Journal of periodontology 2010 romanos


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Journal of periodontology 2010 romanos

  1. 1. Volume 81 • Number 1 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 T were placed 4 months after loading without removal of the he present focus of implant re- original abutments. After 10 months, the patient died, and search in dentistry principally the implants were removed en block and processed for histol- involves the peri-implant soft tis- ogy. sues because of an increasing aware- Results: The BW in the maxilla was 6.5 – 2.5 mm, whereas ness of the importance of a stable and in the mandible, it was 4.8 – 1.3 mm (P = 0.017). The sulcular healthy soft tissue–implant interface. Soft epithelium (SE) in the maxilla was 2.7 – 0.8 mm, whereas in tissue health is critical to the patient’s the mandible, it was 1.7 – 0.4 mm (P <0.001). The junctional perception of a successful restoration, epithelium (JE) in the maxilla was 1.3 – 0.4 mm, whereas in and long-term biofunctionality and es- the mandible, it was 1.5 – 0.5 mm (P = 0.164). The connective thetic appearance are mainly based on tissue (CT) in the maxilla was 2.5 – 1.3 mm, whereas in the the stability of the biologic width (BW).1 mandible, it was 1.6 – 0.4 mm (P = 0.006). In the maxillary The BW around natural teeth was first bone, the BW, SE, and CT were significantly longer than in defined in the 1960s.2 As reported in the mandible, whereas for the JE, no statistically significant a number of studies,3-10 the peri-implant difference was observed. BW is composed of an epithelium over- Conclusion: The soft tissue organization around dental im- lying connective tissue (CT), with many plants was different for upper and lower jawbones. J Periodon- similarities to the dento-gingival tissues tol 2010;81:70-78. around teeth.11,12 It was reported that the maintenance and stability of the load- KEY WORDS bearing implant are dependent on the Connective tissue; dental implants; dental prosthesis, establishment of a functional barrier at implant supported; epithelial cells; junctional epithelium. the transmucosal passage of the abut- ment,13 which is important to protect the implant interface from invasion of bacte- * Unit of Laser Dentistry, Division of Periodontology, Eastman Institute for Oral Health, University of Rochester, Rochester, NY. ria from the oral cavity.6,14,15 The for- † Dental School, University of Chieti–Pescara, Chieti, Italy. mation of a stable peri-implant seal ‡ School of Health and Medical Sciences, University of Orebro, Sweden. 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 doi: 10.1902/jop.2009.09036470
  2. 2. J Periodontol • January 2010 Romanos, Traini, Johansson, Piattelliwith the surface of implants in a scar-like manner. under unloaded and loaded conditions. Moreover,The differences indicate that important dynamic Abrahamsson and Cardaropoli35 recently reportedfactors affect the organization of the sulcular epithe- no significant differences in the peri-implant softlium (SE), junctional epithelium (JE), and CT.17,18 tissue dimensions for gold and titanium used in the The SE and JE form the first line of defense against marginal zone of the implant.microbial invasion, and they hinder microbial colo- While referring to the implant component mor-nization by a rapid exfoliation. Recently, Schupbach ¨ phology as a variable for the organization of theand Glauser19 described remnants in hemidesmo- soft tissue, Abrahamsson et al.,8 in a beagle dogsomes (HDs) at the surface of sulcular epithelial study using three dental implant systems withcells around implants due to the high rate of cell des- one- and two-stage surgical implants, reportedquamation, which is 50 times higher than that re- that the geometry of the titanium implant seemedported in the oral epithelium.20 The histologic and to be of limited importance for the peri-implant softphysiologic organization of the JE was well de- tissue organization. Nevertheless, in a dog modelscribed elsewhere.21-27 It was also reported that using unloaded Ankylos implants, Tenenbaumhuman JE cells are able to connect to a titanium- et al.36 reported a greater length and larger widthcoated resin implants by either the basal lamina or of CT as well as a shorter epithelial downgrowthHDs.28 compared to studies on AstraTech, Branemark, ˚ The fiber apparatus of the CT provides a dense and ITI