biologic width around one- and two-piece titanium implants

13
Joachim S. Hermann Biologic Width around one- and Daniel Buser two-piece titanium implants Robert K. Schenk A histometric evaluation of unloaded John D. Schoolfield David L. Cochran nonsubmerged and submerged implants in the canine mandible Authors’ affiliations: Joachim S. Hermann, David L. Cochran, Department of Periodontics, Dental School, University of Texas Health Science Center at San Antonio, Texas, USA Joachim S. Hermann, Department of Preventive Dentistry, Periodontics, and Cariology, University of Zu ¨ rich Dental School, Zu ¨ rich, Switzerland Daniel Buser, Robert K. Schenk, Department of Oral Surgery, University of Bern School of Dental Medicine, Bern, Switzerland John D. Schoolfield, Statistical/Mathematical Consulting, Computing Resources, University of Texas Health Science Center at San Antonio, Texas, USA Correspondence to: Dr. med. dent. Joachim S. Hermann, FICOI Department of Preventive Dentistry, Periodontics, and Cariology University of Zu ¨ rich Dental School Plattenstrasse 11 CH-8028 Zu ¨ rich Switzerland Tel: π41 1 634 0310 Fax: π41 1 634 4308 e-mail: hermann/zzmk.unizh.ch Date: Accepted 29 November 2000 To cite this article: Hermann JS, Buser D, Schenk RK, Schoolfield JD, Cochran DL. Biologic Width around one- and two- piece titanium implants. A histometric evaluation of unloaded nonsubmerged and submerged implants in the canine mandible Clin. Oral Impl. Res. 12, 2001; 559571 Copyright C Munksgaard 2001 ISSN 0905-7161 559 Key words: animal study, titanium implants, endosseous, unloaded, one-piece, two- piece, soft tissue, histometry, Biologic Width, esthetics Abstract: Gingival esthetics around natural teeth is based upon a constant vertical dimension of healthy periodontal soft tissues, the Biologic Width. When placing endosseous implants, however, several factors influence periimplant soft and crestal hard tissue reactions, which are not well understood as of today. Therefore, the purpose of this study was to histometrically examine periimplant soft tissue dimensions dependent on varying locations of a rough/smooth implant border in one-piece implants or a microgap (interface) in two-piece implants in relation to the crest of the bone, with two- piece implants being placed according to either a submerged or a nonsubmerged technique. Thus, 59 implants were placed in edentulous mandibular areas of five foxhounds in a side-by-side comparison. At the time of sacrifice, six months after implant placement, the Biologic Width dimension for one-piece implants, with the rough/smooth border located at the bone crest level, was significantly smaller (P,0.05) compared to two- piece implants with a microgap (interface) located at or below the crest of the bone. In addition, for one-piece implants, the tip of the gingival margin (GM) was located significantly more coronally (P,0.005) compared to two-piece implants. These findings, as evaluated by nondecalcified histology under unloaded conditions in the canine mandible, suggest that the gingival margin (GM) is located more coronally and Biologic Width (BW) dimensions are more similar to natural teeth around one-piece nonsubmerged implants compared to either two-piece nonsubmerged or two-piece submerged implants. In 1921, Gottlieb initially described the ‘‘epithelial attachment’’ around a natu- ral tooth by covering distinct areas of the enamel surface or the cementum and not by just being attached to the ce- mento-enamel junction at a certain point or level, respectively (Gottlieb 1921). Later on, these findings have been confirmed (Orban & Mueller 1929), and in addition, the ‘‘gingival crevice’’ or sul- cus has been defined. Subsequently, Feneis showed that connective tissue consists of three-dimensionally oriented fibers firmly connecting tooth structures to the surrounding gingiva (Feneis 1952). Thus, it became clear that both epi- thelial as well as connective tissue attachment contribute to a ‘protection mechanism’ in a most challenging area where the natural tooth penetrates the ectodermal integrity of the body. Sicher confirmed these findings in 1959 and called this functional unit the ‘‘dento- gingival junction’’ (Sicher 1959). In 1961, Gargiulo et al. found out that the verti- cal dimension of the dentogingival junc- tion, comprised of sulcus depth (SD), junctional epithelium (JE), and connec- tive tissue attachment (CTA), is a physiologically formed and stable di-

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Page 1: Biologic Width Around One- And Two-piece Titanium Implants

Joachim S. Hermann Biologic Width around one- andDaniel Buser two-piece titanium implantsRobert K. Schenk

A histometric evaluation of unloadedJohn D. SchoolfieldDavid L. Cochran nonsubmerged and submerged implants in the

canine mandible

Authors’ affiliations:Joachim S. Hermann, David L. Cochran,Department of Periodontics, Dental School,University of Texas Health Science Center at SanAntonio, Texas, USAJoachim S. Hermann, Department of PreventiveDentistry, Periodontics, and Cariology,University of Zurich Dental School, Zurich,SwitzerlandDaniel Buser, Robert K. Schenk, Department ofOral Surgery, University of Bern School of DentalMedicine, Bern, SwitzerlandJohn D. Schoolfield, Statistical/MathematicalConsulting, Computing Resources, University ofTexas Health Science Center at San Antonio,Texas, USA

Correspondence to:Dr. med. dent. Joachim S. Hermann, FICOIDepartment of Preventive Dentistry,Periodontics, and CariologyUniversity of Zurich Dental SchoolPlattenstrasse 11CH-8028 ZurichSwitzerlandTel: π41 1 634 0310Fax: π41 1 634 4308e-mail: hermann/zzmk.unizh.ch

Date:Accepted 29 November 2000

To cite this article:Hermann JS, Buser D, Schenk RK, Schoolfield JD,Cochran DL. Biologic Width around one- and two-piece titanium implants. A histometric evaluation ofunloaded nonsubmerged and submerged implants inthe canine mandibleClin. Oral Impl. Res. 12, 2001; 559–571

Copyright C Munksgaard 2001

ISSN 0905-7161

559

Key words: animal study, titanium implants, endosseous, unloaded, one-piece, two-piece, soft tissue, histometry, Biologic Width, esthetics

Abstract: Gingival esthetics around natural teeth is based upon a constant verticaldimension of healthy periodontal soft tissues, the Biologic Width. When placingendosseous implants, however, several factors influence periimplant soft and crestal hardtissue reactions, which are not well understood as of today. Therefore, the purpose ofthis study was to histometrically examine periimplant soft tissue dimensions dependenton varying locations of a rough/smooth implant border in one-piece implants or amicrogap (interface) in two-piece implants in relation to the crest of the bone, with two-piece implants being placed according to either a submerged or a nonsubmergedtechnique. Thus, 59 implants were placed in edentulous mandibular areas of fivefoxhounds in a side-by-side comparison. At the time of sacrifice, six months after implantplacement, the Biologic Width dimension for one-piece implants, with the rough/smoothborder located at the bone crest level, was significantly smaller (P,0.05) compared to two-piece implants with a microgap (interface) located at or below the crest of the bone. Inaddition, for one-piece implants, the tip of the gingival margin (GM) was locatedsignificantly more coronally (P,0.005) compared to two-piece implants. These findings,as evaluated by nondecalcified histology under unloaded conditions in the caninemandible, suggest that the gingival margin (GM) is located more coronally and BiologicWidth (BW) dimensions are more similar to natural teeth around one-piecenonsubmerged implants compared to either two-piece nonsubmerged or two-piecesubmerged implants.

In 1921, Gottlieb initially described the‘‘epithelial attachment’’ around a natu-ral tooth by covering distinct areas of theenamel surface or the cementum andnot by just being attached to the ce-mento-enamel junction at a certainpoint or level, respectively (Gottlieb1921). Later on, these findings have beenconfirmed (Orban & Mueller 1929), andin addition, the ‘‘gingival crevice’’ or sul-cus has been defined. Subsequently,Feneis showed that connective tissueconsists of three-dimensionally orientedfibers firmly connecting tooth structuresto the surrounding gingiva (Feneis 1952).

Thus, it became clear that both epi-thelial as well as connective tissueattachment contribute to a ‘protectionmechanism’ in a most challenging areawhere the natural tooth penetrates theectodermal integrity of the body. Sicherconfirmed these findings in 1959 andcalled this functional unit the ‘‘dento-gingival junction’’ (Sicher 1959). In 1961,Gargiulo et al. found out that the verti-cal dimension of the dentogingival junc-tion, comprised of sulcus depth (SD),junctional epithelium (JE), and connec-tive tissue attachment (CTA), is aphysiologically formed and stable di-

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Hermann et al . Biologic Width around one- and two-piece titanium implants

mension, subsequently called ‘‘BiologicWidth’’, and that this unit forms at alevel dependent on the location of thecrest of the alveolar bone (Gargiulo et al.1961).

Taking these biological principles intoconsideration, two major clinical pro-cedures have been derived from thesefindings and are widely used today, onebeing the ‘‘forced eruption’’ (Ingber1976) and the other one being the ‘‘surgi-cal lengthening of the crown’’ (Ingber etal. 1977). Both procedures are basedupon the understanding that changingthe level of the alveolar bone will movethe complete dentogingival junction as aunit on a predictable basis towards thesame direction (apically or coronally, re-spectively). These procedures have greatimpact as to the location of the gingivalmargin (tip of the papilla) and, therefore,provide a major tool to achieve stableand esthetic gingival harmony around ahealthy natural crown or a tooth-bornerestoration.

