined were free from infiltratesof inflammatory cells. It was sug-gested that under the conditions ofthat study, both types of soft tissues,

Introduction

The large use of osteointegrated im-plants in modern dentistry and theincreasing esthetic demands for im-plant rehabilitations has focused at-tention on soft tissue reactions toimplant placement specially in thearea of soft tissue relationship to im-plant surface. Probably this is, at thepresent time, the most challengingarea for implant manufacturers as itis evident by different kind of connec-tions, implant shoulders and plat-forms. The transmucosal area consti-tutes an effective barrier betweenthe oral environment and the peri-implant bone and in many featuresit is similar to dentogingival junction.The morphology of dentogingivaljunction has been studied since 1959by Sicher, who found both an epi-thelial and a connective tissue at-tachment to the tooth (Sicher, 1959).In 1961, Gargiulo et al. measuredthe vertical dimension of this struc-ture and named it “biological wid-th” (Gargiulo et al., 1961). Biologicalwidth was composed by sulcus dep-th (SD), junctional epithelium (JE)and connective tissue attachment(CTA). The mean value was 2.73 mmand 2.04 mm for JE + CTA.These findings have been confirmedby Vacek in 1994: in this study, meanmeasurements were 1.34 ± 0.84 mmfor sulcus depth; 1.14 ± 0.49 mmfor epithelial attachment; 0.77± 0.32 mm for connective tissue at-tachment (Vacek et al., 1994). Au-thors emphasized that connectivetissue attachment has a variable wid-th within a more narrow distributionand range than the epithelial attach-ment and sulcus depth.Peri-implant tissues have many simi-larities with periodontal tissues and


the gingiva and the peri-implant mu-cosa, present a proper potential toprevent subgingival plaque forma-tion.Buser et al. investigated the soft tis-sue dimensions around three diffe-rent titanium surfaces, a rough sur-face, a sandplasted surface and a

polished surface (Buser et al., 1992).No significant difference concerningsoft tissue reactions were found bet-ween the three implant surfaces. Thesoft tissue barrier was composed bya sulcus with a non keratinizedsulcular epithelium, a junctional epi-thelium, and a supracrestal connec-

tive tissue with an area of dense cir-cular fibers near to the implant sur-face.Circular fibers were found in the in-ner zone of connective tissue, nextto the titanium surface; in theouter layer, horizontal and verticalfibers were found: these fibers were

M. DE SANCTIS, N. BALDINI, F. VIGNOLETTI

Fig. 1. a. Immediate implant (3i Osseotite Cer-tain, Biomet 3i, USA) and surrounding tissuesafter 8 weeks of healing. The keratinized oralepithelium continues with the junctional epi-thelium which is in intimate contact with thetitanium surface of the abutment. Toluidine bluestaining. Original augmentation 5X. b. Detail of(a). The connective tissue located immediatelybelow the epithelium is rich in collagen fibersand poor in cells.

Fig. 1. a. Implant à mise en charge immédiate(3i Osseotite Certain, Biomet 3i, États-Unis) ettissus environnants après 8 semaines de cicatri-sation. L’épithélium oral kératinisé est en conti-nuité avec l’épithélium de jonction qui est encontact intime avec la surface en titane du pilier.Coloration au bleu de toluidine. (grossissement× 5) b. Détail. Le tissu conjonctif situé immédia-tement en dessous de l’épithélium est riche enfibres de collagène et pauvre en cellules.

Fig. 2. Immediate implant (3i Osseotite Certain,Biomet 3i, USA) and surrounding tissues after8 weeks of healing. The supracrestal connectivetissue is cell rich in the area located close to theimplant. Collagen fibers extend from periosteumof the bone crest and run lateral to this areawith a direction that is parallel to the implant-abutment surface. Toluidine blue staining. Ori-ginal augmentation 2.5X.

Fig. 2. Implant à mise en charge immédiate (3iOsseotite Certain, Biomet 3i, États-Unis) et tis-sus environnants après 8 semaines de cicatrisa-tion. Le tissu conjonctif supracrestal est riche encellules dans la zone située à proximité de l’im-plant. Les fibres de collagène s’étendent du péri-oste de la crête osseuse et se dirigent latérale-ment par rapport à cette zone dans une directionqui est parallèle à la surface implant/pilier.Coloration au bleu de toluidine. Grossissement× 2,5.