implants. Moreover, the histologic mild in-framework that results in mechanical resistance of flammation noted in the CT was related to the ab-the gingiva, allowing it to withstand frictional forces sence of a microgap in the Ankylos implantthat result from mastication.29 The direct attachment system. In a retrospective histologic study in mon-of the collagen fibers to the implant surface is contro- keys on early and immediately loaded implantsversial in the dental literature19 due to the absence of inserted in postextraction sites, Piattelli et al.37 re-cementum to anchor the collagen fibrils. Moreover, ported that less bone loss was observed as the mi-depending on the implant surface texture, substantial crogap was moved coronally away from the alveolardifferences were reported.19 crest. The bone loss was not dependent on the load- The peri-implant CT collagen fiber orientation was ing regimen. In a case-control study38 of 60 sub-studied in several animal models. In beagle dogs, sev- merged and non-submerged implants placed in 30eral reports4,30,31 described collagen fibers running patients (smokers and non-smokers), a significantparallel to the implant surface, more or less in the reduction of bone loss in the implants with a plat-coronal-apical direction. Other authors reported form-switching (PS) abutment was reported. In acollagen fibers oriented circumferentially around recent case report, Degidi et al.,39 explaining theimplants in monkeys32 and humans.33 However, an- observed absence of bone resorption, concluded thatother article31 reported the presence of fibers directed the combination of PS implants with an absence ofperpendicular/oblique to the implant surface in dogs. a microgap may protect the peri-implant soft andAlso, the fibers appeared to be more prominent on mineralized tissues. In summary, most of the histo-microtextured, compared to smooth transmucosal, morphometric studies1,4-40 in the literature aboutsurfaces in a dog experiment.19 peri-implant soft tissue dimensions were performed In a recent human study, Schierano et al.34 evalu- in animals and usually confined to mandibular im-ated the organization of the CT around nine loaded plants fitted with healing or standard abutments. Toimplants in seven patients. They found a constant our knowledge, no comparative evaluations on peri-spatial arrangement of the peri-implant CT. In the implant soft tissue dimensions were carried out onfirst 200 mm from the implant surface, longitudinal maxillary and mandibular implants in humans orcollagen fibers were observed, and between 200 around immediately loaded implants with a PS abut-and 800 mm from the implant surface, circular col- ment placed in one-stage surgery. The aim of the pres-lagen fibers were found, whereas externally, only ent study is to histomorphometrically evaluate theoblique collagen fibers were noted. The organiza- peri-implant soft tissues around immediately loadedtion of the peri-implant soft tissues related to the implants with PS abutments placed in the maxillaloading regimen was also evaluated. Siar et al.15 and mandible.reported that the dimensions of the peri-implantsoft tissues were within the biologic range of nat-ural teeth and were not influenced by immediate MATERIALS AND METHODSfunctional loading or posterior location of the im- The clinical patient report and sample preparationplants in the macaque mandible. Also, in a dog study, were reported in a previous publication.41 Neverthe-Hermann et al.17 found no differences in the BW less, for convenience, some data are reported in thearound non-submerged, one-piece titanium implants present study. 71
  3. 3. Biologic Width Around Immediately Loaded Implants Volume 81 • Number 1 Twelve 11 · 3.5-mm implants§ were placed in a fully RESULTS edentulous 50-year-old heavy woman who smoked. The bone–implant contact percentage around these The bone quality was very poor (class 3 or 4 according implants was reported in an article by Romanos and to Lekholm and Zarb42). Standard abutments were im- Johansson,41 which provided an in-depth evaluation mediately fixed in place after implant placement with of the peri-implant hard tissues. For the soft tissues a controlled torque (15 Ncm for angulated abutments in the maxilla, the mean dimension (– SD) of the SE and 25 Ncm for straight abutments). The temporary was 2.7 (– 0.8) mm, whereas in the mandible, it fixed restorations made with resin materiali were was 1.7 (– 0.4) mm. A statistically significant differ- immediately placed after suturing the flaps. The ence was found in the dimensions of the SE between definitive ceramometal fixed restorations were the two jaws (P <0.001) (Figs. 1A and 1B; Table 1). placed and temporarily cemented 4 months after The SE was composed of about five to six layers of loading without removal of the original abutments. parakeratinized epithelial cells; no ulceration was Histomorphometric Analyses of Soft Tissues present. However, in the lamina propria of some max- The specimens were analyzed by means of a light illary sections, an inflammatory cell infiltrate was microscope¶ connected to a high-resolution digital present, mainly constituted by lymphocytes and mac- camera# and confocal laser scanning microscopy rophages. In the maxilla, the mean (– SD) dimension (CLSM)** equipped with three lasers, helium-neon of the JE was 1.3 (– 0.4) mm, whereas in the mandi- (543 nm; 1 mW), helium-neon (633 nm; 5 mW), and ble, it was 1.5 (– 0.5) mm. No statistically significant argon (458, 477, 488, and 514 nm; 30 mW). The im- difference was found in the height of the JE between ages were collected in tif format at 12 bits (1,024 · the maxilla and mandible (P = 0.164) (Table 1). 768 pixels) with the line-average technique. The mea- The JE had the following appearance (Figs. 2A surements were performed on digital images using through 2C): in the most coronal part, at the level of software.†† To ensure accuracy, the software was cali- the bottom of the SE, the JE was composed of about brated for each experimental image applying the five to 10 layers of epithelial cells coronally spread to Pythagorean theorem for distance calibration, which form a pocket of epithelial cells apparently attached to reports the number of pixels between two selected the abutment surface (Figs. 2C1 and 2C2). This char- points (diameter of the implant platform). The linear re- acteristic of epithelial adherence was observed in the mapping of the pixel numbers was used to calibrate the majority of specimens. The middle part of the JE con- distance in millimeters. Four peri-implant soft tissue sisted of three to five layers of epithelial cells that had indexes were quantified. The SE was determined as adhered to the neck surface of the abutment (Fig. 2B). the distance between the gingival margin and the most The most apical portion of the JE was thicker than that coronal point of the JE. The JE was determined as the found in the middle part of the JE. This area was distance between the bottom of the SE and the most closely related to the angle formed by the abutment apical point of the JE. The CT was determined as the neck inserted into the implant platform. In this area, distance between the bottom of the JE and the first the JE was composed of about six to seven layers bone-to-implant contact, and the BW equated the of cells (Fig. 2B). No epithelial cells migrating apically sum of the vertical dimension of SE, JE, and CT.15,18,43 beyond the implant platform shoulder were found. In- stead, a CT in contact with the implant platform was Statistical Analyses found. The basal membrane of the JE showed a nor- One person (TT) performed all measurements, and mal morphology with no pathologic characteristics or due to this, intraexaminer variability was controlled underlying inflammatory infiltration. In the maxilla, the by carrying out two measurements for each soft tissue mean (– SD) height of the CT was 2.5 (– 1.3) mm, index. Fourteen to 21 implant sites were evaluated, whereas in the mandible, it was 1.6 (– 0.4) mm. A sta- excluding those sections and /or sites not measurable tistically significant difference was present (P = 0.017) because of cutting or staining problems. When the dif- (Figs. 3A through 3C; Table 1). With the aid of two po- ference in the two performed readings was >0.15 mm larizing filters and a lambda/4 filter, it was possible to for the same soft tissue index, the measure was re- differentiate the orientation of the collagen fibers. From peated. For each parameter measured (SE, JE, CT, the bottom to the top, we noted fibers and bundles of and BW), a single value was calculated as the mean collagen running parallel to the implant surface in an of the readings among the implant sites evaluated. § Ankylos (with Tissue Care Connection), DENTSPLY Friadent, Mannheim, