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    The soft tissue barrier at implants and teeth Berglundh T. Lindhe J, Eriesson 1, Marinetlo CP. Liljenberg B. Thom- sen P. The soft tissue barrier at implants and teeth. Clin Oral Impl Res 1991: 2: 81-99. Abstract: In the present animal experiment. analyses and comparisons were made between the structure and composition of clinically healthy supraalveolar soft tissues adjacent to implants and teeth. 5 beagle dogs were used. The right mandibular premolar region was selected in each dog for placement of titanium implants, while the left mandibular pre- molar region served as control. Extractions of the mandibular premolars were performed. healing allowed, following which titanium fixtures were installed in the edentolous premolar region, Abutment connection was carried out 3 months later. After another 2 months of healing. plaque control was initiated and maintained for 8 weeks. At the end of the plaque control period. clinical examinations were performed and biop- sies harvested from the implant site and the contralateral premolar tooth region. Following fixation and decalcification. all tissue samples were embedded in EPON and examined by histometric and morphometric means. The result from the analyses demonstrated that the periimplant mucosa which formed at titanium implants following abutment connec- tion had many features in common with gingival tissue at teeth, Thus. like the gingiva. the peri-implant mucosa established a cuff-like barrier which adhered to the surface of the titanium abutment. Further. both the gingiva and the peri-implant mucosa had a well-keratinized oral epithelium which was continuous with a junctional epithelium that faced the enamel or the titanium surface. In the periimplant mucosa. the col- lagen fibers appeared to commence at the marginal bone and were par- allel with the abutment surface. All gingival and periimplant units exam: ined were free from infiltrates of inflammatory cells. It was suggested that under the conditions of study. both types of soft tissues. gingi periimplant mucosa. have a proper potential to prevent subgingival plaque formation. T.Berglundh,' J. Lindhe |. Ericsson,* .P.Marinello,” B.Liljenberg’ and P.Thomsen® "Departnent of Priadontlony Faculty of (Odontology, University of Gothenburg, Gotenbug, Sweden; “Department of Fixed and Fenovable Proshodontis,Faculy of Odontology University of rch 2arih, Switzerland, Deparment of Anatomy, University of Gotenburg, Sweden Koy words: anu - sof tssue—toth- gingiva = hitamatie measurements = morphometric ‘Tor Berlundh, Department of Periodontology Schoo of Dents, University of Gothenburg. Box 3907, $-40038 Gothenburg, ‘Sweden ‘Accaptd for publication 7 February 1981 The free marginal/interproximal gingiva has a bar- rier function and guards the periodontium proper (root cementum with investing principal fibers, pe- riodontal ligament and alveolar bone proper) from insults from the external environment. The protec- tive mechanism includes both structural compo- nents, such as (i) the junctional epithelium and its, constituents. (ii) the valeular plexus, (iii) the colla- gen fibers and (iv) other connective tissue ele- ments and inflammatory reactions (vascular and/or cellular) in sub- and intra-epithelial cell infiltrates, In subjects who are resistant to periodontal disease (Lée et al. 1986. Papapanou et al. 1991) this bar- rier is obviously effective throughout life. In other subjects. however, the protective mechanism ap- pears inadequate. and as subgingival plaque forms a process of periodontal tissue destruction is initi- ated and without treatment maintained until the teeth are lost (Van der Velden et al. 1985, Lée et al. 1986, Sjddin et al. 1989). In this context, the apparent longevity of threaded, commercially pure titanium implants for the treatment of edentulous- ness and cranio-facial defects (Branemark et al 1977) is of interest. Obviously it is through the process of osseointegration that the stability of the anchor part, the fixture. of the implant is secured. The maintenance of stability and function of the load carrying implant, however. is dependent on a well functioning barrier mechanism established at, the transmucosal passage of the implant (Ten Cate 1985. McKinney et al, 1988, Akagawa ct al. 1989). Results from different investigations have