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Biologic Width and Morphologic Characteristics of Soft Tissues Around Immediately Loaded Implants: Studies Performed on Human Autopsy Specimens George E. Romanos,* Tonino Traini, Carina B. Johansson, and Adriano Piattelli Background: Esthetics and the health of oral implants are based upon the soft tissue reaction and biologic width (BW). Methods: Twelve dental implants were placed in the maxilla and mandible of a patient who smoked. Permanent standard abutments and temporary restorations were immediately fixed in place during the surgery stage. The definitive restorations were placed 4 months after loading without removal of the original abutments. After 10 months, the patient died, and the implants were removed en block and processed for histol- ogy. Results: The BW in the maxilla was 6.5 2.5 mm, whereas in the mandible, it was 4.8 1.3 mm (P = 0.017). The sulcular epithelium (SE) in the maxilla was 2.7 0.8 mm, whereas in the mandible, it was 1.7 0.4 mm (P <0.001). The junctional epithelium (JE) in the maxilla was 1.3 0.4 mm, whereas in the mandible, it was 1.5 0.5 mm (P = 0.164). The connective tissue (CT) in the maxilla was 2.5 1.3 mm, whereas in the mandible, it was 1.6 0.4 mm (P = 0.006). In the maxillary bone, the BW, SE, and CT were significantly longer than in the mandible, whereas for the JE, no statistically significant difference was observed. Conclusion: The soft tissue organization around dental im- plants was different for upper and lower jawbones. J Periodon- tol 2010;81:70-78. KEY WORDS Connective tissue; dental implants; dental prosthesis, implant supported; epithelial cells; junctional epithelium. T he present focus of implant re- search in dentistry principally involves the peri-implant soft tis- sues because of an increasing aware- ness of the importance of a stable and healthy soft tissue–implant interface. Soft tissue health is critical to the patient’s perception of a successful restoration, and long-term biofunctionality and es- thetic appearance are mainly based on the stability of the biologic width (BW). 1 The BW around natural teeth was first defined in the 1960s. 2 As reported in a number of studies, 3-10 the peri-implant BW is composed of an epithelium over- lying connective tissue (CT), with many similarities to the dento-gingival tissues around teeth. 11,12 It was reported that the maintenance and stability of the load- bearing implant are dependent on the establishment of a functional barrier at the transmucosal passage of the abut- ment, 13 which is important to protect the implant interface from invasion of bacte- ria from the oral cavity. 6,14,15 The for- mation of a stable peri-implant seal derives from the equilibrium between the host epithelium and bacterial plaque aggression. 16 Nevertheless, despite sim- ilarities in organization and function, differences exist in the way CT, in the absence of root cementum, connects * Unit of Laser Dentistry, Division of Periodontology, Eastman Institute for Oral Health, University of Rochester, Rochester, NY. † Dental School, University of Chieti–Pescara, Chieti, Italy. ‡ School of Health and Medical Sciences, University of Orebro, Sweden. doi: 10.1902/jop.2009.090364 Volume 81 • Number 1 70

Transcript of Journal of periodontology 2010 romanos

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Biologic Width and MorphologicCharacteristics of Soft Tissues AroundImmediately Loaded Implants: StudiesPerformed on Human AutopsySpecimensGeorge E. Romanos,* Tonino Traini,† Carina B. Johansson,‡ and Adriano Piattelli†

Background: Esthetics and the health of oral implants arebased upon the soft tissue reaction and biologic width (BW).

Methods: Twelve dental implants were placed in the maxillaand mandible of a patient who smoked. Permanent standardabutments and temporary restorations were immediately fixedin place during the surgery stage. The definitive restorationswere placed 4 months after loading without removal of theoriginal abutments. After 10 months, the patient died, andthe implants were removed en block and processed for histol-ogy.