cosa thin capillary loops were found,they were terminal branches of su-praperiosteal vessels with a diame-ter of 7-10 µm, similar to those ob-served in the periodontal tissues.Lateral to the junctional epitheliumat a distance of 50 µm, a crevicularplexus could be observed. In thearea of connective tissue two diffe-rent portions could be found: a cen-tral part 300-500 µm wide in intima-te contact with the implant-abutmentinterface that was poor of blood ves-sels with only few capillaries presentand a lateral part with larger vesselsoriginating from the supraperiostealarterioles.The existence of a central area poorof vessels have been well documen-ted by Moon et al. in an histologicalanimal experiment (Moon et al.,1999). Authors concluded that thejunctional epithelium was 2 mm longand 40 µm wide. Apical to the junc-tional epithelium the connective tis-sue portion (200 µm wide) presen-ted a 40 µm wide zone in closecontact to the titanium surface. Thiszone was characterized by the ab-sence of blood vessels, abundanceof fibroblasts oriented with their longaxis parallel to the implant surfaceand thin collagen fibers that exten-ded from the periosteum of the bonecrest parallel to the implant surface(Astra Tech Implants) (fig. 3).Laterally, an area with less fibro-blasts, greater collagen fibers andvascular structures could be eviden-ced. Connective attachment wascomposed by 80,61% collagen fi-bers, 12,98% fibroblasts, 3,42% vas-cular structures and 3,0% residualtissues. Authors concluded that dueto the presence of a fibroblast richlayer next to the implant surface theperi-implant connective tissue was

a tissue with a high turnover. Thesedata were in contrast with previousstudies that described the peri-implant tissue as scar-like tissue(Buser et al., 1992).Some authors have stressed the hy-pothesis of a connective tissue at-tachment to the implant surface. Fewexperiments and human biopsieshave demonstrated collagen fiberbundles functionally orientated andrunning in different directions(Schwarz et al., 2007; Nevins et al.,2008). The precise tridimensionalorientation of the collagen fibresin the periimplant mucosa havebeen described by Schierano et al.(Schierano et al., 2002) contrastingthis hypothesis.

running from the periosteum and thealveolar crest towards the oral epi-thelium. Authors reported that theorientation of the fibers differs inrough and smooth surfaces: smoo-th surfaces revealed an orientationof fibers parallel to the implant sur-face, while porous-coated surfacespromoted the formation of perpen-dicular fibers. The presence of thisfibers has been confirmed in a re-cent study of Shioya et al. (Shioyaet al., 2009). The overall tissue wasdescribed as “an inflammation freescar tissue”. The zone of dense col-lagen fibers was surrounded by alooser connective tissue with a 3-dimensional network of collagen fi-bers running in different directions.Berghlund et al. compared the vas-cular system of the periodontal andperi-implant tissues in the beagledog (Berglundh et al., 1994). In thetooth, blood vessels of the sub-epi-thelial oral plexus appeared as theywere terminal branches of the lar-ger supraperiosteal blood vessels.The density of the vascular units inthis plexus was increased in the mar-ginal portion of the free gingival tis-sue unit; there were capillary loopsprojected into the papillae with a dia-meter of 7-10 µm. The vasculatureof tissue portion lateral to the en-amel surface was located a few mi-crons from the basal cell layer of thejunctional epithelium and formed amesh of vascular units called crevi-clular plexus. The vessels of the su-pracrestal connective tissue, lateralto the root cementum, were foundto originate mainly from the vascu-lature of the periodontal ligamentwith a minor contribution from thelarger supraperiosteal vessels. Thetwo systems showed an anastomo-tic system. In the peri-implant mu-

Fig. 3. Densely packed connective tissue withabsence of blood vessels, abundance of fibro-blasts with thin collagen fibers. Fibroblast areoriented with their long axis parallel to implantsurface. Toluidine blue staining. Original aug-mentation 10X.

Fig. 3. Tissu conjonctif tassé de façon dense avecabsence de vaisseaux sanguins, abondance defibroblastes avec de fines fibres de collagène.Les fibroblastes sont orientés selon leur grandaxe parallèlement à la surface de l’implant. Colo-ration au bleu de toluidine. Grossissement × 10.