empha- ‘SoeoRnEONNESENDEISEI tooth/gin- and the implant/mucosa interface (Schroeder etal. 1981. Jansen 1985. Gould 1985. McKinney et al. 1988. Van Drie et al. 1988. Akagawa et al 1989, Buser ct al. 1989, Carmichael 1989). ‘#869 ing both epithelial structures and connective tissue ¢lemeEntsH The lack of root cementum on the im- plant surface, however. also establishes certain fundamental differences between the two units Berglundh et al. Fig. 1. Outline of the study. $ beagle dogs were used, The Ist 2nd, 3rd and 4th mandibular premolars (right side) were ex: acted, After a healing period of 3 months, the titanium fixtures were installed and after another healing period of 3 ‘months the abutment connection was performed. Abutment connection was followed first by a healing period of 2 months and consecutively by a plaque control period of 2 months. At the end of the plague control period a clinical examination was performed and biopsies harvested. both with respect to fiber orientation and fiber attachment (Buser et al. 1989). The present report is the first in a series of investigations aimed at analyzing the interface and interaction between titanium implants and the ad- jacent soft and hard tissues in health and e ‘The objective of the animal experiment reported below was to compare the structure and compo: tion of the clinically healthy supraalveolar soft tis- sue adjacent to titanium implants with the corr sponding gingival tissue adjacent to teeth. Materi 5 beagle dogs were used. They were at the start of the experiment 15 months oid. In each dog, the right mandibular premolar region was selected for placement of titanium implants (test) while the left mandibular premolar region served as control ‘Thus, extractions of the mandibular right premo- lars (4P, 3P, 2P, 1P) were performed and healing, allowed for 3 months (Fig. 1). 3 titanium fixtures (Branemark®; length: 7 mm, diameter: 3.75 mm, Nobelpharma, Gothenburg, Sweden) were in- stalled (Branemark et al. 1977, Adell et al. 1985) in the edentulous mandibular premolar region. 3, months following fixture installation, abutment connection was performed (Brinemark et al 1977, Adell et al. 1985). After a 2-month healing period, a plaque control program was initiated and maintained for 8 weeks. During this period the dogs were. once daily. subjected to meticulous tooth- and titanium abutment cleaning with the use of toothbrush and dentifrice At the end of the plaque control period, clinical examinations including assessment of plaque and gingival inflammation were performed at the buc- cal surfaces of the titanium abutments (test) and the corresponding contralateral mandibular pre- molars (control) (Fig. 2) Block-biopsies were harvested from the implant site of 2P (i.c., the region of the right mandibular ‘and methods Fig. 2. Clinical photographs of the lower mandibular premolar regions of one of the dogs. The photographs were obtained at the end of the plague control period. (a) Implant region 4P. 3? and 2P. (b) Tooth region P2, P3 and Pd 2nd premolar) (Fig. 3). The biopsies from the test, sites included not only the entire imlant but also the adjacent bone and the supraalveolar soft tis- sue. Following fixation and decalcification (Ber- glundh et al. 1990) all tissue samples were embed- ded in EPON (Schroeder 1969). Fig. 3. Photograph of a block biopsy harvested from the im= plant region 2P. The biopsy included the entire implant and the adjacent hard and soft tissues. Fig. 4. Photographs of the implant (a) and the EPON-embedded soft and hard tissue (h) after separation by the “fracture technique”. The 2 vertical sgrooves (arrows) in the Implant surface (a1) represents the cuts through the plastic material made to facilitate “fracture Fig. 5. (a) Survey scanning electron micrograph of the surface ‘of the plastic-embedded tissue after separation from the im plant. The smooth. upper surface (A) represents the tissue Which before separation faced the coronal portion of the fix- ture. The central and lower part of the micrograph (T) repre- sents the tissue within the threaded part of the fixture. Bar 1000 urn. (b) Scanaing electron micrograph of an area of the abutment surface after separation of the plastic-embedded tis- sue. The striated topogeaphy of the surface is the result of the machining procedure. No large plastic remnants are observed, Bar = 10 am. Soft tissue