Results: The BW in the maxilla was 6.5 – 2.5 mm, whereasin the mandible, it was 4.8 – 1.3 mm (P = 0.017). The sulcularepithelium (SE) in the maxilla was 2.7 – 0.8 mm, whereas inthe mandible, it was 1.7 – 0.4 mm (P <0.001). The junctionalepithelium (JE) in the maxilla was 1.3 – 0.4 mm, whereas inthe mandible, it was 1.5 – 0.5 mm (P = 0.164). The connectivetissue (CT) in the maxilla was 2.5 – 1.3 mm, whereas in themandible, it was 1.6 – 0.4 mm (P = 0.006). In the maxillarybone, the BW, SE, and CT were significantly longer than inthe mandible, whereas for the JE, no statistically significantdifference was observed.

Conclusion: The soft tissue organization around dental im-plants was different for upper and lower jawbones. J Periodon-tol 2010;81:70-78.

KEY WORDS

Connective tissue; dental implants; dental prosthesis,implant supported; epithelial cells; junctional epithelium.

The present focus of implant re-search in dentistry principallyinvolves the peri-implant soft tis-

sues because of an increasing aware-ness of the importance of a stable andhealthy soft tissue–implant interface. Softtissue health is critical to the patient’sperception of a successful restoration,and long-term biofunctionality and es-thetic appearance are mainly based onthe stability of the biologic width (BW).1

The BW around natural teeth was firstdefined in the 1960s.2 As reported ina number of studies,3-10 the peri-implantBW is composed of an epithelium over-lying connective tissue (CT), with manysimilarities to the dento-gingival tissuesaround teeth.11,12 It was reported that themaintenance and stability of the load-bearing implant are dependent on theestablishment of a functional barrier atthe transmucosal passage of the abut-ment,13 which is important to protect theimplant interface from invasion of bacte-ria from the oral cavity.6,14,15 The for-mation of a stable peri-implant sealderives from the equilibrium betweenthe host epithelium and bacterial plaqueaggression.16 Nevertheless, despite sim-ilarities in organization and function,differences exist in the way CT, in theabsence of root cementum, connects

* Unit of Laser Dentistry, Division of Periodontology, Eastman Institute for Oral Health,University of Rochester, Rochester, NY.

† Dental School, University of Chieti–Pescara, Chieti, Italy.‡ School of Health and Medical Sciences, University of Orebro, Sweden.

doi: 10.1902/jop.2009.090364

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with the surface of implants in a scar-like manner.The differences indicate that important dynamicfactors affect the organization of the sulcular epithe-lium (SE), junctional epithelium (JE), and CT.17,18

The SE and JE form the first line of defense againstmicrobial invasion, and they hinder microbial colo-nization by a rapid exfoliation. Recently, Schupbachand Glauser19 described remnants in hemidesmo-somes (HDs) at the surface of sulcular epithelialcells around implants due to the high rate of cell des-quamation, which is 50 times higher than that re-ported in the oral epithelium.20 The histologic andphysiologic organization of the JE was well de-scribed elsewhere.21-27 It was also reported thathuman JE cells are able to connect to a titanium-coated resin implants by either the basal lamina orHDs.28

The fiber apparatus of the CT provides a denseframework that results in mechanical resistance ofthe gingiva, allowing it to withstand frictional forcesthat result from mastication.29 The direct attachmentof the collagen fibers to the implant surface is contro-versial in the dental literature19 due to the absence ofcementum to anchor the collagen fibrils. Moreover,depending on the implant surface texture, substantialdifferences were reported.19

The peri-implant CT collagen fiber orientation wasstudied in several animal models. In beagle dogs, sev-eral reports4,30,31 described collagen fibers runningparallel to the implant surface, more or less in thecoronal-apical direction. Other authors reportedcollagen fibers oriented circumferentially aroundimplants in monkeys32 and humans.33 However, an-other article31 reported the presence of fibers directedperpendicular/oblique to the implant surface in dogs.Also, the fibers appeared to be more prominent onmicrotextured, compared to smooth transmucosal,surfaces in a dog experiment.19