In 1996, Berglundh and Lindhe eva-luated in an animal study the biolo-gic width around implants (Bråne-mark Implant System) at sitesshowing a surgically created thinmucosa compared to control sitesdemonstrating a normal mucosa(Berglundh and Lindhe, 1996). Re-sults after 6 months of healing de-monstrated that the biological wid-th dimensions were rather similar:the junctional epithelium measuredapproximately 2.1 mm and 2.0 mmin the control and test groups, res-pectively; the corresponding valuesfor the connective tissue were 1.8and 1.3 mm. Interestingly the woundhealing processes at the test sitesincluded bone resorption and thusthe formation of an angular bone de-fects. The authors indicated the needof a minimum dimension of the bio-logical width in order to accommo-date the soft tissue healing process.Recently, Berglundh et al. describedin detail the morphogenesis of theperi-implant mucosa around tita-nium implants in dogs (ITI ImplantSystem) (Berglundh et al., 2007).Immediately after surgery (day 0) acoagulum occupied the space bet-ween the mucosa and implant sur-face and between the mucosa andthe alveolar process (fig. 4). At 4 daysof healing, the blood clot was infil-trated by numerous granulocytesand an initial mucosal seal was es-tablished by the clustering of leuko-cytes in a dense fibrin network. At1 week of healing, an area of leuko-cyte-infiltrated fibrin tissue was stillpresent, but it was smaller and lo-calized only close to the soft tissuemargin. The central part of the tis-sue was occupied by fibroblasts andcollagen fibers. At 2 weeks, the peri-implant mucosa adhered to the

implant surface through a connec-tive tissue that was rich in cells andvascular structures. First signs ofproliferation of junctional epitheliumcould be observed. At 4 weeks, thejunctional epithelium was comple-tely formed and in a more apical po-sition a mature connective tissuecould be observed. In later speci-mens (6-8 weeks), maturation of theconnective tissue with a dense layerof elongated fibroblasts at titaniuminterface was evident. Fibroblastswere situated between the collagenfibers which were oriented mainlyparallel to the titanium surface. From

a dimensional point of view, the bio-logic width increased during the hea-ling period (mainly between 1 and 2weeks) from 3.1 to 3.5 mm. Barrierepithelium extended to a positionabout 0.5 mm apical to the muco-sal margin, while at 4 weeks the dis-tance was 1.42 mm. At the end ofthe study (6-12 weeks), the barrierepithelium varied between 1.7 and2.1 mm.These findings corroborated pre-vious clinical results from a longitu-dinal study (Bengazi et al., 1996).Authors evaluated the alterations inthe position of the peri-implant soft


Fig. 4. a. Immediate implant (3i Osseotite Certain, Biomet 3i, USA) and surrounding tissues after4 hours of healing. A coagulum occupies the void between the implant surface and the socket wall.Toluidine blue staining. Original augmentation 2.5X. b. Detail of (a). Remnants of a junctional epi-thelium can be recognized. Toluidine blue staining. Original augmentation 5X.

Fig. 4. a. Implant à mise en charge immédiate (3i Osseotite Certain, Biomet 3i, États-Unis) et tissusenvironnants après 4 heures de cicatrisation. Un coagulum occupe l’espace entre la surface implan-taire et la paroi de l’alvéole. Coloration au bleu de toluidine. Grossissement × 2,5. b. Détail. On peutidentifier les restes d’un épithélium de jonction. Coloration au bleu de toluidine. Grossissement × 5.



Hermann et al. who compared non-loaded implants with loaded implants(ITI Implant System) at different timeintervals (3-12 months) and accor-ding to a submerged or non-sub-merged healing (Hermann et al.,2000). The study demonstrated thatthe dimension of the biological wid-th around non-submerged, one-pie-ce titanium dental implants was notdifferent whether the implants wereunloaded or loaded for a period of1 year. Nevertheless differences wereobserved in the dimensions of thecomponents of the biological width(sulcus depth, epithelial junction andconnective tissue) at the three dif-ferent healing intervals. Histometricmeasurements demonstrated thatalthough the biologic width dimen-sion remained constant over the15-month healing period, a decrea-se of the sulcus depth and connec-tive tissue contact were observedwhereas an increase of the junctio-nal epithelium occurred.Thereafter data from different au-thors support the conclusion that asimilar soft tissue dimensions is es-tablished regardless the use of asubmerged or a nonsubmerged ins-tallation technique.

Loading

The influence of loading on soft tis-sue healing around implants wasone of the topics most frequentlyinvestigated.Cochran et al. evaluated the dimen-sion of the implanto-gingival junc-tion around non submerged loadedand not loaded implants testing twodifferent surfaces (SLA and TPS) at3 and 12 months after implant pla-cement (Cochran et al., 1997). At3 months, the dimension of the

constituents of the biological widthin the unloaded group were 0.49 mmfor the sulcus depth (SD), 1.16 mmfor the junctional epithelium (JE), and1.36 mm for the connective tissuecomponent (CTC). The correspon-ding measurements in the loadedgroup were 0.50 mm for SD,1.44 mm for JE, and 1.01 mm forCTC for the loaded group. Resultswere similar after 12 months of loa-ding, confirming that the biologicalwidth around implants resemblesthe one present around teeth andthat the dimension of its constituentsare independent from the loadingvariable.Siar found similar results comparingimmediate versus delayed implantloading (Siar et al., 2003). The ove-rall mean value of the biologic width was 3.9 mm in the immedia-te group and 3.8 mm in the delayedgroup. They concluded that no sta-tistical differences were observed inthe dimensions and compositionsbetween the two groups.In a review of Glauser, it was conclu-ded that, on the basis of the fewavailable data, “once immediatelyloaded or loaded and restored im-plants integrate successfully, theyappear to show a soft-tissue reac-tion with regard to periodontal aswell as morphologic aspects com-parable with those of conventional-ly loaded implants” (Glauser et al.,2006).