In the early years of implant dentistry,research mainly focused on hard tissueintegration. Based upon positive long-term results with implant-borne fixedpartial dentures as well as overdenturesusing submerged as well as nonsub-merged implants (for review see Cochran1996), implant-borne single tooth res-torations became more and more popu-

Fig. 1. a. Schematic (true to scale) of implant whereas the dashed line shows the location of (Cochran et al. 1997; Hermann et al. 2000a). Thetypes A–C at time of implant placement in re- the microgap (interface). Note that all three types dark red compartment indicates the vertical di-lation to soft tissues and bone. Soft tissue dimen- (A–C) were inserted according to a nonsub- mension of the sulcus depth (SD), the pink com-sions are adapted from the literature (Cochran et merged approach. Implant types A and B are one- partment the junctional epithelium (JE), and theal. 1997; Hermann et al. 2000a). The dark red piece implants exhibiting no microgap (inter- yellow compartment the connective tissue con-compartment represents the vertical dimension face), while type C implants are two-piece im- tact (CTC). Note that all these implants wereof the sulcus depth (SD), the pink compartment plants with a microgap (interface) located at the placed using a submerged technique. Implantthe junctional epithelium (JE), and the yellow bone crest level. b. Schematic (true to scale) of im- types D–F are two-piece implants with acompartment the connective tissue contact plant types D–F at time of implant placement in microgap (interface) located at different levels in(CTC). The solid black line delineates the bor- relation to soft tissues and bone. Soft tissue di- relation to the crest of the bone.der between rough and smooth implant surface, mensions are adapted from the literature

560 | Clin. Oral Impl. Res. 12, 2001 / 559–571

lar during the 1990s. As a consequence,increasing attention was given to studyperiimplant crestal bone as well as softtissue reactions. Thus, Berglundh andcoworkers (Berglundh et al. 1991; Ber-glundh & Lindhe 1996) and Abrahams-son and collaborators (Abrahamsson etal. 1996; Abrahamsson et al. 1997; Abra-hamsson et al. 1999) presented histo-metric data on two-piece, submerged aswell as nonsubmerged implants.Cochran et al. (1997) and Hermann et al.(2001) first published periimplant histo-metric results based upon an experimen-tal study analyzing and confirming theBiologic Width dimensions around anatural tooth with those around a one-piece, nonsubmerged implant. Thissame research group also comparedcrestal bone reactions around one- andtwo-piece titanium implants placed ac-cording to a nonsubmerged or sub-merged technique in a side-by-side com-parison (Hermann et al. 1997; Hermannet al. 2000b, Hermann et al. 2001), show-ing significant changes in crestal bonereactions dependent on the implant de-sign and/or technique used (one-piece vs.two-piece implant; nonsubmerged vs.submerged approach), which, in part, hasalso been confirmed in a series of casereports involving 11 patients (Hammerleet al. 1996).

The purpose of this study was to ana-

lyze the dimensions of the Biologic Widtharound implants of varying designs: one-piece implants with a rough/smooth bor-der vs. two-piece implants with amicrogap (interface) as well as surgicaltechnique used (nonsubmerged vs. sub-merged). In addition, the relationship ofthe gingival margin (GM) to the implantwas of particular interest since its loca-tion and stability is important for per-iimplant soft tissues, and the resulting es-thetics of the implant-borne restoration.

Material and methods

Implant design and surfaces

All six different experimental implants(types A-F; Figs la, lb) were based on acylindrical full-body screw design andwere made from cold-worked, grade-IVcommercially pure titanium (InstitutStraumann AG, Waldenburg/BL, Switz-erland). The outer diameter (thread tips)measured 4.1 mm, whereas the inner di-ameter was 3.5 mm at a total length of9 mm. The coronal portion of each one-piece implant and the abutments in two-piece implants consisted of a machined,relatively smooth titanium surface. Theapical part of each implant had a sand-blasted (large-grit) and HCI/H2SO4 acid-etched surface (SLA) with two levels ofroughness, one at 20–40 mm peak to

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Hermann et al . Biologic Width around one- and two-piece titanium implants

peak, and a superimposed second one at2–4 mm peak to peak.

The apical, rough portion (SLA surface)of type A implants was 6.0 mm in lengthwith the rough/smooth implant borderclinically placed at the alveolar crest.Type B implants had a 5.0 mm long SLAportion, with the rough/smooth borderplaced 1.0 mm below the crest. For allother implants (types C-F), the rough im-plant surface (SLA) was 4.5 mm in verti-cal dimension with the rough/smoothimplant border located about 1.5 mm be-low the crest (Figs 1a and 1b). Type A andB implants were one-piece implantswithout a microgap (interface) present,while implant types C-F consisted of twopieces, with a clinically relevantmicrogap (interface) of about 50 mm insize (Binon et al. 1992; Keith et al. 1999)between the implant and the secondarycomponent, the abutment. The locationof the microgap (interface) was defined tobe clinically at the bone crest level fortypes C and D, however, for types E and F,the microgap (interface) was located 1mm above or 1 mm below the crest, re-spectively. Implant types A-C wereplaced according to a nonsubmergedtechnique, whereas types D-F were in-serted using a submerged approach.

Study animals

For this study, five lab-bred, male Ameri-can foxhounds were used. Prior to thestart of the experiment, the protocol wasapproved by the ‘Institutional AnimalCare and Use Committee’ of the Univer-sity of Texas Health Science Center atSan Antonio (UTHSCSA). The dogs wereapproximately two years of age at the be-ginning of the study and had a bodyweight of about 30–35 kg. None of the

Fig. 2. Study design.

561 | Clin. Oral Impl. Res. 12, 2001 / 559–571

dogs had heart worms and all of themwere quarantined before the experimentwas started.

Surgeries – Extraction

The extraction technique removing allmandibular premolars and the first mo-lar bilaterally has already been describedin detail and published recently (Her-mann et al. 1997; Hermann et al. 2000b).

Surgeries – Implant placement

Nonsubmerged and submerged implants(types A–F) were placed after a healingperiod of 6 months (Fig. 2), under thesame surgical conditions as tooth extrac-tion had been performed (operating room,anesthesia, sterility). A crestal incisionwas performed maximizing keratinizedgingiva on each side of the incision. Full-thickness flaps were carefully reflectedon the lingual and buccal aspect. Foram-ina mentalia were dissected and exposed.The edentulous osseous ridge was care-fully flattened utilizing an acrylic burcombined with copious irrigation withchilled sterile physiologic saline. Meas-urements were made using a boley gaugeto help distribute six test implants oneach side of the mandible. Implant sitepreparations were carried out with low-torque reduction rotary instruments at500 rpm using chilled saline. Implanttypes A–C were placed according to anonsubmerged approach (Fig. 1a), i.e. fortype C, implants and abutments werescrewed together at the time of first-stagesurgery. Implant types D–F were placedaccording to a submerged technique (Fig.1b). Finally, one of each kind of test im-plant was placed per side in a randomizedfashion. Thus, no implant type had a bi-ased position in the arch. Periosteal re-

lieving and contouring incisions werecarried out on the buccal and lingual as-pects of each implant in order to obtaintension-free adaptation of the woundmargins for close adaptation of the gin-giva to the transgingival portion of thenonsubmerged one-piece implants (typesA and B), and the abutment of type C im-plants. Wound closure over the sub-merged implants (types D–F) wasachieved using horizontal mattress com-bined with interrupted sutures. At theday of surgery, the dogs received 20 mgNubainA (nalbuphine 10 mg/ml – AstraPharmaceutical Products Inc., Westbor-ough, MA, USA) s.c. BID. Three ml Pen-BA (benzathine penicillin 150,000 I.U.combined with procaine penicillin G150,000 I. U. – Pfizer Inc., Lee’s Summit,MO, USA) were given s.c. SID every 48 hfor 14 days. On day 1, 100 mg of the anti-biotic GentocinA (gentamicin 50 mg/ml –Schering-Plough Animal Health Corp.,Kenilworth, NJ, USA) were administereds.c. BID, and the same amount SID fromday 2–10. To reduce swelling, the fox-hounds received 2 ml of the antiinflam-matory DexajectA (dexamethasone 2 mg/ml – Burns Veterinary Supply, Oakland,CA, USA) i.m. SID day 1 and at day 4. Su-ture removal was carried out after 7–10days as described above. To minimizeloading, the animals were fed a softeneddiet for the duration of the study. Mech-anical and chemical plaque control wascarried out three times per week, using asoft toothbrush and a soft sponge in com-bination with PlakOutA Gel (chlorhex-idine digluconate 0.2% – Hawe-Neos AG,Bioggio/TI, Switzerland).

Surgeries – Abutment connection

Second-stage surgery was performedthree months after implant placement,and abutments were connected for sub-merged implant types D–F. Surgical con-ditions were the same as described above.First, the surgical sites were disinfectedand the local anesthesia given. Over thetop of these implants, a midcrestal in-cision was used combined with a smallvertical relieving incision at the buccaland lingual aspect. Implants were un-covered after the elevation of a full-thick-ness flap. In the case of implants partiallycovered with bone (mostly in type F im-plants) a minor osteotomy was performedusing hand instruments (chisel, mallet).