In a recent human study, Schierano et al.34 evalu-ated the organization of the CT around nine loadedimplants in seven patients. They found a constantspatial arrangement of the peri-implant CT. In thefirst 200 mm from the implant surface, longitudinalcollagen fibers were observed, and between 200and 800 mm from the implant surface, circular col-lagen fibers were found, whereas externally, onlyoblique collagen fibers were noted. The organiza-tion of the peri-implant soft tissues related to theloading regimen was also evaluated. Siar et al.15

reported that the dimensions of the peri-implantsoft tissues were within the biologic range of nat-ural teeth and were not influenced by immediatefunctional loading or posterior location of the im-plants in the macaque mandible. Also, in a dog study,Hermann et al.17 found no differences in the BWaround non-submerged, one-piece titanium implants

under unloaded and loaded conditions. Moreover,Abrahamsson and Cardaropoli35 recently reportedno significant differences in the peri-implant softtissue dimensions for gold and titanium used in themarginal zone of the implant.

While referring to the implant component mor-phology as a variable for the organization of thesoft tissue, Abrahamsson et al.,8 in a beagle dogstudy using three dental implant systems withone- and two-stage surgical implants, reportedthat the geometry of the titanium implant seemedto be of limited importance for the peri-implant softtissue organization. Nevertheless, in a dog modelusing unloaded Ankylos implants, Tenenbaumet al.36 reported a greater length and larger widthof CT as well as a shorter epithelial downgrowthcompared to studies on AstraTech, Branemark,and ITI implants. Moreover, the histologic mild in-flammation noted in the CT was related to the ab-sence of a microgap in the Ankylos implantsystem. In a retrospective histologic study in mon-keys on early and immediately loaded implantsinserted in postextraction sites, Piattelli et al.37 re-ported that less bone loss was observed as the mi-crogap was moved coronally away from the alveolarcrest. The bone loss was not dependent on the load-ing regimen. In a case-control study38 of 60 sub-merged and non-submerged implants placed in 30patients (smokers and non-smokers), a significantreduction of bone loss in the implants with a plat-form-switching (PS) abutment was reported. In arecent case report, Degidi et al.,39 explaining theobserved absence of bone resorption, concluded thatthe combination of PS implants with an absence ofa microgap may protect the peri-implant soft andmineralized tissues. In summary, most of the histo-morphometric studies1,4-40 in the literature aboutperi-implant soft tissue dimensions were performedin animals and usually confined to mandibular im-plants fitted with healing or standard abutments. Toour knowledge, no comparative evaluations on peri-implant soft tissue dimensions were carried out onmaxillary and mandibular implants in humans oraround immediately loaded implants with a PS abut-ment placed in one-stage surgery. The aim of the pres-ent study is to histomorphometrically evaluate theperi-implant soft tissues around immediately loadedimplants with PS abutments placed in the maxillaand mandible.

MATERIALS AND METHODS

The clinical patient report and sample preparationwere reported in a previous publication.41 Neverthe-less, for convenience, some data are reported in thepresent study.

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Twelve 11 · 3.5-mm implants§ were placed in a fullyedentulous 50-year-old heavy woman who smoked.The bone quality was very poor (class 3 or 4 accordingto Lekholm and Zarb42). Standard abutments were im-mediately fixed in place after implant placement witha controlled torque (15 Ncm for angulated abutmentsand 25 Ncm for straight abutments). The temporaryfixed restorations made with resin materiali wereimmediately placed after suturing the flaps. Thedefinitive ceramometal fixed restorations wereplaced and temporarily cemented 4 months afterloading without removal of the original abutments.