Titanium surfacesand abutment materials

The reaction of cells and tissues toimplanted foreign bodies dependson the material’s properties andits behavior upon contact with thebody fluids. Abrahamsson et al.

tissue margin, during a 2-year per-iod follow-up. One hundred and six-ty-three Brånemark implants wereinserted into 41 patients that wereperiodonatlly evaluated and re-exa-mined after 6 months, 1 and 2 years.The results indicated an apical dis-placement of the soft tissue marginthat mainly occurred during the first6 months of observation. Lingualsites in the mandible showed themost pronounced soft tissue reces-sion, decrease of probing depth, anddecrease of width of masticatorymucosa. Authors suggested that therecession of the periimplant soft tis-sue margin could be the result of there-modelling of the soft tissue in or-der to establish the “appropriate bio-logical dimensions” of the peri-im-plant soft tissue barrier.

Factors that mayinfluence peri-implantbiologic width

Surgical technique

Abrahamsson et al. evaluated theinfluence of the surgical protocol (i.e.one stage versus two stage) on thesoft tissue healing around 3 diffe-rent implant systems (Astra Tech Im-plants, Brånemark and Bonefit-ITI)(Abrahamsson et al., 1996). The his-tological results demonstrated simi-lar dimension and composition ofthe epithelial and connective tissuecomponents.Ericsson et al. found similar soft tis-sue adaptation and proper osseoin-tegration in Brånemark implants ins-talled according to a 1-stage orto a 2-stage surgical procedure(Ericsson et al., 1996). These fin-dings were further confirmed by


demonstrated that surface charac-teristics (smooth vs rough titaniumsurfaces) do not influence the bio-logical width dimension (3i ImplantSystem) (Abrahamsson et al., 2002).More recently, new titanium surfaceshave been indicated to determine abetter quality of peri-implant soft tis-sues relationship (Rossi et al., 2008)(ITI Implant System). Glauser et al.demonstrated in a histological stu-dy that the dimension of the biolo-gic width (range 4-4.5 mm) in hu-mans are similar to values found onanimal models and that the softtissue formed to oxidized andacid etched implants showed a mi-nor epithelial down-growth and lon-ger connective tissue seal whencompared to machined implants(Glauser et al., 2005).In two different works, it has beendemonstrated that abutment mate-rials influenced the histologicaloutcome on biologic width dimen-sions and in particular, titanium andzirconia abutments seemed toproduce better histological resultsthan gold and platinum abutments(Welander et al., 2008; Abrahamssonet al., 1998). Nevertheless, these fin-dings were not consistent with a la-ter study from the same group(Abrahamsson et Cardaropoli, 2007)that reported that the peri-implantsoft tissue dimensions were not in-fluenced by the use of titanium orgold alloy in the marginal zone of theimplant. Kohal et al. further investi-gated the influence of zirconia andtitanium abutments on soft tissuehealing and demonstrated no signi-ficant differences (Kohal et al., 2004).In a review article by Rompen et al.,it was concluded that titanium wasthe only material that demonstratedsoft tissue biocompatibility; zirco-

nium and aluminum oxide showedfavorable histological outcomeswhereas dental porcelain and goldwere less biocompatible and it wassuggested to avoid them (Rompenet al., 2006).

Implant structureand position

Implant structure may differ betweenvarious implant systems: one pieceimplants present a transmucosal partin continuity with the endosseouspart, whereas two piece implantspresent an interface between the im-plant (endosseous component) andthe abutment (transmucosal com-ponent), resulting in a microgap bet-ween the two components (fig. 5to 7).Abrahamsson et al. evaluated theinfluence of three different implantsystems on the biological width(Astra Tech Implants, Brånemarkand Bonefit-ITI) in beagle dogs(Abrahamsson et al., 1996). The au-thors compared a one-piece implant(Bonefit) versus two two-piece im-plants (Astra Techand Brånemark).The histological results demonstra-ted similar dimension and compo-sition of the epithelial and connec-tive tissue components at the endof the study.Abrahamsson et al. further investi-gated the influence of the abutmentdis/reconnection on the marginalperi-implant tissues (BrånemarkSystem) (Abrahamsson et al., 1997).The authors observed that abutmentmanipulation compromised the mu-cosal barrier and induced an apicalmigration of the connective tissue.Thus, while normal proportions anddimensions of the hard and soft tis-sues were observed in the control