at implants and teeth The EPON cylinders which included the implant with adjacent soft and hard tissues were each di- vided into 1 marginal and 1 apical portion. The smaller apical portion was discarded. In the mar- ginal portion 4 grooves were prepared in “apico- coronal” direction. The grooves, which extended from the periphery of the specimen to the surface of the titanium implant, divided the specimen into 4 units (buccal, mesial. distal and lingual) out of which only the buccal was further processed (“frac ture technique”, Thomsen & Ericson 1985) (Fig. 4). In order to facilitate analysis of the in- terface tissue, i.c., the soft and hard tissue immedi- ately adjacent to the implant. the inner surface of each unit was sputtered with goold and the tissue section re-embedded in EPON (Thomsen & Eric- son 1985). The titanium abutment- and the tita- nium fixture-surface as well as the tissue surface were sputtered with gold and examined by scan- ning electron microscopy (SEM) (JEOL. T-300) (Fig. 5). Bucco-lingual sections were cut with the microtome set at 3 wm. The sections were stained in PAS and toluidine blue (Schroeder 1969). From each unit 5 sections, representing the central part of the tissue, were used for histometric and mor- phometric analyses. The control biopsies. ic... from the left 2nd man- dibular premolar region, were obtained according to a procedure described by Schroeder et al (973) Histometric analysis ‘The following linear distances were measured. (a) In the sections from the implant sites (Fig, 6b): (i) the margin of the soft tissue adjacent to the titanium abutment (GM) to the apical termi- nation of the junctional epithelium (aJE); (ii) the apical termination of the junctional epithelium (JE) to the marginal bone crest (BC) Berglundh et al. | —f Fig. 6. Schematic drawing demonstrating the landmarks which were used for the assessment of certain linear distances (histometvic measurements. (a) At the tooth section (let). (i) The gingival margin (GM) to the apical termination of the junctional epithelium (aE). (i) The apical termination of the junctional epithelium (aJE) to the marginal bone crest (BC). (ii) The gingival margin (GM) to the marginal bone crest (BC). (b) At the implant section (right). (i) The margin of the soft tissue adjacent to the titanium abutment (GM) to the apical termination of the junctional epithelium (aJE). (ii) The apical termination of the junctional epithelium (aJE) to the marginal bone crest (BC). (ii) The margin of the soft tissue adjacent to the titanium abutment (GM) to the ‘marginal bone crest (BC). Fig. 7. Schematic drawing itsstrating the compartments exposed to morphometric measurements. At level IV, a determination was made of the connective tissue proportions that were ovcupied by collagen (Co). vascular structures (V), fibroblasts (Fi). leukocytes (Leu) and residual tissue (R) in one area located immediately below the junctional epithelium (Area 1) and in asecond area adjacent to the interface between the connective tssuetitanium implant and root ct b cementum (Atea 1), Fig, 8. Cross-section of the buccal dento-gingival region repre: senting 2 months of plaque control, PAS and toluidine blue Original magnification > 40. (b) In the sections from the tooth sites (Fig. 6a): (i) the gingival margin (GM) to the apical termin: tion of the junctional epithelium (aJE); (ii) the apical termination of the junctional epithelium {aJE) to the marginal bone crest (BC). Morphometric analysis ‘The composition of the connective tissue with re- spect to content of collagen (Co). vascular struc- tures (V). fibroblasts (Fi). leukocytes (Leu) and residual tissue (R; matrix. nerves, unidentified cells and other tissue constituents) was determined using a point counting procedure described by Schroeder & Miinzel-Pedrazzoli (1973). The a sessment were made at level IV (Schroeder & Minzel-Pedrazzoli 1973) utilizing a Wild micro- scope, mag. 1000 and a lattice containing 100 light points, ‘The following regions were analyzed: (i) a 100-m wide zone of the connective tissue immedi ately lateral to the junctional epithelium (Area 1) (Fig. 7); (ii) a 100-um wide zone of the connective Soft tissue at implants and teeth Fig. 9. Cross-section of the buccal and coronal part of the periimplant hone and mucosa representing 2 months of plague control. PAS and toluidine blue. Original