Histomorphometric Analyses of Soft TissuesThe specimens were analyzed by means of a lightmicroscope¶ connected to a high-resolution digitalcamera# and confocal laser scanning microscopy(CLSM)** equipped with three lasers, helium-neon(543 nm; 1 mW), helium-neon (633 nm; 5 mW), andargon (458, 477, 488, and 514 nm; 30 mW). The im-ages were collected in tif format at 12 bits (1,024 ·768 pixels) with the line-average technique. The mea-surements were performed on digital images usingsoftware.†† To ensure accuracy, the software was cali-brated for each experimental image applying thePythagorean theorem for distance calibration, whichreports the number of pixels between two selectedpoints(diameterof the implantplatform).Thelinearre-mappingof thepixel numbers wasused to calibrate thedistance in millimeters. Four peri-implant soft tissueindexes were quantified. The SE was determined asthe distance between the gingival margin and the mostcoronal point of the JE. The JE was determined as thedistance between the bottom of the SE and the mostapical point of the JE. The CT was determined as thedistance between the bottom of the JE and the firstbone-to-implant contact, and the BW equated thesumof theverticaldimensionofSE,JE,andCT.15,18,43

Statistical AnalysesOne person (TT) performed all measurements, anddue to this, intraexaminer variability was controlledby carrying out two measurements for each soft tissueindex. Fourteen to 21 implant sites were evaluated,excluding those sections and /or sites not measurablebecause of cutting or staining problems. When the dif-ference in the two performed readings was >0.15 mmfor the same soft tissue index, the measure was re-peated. For each parameter measured (SE, JE, CT,and BW), a single value was calculated as the meanof the readings among the implant sites evaluated.Student unpaired t tests were performed to determineany differences between mandibular and maxillaryperi-implant soft tissue variables. A P value <0.05was considered statistically significant. Statisticalanalyses were performed by means of a computerizedstatistical package.‡‡

RESULTS

The bone–implant contact percentage around theseimplants was reported in an article by Romanos andJohansson,41 which provided an in-depth evaluationof the peri-implant hard tissues. For the soft tissuesin the maxilla, the mean dimension (– SD) of the SEwas 2.7 (– 0.8) mm, whereas in the mandible, itwas 1.7 (– 0.4) mm. A statistically significant differ-ence was found in the dimensions of the SE betweenthe two jaws (P <0.001) (Figs. 1A and 1B; Table 1).The SE was composed of about five to six layers ofparakeratinized epithelial cells; no ulceration waspresent. However, in the lamina propria of some max-illary sections, an inflammatory cell infiltrate waspresent, mainly constituted by lymphocytes and mac-rophages. In the maxilla, the mean (– SD) dimensionof the JE was 1.3 (– 0.4) mm, whereas in the mandi-ble, it was 1.5 (– 0.5) mm. No statistically significantdifference was found in the height of the JE betweenthe maxilla and mandible (P = 0.164) (Table 1).

The JE had the following appearance (Figs. 2Athrough 2C): in the most coronal part, at the level ofthe bottom of the SE, the JE was composed of aboutfive to 10 layers of epithelial cells coronally spread toform a pocket of epithelial cells apparently attached tothe abutment surface (Figs. 2C1 and 2C2). This char-acteristic of epithelial adherence was observed in themajority of specimens. The middle part of the JE con-sisted of three to five layers of epithelial cells that hadadhered to the neck surface of the abutment (Fig. 2B).The most apical portion of the JE was thicker than thatfound in the middle part of the JE. This area wasclosely related to the angle formed by the abutmentneck inserted into the implant platform. In this area,the JE was composed of about six to seven layersof cells (Fig. 2B). No epithelial cells migrating apicallybeyond the implant platform shoulder were found. In-stead, a CT in contact with the implant platform wasfound. The basal membrane of the JE showed a nor-mal morphology with no pathologic characteristics orunderlying inflammatory infiltration. In the maxilla, themean (– SD) height of the CT was 2.5 (– 1.3) mm,whereas in the mandible, it was 1.6 (– 0.4) mm. A sta-tistically significant difference was present (P = 0.017)(Figs. 3A through 3C; Table 1). With the aid of two po-larizing filters and a lambda/4 filter, it was possible todifferentiate the orientation of the collagen fibers. Fromthe bottom to the top, we noted fibers and bundles ofcollagen running parallel to the implant surface in an

§ Ankylos (with Tissue Care Connection), DENTSPLY Friadent, Mannheim,Germany.

i Protemp, Espe, Seefeld, Germany.¶ Axiolab, Zeiss, Oberchen, Germany.# FinePix S2 Pro, Fuji Photo Film, Minato-Ku, Japan.** Zeiss Axiovert 200 M with the 510 META scanning module, Carl Zeiss,

Jena, Germany.†† Image J, version 1.39f, National Institutes of Health, Bethesda, MD.‡‡ Sigma Stat 3.0, SPSS, Erkrath, Germany.