group, at test sites the abutment ma-nipulation resulted in a mechanicalinjury to the soft tissue barrier thathad to reestablish more apically, cau-sing a marginal bone resorption(1.5 mm).In contrast, a single abutmentreconnection proved to induce nomarginal bone remodeling (AstraTech Implant System) resulting ina transmucosal attachment ofadequate quality and dimensions(Abrahamsson et al., 2003).Hermann et al. further tested the hy-pothesis of a different biologic wid-th between 1-piece and 2-piece im-plants (Hermann et al., 2001).Authors reported that dimensions ofthe peri-implant soft tissues, as eva-luated by histometric measurements,were significantly influenced by thepresence/absence of a microgap (in-terface) between the implant and theabutment, and the location of mi-crogap (interface) in relation to thecrest of the bone.Hermann et al. evaluated in an ani-mal study (5 dogs, 59 ITI Implants)six different clinical situations: non-submerged one-piece implants withrough-smooth border placed at bonecrest (group A), non-submerged one-piece implants with rough-smoothborder placed 1 mm below crest(group B), non-submerged two-pie-ce implants with a microgap placedat bone crest (group C), submergedtwo-piece implants with microgapplaced at bone crest (group D), two-piece implants with the microgapplaced above the bone crest(group E), two-piece implants withthe microgap placed below the bonecrest (group F) (Hermann et al., 1997).Authors concluded that one-piece,non submerged implants with arough/smooth border placed at the




Fig. 5. Implant into fresh extraction socket. Two-piece implant (Astra Micro Thread, Osseospeed,Astra Tech, Sweden) with surrounding tissues.Biological width after 6 weeks of healing. Notethe inflammation free connective tissue in inti-mate contact with the implant-abutment inter-face. Levai-Laczko staining. Original augmenta-tion 5X.

Fig. 5. Implant dans une alvéole d’extractionfraîche. Implant en deux parties (Astra MicroThread, Osseospeed, Astra Tech, Suède) avec lestissus environnants. Espace biologique après6 semaines de cicatrisation. Noter l’absence d’in-flammation du tissu conjonctif en contact intimeavec l’interface implant/pilier. Coloration deLevai-Laczko. Grossissement × 5.

Fig. 7. Implant into fresh extraction socket.One-piece implant (Straumann StandardPlus, AG, Switzerland) with surroundingtissues. Biological width after 6 weeks ofhealing. PM : marginal mucosaa.JE : most apical junctional epitheliumB : most coronal bone to implant contactLevai-Laczko staining. Original augmenta-tion 2.5X.

Fig. 7. Implant dans une alvéole d’extrac-tion fraîche. Implant monobloc (StraumannStandard Plus, AG, Suisse) avec les tissus envi-ronnants. Espace biologique après6 semaines de cicatrisation. PM : muqueuse marginaleaJE : épithélium de jonction le plus apicalB : os le plus coronaire au contact de l’im-plantColoration de Levai-Laczko. Grossissement× 2,5.

Fig. 6. Implant into fresh extraction socket.Two-piece implant (Thommen SPI Element,Thommen Medical AG, Switzerland) withsurrounding tissues. Biological width after6 weeks of healing. PM : marginal mucosaaJE : most apical junctional epitheliumB : most coronal bone to implant contactLevai-Laczko staining. Original augmenta-tion 2.5X.

Fig. 6. mplant dans une alvéole d’extractionfraîche. Implant en deux parties (ThommenSPI Element, Thommen Medical AG, Suisse)avec les tissus environnants. Espace biolo-gique après 6 semaines de cicatrisation. PM :muqueuse marginale. aJE : épithélium de jonction le plus apical.B : os le plus coronaire au contact de l’im-plant.Coloration de Levai-Laczko. Grossissement× 2,5.