magnification 40, tissue immediately lateral to the titanium implant or the root cementum (Area II) (Fig. 7) Differences were analyzed using the Student test for paired observations (N= 5), Results Clinical features ‘The clinical examination performed prior to biopsy revealed that all titanium abutments as well as all mandibular premolar surfaces were free from plaque deposits (Fig. 2). The adjacent soft tissues. the periimplant mucosa and the gingiva. showed no signs of inflammation ‘The soft tissue adjacent the titanium implants (Fig. 2a) had pink color and appeared to be firmly adapted to the abutment surface. The borderline between the alveolar mucosa and the attached gin gival tissue was at the buccal aspect located about, 1-2 mm apical to the soft tissue margin. the lingual side the corresponding distance varied between 2-4 mm. The free and attached ging face of the premolars ( a at the buccal sur- ig. 2b) had pink color and 85 Berglundh et al. Tal 1 Results (mm) from the histometric measurements; mean value (x) and standard deviation (6.0) Test Conta! bit. Te x 8D x SD x 80 SE Male 24 047 205 005 009 0a ot EBC 185 023112 003058 «028 GM-eC 380 085 317 oof 083062 at Te various distances measured are described in Fig.6. The ference between the implant (Test and the tooth control; mean vale standard deviation (§.D) and standard eror (SE) Difference within 95% confidence fr was at the muco-gingival junction separated from the movable alveolar mucosa. A gingival groove. located about 1 mm apical to the gingival margin, separated the attached gingiva from the free mar- ginal gingiva Gross histological appearance The gross morphology of the soft tissue specimens, from teeth (gingiva) (Fig. 8) and from implant sites (Fig. 9), had many features in common. Both cate. gories of tissue had (i) a triangular configuraiton, (ii) a well-keratinized oral epithelium which termi- nated at the crest of the gingival margin where (iii) it_was continuous with a junctional epithe- lium. In sections representing the tooth sites, the junctional epithelium terminated at the cemento- enamel junction (CEJ). At the implant sites, the junctional epithelium ended at a varying distance from the gingival margin consistently leaving connective tissue portion coronal to the bone crest, in direct contact with the titanium surface. ‘The connective tissue was in both types of specimens devoid of inflammatory cell infiltrates and charac- terized by its collagen fiber structures. Table 2% volume ofthe connective tissue components in the ares located immediately below the junctional epithelium; collagen (Co), vascular struc- tures (V}, iorobasts (Fi leukocytes {Lou} and residual tissue (R}caeulate from the morphometric measurements performed at level; rpean vale x) and standard deviation (8.0) Tost Control bit TC x Si. x SD x SD SE %Co 72 31 «109k 38g %Y 64 1931-09251 R08) oOT 7-48 %leu 08 «04 «19 OF -13 a WR «48 «1519 BT ae ‘The difference between the implant (Test! and the tooth (Contrlh; mean valu (x, standard deviation SD.) and standard error (SE. Difloronc with 96% confidence int () 86 ‘Table 3. % volume ofthe connective tissue components in the area located adjacent to the interface between the connective tissuefitanium implant ‘and root cementum; collagen (Co), vascular structures (V), fibroblasts (Fi, leukocytes (Leu) and residue tissue (R cleulatd from the morphometric ‘measurements performed at evel 4; mean value [xl and standard deviation 6D Test x $0 x SD » 8D SE Co 0-23 HOH HV 83 14-2857 17st SR 3120S B 2d 13 %lu 03 02-0 «02-0102 HR 4415182051081 ‘The diference between the implant (Test) and the tooth (Control); mean value (2, standard deviation (SD. and standard errr (SE). Difference ‘within 95% confence limit The soft tissue adjacent to teeth and implant sites, however, also differed in several respects. Thus, the connective tissue in specimens from the implant site harbored a dense network of collagen fibers which, in major bundles. extended from the alveolar bone crest to the gingival margin. Most of the major fiber bundles were aligned in a direction parallel to the implant surface (Fig. 9) In the specimens obtained from the tooth sites. the collagen fiber bundles of the supracrestal con- nective tissue could be distinguished into (i) dento- gingival fibers, extending from the supraalveolar root cementum to the marginal gingival connective