/ Clin Periodontal 1996: 23: 971-973Printed iti Denmark . Alt rights' reserve

Copyright C Munksgaard l'>96

!SS\ 0303-6979

Dimension of the periimplantmucosaBiological width revisited

Short CommunicationT. Berglundh and J. LindheDepartment of Periodontology, GoteborgUniversity, Sweden

Berglundh T. Lindhe J: Dimension of the periimplant mucosa. Biological widthrevisited. J Ctin Periodontol 1996: 23: 971-973. © Munksgaard, 1996.

Abstract. The objective of the present study was to determine the dimension ofthe mucosal-impiant attachment at sites with insufficient width of the ridge mu-cosa, 5 beagle dogs were used. Extractions of ail mandibuiar premoiars wereperformed and 3 months later, 3 fixtures of the Branemark System® were in-stalled in each side. Foiiowing 3 months of healing, abutment connection wascarried out. On the right or ieft side of Ihe mandibie, abutment connection wasperformed according to the Branemark System® manual ~ (control side). On thecontralateral side (test side), an incision not extending through the periosteumwas made at the crest of the ridge. The soft tissue was dissected and a criticalamount of connective tissue on the inside of the flap was excised. The periosteumwas subsequently incised, abutment connection performed, and the trimmed flapssutured. The sutures were removed after 10 days. After a 6-month period of plaquecontroi, the animals were sacrificed, biopsies sampled and processed for lightmicroscopy. The length of the junctional epitheiium varied within a rather narrow-range; 2.i mm (control side) and 2.0 mm (test side). The height of the suprabonyconnective tissue in this model varied between 1.3i0.3 mm (test side) andl,8±0,4 mm (control side). At sites where the ridge mucosa prior to abutmentconnection was made thin (S2 mm), wound heaiing consistentiy inciuded boneresorption. This implies that a certain minimum width of the periimplant mucosamay be required, and that bone resorption may take place to allow a stable softtissue attachment to form.

Key words: periiimplant mucosa; attachment;histometry; bioiogical width

Accepted for publication 4 January 1996

In a series of studies from our laboratorythe structure and function of the kera-tinized, non-mobile gingiva and the cor-responding periimplant mucosa wereexamined in the beagle dog modei (Ber-glundh et al. 1991, 1992, 1994, Ericssonet al. 1992), The 2 tissues were found tohave many features in common. Thus,both soft tissues included a junctionaiepithelium that was about 2 mm in "ap-ico-coronal" direction and was separ-ated from the bone crest by a zone ofconnective tissue attachment > i mmhigh. The fibers within the supraaiveolartissue at the tooth site originated fromthe aceliular, extrinsic fiber cementumon the root surface, while the majority ofthe fibers at the iinpla.nt sites occurred in

an avascular compartment and were ap-parently anchored in the periosteum ofthe bone crest. In a recent experiment inthe dog (Abrahamsson et a], 1996), itwas observed that the mucosal barrierthat formed following successful 1- and2- stage implant installations had similarcomposition, i.e. it was comprised of onezone of junctional epithelium and onezone of connective tissue. Furthermore,it was detected that at sites where themucosa of the edentuious ridge was thin,(i) angular bone defects occurred at themarginal border of the implants, and (ii)the dimension of the mucosal attach-ment to the implant was similar to thatof sites with a thick mucosa. This featureof the implant - tissue interface was

characteristic for both 1- and 2- stageimplant systems. Abrahamsson et ai.(1996) suggested that a certain width ofthe periimpiant mucosa is required toenable a proper epithelial-connectivetissue attachment, and if this soft tissuedimension is not satisfied, "bone resorp-tion will occur to ensure" the establish-ment of attachment with a appropriate"biological width"". The objective of thepresent study was to further test thishypothesis.

Material and Methods

5 beagle dogs, about 1 year oid, wereused. Extractions of all mandibular pre-

972 Berglundh & Lindhe

molars were performed. After 3 monthsof healing, fixtures of the BrftnemarkSystem* (length: 7 mm, 0: 3,75 mm;Npbelpharma AB, Goteborg, Sweden)were installed according to methods de-scribed by Berglundh et al, (1991), Eaehanimal was fitted with 3 implants oneach side of the mandible; in all 6 im-plants. Following a healing period of 3months, abutment connection was car-ried out. On the right or the left side ofthe mandible, muco-periostal flaps wereelevated, and abutment connection per-formed according to he Br4nemarkSystem* manual - (control side). Theflaps were sutured. On the contralateralside (test side), an incision not ex-tending through the periosteum wasmade at the crest of the ridge. Using ablunt elevator, the soft tissue was dis-sected, and in order to obtain a thinridge mucosa, a critical amount of con-nective tissue on the inside of the flapwas excised. The periosteum was subse-quently incised, abutment connectionperformed, and the trimmed flaps su-tured. The sutures were removed after10 days, A 6-month period of plaquecontrol was initiated, This includeddaily cleaning with toothbrush and den-tifrice. The animals were sacrificed withan overdose of Sodium-Pentothal andperfused through the bilateral carotidartery by a fixative (Karnowsky 1965),The mandibles were removed andplaced in the fixative. Each implant re-gion was dissected using a diamond saw(Exakt*, Kulzer, Germany), The tissuesamples, comprising the implant andthe surrounding soft and hard peri-im-plant tissues, were decalcified in EDTAand processed using a modification ofthe "fracture technique" (Thomsen &Ericson 1985) as described by Ber-glundh et al, (1994), Decalciflcation wasperformed in EDTA and dehydrationperformed in serial steps of alcoholconcentrations, Secondary fixation inOSO< of the tissue samples was carriedout and the units were finally embeddedin EPON* (Schroeder 1969), Sectionswere produced from each tissue unitwith the microtome set at 3 ^m. Thesections were stained in PAS and tol-uidine blue (Schroeder 1969),