alveolar crest (group A) presentedthe smallest value of soft tissuesdimension at the end of the study.The apical displacement of therough/smooth border of the implant(type B) resulted in a wider biologicwidth (average increase of 0.73 mm).This change occurred through bothan increase of the junctional epithe-lium (average 0.41 mm) and ofconnective tissue dimension (ave-rage 0.34 mm). Furthermore, the au-thors observed the negative influen-ce of the microgap on the histologicaloutcome evidenced by higher softtissues dimensions as well as an in-crease in bone resorption. Authorsspeculated that this finding was pro-bably due to a bacterical coloniza-tion as indicated by previous reports(Persson et al., 1996; Quirynen et al.,1993), or to abutment micromove-ments (King et al., 2002).Todescan et al. investigated the in-fluence of the implant shoulder po-sition on the soft tissue healing(Todescan et al., 2002). The authorsplaced 24 implants (BrånemarkSystem) in the mongrel dog and di-vided the implants into three groups:group 1, implants remained 1 mmabove the bone crest, group 2, theimplant shoulder was placed at thelevel of the bone crest and group 3,implants remained 1 mm below thebone crest. In group 2 and 3, a coun-tersink bur was used. The junctio-nal epithelium showed a mean va-lue of 1.67 mm in group 1, 1.93 mmin group 2 and 2.78 mm in group 3.The corresponding values for theband of connective tissue were1.13 mm, 0.92 mm and 1.60 mm,respectively. Differences betweenthe groups were not statistically dif-ferent, except for group 2 versusgroup 3. The authors demonstrated

a tendency towards longer junctio-nal epithelium and connective tis-sue component the deeper the im-plants were placed.Pontes reported in a study in themongrel dogs on 2-piece implants(Conexao System) positioned at bonelevel, 1 and 2 mm below the bonecrest (Pontes et al., 2008). Implantswere further divided in two groups:immediate loading (24 hours, nonocclusal contact) and conventionalloading (30 days after second stagesurgery). Animals were killed for his-tological analysis after 3 months ofnon-submerged healing. Findingsfrom this study are partially consis-tent with Todescan et al. (Todescanet al., 2002) demonstrating a tenden-cy towards a longer connective tis-sue component the deeper the po-sition of the implant, whereas thelength of the junctional epitheliumresulted to be independent of the im-plant position. The effect of the loa-ding did not demonstrate any influen-ce on the soft tissue healing.Recently, Lazzara and Porter intro-duced the platform switching tech-nique represented by a non mat-ching implant/abutment interface(Lazzara and Porter, 2006). They ela-borated the concept on the basis ofa 13 years follow-up case series. Im-plants that presented non-matchingabutments (i.e. the implant platformwas wider than the abutment) sho-wed limited marginal bone resorp-tion when compared with normalimplants covered by matching abut-ments. Authors speculated that thesoft tissue healing around a non mat-ching abutment might exploit a ho-rizontal direction and utilize the spa-ce available between the implantshoulder and the abutment for theestablishment of the biological wid-

th. This hypothesis would justify aless marginal bone loss apical to im-plant-abutment interface.Recently, Luongo et al. reported onthe soft tissues response to the plat-form switching technique (Luongoet al., 2008). Authors observed in ahuman biopsy of one implant thatthe inflammatory connective tissueinfiltrate measured about 0.35 mmapical and coronal to the implant-abutment interface. This finding isnot consistent with data reported byEricsson et al. (Ericsson et al., 1996)who demonstrated in an experimen-tal study in dogs the presence of aninflammatory connective tissue infil-trate that measured approximately0.75 mm apical and coronal to theinterface. The smaller inflamma-tory reaction observed with the plat-form switching technique (Luongoet al., 2008) may in part justify the li-mited marginal bone loss observedby Lazzara and Porter (Lazzara andPorter, 2006).In conclusion, the type of implant (i.e.one- or two-piece implants) and thesurgical procedure (i.e. one- or two-stage surgical protocol) do no in-fluence the dimensions and compo-sition of the biological width.Nevertheless, limited data are avai-lable on the influence of the positionof the implant shoulder in relation tothe bone crest. It may be suggestedthat the deeper the implant shoulderposition the longer the biological wid-th. The clinical consequences of suchhistological findings are still unknown.

Immediate post-extractiveinsertion

In the past two decades, the imme-diate implant placement protocolhas been introduced into clinical




the lingual sites whereas at 3 monthsthe corresponding values were4.2 ± 0.8 mm and 2.7 ± 0.2 mmrespectively. As previously reported,the difference was due to the dimen-sions of the connective tissue thatreached 1.9 ± 0.6 mm and 0.6 ±0.2 mm at the buccal and lingualsites after 3 months of healing.Nevertheless, other experimentalstudies that have compared healingat implants placed in a healed rid-ge and implants immediately placedin fresh extraction sockets have re-ported, at 8 months, a larger dimen-sion of the soft tissue barrier in im-plants placed immediately (Schultes