tissue, (ii) dento-periostal fibers, extending from the root cementum to the alveolar bone crest. (iii) circular fibers present in the connective tissue of the marginal gingiva and the supra alveolar con- nective tissue (Fig. 8) 1m Titanium i Tooth co v Fi Leu R Fig. 10, Histograms describing the % volume of the connective tissue components in the area located immediately below the junetional epithelium (area 1); collagen (Co). vascular struc- tures (V), fibroblasts (Fi), leukocytes (Leu) and residual tissue (R) of implant and tooth calculated from the morphometric ‘measurements performed at level 4 on in 5 D ete B 3 a wi Fig. 11. Histograms illustrating the % volume of the connec: tive tissue components in the area located adjacent to the interface between the connective tissuertitanium implant and root cementum: collagen (Co). vascular structures (V). fibro blasts (Fi) leukocytes (Leu) and residual tissue (R) of implant aand tooth caleulated from the morphometric measurements performed at level 4 Histometric measurements The results of the histometric measurements are reported in Table 1. The overall height of the su- pra crestal soft tissue (GM-BC) was at the implant site 3.80 mm and at the tooth site (the gingiva) 3.17 mm. While the variation of the height of the buccal gingiva was small (S.D. 0.04 mm), the soft tissue adjacent to titanium implants varied be- tween 3.42 mm and 4.76 mm (S.D. 0.65 mm). The average height of the junctional epithelium (GM- aJE) was at the tooth site 2.05 mm compared to 2.14 mm at the implant site. This difference in the length of the junctional epithelium was not found to be statistically significant. The length of the supraalveolar connective tissue, i.e., aJE-BC, was 1,66 mm at the implant site. The corresponding distance at the tooth site was 1.12 mm. Thus, while the portion of the soft tissue interface that carried a junctional epithelium was of similar height in the two categories of specimen, a significant difference between the two units was observed with respect to the length of the supraalveolar connective tissue. Morphometric measurements ‘The results from the morphometric measurements of the soft tissue adjacent to implants and teeth are reported in Tables 2,3 and Figures 10,11, The connective tissue located immediately lateral to the junctional epithelium (Area 1) (Table 2. Fig. 10) was at the tooth site comprised of about 63% collagen fibers, 16% fibroblasts, 7% vascular structures, 2% inflammatory cells and 12% resid- ual tissue. In Area 2 (Table 3, Fig. 11) from the tooth site, there was about 76% collagen, 5% fi- Soft tissue at implants and teeth broblasts, 3% vascular structures. 0.5% inflamma- tory cells and 15% residual tissue. It is obvious that, the connective tissue of the free gingiva immedi- ately lateral to the junctional epithelium contained a larger volume of fibroblasts, but a smaller vol- ume of collagen and vascular structures than the supraalveolar connective tissue lateral to the root cementum (Area 1 versus Area 2) ‘The corresponding connective tissue areas at the implant sites had a more uniform composition Thus, the collagen content, the amount of vascular structures, inflammatory cells and residual tissue were close to similar in Areas 1 and 2. In Area 1 from the implant sites, however. the volume of collagen was larger and the amount of fibroblasts. inflammatory cells and residual tissue smaller than, in the corresponding area from the tooth sites. The differences between the two sites with respect to collagen and fibroblasts persisted but were less conspicuous in Area 2. ussion The present inve: n, performed in dogs maintained in a careful plaque control program, demonstrated that the soft tissue. the periimplant mucosa, that formed at titanium implants follow- ing abutment connection had many features in common with gingival tissue at teeth. Thus, like the gingiva the periimplant mucosa established a cuff-like barrier (seal) which clinically (i) seemed to adhere to the surface of the titanium abutment and (ii) failed to bleed on gentle probing, Further. a microscopic examination of the two soft tissue units disclosed that both varieties had a well ker- atinized oral epithelium which was continuous with a junctional epithelium that faced the enamel or the titanium surface. While a majority of the colla- gen fiber bundles of the free