HMetnttrle anitysla

In each section, 5he following land-marks were identified and used for thelinear measurements; PM: the marginalportion of the periimplant mucosa;•JE: the levei of the apical termination

of the junctional epithelium; B: themarginal level of bone to implant con-tact; BC; the bone crest, i,e,, the mostcoronal portion of the periimplantbone; A/F: the abutment/fixture junc-tion. The distances between the land-marks were determined in an Olympus®Research Stereo Macroscope connectedto a PC (Compac*) equipped with animage system and a mouse cursor.

Results and conclusion

The vertical dimension of the periimpl-ant mucosa (Fig, 1) in the control side,i,e,, the distance between the bone crest(BC) and the outer surface of the oralepithelium (PM), was on average3,65 ±0,44 mm. The corresponding mu-cosa in the test jaw was in 4 out of 5 jawquadrants thin, on the average 2,4±0.23mm, while in 1 test quadrant, the per-iimplant soft tissue had adopted dimen-sions similar to those characterising thedimensions ofthe control sites (3,3 mm).

The junctional epithelium of the per-iimplant mucosa at both the test andcontrol side; of the mandible was con-sistently separated from the crestal

bone by a zone of collagen rich and cellpoor connective tissue. The length ofthe junctional epithelium varied withina rather narrow range; 2,1 mm (controlside) and 2,0 mm (test side). The heightof the suprabony connective tissue(aJE-B) in this model varied between1.3±O,3 (test side) and l,8±0,4 mm(control side). At sites where the ridgemucosa prior to abutment connectionwas made thin ( s 2 mm) and remainedthin, wound healing consistently in-cluded bone resorption and the estab-lishment of an angular bone defect (Fig,1), This implies that a certain minimumwidth of the periimplant mucosa is re-quired, and that bone resorption maytake place to allow a proper soft tissueattachment to form. The present find-ing may in part explain the loss of al-veolar bone that occurs during the 1styear following abutment connectionand the subsequent loading of the im-plant system (Adell et al, 1981, Pilliaret al, 1991), It is suggested that once theimplant is exposed to the oral environ-ment and in function, a mucosal attach-ment of a certain minimum dimensionis required to protect osseointegration.

Fig, I, Microphotograph of one test (TJ and one control (C) site. Note in the test side, thepresence of an angular bone defect: PM: the marginal portion of the periimplant mucosa; «JE:the level of the apical termination of the junetional epithelium; A/F: the abutment/fixturejunction, BC: the bone crest, i,e, the most coronal portion of the periimplant bone; B: themarginal level of bone to implant contact,

Dimension of the periimplant mucosa 973

Zusammentassung

Die Abmessung der periimplantSren Mukosa.OberprUfung hinsichtlieh eines biologisch gUn-stigen DurchmessersGegenstand der vorliegenden Studie war dieDimensionsbestimmung des implantirenMukosaattachments in Regionen mit unzu-reichendem Durchmesser der Mukogingivades Alveolarfortsatzes, Die Studie wurde an5 Beagle Hunden vorgenommen, S£mtlicheUnterkieferpramolaren wurden extrahiert. 3Monate danach wurden in jede der beidenKieferseiten 3 Fixturen des Implantatsystemsnach Brinemark* inkorporiert. Das Auf-bringen der DistanzhUlsen fand nach einerEinheilungsperiode von 3 Monaten statt. Inder rechten oder der linken Unterkieferseite(in der KontroUseite) wurden die DistanzhUl-sen nach den Anweisungen des Handbuchsftlr das Br4nemark System* fixiert. An derkontralateralen Seite (Testseite) wurde vor-erst ein Schnitt in den Alveolarkamm gelegtohne die Knochenhaut zu perforieren. DasWeichgewebe wurde dargestellt und eine be-achtliche Menge Bindegewebe an der Innen-seite des Lappens exzidiert, AnschlieBendwurde das Periost inzidiert. Nach Aufbrin-gen der Distanzhdlsen wurden die angepaB-ten Lappen mit Nahten fixiert. Die Nahtewurden nach 10 Tagsn entfernt, Nach einerZeitspanne von 6 Monaten mit Plaquekon-trolle, wurden die Tiere geopfert, Gewebe-proben wurden entnommen und fto licht-mikroskopische Untersuchungen vorbereitet.Die L4nge des Saumepithels schwankte inziemlich engen Grenzen: 2,1 mm (KontroU-seite) und 2,0 mm (Testseite). Die HOhe desoberhalb des knOchernen Alveolarfortsatzesgelegenen Bindegewebes streute bei diesemVersuchsmodel! zwischen l,3±0.3 mm (Test-seite) und l,8±0,4 mm (Kontrollseite), Anden vor der Fixation der Distanzhttlsen dUnngestalteten Stellen der Mukosa des Alveolar-kamms ( s 2 mm) ging die Wundheilungdurchweg mit Knochenresorption einher.Das bedeutet, dafl es einer gewissen Mindest-breite der periimplantaren Mukosa bedarf.Um die Bildung eines stabilen weichgeweb-lichen Attachments zu erlauben, kann es zurResorption des alveolSren Knochenskommen.