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This osteotomy likely had little effect onthe outcome as the bone was quite thin,as evidenced by no changes during thesubmerged healing phase as shown in anearlier study of these implants (Hermannet al. 1997). Consequently, flat-headcover screws could be removed in thesubmerged implant group. Abutments ofindividual lengths were connected speci-fic for each implant type so that afterabutment connection all implantsemerged to the same level. Interruptedsutures combined with a small V-shapedgingivectomy were used for wound clo-sure around the abutments. Postopera-tive care and suture removals were donethe same way as after extraction.

Abutments on type C–F implants wereloosened and immediately tightenedafterwards at four, eight, and ten weeksafter second-stage surgery to imitate theplacement of another healing abutment,impression taking, as well as the place-ment of the final prosthetic component.

Surgeries – Sacrifice

All dogs were sacrificed three monthsafter abutment connection of the sub-merged implants (Fig. 2). Euthanasia wascarried out with an overdose of Eutha-nasia-5A Solution i.v. (pentobarbital so-dium 0.2 mlΩ65 mg/kg bw. – HenrySchein Inc., Port Washington, NY, USA).Mandibles were block-resected with anoscillating autopsy saw (Stryker Co., Ka-lamazoo, MI, USA). The recovered seg-ments with the implants were immersedin a solution of formaldehyde 4% com-bined with CaCI2 1% for histologic prep-aration and analysis.

Nondecalcified histologic analysis –

preparation

Each implant with surrounding tissueswas prepared for nondecalcified his-tology (Schenk et al. 1984). Specimenswere carefully dehydrated and embeddedin methyl methacrylate. Per implant,first one well-centered mesio-distal sec-tion was cut with a diamond saw (Vari/Cut VC-50A, Leco Corporation, St.Joseph, MI, USA). The two remainingblocks were then glued together with aninterposed plastic spacer (cyanoacrylate;MiocollA, Migros Company, Zurich,Switzerland), and subsequently section-ed in an oro-facial direction, resulting inup to five oro-facial sections. All sec-

562 | Clin. Oral Impl. Res. 12, 2001 / 559–571

tions were ground to a final thickness ofapproximately 80 mm and superficiallystained with toluidine blue and basicfuchsin (Figs 4a–9b).

Nondecalcified histologic analysis –

histometry

Histometric quantification was carriedout using a light microscope (Vanox-TA,Olympus, Tokyo, Japan) at differentmagnifications (¿40–¿200) to best lo-cate anatomical reference points. Themicroscope was connected to a high-res-olution video camera (CCD-IrisA ColorVideo Camera, Sony Corp., Fujisawa, Ja-pan) and interfaced to a monitor (Multi-syncA XV17π, NEC, Itasca, IL, USA) aswell as a personal computer (Vectra VLA,Hewlett Packard, Palo Alto, CA, USA).This optical system was associated witha digitizing pad and a bone histometrysoftware package with image capturingcapabilities (Image-Pro PlusA, Media Cy-bernetics, Silver Spring, MD, USA). Fi-nally, the following measurements/cal-culations were performed at each im-plant site (Fig. 3):1. Distance between the gingival margin

(GM) and the most coronal point ofthe junctional epithelium (cJE)Ωsul-cus depth (SD)

2. Distance between cJE and the mostapical point of the junctional epithel-ium (aJE)Ωjunctional epithelium (JE)

Fig. 3. Composite schematic (not true to scale) ofhistometric evaluation with the followingmeasurements/calculations: Distance betweenthe gingival margin (GM) and the most coronalpoint of the junctional epithelium (cJE)Ωsulcusdepth (SD). Distance between cJE and the mostapical point of the junctional epithelium (aJE)Ωjunctional epithelium (JE). Distance betweenaJE and the first bone-to-implant contact (fBIC)Ωconnective tissue contact (CTC). SD π JE π

CTCΩBiologic Width (BW). Distances betweenthe top of the implant (Top) and the GM, cJE, aJE,rough/smooth border (r/s), and the fBIC.

Fig. 4. a. Mesio-distal section (overview) of a typeA implant (one-piece, nonsubmerged). Nonde-calcified histologic section; toluidine blue andbasic fuchsin stain; original magnification ¿2.5;original inner/outer implant diameterΩ3.5 mm/4.1 mm; black barΩ1 mm. b. Close-up view of Fig.4a. Left (distal) aspect of type A implant (one-piece, nonsubmerged). Note mild signs of peri-implant inflammation. The white bar indicatesthe level of the first bone-to-implant contact(fBIC), the white arrow the most apical cell of thejunctional epithelium (aJE), and the black arrowthe top of the implant (Top). Nondecalcified his-tologic section; toluidine blue and basic fuchsinstain; original magnification¿8; black barΩ0.5mm.

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Hermann et al . Biologic Width around one- and two-piece titanium implants

Fig. 5. a. Mesio-distal section (overview) of a typeB implant (one-piece, nonsubmerged). Nonde-calcified histologic section; toluidine blue andbasic fuchsin stain; original magnification ¿2.5;original inner/outer implant diameterΩ3.5 mm/4.1 mm; black barΩ1 mm. b. Close-up view of Fig.5a. Left (mesial) aspect of type B implant (one-piece, nonsubmerged). Note mild signs of peri-implant inflammation. The white bar shows thelevel of the first bone-to-implant contact (fBIC),the white arrow the most apical cell of the junc-tional epithelium (aJE), and the black arrow thetop of the implant (Top). Nondecalcified histo-logic section; toluidine blue and basic fuchsinstain; original magnification¿8; black barΩ0.5mm.

563 | Clin. Oral Impl. Res. 12, 2001 / 559–571

Fig. 6. a. Mesio-distal section (overview) of a typeC implant (two-piece, nonsubmerged). Nonde-calcified histologic section; toluidine blue andbasic fuchsin stain; original magnification ¿2.5;original inner/outer implant diameterΩ3.5 mm/4.1 mm; black barΩ1 mm. b. Close-up view of Fig.6a. Left (distal) aspect of type C implant (two-piece, nonsubmerged). Note moderate to severesigns of periimplant inflammation. The whitebar delineates the level of the first bone-to-im-plant contact (fBIC), the white arrow the mostapical cell of the junctional epithelium (aJE), andthe black arrow the microgap (interface). Notethat the abutment is not visible due to properhistological processing. Nondecalcified histo-logic section; toluidine blue and basic fuchsinstain; original magnification¿8; black barΩ0.5mm.

3. Distance between aJE and the firstbone-to-implant contact (fBIC)Ωcon-nective tissue contact (CTC)

4. SD π JE π CTCΩBiologic Width (BW)5. – 9. Distances between the top of the

implant (Top) and the GM, cJE, aJE,the rough/smooth border (r/s), and thefBIC.

Statistical analysis

The two principal soft tissue measuresof interest for this study were the deter-mination of the Biologic Width dimen-sions (Fig. 3) and the location of the gin-gival margin in relation to the implant.Each implant had one to three mesio-dis-tal and up to five oro-facial sectionsyielding a total of 566 sites for histo-metric examination. In order to verifythat the soft tissue values obtained fromthe histometric evaluation were not in-fluenced by examiner bias, the primaryexaminer obtained two measures, as dida second examiner, for a subsample of 51sites taken from six implants. The re-sults of the comparison of the four read-ings of BW measures indicated the histo-metric evaluation was highly calibrated,with the four readings differing by lessthan 0.20 mm for 46 (90.2%) of 51 sites,with a maximum difference of 0.42 mm.

Data were unavailable for 22.4% ofsites (including all sites of one type Cand one type E implant) that were un-readable due to histological processing(16.8%) or the degree of periimplant in-flammation (5.6%). Also, the first bone-to-implant contact (fBIC) for buccal sitestended to be lower than that for the cor-responding lingual, mesial, or distal sitesobtained from an implant. BiologicWidth measures for nonbuccal siteswithin an implant generally rangedwithin 0.5 mm, but buccal sites tendedto have distances 0.5 to 1.0 mm largerthan any of the nonbuccal sites obtainedfrom the same implant. Consequently,buccal sites tended to have BW valuesthat were extreme outliers relative tothe overall distribution of BW values forsites within an implant. These resultsindicated that only lingual, mesial, anddistal sites should be used in this studyto calculate mean values of the BiologicWidth for each implant. For the purposesof consistency, buccal sites were also ex-cluded in the calculation of mean valuesfor each implant of all soft tissue meas-

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Hermann et al . Biologic Width around one- and two-piece titanium implants

urements. The remaining four to sixsites per implant provided a sample suf-ficient to develop precise individual im-plant measures after averaging.

A mixed-model Analysis of Variancewas performed for each soft tissue meas-urement to check if implant types dif-fered in a consistent fashion for eachdog. If the resulting F-test was signifi-cant (P,0.05), then Bonferroni-correctedpairwise comparisons were made toidentify implant type differences. Also,separate mixed-model ANOVAs wereperformed to ensure that position on thearch and side of the mandible did not in-fluence the implant type results.