gingival units exa ined originated from the root cementum, in the mucosa at implants they appeared to commence from the marginal bone crest and were orient parallel with the abutment surface. All ginj and periimplant units examined in this model ex- periment were free from infiltrates of inflamma- tory cells. There are reasons to suggest, therefore, that under the conditions of study both kinds of soft tissue units have a proper potential to prevent, subgingival plaque formation. In the present study, the titanium implants were installed in the alveolar process and the coronal portion of the fixtures were, following surgery, covered by the mucosa of the edentulous alveolar ridge. Thus, the tissue which after abutment con- nection formed the soft periimplant cuff originated from masticatory mucosa. The histological exam- ination of the gingiva and the periimplant mucosa 87 Berglundh et al. demonstrated that there were marked differences between the two units with respect to the orien- tation of the collagen fibers. In the gingiva, the collagen fibers were (i) attached to the root ce- mentum and advanced in perpendicular direction into the lateral portions of the soft tissue, or ii) occurred as circular fibers without attachment to the tooth. In the periimplant tissue, the vast majority of the coarse fiber bundles were attached to the marginal bone, not to the titanium surface, and mainly arranged in a direction parallel to the surface of the titanium abutment. This observation appears to be at variance with data previously re- ported from similar experiments in the monkey and dogs (¢.g., Schroeder et al. 1981, Buser et al 1989). In these studies. using titanium implants (ITI), it was observed that: (i) the collagen fibers of the periimplant mucosa “inserted into the neck of the implant and were obviously so firmly tached...” (Schroeder et al. 1981); (ii) “around the implants anchored in keratinized mucosa, perpen- dicularly arranged horizontal connective-tissue fi- bers firmly attached to the implant surface. were found prevailing” (Buser et al. 1989). The reason for this difference in the composition of the peri- implant mucosa of this study and in the experi- ments by Schroeder et al. (1981) and Buser et al (1989) is presently not understood but may be related to differences inherent in the design of the implant systems used. The histometric analysis of the biopsy material from the present experiment revealed that the pe- riimplant mucosa as well as the gingival unit har- bored a junctional epithelium. the length of which was about 2 mm. The observation that a junctional epithelium formed at the interface between the titanium surface and the periimplant mucosa is, consistent with findings previously reported by Gould et al. (1981, 1984), Jansen et al. (1985), McKinney et al. (1988) and Van Drie et al. (1988), ‘The formation of a junctional epithelium adjacent to implants is according to Ten Cate (1985) a log- ical result of wound healing. Thus, the epithelial cells proliferate and migrate on the exposed con- nective tissue surface until the epithelial continuity is restored. At both the tooth and implant sites, the apical cells of the junctional epithelium (IE) terminated about I-1.5 mm coronal of the alveolar bone crest At the dentogingival region, the presence of a root cementum apical of the cementoenamel junction (CEJ) explains why under normal conditions the junctional epithelium terminates at or close to CEI. The reason why at the implant sites the JE failed to reach the bone crest is not properly un- derstood. Obviously, however, during healing, the interface between the supraalveolar portion of the 88 titanium susface and the mucosa must not be rec~ ognized as “exposed” connective tissue. There are reasons to suggest. therefore, that an interaction must occur between the surface layer of the tita- nium implant and the connective tissue. and that this interaction or “connective tissue integration” may prevent further epithelial migration. Such a ive tissue integration” must occur during I phase of wound healing after abutment connection and may establish an important biolog- ical barrier to ensure implant success. ‘A morphological analysis of the tissue immedi- ately adjacent to bulk metal implants is hampered by the difficulty to obtain thin sections (

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