and Gaggl, 2001). Similar resultswere reported in a recent experimen-tal study in the minipig model(Rimondini et al., 2005). They eva-luated the epithelial dimensions af-ter placing implants in fresh extrac-tion sockets in minipigs and reportedthat the epithelial length was3.02 mm 30 days after implant ins-tallation and then remained stableup to 60 days (fig. 8 to 10).In a recent study, Vignoletti descri-bed the differences in the healingof the soft tissue barrier when pla-cing four different implant systemsimmediately in fresh extraction soc-kets (3i Implant System, Astra Tech

practice, while most of the studieson biological width on animal mo-dels have been conducted on hea-led ridge models. It may be specu-lated that the surgical protocol ofplacing an implant immediately upontooth extraction may influence theformation and maturation of the bio-logical width.Araùjo et al. investigated in thebeagle dog the healing of implants(Straumann Implant System) placedinto the distal sockets of third andfourth mandibular premolars (Araùjoet al., 2005). Findings from this ex-periment demonstrated that the di-mensions and composition of the mu-cosal seal around immediate implantswere similar to those around stan-dard implants (Berglundh et al., 1991).The histometrical analysis only sho-wed a different dimension of the softtissue barrier when comparing buc-cal and lingual sites. The overalldimensions of the biological widthafter 3 months of healing was 3.9 ±0.5 mm and 2.6 ± 0.4 mm, at thebuccal and lingual aspect, respecti-vely. The difference between buccaland lingual dimensions was due tothe connective tissue component thatwas 1.8 ± 0.8 mm and 0.7 ± 0.2 mmon the buccal and lingual aspects,respectively. This difference could bein part explained by a greater margi-nal bone loss observed on the buc-cal aspect of the implants that cor-responded to 2.6 ± 0.4 mm.These differences were confirmedby another study from the same la-boratory (Araùjo et al., 2006) that uti-lized a similar experimental modelwith different time intervals. At1 month of healing the distance fromthe mucosal margin to the first bone-implant contact varied from 3.3 mmat the buccal sites and 3.5 mm at

Fig. 8. a. Implant into fresh extraction sockets. Two-piece implant (3i Osseotite Certain, Biomet 3i,USA). Biological width formation at 1 week of healing. A junctional epithelium can be clearly detec-ted. Toluidine blue staining. Original augmentation 2.5X. b. Detail of (a). The connective tissueimmediately apical of the junctional epithelium is rich in inflammatory cells. Toluidine blue staining.Original augmentation 5X.

Fig. 8. a. Implant dans une alvéole d’extraction fraîche. Implant en deux parties (3i Osseotite Cer-tain, Biomet 3i, États-Unis). Formation d’un espace biologique au bout de 1 semaine de cicatrisa-tion. Un épithélium de jonction peut être clairement détecté. Coloration au bleu de toluidine. Gros-sissement × 2,5. b. Détail. Le tissu conjonctif situé immédiatement apicalement à l’épithélium dejonction est riche en cellules inflammatoires. Coloration au bleu de toluidine. Grossissement × 5.


Implants, Thommen Implant Sys-tem, ITI Implant System) (Vignolettiet al., 2009). The biological width6 weeks after implant placementaveraged between 3.5-4.1 mm and

2.8-3.2 mm at the buccal and lin-gual aspects, respectively. On thebuccal aspect the soft tissues bar-rier was comprised of a junctionalepithelium that measured between2-2.7 mm and a connective tissuethat ranged between 1-1.8 mm. Thecorresponding values at the lingualside were 1.6-2 mm of epitheliumand 0.9-1.4 mm of connective tis-sue. The study failed to demonstra-te differences in the healing patternwhen placing four different implantsystems in fresh extraction sockets.Nevertheless, the obtained lengthof the epithelium with the four im-plant systems is longer than whathas been reported when placing im-plants in healed-ridge experimentalmodels.


Fig. 9. Implant into fresh extraction sockets. Two-piece implant (3i Osseotite Certain, Biomet 3i,USA). Biological width formation at 2 weeks ofhealing. A gap is present between the implantshoulder and the abutment. Proliferation of thejunctional epithelium can be detected at theimplant-abutment interface. Toluidine blue stai-ning. Original augmentation 2.5X.

Fig. 9. Implant dans une alvéole d’extractionfraîche. Implant en deux parties (3i OsseotiteCertain, Biomet 3i, États-Unis). Formation d’unespace biologique au bout de 2 semaines de cica-trisation. Il existe un hiatus entre l’épaulementde l’implant et le pilier. La prolifération de l’épi-thélium de jonction peut être détectée à l’inter-face implant/pilier. Coloration au bleu de tolui-dine. Grossissement × 2,5.