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apico-coronal direction below the level of the outerangle of the implant shoulder (platform) (Fig. 3A).

At the level of the implant shoulder, the collagenbundles showed a perpendicular direction from thebone toward the abutment surface. In the majorityof the measured regions (n = 16) of the 38 measured

sites and irrespective of location (mandible or max-illa), the collagen bundles were in contact with theouter margin of the implant shoulder (Figs. 3A and3B). In general, the CT was composed of two differentlayers of collagen bundles: a first layer (yellow in Fig.3A) of thin collagen bundles (constituting the laminapropria of the JE) of 80 to 170 mm in thickness run-ning parallel to the abutment surface and a secondlayer (blue in Fig. 3A) of thick collagen bundles run-ning circularly around the abutments. In the secondlayer of the CT, from the bottom (below the implantplatform) to the top (below the oral epithelium), col-lagen bundles had a direction parallel to the implantsurface until the outer angle of the implant shoulder(A in Fig. 3C); then, the collagen bundles turned per-pendicularly toward the abutment surface (B in Fig.3C) until about 150 to 200 mm from the metal surface,where they became parallel to the abutment surface inan apico-coronal direction forming the lamina propriaof the SE (A in Fig. 3C). At this level, the collagen bun-dles turned outward again to the abutment surface to-ward the supracrestal CT (D in Fig. 3C). As a result, itwas possible to observe collagen bundles of the CToriented in an S-shape fashion around these implants.In some areas, it was possible to see collagen fibersand bundles oriented perpendicularly or obliquely tothe section plane. Few scattered monocytes and mac-rophages were present. Some elongated fibroblastswere present. The mean of the BW measured in themaxilla (n = 19) was 6.5 – 2.5 mm, whereas the meanof the BW in the mandible (n = 17) was 4.8 – 1.3 mm. Astatistically significant difference was obtained be-tween the dimensions of the two BW (P = 0.017)(Fig. 4; Table 1). The SE and CT extensions increasedin the maxilla, contributing significantly to the differ-ence, whereas the JE remained constant.

DISCUSSION

The present study overcame the limitations of a one-case report because it is unique, to our knowledge, inthat it presents histologic human data on peri-implant

Table 1.

Mean Values of Soft Tissue Parameters Around Immediately Loaded Implants Placed inMandibular and Maxillary Bones

Parameter (mm) n Mandible (mean – SD) n Maxilla (mean – SD) P Value

SE 14 1.7 – 0.4 16 2.7 – 0.8 <0.001*

JE 20 1.5 – 0.5 21 1.3 – 0.4 0.164

CT 20 1.6 – 0.4 18 2.5 – 1.3 0.006*

BW 17 4.8 – 1.3 19 6.5 – 2.5 0.017*

n = number of measured sites.* Statistically significantly different.

Figure 1.A) CSLM image of undecalcified cut and ground section with peri-implantsoft tissue. B) Magnification of the square area (*) in A. Note thepresence of a parakeratinized epithelial multicell layer. (Toluidine bluestain; original magnification: A, ·50; B, ·630.)

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soft tissue extensions around 12 immediately loadedimplants with PS. The implants, placed in upper andlower jaws in a single surgical stage were retrievedafter 7 months of loading. All of the implants hadabutments with machined surfaces connected tothe implant by a Morse taper conical connection.The most significant finding was that the BW changed

significantly as a result of the site of insertion (mandi-ble versus maxilla). The analysis of each singleparameter comprising the BW showed an interdepen-dence among CT, SE, and BW dimensions, whichtended to increase in the maxilla more than in themandible. Surprisingly, the JE dimension did not sig-nificantly contribute to the BW dimension (Fig. 4).