Results

Clinical observations

One out of the possible 60 implantscould not be placed since the implant re-cipient site was too soft and, therefore,primary stability could not be achieved.All other 59 implants were clinicallystable and no complications occurredduring healing or during the follow-upperiod. In a recent publication based onthe same data set analyzing radiographicchanges on a monthly basis over time,no periimplant radiolucencies werefound around any of the implants, how-ever crestal bone loss could be detecteddependent on specific implant designs(one-piece vs. two-piece implants) andtechniques (nonsubmerged vs. sub-merged) used (Hermann et al. 1997).Thus, all implants achieved hard tissueintegration by clinical as well as radio-graphic means. Although a meticulouscombination of mechanical and chemi-cal plaque control was carried out threetimes per week, different degrees of peri-implant inflammation could be iden-tified when comparing one-piece (typesA and B; Figs 4b, 5b) vs. two-piece im-plants (types C-F; Figs 6b, 7b, 8b, 9b)with types A and B exhibiting minimalsigns of inflammation, as opposed totypes C–F showing moderate to severedegrees of inflammation.

Histometric analysis

Light microscopic evaluation of thebone-to-implant contact in nondecalci-fied sections showed that hard tissue in-

564 | Clin. Oral Impl. Res. 12, 2001 / 559–571

Fig. 7. a. Mesio-distal section (overview) of a typeD implant (two-piece, submerged). Nondecalci-fied histologic section; toluidine blue and basicfuchsin stain; original magnification ¿2.5; orig-inal inner/outer implant diameterΩ3.5 mm/4.1mm; black barΩ1 mm. b. Close-up view of Fig. 7a.Left (mesial) aspect of type D implant (two-piece,submerged). Note moderate to severe signs of peri-implant inflammation. The white bar reveals thelevel of the first bone-to-implant contact (fBIC),the white arrow the most apical cell of the junc-tional epithelium (aJE), and the black arrow themicrogap (interface). Note that the abutment isnot visible due to proper histological processing.Nondecalcified histologic section; toluidine blueand basic fuchsin stain; original magnification¿8; black barΩ0.5 mm.

Fig. 8. a. Mesio-distal section (overview) of a typeE implant (two-piece, submerged). Nondecalci-fied histologic section; toluidine blue and basicfuchsin stain; original magnification ¿2.5; orig-inal inner/outer implant diameterΩ3.5 mm/4.1mm; black barΩ1 mm. b. Close-up view of Fig. 8a.Left (mesial) aspect of type E implant (two-piece,submerged). Note moderate to severe signs of peri-implant inflammation. The white bar representsthe level of the first bone-to-implant contact(fBIC), the white arrow the most apical cell of thejunctional epithelium (aJE), and the black arrowthe microgap (interface). Note that the abutmentis not visible due to proper histological pro-cessing. Nondecalcified histologic section; tol-uidine blue and basic fuchsin stain; originalmagnification ¿8; black barΩ0.5 mm.

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Fig. 9. a. Mesio-distal section (overview) of a typeF implant (two-piece, submerged). Nondecalci-fied histologic section; toluidine blue and basicfuchsin stain; original magnification ¿2.5; orig-inal inner/outer implant diameterΩ3.5 mm/4.1mm; black barΩ1 mm. b. Close-up view of Fig. 9a.Left (mesial) aspect of type F implant (two-piece,submerged). Note moderate to severe signs of peri-implant inflammation. The white bar exhibitsthe level of the first bone-to-implant contact(fBIC), and the black arrow the microgap (inter-face). Due to the severe degree of inflammation,the most apical cell of the junctional epithelium(aJE) could not be detected. Note that the abut-ment is not visible due to proper histological pro-cessing. Nondecalcified histologic section; tol-uidine blue and basic fuchsin stain; original mag-nification¿8; black barΩ0.5 mm.

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tegration was achieved (Figs 4a-9b). Forall implants (types A–F), an intimatecontact of bone was found directly ad-jacent to the sandblasted (large-grit) andacid-etched surface (SLA). As expected,dense cortical bone had large areas ofbone-to-implant contact compared tocancellous bone areas where more mar-row space was found. In more cancellousbone, however, osseous tissue was foundalong the SLA surface demonstratingand confirming the excellent osteocon-ductive nature of this specific surface. Inthe most coronal area, however, differ-ent crestal bone loss patterns could befound dependent on different implanttypes. These results have already beendescribed and discussed in detail re-cently in three other publications (Her-mann et al. 1997; Hermann et al. 2000b;Hermann et al. 2001).

Nine one-piece, nonsubmerged im-plants (type A; Fig. 1a) with 37 histologi-

Table l. Histometric data for the three different implant groups A–C (nonsubmerged approach)six months after implant placement. Mean values∫standard deviation [mm]; (ni)Ωnumber ofmeasured implants/(nis)Ωnumber of measured implant sites. ‘‘Top’’ refers to the most coronalaspect of the implant for types A and B and the coronal aspect of the abutment on type C.

Variables A (niΩ9/nisΩ45) B (niΩ10/nisΩ50) C (niΩ9/nisΩ40)

SD 0.23∫0.16 0.21∫0.11 0.24∫0.08

JE 1.33∫0.31 1.74∫0.37 1.75∫0.46

CTC 1.28∫0.28 1.62∫0.48 1.39∫0.16

BW 2.84∫0.28 3.57∫0.61 3.38∫0.36

Top: GM 0.32∫0.58 0.42∫0.52 1.38∫0.43

Top: cJE 0.54∫0.47 0.64∫0.46 1.62∫0.46

Top: aJE 1.87∫0.60 2.38∫0.66 3.37∫0.26

Top: r/s 2.80∫0.12 3.89∫0.19 4.30∫0.04

Top: fBIC 3.13∫0.38 3.99∫0.46 4.77∫0.15

Table 2. Histometric data for the three different implant groups D–F (submerged approach)six months after implant placement, or three months after abutment connection, respectively.Mean values∫standard deviation [mm]; (ni)Ωnumber of measured implants / (nis)Ωnumber ofmeasured implant sites. ‘‘Top’’ refers to the coronal aspect of the abutments.

Variables D (niΩ10/nisΩ48) E (niΩ9/nisΩ47) F (niΩ10/nisΩ50)

SD 0.14∫0.05 0.13∫0.10 0.14∫0.11

JE 2.11∫0.60 1.50∫0.29 2.31∫0.34

CTC 1.41∫0.28 1.70∫0.40 1.35∫0.26

BW 3.67∫0.67 3.33∫0.34 3.80∫0.39

Top: GM 1.03∫0.80 1.42∫0.24 1.55∫0.58

Top: cJE 1.17∫0.77 1.55∫0.30 1.69∫0.64

Top: aJE 3.28∫0.38 3.06∫0.42 4.00∫0.46

Top: r/s 4.26∫0.05 4.58∫0.07 4.36∫0.05

Top: fBIC 4.70∫0.21 4.75∫0.22 5.35∫0.40

cal sections and 45 measurable implantsites were analyzed. The Biologic Widthdimension (BW) measured 2.84∫0.28mm (standard deviation) and the meandistance between the top of the implant(Top) to the gingival margin (GM) was0.32∫0.58 mm (Figs 4a, 4b, 11, Table 1).Ten one-piece, nonsubmerged implants(type B; Fig. 1a) with 39 histological sec-tions and 50 readable implant sites werestudied. For this implant group, the BWwas 3.57∫0.61 mm whereas the meandistance from the top of the implant(Top) to the gingival margin (GM) was0.42∫0.52 mm (Figs 5a, 5b, 11, Table 1).For the third nonsubmerged group, ninetwo-piece implants (type C; Fig. 1a) with33 histological sections and 40 sitescould be analyzed. The dimension forBW in this group was 3.38∫0.36 mmwith a distance from the top of the im-plant (Top) to the GM of 1.38∫0.43 mm(Figs 6a, 6b, 11, Table 1).

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Fig. 10. a. Schematic (true to scale) of soft and gin (GM) was significantly located more co- exhibits the vertical dimension of the sulcushard tissues around nonsubmerged implant types ronally (P,0.04) as compared to two-piece im- depth (SD), the pink compartment the junctionalA–C at time of sacrifice in relation to the rough/ plants (types C–F; see also Fig 10b). Arrows indi- epithelium (JE), and the yellow compartment thesmooth border (solid black line) as well as the cate the level of the crest of the bone at the time connective tissue contact (CTC). Note that forlocation of the microgap (interface; dashed black of implant placement. b. Schematic (true to two-piece titanium implants (types C–F), the tipline). The dark red compartment shows the verti- scale) of soft and hard tissues around submerged of the gingival margin (GM) was significantlycal dimension of the sulcus depth (SD), the pink implant types D–F at time of sacrifice in relation located more apically (P,0.04) as compared tocompartment the junctional epithelium (JE), and to the rough/smooth border (solid black line) as one-piece implants (types A, B; see also Fig.the yellow compartment the connective tissue well as the location of the microgap (interface; lOa). Arrows indicate the level of the crest of thecontact (CTC). Note that for one-piece titanium dashed black line). The dark red compartment bone at the time of implant placement.implants (types A, B), the tip of the gingival mar-

In the submerged group, ten two-pieceimplants (type D; Fig. 1b) with 38 histo-logical sections and 48 readable sitescould be measured. The dimension forBW was 3.67∫0.67 mm with a mean dis-tance from the top of the implant (Top)to the GM of 1.03∫0.80 mm (Figs 7a, 7b,11, Table 2). Nine submerged implants

Fig. 11. Histometric data for the six different im-plant groups A–F six months after implantplacement (mean values [mm]). Comparisonamong Biologic Width (BW) dimensions revealedsignificantly higher values for implant types B(P,0.04), D (P,0.02), and F (P,0.005; see aster-isks) as compared to type A implants. No sig-nificant changes (P.0.05) were evident comparingthe sulcus depth (SD) as well as the connectivetissue contact (CTC) dimensions among all im-plant types (A–F). However, the dimensions forjunctional epithelium (JE) were significantlylower comparing type A with type F implants(P,0.005), type A with type D (P,0.03), type Ewith type F (P,0.02).