Fig. 10. Implant into fresh extraction sockets. a. Two-piece implant (3i Osseotite Certain, Biomet 3i, USA). Biological width formation at 4 weeks of hea-ling. Note the mature connective tissue. b. Detail of (a). No inflammatory cells can be detected at the implant-abutment interface.

Fig. 10. Implant dans une alvéole d’extraction fraîche. a. Implant en deux parties (3i Osseotite Certain, Biomet 3i, États-Unis). Formation d’un espacebiologique au bout de 4 semaines de cicatrisation. Noter le tissu conjonctif mature. b. Détail. Aucune cellule inflammatoire ne peut être détectée àl’interface implant/pilier.



described around teeth. This dimen-sion has been described as “peri-implant biologic width”: This is com-posed by the dimension of thesulcus, and by the supra-crestal epi-thelial and connective tissue com-ponent.Most studies report bigger valuesfor peri-implant biologic width thanthe ones reported for periodontalbiologic width. The difference is ge-nerally related to a bigger epithelialcomponent at implant sites whencompared to the tooth.A minimum dimension of the biolo-gical width is needed in order to ac-commodate for the soft tissue hea-ling process: when this dimensionis not present, bone resorption mayoccur, to allow for an “appropriatebiological dimension” of the peri-im-plant soft tissue barrier.The influence of five different fac-tors on peri-implant biologic widthdimensions has been evaluated re-viewing the available literature, the-se are: surgical technique, loadingtime, titanium surfaces and abut-ment materials, implant structureand position, immediate post-extra-ctive insertion.Surgical technique, one-stage ortwo-stage surgery and loading time,both immediate or delayed, do notinfluence the dimensions of the softtissue barrier around the implants.More controversial is the issue of theinfluence of titanium surfaces andabutment materials.Titanium is the only material that de-monstrated soft tissue biocompati-bility, zirconium and aluminum oxidehave showed favorable histologicaloutcomes whereas dental porcelainand gold were less biocompatible.There is no agreement in literatureon the influence of titanium surface,

in fact while there are studies indi-cating a smaller dimension of thebiologic width in smooth surfacesnevertheless while other studies sug-gest that these differences are notpresent.Further research is needed to allowfor a conclusion.The type of implant (i.e. one- or two-piece implants) and the surgical pro-cedure (i.e. one- or two-stage sur-gical protocol) do not influence thedimensions and composition of thebiological width. Nevertheless limi-ted data are available on the influen-ce of the position of the implantshoulder in relation to the bone crest.It may be suggested that the dee-per the implant shoulder position is,the longer the biological width.Microgap between implant and abut-ment when present can modify thedimension of biologic width, the lon-ger epithelial component describedmay be determined by bacterial co-lonization or abutments micro mo-vements.The clinical consequences of suchhistological findings are still unk-nown.Contradictory data are present ondimension of the biological widthwhen an immediate postextractiveapproach is utilized: differences bet-ween buccal and lingual sites havebeen documented, demonstratinga bigger biologic width in buccalsites of immediately placed implants.This difference is related to a biggerconnective component in buccalsites.The limited experimental evidenceavailable seems to indicate a ten-dency towards larger dimensions ofthe mucosal seal around implantsplaced according to this surgical pro-tocol. !

In conclusion, contradictory data areavailable on the influence of placingimplants immediately upon tooth ex-traction on the biological width. Thelimited experimental evidence avai-lable seem to indicate a tendency to-wards higher dimensions of the mu-cosal seal around implants placedaccording to this surgical protocol.

Conclusion

The structure of peri-implant muco-sa has many similarities with perio-dontal tissues. The soft tissue bar-rier is composed by a sulcus with anon keratinized sulcular epithelium,a junctional epithelium, and a supra-crestal connective tissue with anarea of dense circular fibers near tothe implant surface. The presenceof a junctional epithelium facing thetitanium surface, similar to the onearound teeth, has been evidencedby a large number of studies.Nevertheless recent ultrastructuralstudies on rats models have failedto demonstrate the presence of a“true” junctional epithelium, becau-se of the absence of the basal lami-na and of the hemidesmosomes inthe samples 8 weeks after implantinsertion. Further researches are nee-ded to clarify these issues.Connective fibers orientation repre-sents the most important differen-ce between periodontal and peri-implant tissues that is while in theperiodontal structure, fibers run per-pendicular the long axis of the too-th, in perimplant tissue, the fibersfrom the bone crest run parallel tothe implant surface.The dimension the soft tissue bar-rier around implant seems to beconstant, similarly to what has been



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