Figure 2.A) Undecalcified cut and ground sections of mandibular implants. The rectangle area, investigated by CSLM, was mapped in B and C. In B, the white arrowindicates the apex of the gingival sulcus, whereas the black arrows indicate the cell basal layer of the JE. The JE extension appeared to be variable in thicknessshowing two thick areas (coronal and apical) separatedbya very thin cell layer of five to six cells. C) Low magnification of the peri-implant soft tissue.C1)Highmagnification of epithelial cells tightly adherent to the surface of the abutment and coronally spread. C2) Highmagnification of the JE adherent to the surfaceof the abutment. (Toluidine blue stain in A; original magnification: A, ·20; B, ·100; C, ·400; C1 and C2, ·1,000). *Bottom of the gingival sulcus. I = implant;E = epithelial tissue.

Figure 3.A) Map reconstruction of the peri-implant soft tissue under a circularly polarized light microscope. Collagen fiber orientations are disclosed by different colorsdue to the diffraction values of the polarized light plane passing throughout the section. Yellow color represent the parallel collagen fibers (black arrows),referring to the long axis of the implant-abutment unit; whereas the blue color shows the collagen fibers that run perpendicular (white arrows) referring to thesectionplane (circularly around the implant-abutment unit). B)Map reconstruction of the soft tissuearounda mandibular implant undera circularly polarizedlight microscope. The pale yellow color indicates the collagen fibers parallel to the long axis of the implant–abutment unit, whereas the blue color shows thecollagen fibers that ran circularly around the implant–abutment unit. C) Schematic diagrams illustrating the main results on the orientation of the collagenbundles in the peri-implant soft tissue. In A, the collagen bundles run parallel to the implant surface until the outer angle of the implant shoulder. In B, they turntoward the abutment surface adjacent to the outer angle of the implant shoulder. In C, they became parallel to the abutment surface in an apico-coronaldirection, and then under SE, they turned outward again to the abutment surface. In D, it is possible to observe the general organization of the circular layer ofcollagen bundles that, just over the bone tissue, ran toward the implant surface, whereas, just under the SE, they turned back forming an S shape. (Originalmagnification: A, ·100; B, ·50.)

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Additionally, at the bottom of the SE, a pocket of ep-ithelial cells, coronally spread in a creeping attach-ment fashion, were tightly adherent to the surface ofthe abutment (Figs. 2C and 2C1).

The BW appeared to be independent of the pres-ence/absence of a microgap because the implant sys-tem used in the present study had virtually no gap dueto the Morse taper connection; nevertheless, the BWwas significantly different in the upper and lower jaws.In the maxilla, it was 6.5 – 2.5 mm, whereas in themandible, it was 4.8 – 1.3 mm. The quality of the boneseemed to be a determinant factor considering thatthe maxillary bone was almost trabecular with widebone-marrow spaces, whereas the mandibular bonewas much more compact. The presence of a mildinflammatory infiltrate in the CT underlying the SE,found in some maxillary specimens (much lower inthe mandibular specimens), might be another factorthat could explain the differences in the BW due topocket formation. The dimension of the CT was signif-icantly increased in the maxilla. Part of the differencesin the BW dimensions was due to a measurement bias.

As actually postulated, the BW dimension was cal-culated measuring the distance from the top of thegingival margin to the first bone-to-implant contactpoint. However, this aspect is questionable, particu-larly in the trabecular bone (maxillary bone) wherethe bone marrow spaces between two trabeculaewere sometimes erroneously considered a BW dimen-sion when they were part of the healthy bone tissue.

A more accurate measuringmethod for the BW will be ad-dressed in future studies.