Dimension de ia muqueuse piri-implanlaire.Retour sur I'espace biologiqueLa presente etude avait pour but de determi-ner les dimensions de I'attache muqueuse-im-plant dans des sites ou la largeur de la mu-queuse du rebord 4tait insuffisante. Nousavons utilise 5 chiens Beagle, Toutes les pie-molaires inferieures ont iti extraites, puis, 3mois plus tard, 3 fixtures du Systeme Brine-mark* ont eti mises en place de chaque c6ti,Apres 3 mois de cicatrisation, on a pratiquela cormexion des piliers, Du c6ti droit ougauche de la mandibule, la connexion des pi-liers a iii faite conformement au manuel duSysteme Brdnemark* (coli temoin=control),Du cote controlaterai (cote test), une incisionne traversant pas le perioste a ixi faite auniveau de la crete du rebord. Le tissu mou aete dissdque et une quantite critique de tissuconjonctif a ete excisee de l'intirieur du lam-beau, Le perioste a ensuite ete incise, laconnexion des piliers effectute, et les lam-beaux rectifies ont ete sutures, Les suturesont ete enlevees apres 10 jours, Apres une pe-riode de 6 mois avec elimination de la plaque,les animaux ont ete sacrifies; des echantillonsont ete preleves et prepares pour examen aumicroscope optique. La longueur de I'epithe-lium de jonction variait dans un intervaiie as-sez etroit; 2,1 mm (cote temoin) et 2,0 mm(cote test). La hauteur du tissu conjonctif su-pra-osseux variait dans oe modele entre1.3±O,3 mm (cote test) et l,8±0,4 mm (c6t6temoin), Dans les sites ou la muqueuse durebord avait iti amincie (£2 nun) avant laconnexion du piiier, une resorption osseuseaccompagnait toujours ia cicatrisation de laplaie, Ceci indique qu'une certaine largeurminimum de la muqueuse p6ri-implantaireest necessaire, et qu'une resorption osseusepeut prendre place pour permettre la forma-tion d'une attache de tissu mou stable,

Rafarancat

Abrahamsson, I., Berglundh, T, WennstrOm,J, & Lindhe, J, (1996) The peri-implanthard and soft tissues at different implantsystems, A comparative study in the dog.Clinical Oral Implants Research, in press.

Adell, R,, Lekholm, U , Rockier, B, & Britie-mark, P,L (1981) A 15-year study of osseo-integrated implants in the treatment of theedentulous jaw International Journal ofOral Surgery 10, iHl-iie.

Berglundh, T, Lindhe, J,, Ericsson, L, Mar-inello, CP,, Liljenberg, B, & Thomsen, P,(1991) The soft tissue barrier at implantsand teeth. Clinical Oral Implants Research2, 81-90,

Berglundh, T, Lindhe, J,, Marinello, C.R,Ericsson, I. & Liljenberg, B, (1992) Softtissue reactions to de novo plaque forma-tion at implants and teeth. Clinical OratImplants Research 3, 1-8,

Berglundh, T, Lindhe, J,, Jonsson, K, & Er-icsson, I. (1994) The topography of thevasctilar systems in the periodontal andperi-implant tissues in the dog. J Clin Peri-odontol 2\, 189-193,

Ericsson, I,, Berglundh, T, Marinello, C P ,Liljenberg, B. & Lindhe, J, (1992) Long-standing plaque and gingivitis at itnplantsand teeth in the dog. Clinical Oral Im-plants Research 3, 99-103

Karnowsky, M, J, (1965) A formaldehyde-glutaraldehyde fixative of high osmolarityfor use in electron microscopy. Journal ofCell Biology V, 137A-138A,

Pilliar, R,M,, Deporter, DA,, Watson,PA, & Valiquette, N, (1991) Dental im-plant design - effect on bone remodelling,Joumal of Biomedical Research 25, 467-483.

Schroeder, H,E, (1969) Ultrastructure of thejunctional epithelium of the human gin-giva, Acta Helvetica Odontologica 13, 65-83,

Thomsen, P , Ericson, L,E. (1985) Light andtransmission electron microscopy used tostudy the tissue morphology close to im-plants, Biomaterials 6, 421-424,

Address:

Tord BerglundhDepartment of PeriodontologyGGteborg UniversityMedicinaregatan 12S-413 90 GeteborgSweden