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of type E (Fig. 1b) based on 39 histologi-cal sections and 47 measurable siteswere analyzed. In this submerged group,the BW dimension was 3.33∫0.34 mm.The mean distance from the top of theimplant (Top) to the GM was 1.42∫0.24mm (Figs 8a, 8b, 11, Table 2). For thethird submerged implant group, type F(Fig. 1b), ten implants with 40 sectionscould be analyzed based on 50 readablesites. The BW measured 3.80∫0.39 mmwith a mean distance from the top of theimplant (Top) to the GM of 1.55∫0.58mm (Figs 9a, 9b, 11, Table 2).

F-tests comparing implant types (A–F)were significant for BW, junctional epi-thelium (JE), and the distance betweenthe top of the implant (Top) to the GM(P,0.005). No significant differences(P.0.10) across implant types could befound for the dimensions of sulcus depth(SD), and for connective tissue contact(CTC). Comparing the implant typemeans for BW (Fig. 11), the mean dimen-sion for type A implants was signifi-cantly smaller than that for types B(P,0.04), D (P,0.02), and F (P,0.005).Differences among implant type meansfor junctional epithelium (JE) were ob-served, with type D implants signifi-cantly greater than type A (P,0.03), andwith type F implants significantlygreater than types A (P,0.005) and E(P,0.02). Finally, the distance betweenthe top of the implant (Top) to the GM

was significantly lower for one-piece im-plants (types A and B) compared to alltwo-piece implants (types C, D, E, and F;P,0.05). The side of the mandible andposition on the arch did not influencethe results (P.0.20).

Discussion

The results of this study indicate thatthe dimensions of the periimplant softtissues (i.e. the Biologic Width), as evalu-ated by histometric measurements, aresignificantly influenced by the presence/absence of a microgap (interface) be-tween the implant and the abutment,and the location of this microgap (inter-face) in relation to the crest of the bone.Furthermore, there was no difference inthe soft tissue dimensions comparingtwo-piece implants that had been placedutilizing a submerged technique as op-posed to placing them using a nonsub-merged approach. In addition, the tip ofthe gingival margin was significantlylocated more coronally for one-piececompared to two-piece titanium im-plants. Thus, the significant factor thatinfluences soft tissue dimensions is thepresence/absence of a microgap (inter-face) between components and not thesurgical technique used (submerged vs.nonsubmerged).

A comparison of the Biologic Width

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(linear vertical dimension of connectivetissue, junctional epithelium, and sulcusdepth) among different implant types(A–F) indicated that one-piece, nonsub-merged implants with a rough/smoothborder at the alveolar crest had thesmallest value of the six implant designstested, and resulted in the gingival mar-gin closest to the top of the implant sixmonths after placement. The BiologicWidth dimension around natural teeth,as measured in the classic work by Garg-iulo and coworkers (Gargiulo et al. 1961)was 2.73 mm, and thus very similar tothe 2.84 mm measured for the type Aimplants. Consequently, of all implanttypes examined in this study, the one-piece, nonsubmerged implant with arough/smooth border placed at the al-veolar crest resulted in soft tissue di-mensions most like the natural den-tition. Moving the rough/smooth borderon the implant (type B) more apically(approximately 1.0 mm) resulted in alarger Biologic Width (average increaseof 0.73 mm). This alteration occurredthrough both an increased junctionalepithelium (average 0.41 mm) and con-nective tissue dimension (average 0.34mm), supporting an earlier study onchanges in these dimensions over time(Hermann et al. 2000a). The gingivalmargin was only slightly displaced apic-ally (0.10 mm) in type B implants com-pared to type A implants that were alsoone-piece and nonsubmerged. Thesefindings suggest that the placement of aone-piece, nonsubmerged implant with arough/smooth border placed 1.0 mm be-low the alveolar crest will have approxi-mately the same gingival level and an in-creased Biologic Width dimension com-pared to a similar implant where therough/smooth border is placed at thelevel of the alveolar crest. The clinicalimplication of these findings is thatslightly submerging the rough/smoothborder on a one-piece, nonsubmergedimplant will not significantly jeopardizethe location of the gingival margin forthe final restoration.

A significant alteration of the softtissues occurs when a clinically relevantsized microgap (interface) of about 50mm is introduced according to several invitro reports which have shown thatmicrogap (interface) sizes of implant/abutment combinations currently used

567 | Clin. Oral Impl. Res. 12, 2001 / 559–571

vary from around 100 mm (Sorensen etal. 1991), to about 50 mm (Binon et al.1992; Keith et al. 1999), or even below10 mm (Besimo et al. 1994; Keith et al.1999). The influence of the microgap (in-terface) was independent of whether im-plants were placed in a nonsubmerged(type C implant) or in a submerged tech-nique (type D implant), by connecting anabutment to the top of the implant. Thisoccurred even when the microgap (inter-face) was located at the alveolar crest,i.e. the top of the implant is at the al-veolar crest and the abutment extendsfrom the top of the implant through thesoft tissues serving as a transgingivalcomponent. The type C implant wasessentially the same as the type B im-plant (both were placed in a nonsub-merged technique) except that amicrogap (interface) existed, making thetype C a two-piece implant placed in anonsubmerged technique. This approachhas been discussed/recommended forclinical use in recent years, trying to ap-ply the advantage of just one surgicalprocedure (as traditionally used for one-piece, nonsubmerged implants) whenemploying a two-piece implant tech-nique (Ericsson et al. 1994; Bernard et al.1995; Ericsson et al. 1996; Levy et al.1996; Becker et al. 1997; Ericsson et al.1997; Schnitman et al. 1997; Tarnow etal. 1997; Collaert & De Bruyn 1998; Ab-rahamsson et al. 1999). In this case, al-though the Biologic Width dimensionwas similar to the type B implant, a sig-nificant loss of gingival height (approxi-mately 300%) occurred (1.38 mm vs.0.42 mm). This finding can be explainedby the fact that the alveolar bone levelhas moved apically in the type C im-plant compared to the type B implant.With the type B implant, the crestalbone level was located at the rough/smooth border (Fig. 1a, Table 1; see alsoHermann et al. 1997; Hermann et al.2000b), while in the case of the type Cimplants, the crestal bone level waslocated apical to the rough/smooth bor-der. These findings, furthermore, suggestthat the influence of the microgap (inter-face) is greater than the effect of therough/smooth border as it relates to thefirst bone-to-implant contact on the im-plant. Consequently, these histologicalfindings also reinforce the radiologicalfindings around these implants and the

similar conclusion that the microgap (in-terface) has a significant influence oncrestal bone levels around two-piece im-plant systems (Hermann et al. 1997).

A comparison of the soft tissue dimen-sions around the type C and D implantsallows a comparison between the surgi-cal placement techniques (nonsub-merged vs. submerged). Both implanttypes were identical in regards to loca-tion of the microgap (interface) and therough/smooth border with the only dif-ference being that the type D implantswere submerged for three months afterwhich they were uncovered and theabutments placed. After abutment con-nection, these implant types were iden-tical. Thus, the difference was when theimplants and abutments were exposed tothe oral cavity (i.e. immediately uponplacement of type C implants, whiletype D implants were exposed threemonths later). The difference in tissuemeasurements between these two typesof implants ranged only from 0.02 mmto a maximum of 0.45 mm indicatingthat the surgical placement of the im-plants as two-piece, nonsubmerged im-plants (type C) or as two-piece, sub-merged implants (type D) did not have asignificant effect on crestal bone levelsas well as soft tissue dimensions. Be-cause the type D dimensions were simi-lar to type C and not similar to the di-mensions around type A or B implantsreinforces the suggestion that the pres-ence of a microgap (interface) signifi-cantly influences hard and soft tissuelevels around an implant. The clinicalimplication for these findings is that ifan abutment is connected to a tradition-ally submerged implant system at thetime of implant placement (Becker &Becker 1990; Ericsson et al. 1994;Bernard et al. 1995; Becker et al. 1997;Ericsson et al. 1997; Schnitman et al.1997; Tarnow et al. 1997; Collaert & DeBruyn 1998), thus creating a two-piece,nonsubmerged implant approach, crestalbone levels and soft tissue dimensionsshould be the same as if the implant isinitially submerged during first-stagesurgery, and three months later un-covered and abutments connected dur-ing second-stage surgery (i.e. crestalbone loss will occur and the gingivalmargin will move apically). Contradic-tory reports from experimental studies

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have been published in the 1990s (Ber-glundh et al. 1991; Abrahamsson et al.1996; Berglundh & Lindhe 1996; Abrah-amsson et al. 1999) where different two-piece, submerged implants have been in-vestigated in animal studies not experi-encing the same amount of crestal boneloss and apical migration of the gingivalmargin as observed clinically in previousstudies. An important detail in that re-gard seems to be the fact that accordingto the protocol in the present study,abutments on all two-piece implants(types C–F) were disconnected and im-mediately tightened afterwards, tryingto imitate clinically relevant steps likethe exchange of a healing abutment, im-pression taking, and the insertion of thesuperstructure. These steps were notcarried out in the four above-mentionedstudies. However, once the same re-search group repeated their experiments(Abrahamsson et al. 1997), including thedisconnection/tightening of the abut-ments, the same amount of crestal boneloss, apical migration of the gingivalmargin, as well as overall dimension forthe Biologic Width could be observedand, thus, the results of this study groupwere confirmed (Hermann et al. 1997;Hermann et al. 2000b; Hermann et al.2001).