The features of the peri-im-plant soft tissues were similar tothose reported in previous humanand animal studies13,15,18,33,43

(Fig. 5). Nevertheless, they werenot completely comparable be-cause no data were found in theliterature regarding peri-implantsoft tissue dimensions surround-ing implants placed in the maxil-lary bone. In the present study,the epithelium tended to de-crease from the coronal to themiddle level, whereas it increasedagain from the middle level to theapical portion (Fig. 2B). This factmight be explained by the pres-ence of the PS, which gave a lat-eral dimension to the BW. In thesespecimens, the abutments werenot removed; no violation of theBW due to removal of the pros-thetic components was present.

Significantly different dimensions for the BW, CT,and SE, but not for JE, were present. Clinically, thelength of the SE in the maxilla (2.7 – 0.8 mm) indi-cated the presence of a peri-implant pocket. This factcould explain the presence of an inflammatory infil-trate in the lamina propria of the SE. Nevertheless,the inflammation was limited, and the normal archi-tecture of the CT was not disrupted.

The dimensions of the JE around implants inanimal studies6,7,18,36 were between 1.16 and 1.90mm. Higher values were reported in human studies.In an autopsy report, the length of the JE was foundto be 3.00 mm.33 In a study on retrieved microim-plants, Glauser et al.13 found different lengths de-pending on the surface structures of the abutments.They found lengths of 1.8 mm in oxidized abutments,1.9 mm in acid-etched abutments, and 3.4 mm in ma-chined abutments. The length of the JE in the presentreport was slightly less than those reported in thesehuman studies. In addition, the loading conditions ofthe implants can probably influence the length ofthe JE: Hermann et al.17 reported lengths of 1.16mm for unloaded implants, 1.44 mm for implantsloaded for a 3-month period, and 1.88 mm for im-plants loaded for 12 months. The apical migrationof the JE could be influenced by the presence of a mi-crogap and its vertical positioning.13 The epitheliumtended to migrate beyond the damaging agent in anattempt to isolate it.38 In the present study, as alreadyreported in an animal study36 using the same implant

Figure 4.Histometric data of the peri-implant soft tissues around maxillary and mandibular immediately loadedimplants. The least-square regression procedure assumed an association between the variable BW(independent) and the variables SE, JE, and CT (explanatory). In the maxilla, the JE did not significantlycontribute to the BW dimension as did the SE and CT.

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system, the most apical epithelial cells of the JE werealways located above the alveolar crest. Moreover,a pocket of cells, coronally spread to form an epithe-lial cell barrier in a creeping attachment fashion on thesurface of the abutment, was noted at the base of theperi-implant sulcular space. This unique aspect couldbe related to the one-stage surgery procedure thatformed and stabilized the epithelial attachment with-out any disturbance as occurs in two-stage proce-dures. The orientation of the basal and suprabasalcells of the JE was parallel to the implant surface.The dimension of the CT was reported to be com-prised between 1.01 and 2.01 mm in animal stud-ies16,18,36 for implants placed in mandibles. In animplant system with a PS, it was reported that the CTwas wider and longer.18 The present findings are con-sistent with these data. The soft tissue changes were re-lated to the occlusal forces acting on implants; in fact,Hermann et al.18 reported an influence of the load onthe length of SE, JE, and CT, but not on the BW, aroundimplants placed in the canine mandible. In a monkeystudy, Siar et al.15 evaluated the influence of a loadingprotocol on theSE,JE,CT, and BWdimensions, report-ing no statistically significant differences among theparameters evaluated for the immediate- or de-layed-loading protocol. In the present study, statis-tically significantly different values for the BW in thetwo jaws were present notwithstanding the sameloading regimen. In addition, the surface topographyof the abutment seemed to have a significant role inthe peri-implant soft tissue organization.

In a human autopsy case report, Piattelli et al.33 re-ported the SE, JE, CT, and BW dimensions aroundthree titanium plasma-sprayed implants placed inthe mandible. They concluded that the results weresimilar to those reported in studies using dogs and

monkeys. Nevertheless, comparing these data tothe results obtained in the present study in the man-dibular bone, we had relatively similar results for theSE and CT but much less length for the JE (3.0 –0.4 mm as reported by Piattelli et al.33 versus 1.5 –0.5 mm as measured in the present study) and forBW (6.9 mm as reported by Piattelli et al.33 versus4.8 – 1.3 mm as measured in the present study). Ina human study on one-piece dental implants mea-sured after 2 months of loading, Glauser et al.13 foundless epithelial downgrowth and a longer CT sealaround oxidized and acid-etched surfaces than ma-chined surfaces. In the present study, we used onlymachined surfaces without any evidence of epithelialdowngrowth. This is probably due to the presence ofa PS. Regarding the collagen fiber orientation, thepresent results are generally consistent with the find-ings of Schierano et al.34 and Glauser et al.,13 eventhough a difference concerning the adaptation of cir-cular collagen bundles to the PS abutment, which pro-duced the S shape, was found. Compared to standardabutments, this latter aspect meant that there wasa higher quantity of space that was able to be occu-pied by collagen bundles in the PS abutments. Clini-cally, this was particularly important in the case oftwo adjacent implants. Moreover, very few inflamma-tory cells inside the CT were found in the presentstudy instead, as reported by Quirynen et al.44 fortwo-stage implants with a screwed implant–abutmentconnection with an interface at the level of the alveo-lar bone was found an association with a significantinflammatory cell infiltrate.

Immediate loading of dental implants was reportednot to have untoward effects on the formation of min-eralized bone at the interface.45-47 The bacteria-proofseal, the lack of micromovements due to the friction

Figure 5.Histometric data of soft tissue around dental implants in humans and animals for comparison.

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grip of the conical connection, and the minimal traumato the periosteal tissues during second-stage surgeryalso helped prevent peri-implant bone loss.48 The lackof the removal of the abutment in this implant systemhas certainly an importance in the results of the presentstudy. In fact, it was reported that the removal and re-connection of the abutment created a wound within thesoft tissues with subsequent bone resorption due to theattempt made by the soft tissues to establish a properbiologic dimension of the mucosal barrier attachmenttoastable implantsurface.49Moreover, the lackofcom-plications of the hard and soft tissues for this implantsystem can be attributed to the thick deposition of softtissues in the narrowed neck of the abutment.48,50 Thiscollar of soft tissue, which appeared wedge shaped incross-section, seemed to provide a supplementaryprotective function for the peri-implant bone.50 Ourresults are consistent with that of other studies.48,50

CONCLUSIONS

In the present human study, we observed:A statistically significant difference between the

BW of the maxilla and mandible (6.5 – 2.5 mm versus4.8 – 1.3 mm, respectively), due to the increase of CTand SE lengths, whereas the dimension of the JE re-mained almost constant.

An SE significantly longer in the maxillary implantsin which either a mild inflammatory infiltrate or trabec-ular bone was present.

A JE attached to the machined abutment surfacewith a pocket of cells at the bottom of the SE andno epithelial downgrowth to the alveolar crest.

A CT with collagen fibers separated into two differ-ent layers of different orientation and a second, thickerlayer of collagen bundles running circularly around theabutment that lined a first layer of 100 to 150 mm inthickness made by thin collagen bundles parallel tothe abutment surface. Because of the spatial variationgenerated by the PS abutments, circular collagen bun-dles, oriented in an S-shape fashion, were present.

ACKNOWLEDGMENTS

Drs. Romanos and Traini contributed equally to thisstudy. Drs. Romanos and Piattelli have received lec-ture fees from DENTSPLY Friadent. Dr. Romanos hasalso conducted long-term research using DENTSPLYFriadent products, and Dr. Piattelli has consultedfor the company. Drs. Johansson and Traini reportno conflicts of interest related to this study.

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Correspondence: Dr. Tonino Traini, Department of Odonto-stomatological Sciences, Dental School, University ofChieti-Pescara, Via dei Vestini 31, 66100, Chieti, Italy.E-mail: [email protected].

Submitted June 29, 2009; accepted for publication August30, 2009.

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