The type E and type F implants weredesigned to test the hypothesis that iftissue levels were influenced by amicrogap (interface), then moving the in-terface coronally one millimeter fromthe alveolar crest (type E) should mini-mize its influence on the tissues, andmoving the interface apically one milli-meter (type F), would result in more sig-nificant tissue changes. These valuescould then be compared to type D im-plants where the interface was located atthe alveolar crest. ln type E implants,the crestal bone was found to be locatedat the rough/smooth border similar tothe type B implant. In this case, the firstbone-to-implant contact reacted as if nomicrogap (interface) was present, i.e.moving the interface coronally mini-mized its influence on the crestal bonelevel (Hermann et al. 1997; Hermann etal. 2000b; Hermann et al. 2001). In re-gards to the soft tissues, the type E im-plants had the smallest Biologic Widthdimension of all the submerged implanttypes. Additionally, the length of the

568 | Clin. Oral Impl. Res. 12, 2001 / 559–571

junctional epithelium was the smallest(1.50 mm) of the submerged implants,and the connective tissue dimension thelargest (1.70 mm). In comparison to thetype B implants which were similar totype E implants except that there was nomicrogap (interface), the differences invalues for sulcus depth, junctional epi-thelium, and connective tissue contactaround type E implants were 0.08 mm,0.24 mm, and 0.08 mm, respectively, in-dicating that moving the microgap (in-terface) coronally minimized its influ-ence on the soft tissues with the resultthat the tissues were more similar to aone-piece implant (an implant without amicrogap/interface).

The type F implants had the microgap(interface) located one millimeter belowthe alveolar crest. As predicted by thehypothesis, this arrangement resulted inthe most significant tissue changesaround the six different implant typesand confirmed the radiographic findings(Hermann et al. 1997). The BiologicWidth dimension had the largest value(3.80 mm) of all the implants, both sub-merged and nonsubmerged, as did thelength of the junctional epithelium (2.31mm). Furthermore, the top of the im-plant to the gingival margin, the top ofthe implant to the apical extent of thejunctional epithelium, and the top of theimplant to the first bone-to-implant con-tact were the largest recorded for all siximplant types. These findings indicatethat the apical placement of a microgap(interface), as recommended clinically inorder to achieve a harmonious emer-gence profile in areas of esthetic concern(Saadoun et al. 1994; Palacci et al. 1995;Spiekermann 1995; Nevins & Stein1998), has the most significant influenceon the hard and soft tissues with thelargest Biologic Width dimension, themost apical location of the crestal bone,small connective tissue contact area,very long epithelial attachment, and themost apical location of the gingival mar-gin. The clinical implications for suchan implant design and placement arethat a recession of the gingival marginshould be expected using such a sub-merged implant technique with the ap-propriate consequences as to an im-paired esthetic result, and a more diffi-cult maintenance as the epithelialcontact will extend apically at least to

the level of the microgap (interface)which was placed below the alveolarcrest. Since it has been reported clin-ically that microgaps (interfaces) in two-piece implant systems show bacterialcolonization (Quirynen & van Steen-berghe 1993; Persson et al. 1996), a moreapical location of such flora may tend tofavor a more pathogenic, anaerobic com-position of bacteria and accordingly, amore severe degree of periimplant in-flammation. This approach (type F im-plants) creates an infrabony defect sinceat the time of abutment connection, theinterface is created below the crestalbone level. These histometric findingsdemonstrate that tissue changes will oc-cur such that the crestal bone will resorbto a level below the microgap (interface),and that the junctional epithelium willextend towards this level with a result-ing small connective tissue contact area.These data confirm the changes intissues around submerged and nonsub-merged implants discussed by Cochranand Mahn (Cochran & Mahn 1992), andthe results by other investigators (Weberet al. 1996; Abrahamsson et al. 1997;Hermann et al. 1997; Hermann et al.2000b).

The precise cause of the tissuechanges that were observed around im-plants in this side-by-side comparisonof implant types is not known. Onepossible explanation is that themicrogap (interface) represents a site ofinfection, and the host reacts with aninflammatory response. Consequently,alveolar bone loss combined with anapical migration of the junctional epi-thelium beneath this area, tries to pro-tect the internal part of the body fromthis source of inflammation by reestab-lishing the ectodermal integrity of thebody. This is similar to what occurs incyst formation, such as that foundaround the apices of nonvital teeth thatbecome infected. Furthermore, it isclear that the microgap (interface) of atwo-piece titanium implant is contami-nated with bacteria (Quirynen & vanSteenberghe 1993; Persson et al. 1996),possibly through microbial leakagethrough the transocclusal screw accesshole (Jansen et al. 1997; Guindy et al.1998; Gross et al. 1999) or due to bac-terial colonization along the abutment.Thus, the tissue changes demonstrated

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could be the result of the inflammationassociated with the bacterial contami-nation of the microgap (interface). Thisis reinforced by the fact that a meticu-lous mechanical as well as chemicalplaque control has been performedthroughout the present study, and byexamining the soft tissue histologicallyaround implant types A and B (Figs 4b,5b) exhibiting minimal signs of peri-implant inflammation, as opposed tothe soft tissue status around implanttypes C-F (Figs 6b, 7b, 8b, 9b) showingmoderate to severe degrees of periimpl-ant inflammation. Thus, if one wants tochoose an implant design with the leastinflammation, and consequently thesmallest resultant tissue changes, a one-piece implant design should be selected.

There are several clinical conse-quences to the histometric tissuechanges demonstrated in this study.One such consequence is when im-plants are being placed in an areawhere minimal bone height is availableto support the implant such as in theposterior mandible above the mandibu-lar canal and nerve, and in the pos-terior maxilla below the maxillary si-nus. In these indications it would beimportant to use an implant designthat will not result in crestal bone lossas the amount of supporting bone is al-ready compromised. Furthermore, inareas of esthetic concern, an implantdesign that results in soft tissue dimen-sions similar to natural teeth (Cochranet al. 1997; Hermann et al. 2000a),with minimal alveolar bone crestchanges (Hermann et al. 1997; Herm-ann et al. 2000b) and the least effect onthe gingival margin (this study) wouldbe advantageous. Stable bone levels re-sult in stable soft tissues as was dem-onstrated in a one-year, longer-term ex-perimental animal study analyzing un-loaded as well as loaded implants(Cochran et al. 1997; Hermann et al.2000a). These data have been recentlyconfirmed in humans by preciselyexamining alveolar bone levels overeight years in patients (Buser et al.1999). In that study, out of 97 patientsanalyzed, a distribution of bonechanges around these one-piece, non-submerged implants indicated thatmore implants actually gained thanlost crestal bone. These findings can be

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contrasted to another implant designwhich utilizes a microgap (interface)placed at or below the alveolar crest(two-piece, submerged approach), whereone major success criterion is the ex-pected crestal bone loss of 1.5 mmafter one year of loading (Albrektssonet al. 1986; Smith & Zarb 1989). Takentogether, these findings support the ex-perimental results in the present studyand demonstrate that there are import-ant clinical consequences to the im-plant design chosen.

Conclusions

The findings from the present experi-mental study show that significantly in-creased amounts of crestal bone lossaround two-piece vs. one-piece implantsalso result in a significant more apicalposition of the gingival margin. In ad-dition, Biologic Width dimensions varydepending on implant design. BiologicWidth around one-piece implants ismore similar to natural teeth dimen-sions as compared to two-piece im-plants, either being placed according toa submerged or a nonsubmerged tech-nique. Additionally, the degree of in-flammation in periimplant tissues is lessaround one-piece implants compared totwo-piece implants. These results mayhave important implications when deal-ing with esthetic implant-borne restora-tions, which are based on healthy andvertically constant soft tissue dimen-sions over time.

Acknowledgements

Sonja A. Bustamante, H.T. (ASCP), University ofTexas Health Science Center at San Antonio(UTHSCSA), is greatly acknowledged for her conti-nuous and valuable support throughout the study.The authors also would like to thank Richard J.Haines, DVM, Clinical Veterinarian, and his team,Laboratory Animal Resources, UTHSCSA, for exem-plary care of the animals. In addition, the authorswould like to express their gratitude to James P.Simpson, B.Sc. (Eng), Ph.D., and the Institut Strau-mann AG, Waldenburg/BL, Switzerland, for manu-facturing the test implants. Last but not least, wewould like to express our appreciation for thesuperb work by Britt Hoffmann, H.T., University ofBern School of Dental Medicine, preparing the his-tological sections. This investigation has been sup-ported by two grants from the ITI (InternationalTeam for Oral Implantology)-Foundation for the Pro-motion of Oral Implantology (. 16–95/094, . 20–97/

134), Waldenburg/BL, Switzerland, and by stipendsfrom the Swiss Society of Periodontology, Bern,Switzerland, the Swiss National Science Founda-tion, Basel, Switzerland, the Swiss Foundation forMedical and Biological Stipends, Bern, Switzerland,as well as the University of Basel Committee forthe Promotion of Philosophiae Doctor candidates,Basel, Switzerland.

Resume

L’esthetique gingivale autour des dents naturellesest basee sur une dimension verticale constante destissus mous parodontaux sains qui porte le nom deLargeur Biologique. Cependant lorsque des implantsendo-osseux sont places, differents facteurs influen-cent les reactions tissulaires paroımplantaires destissus dur et mou qui ne sont pas toujours biencomprises. Le but de cette etude a ete d’examinerhistomorphometriquement les dimensions des tissusmous paroımplantaires sur les differentes localisa-tions, soit d’implants en une piece au niveau de lafrontiere lisse/rugueuse soit d’implants en deux par-ties au niveau du micro-interstice (interface), en re-lation avec la crete osseuse; les implants en deuxparties ayant ete places suivant la technique enfouieou non-enfouie. Cinquante-neuf implants ont ainsiete places dans les aires mandibulaires edentees decinq chiens dans une comparaison par site. Au mo-ment de tuer les chiens, six mois apres le place-ment des implants, la dimension de la Largeur Bio-logique pour les implants en une piece avec la limi-te lisse/rugueuse placee au niveau de la cretealveolaire etait significativement inferieure(P,0.005) comparee a celle des implants en deuxparties qui avaient leur interface placee au niveauou en-dessous de la crete osseuse. De plus pour lesimplants en une piece, le sommet de la gencivemarginale etait place significativement plus en coro-naire (P,0.005) compare aux implants en deux pie-ces. Ces decouvertes evaluees par histologie de cou-pes non-decalcifiees sans charge dans la mandibuledu chien suggerent que la gencive marginale est si-tuee plus coronairement et que les dimensions de laLargeur Biologique sont plus semblables aux dentsnaturelles autour des implants non-enfouis en unepiece qu’au niveau des implants en deux partiesqu’ils soient non-enfouis ou enfouis.

Zusammenfassung

Die rote Asthetik um naturliche Zahne basiert im We-sentlichen auf einer Konstanten in der vertikalen Di-mension der gesunden parodontalen Weichgewebe,der sogenannten biologischen Breite. Wenn enossaleImplantate eingesetzt werden beeinflussen aber ver-schiedene Faktoren, welche bis heute noch nicht imDetail bekannt sind, die Reaktionen der periimplanta-ren Weich- und crestalen Hartgewebe. Das Ziel dieserStudie war es daher, die periimplantaren Weichge-websdimensionen in Abhangigkeit der Lokalisationeneines Implantatuberganges von der glatten zur rauhenOberflache beim einteiligen Implantat, oder desMikrospaltes (Verbindungsstelle) beim zweiteiligenImplantat histometrisch zu untersuchen. Insbesonde-re besprach man die Relationen zum Knochenkamm,wenn das zweiteilige Implantat mit einem submuko-

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sen oder aber einem transmukosen Operationsproto-koll gesetzt worden war. Es konnten 59 Implantate imdirekten Vergleich beidseits in die zahnlosen Unter-kieferregionen von funf Jagdhunden eingesetzt wer-den. Bei Abschluss der Studie, sechs Monate nach derImplantation, war die ‘‘Biologische Breite’’ bei eintei-ligen Implantaten (Grenzlinie zwischen rauher undglatter Oberflache direkt an der Knochenlinie) signi-fikant kleiner (P,0.05) als bei zweiteiligen Implanta-ten mit der Mikrospalte (Schnittstelle kommt direktan oder leicht unter die Knochenlinie zu liegen). Dazukommt, dass bei einteiligen Implantaten der Gingival-saum (GM) signifikant deutlich koronaler zu liegenkam (P,0.005) als bei zweiteiligen Implantaten. DieAnalysen von nichtentkalkten histologischen Schnit-ten dieser unbelasteten Implantate im Unterkiefer desHundes lassen vermuten, dass der mehr koronal gele-gene Gingivalsaum (GM) und die Dimensionen der‘‘Biologische Breite’’ (BW) bei einteiligen transmuko-sen Implantaten den Verhaltnissen eines naturlichenZahnes weit naher kommen, als es bei den zweiteili-gen transmukosen oder submukosen Implantaten derFall ist.

Resumen

La estetica gingival alrededor de dientes naturales estabasada sobre una dimension vertical constante de lostejidos blandos periodontales sanos, la anchura biologi-ca. Cuando se colocan implantes endooseos, de todos

ReferencesAbrahamsson, I., Berglundh, T., Wennstrom, J. &

Lindhe, J. (1996) The peri-implant hard and softtissues at different implant systems. A comparativestudy in the dog. Clinical Oral Implants Research

7: 212–219.Abrahamsson, I., Berglundh, T. & Lindhe, J. (1997) The

mucosal barrier following abutment dis/reconnec-tion. An experimental study in dogs. Journal of

Clinical Periodontology 24: 568–572.Abrahamsson, I., Berglundh, T., Moon, I.S. & Lindhe,

J. (1999) Peri-implant tissues at submerged and non-submerged titanium implants. Journal of Clinical

Periodontology 26: 600–607.Albrektsson, T., Zarb, G., Worthington, P. & Eriksson,

A.R. (1986) The long-term efficacy of currently useddental implants: a review and proposed criteria ofsuccess. International Journal of Oral and Maxillo-

facial Implants 1: 11–25.Becker, W. & Becker, B.E. (1990) Guided tissue re-

generation for implants placed into extractionsockets and for implant dehiscences: surgical tech-niques and case report. International Journal of

Periodontics and Restorative Dentistry 10: 376–391.

Becker, W., Becker, B.E., Israelson, H., Lucchini, J.P.,Handelsman, M., Ammons, W., Rosenberg, E., Rose,L., Tucker, L.M. & Lekholm, U. (1997) One-step sur-gical placement of Brånemark implants: a prospec-tive multicenter clinical study. International

Journal of Oral and Maxillofacial Implants 12: 454–462.

Berglundh, T., Lindhe, J., Ericsson, I., Marinello, C.P.,Liljenberg, B. & Thomsen, P. (1991) The soft tissuebarrier at implants and teeth. Clinical Oral Im-

plants Research 2: 81–90.

570 | Clin. Oral Impl. Res. 12, 2001 / 559–571

modos, existen diversos factores que influyen en lasreacciones de los tejidos blandos periimplantarios y te-jidos duros crestales, que no han sido bien comprendi-dos hasta la fecha. Por lo tanto, el proposito de esteestudio fue examinar histometricamente las dimen-siones de los tejidos blandos periimplantarios depen-diendo de varias localizaciones de un borde de implan-tes de una sola pieza rugoso/liso o un microespacio(interfase) en implantes de dos piezas en relacion conla cresta osea, con implantes de dos piezas colocadostanto con la tecnica sumergida como con la no sumer-gida. De este modo, se colocaron 59 implantes enareas mandibulares edentulas de cinco foxhounds enuna comparacion lado a lado. En el momento del sacri-ficio, seis meses despues de la colocacion de los im-plantes, la dimension de la anchura biologica para im-plantes de una pieza, con el borde rugoso/liso localiza-do en el nivel de la cresta osea, fue significativamentemenor (P,0.05) comparado con los implantes de dospiezas con un microespacio (interfase) localizado en opor debajo la cresta osea. Ademas, para implantes deuna pieza, el extremo del margen gingival (GM) se lo-calizo significativamente mas coronal (P,0.005) com-parado con los implantes de dos piezas. Estos hallaz-gos, evaluados por histologıa no descalcificada bajocondiciones sin carga en la mandıbula canina, sugie-ren que el margen gingival (GM) esta localizado mascoronal y dimension de la anchura biologica (BG) esmas similar a dientes naturales alrededor de implantesde una pieza no sumergidos comparados con tanto losimplantes de dos piezas no sumergidos como los dedos piezas sumergidos.

Berglundh, T. & Lindhe, J. (1996) Dimension of theperiimplant mucosa. Biological width revisited.Journal of Clinical Periodontology 23: 971–973.

Bernard, J.P., Belser, U.C., Martinet, J.P. & Borgis, S.A.(1995) Osseointegration of Brånemark fixtures usinga single-step operating technique. A preliminaryprospective one-year study in the edentulous man-dible. Clinical Oral Implants Research 6: 122–129.

Besimo, C., Bodenschatz, V., Guggenheim, R., Duggel-in, M., Mathys, D., Maurer, J., Jahn, M. & Graber,G. (1994) Marginale Passgenauigkeit prafabrizierterKronen auf Ha-Ti Implantaten. Zeitschrift fur Zah-

narztliche Implantologie 10: 191–198.Binon, P., Weir, D., Watanabe, L. & Walker, L. (1992)

Implant component compatibility. In: Laney, W.R.,Tolman, D.E., eds. Tissue Integration in Oral,

Orthopedic and Maxillofacial Reconstruction, 1stedition, pp. 218–226. Chicago: Quintessence.

Buser, D., Mericske-Stern, R., Dula, K. & Lang, N.P.(1999) Clinical experience with one-stage, non-sub-merged dental implants. Advances in Dental Re-

search 13: 153–161.Cochran, D.L. & Mahn, D.H. (1992) Dental implants

and regeneration. Part I. Overview and biologicalconsiderations. In: Hardin, J., ed. Clarks Clinical

Dentistry 5th edition, Chapter 59 : pp. 1–7. Philadel-phia: J. B. Lippincott Company.

Cochran, D.L. (1996) Implant Therapy I. In: TheAmerican Academy of Periodontology, ed. 1996

World Workshop in Periodontics, 1st edition, pp.707–790. Chicago: The American Academy of Peri-odontology.

Cochran, D.L., Hermann, J.S., Schenk, R.K., Higgin-bottom, F.L. & Buser, D. (1997) Biologic widtharound titanium implants. A histometric analysis of

the implanto-gingival junction around unloaded andloaded nonsubmerged implants in the canine man-dible. Journal of Periodontology 68: 186–198.

Collaert, B. & De Brnyn, H. (1998) Comparison ofBrånemark fixture integration and short-term sur-vival using one-stage or two-stage surgery in com-pletely and partially edentulous mandibles. Clinical

Oral Implants Research 9: 131–135.Ericsson, I., Randow, K., Glantz, P.O., Lindhe, J. &

Nilner, K. (1994) Clinical and radiographical fea-tures of submerged and nonsubmerged titanium im-plants. Clinical Oral Implants Research 5: 185–189.

Ericsson, I., Nilner, K., Klinge, B. & Glantz, P.O. (1996)Radiographical and histological characteristics ofsubmerged and nonsubmerged titanium implants.An experimental study in the Labrador dog. Clinical

Oral Implants Research 7: 20–26.Ericsson, I., Randow, K., Nilner, K. & Petersson, A.

(1997) Some clinical and radiographical features ofsubmerged and non-submerged titanium implants.A 5-year follow-up study. Clinical Oral Implants

Research 8: 422–426.Feneis, H. (1952) Gefuge und Funktion des normalen

Zahnfleischbindegewebes. Deutsche Zahnarztliche

Zeitschrift 2: 467–476.Gargiulo, A.W., Wentz, F.M. & Orban, B. (1961) Dimen-

sions and relations of the dentogingival junction inhumans. Journal of Periodontology 32: 261–267.

Gottlieb, B. (1921) Der Epithelansatz am Zahne. Deut-

sche Monatsschrift fur Zahnheilkunde 5: 142–147.Gross, M., Abramovich, I. & Weiss, E.I. (1999) Micro-

leakage at the abutment-implant interface of osseo-integrated implants: a comparative study. Interna-

tional Journal of Oral and Maxillofacial Implants

14: 94–100.

Page 13: Biologic Width Around One- And Two-piece Titanium Implants

Hermann et al . Biologic Width around one- and two-piece titanium implants

Guindy, J.S., Besimo, C.E., Besimo, R., Schiel, H. &Meyer, J. (1998) Bacterial leakage into and from pre-fabricated screw-retained implant-borne crowns in

vitro. Journal of Oral Rehabilitation 25: 403–408.Hammerle, C.H., Bragger, U., Burgin, W. & Lang, N.P.

(1996) The effect of subcrestal placement of thepolished surface of ITIA implants on marginal softand hard tissues. Clinical Oral Implants Research

7: 111–119.Hermann, J.S., Cochran, D.L., Nummikoski, P.V. &

Buser, D. (1997) Crestal bone changes around ti-tanium implants. A radiographic evaluation of un-loaded nonsubmerged and submerged implants inthe canine mandible. Journal of Periodontology 68:1117–1130.

Hermann, J.S., Buser, D., Schenk, R.K., Higginbottom,F.L. & Cochran, D.L. (2000a) Biologic Width aroundtitanium implants. A physiologically formed andstable dimension over time. Clinical Oral Implants

Research 11: 1–11.Hermann, J.S., Buser, D., Schenk, R.K. & Cochran,

D.L. (2000b) Crestal bone changes around titaniumimplants. A histometric evaluation of unloadednonsubmerged and submerged implants in the can-ine mandible. Journal of Periodontology 71: 1412–1424.

Hermann, J.S., Schoolfield, J.D., Nummikoski, P.V.,Buser, D., Schenk, R.K. & Cochran, D.L. (2001)Crestal bone changes around titanium implants. Amethodological study comparing linear radiographicversus histometric measurements. International

Journal of Oral and Maxillofacial Implants, inpress.

Ingber, J.S. (1976) Forced eruption: Part II. A methodof treating nonrestorable teeth: periodontal and re-storative considerations. Journal of Periodontology

47: 203–216.Ingber, J.S., Rose, L.F. & Coslet, J.G. (1977) The ‘‘Bio-

logic Width ‘’ – a concept in periodontics and re-storative dentistry. Alpha Omegan 70: 62–65.

571 | Clin. Oral Impl. Res. 12, 2001 / 559–571

Jansen, V.K., Conrads, G. & Richter, E.J. (1997) Mi-crobial leakage and marginal fit of the implant-abut-ment interface. International Journal of Oral and

Maxillofacial Implants 12: 527–540.Keith, S.E., Miller, B.H., Woody, R.D. & Higginbot-

tom, F.L. (1999) Marginal discrepancy of screw-re-tained and cemented metal-ceramic crowns on im-plant abutments. International Journal of Oral and

Maxillofacial Implants 14: 369–378.Levy, D., Deporter, D.A., Pilliar, R.M., Watson, P.A. &

Valiquette, N. (1996) Initial healing in the dog ofsubmerged versus non-submerged porous-coated en-dosseous dental implants. Clinical Oral Implants

Research 7: 101–110.Nevins, M. & Stein, J.M. (1998) The placement of

maxillary anterior implants. In: Nevins, M., Mel-lonig, J.T., eds. Implant Therapy – Clinical Ap-

proaches and Evidence of Success 1st edition, pp.111–127. Chicago, Berlin, London, Tokyo, Paris,Barcelona, Sao Paulo, Moscow, Prague, Warsaw:Quintessence Publishing Co., Inc.

Orban, B. & Mueller, E. (1929) The gingival crevice.Journal of the American Dental Association 16:1206–1242.

Palacci, P., Ericsson, I. & Engstrand, P. (1995) ImplantPlacement. In: Palacci, P., Ericsson, I., Engstrand, P.,Rangert, B., eds. Optimal Implant Positioning and

Soft Tissue Management for the Brånemark System

1st edition, pp. 35–39. Chicago, Berlin, London,Tokyo, Sao Paulo, Moscow, Prague, Warsaw: Quin-tessence Publishing Co., Inc.

Persson, L.G., Lekholm, U., Leonhardt, A., Dahlen,G. & Lindhe, J. (1996) Bacterial colonization oninternal surfaces of Brånemark systemA implantcomponents. Clinical Oral Implants Research 7:90–95.

Quirynen, M. & van Steenberghe, D. (1993) Bacterialcolonization of the internal part of two-stage im-plants. An in vivo study. Clinical Oral Implants Re-

search 4: 158–161.

Saadoun, A.P., Sullivan, D.Y., Krischek, M. & Le Gall,M. (1994) Single tooth implant – management forsuccess. Practical Periodontics and Aesthetic Den-

tistry 6: 73–80.Schenk, R.K., Olah, A.J. & Hermann, W. (1984) Prep-

aration of calcified tissues for light microscopy. In:Dickson, G.R., ed. Methods of Calcified Tissue

Preparation 1st edition, pp. 1–56. Amsterdam, NewYork, Oxford: Elsevier Science Publishers B. V.

Schnitman, P.A., Wohrle, P.S., Rubenstein, J.E., DaSil-va, J.D. & Wang, N.H. (1997) Ten-year results forBrånemark implants immediately loaded with fixedprostheses at implant placement. International

Journal of Oral and Maxillofacial Implants 12: 495–503.

Sicher, H. (1959) Changing concepts of the supportingdental structures. Oral Surgery, Oral Medicine,

Oral Pathology 12: 31–35.Smith, D.E. & Zarb, G.A. (1989) Criteria for success

of osseointegrated endosseous implants. Journal of

Prosthetic Dentistry 62: 567–572.Sorensen, J.A., Avera, S.P. & Tomas, C. (1991) Com-

parison of interface fidelity of implant systems.Journal of Dental Research 70: 540.

Spiekermann, H. (1995) Single-tooth implants. In:Spiekermann, H., ed. Implantology 1st edition, pp.267–298. New York: Thieme Medical PublishersInc.

Tarnow, D.P., Emtiaz, S. & Classi, A. (1997) Immedi-ate loading of threaded implants at stage 1 surgeryin edentulous arches: ten consecutive case reportswith 1- to 5-year data. International Journal of Oral

and Maxillofacial Implants 12: 319–324.Weber, H.P., Buser, D., Donath, K., Fiorellini, J.P.,

Doppalapudi, V., Paquette, D.W. & Williams, R.C.(1996) Comparison of healed tissues adjacent to sub-merged and nonsubmerged unloaded titanium den-tal implants. A histometric study in beagle dogs.Clinical Oral Implants Research 7: 11–19.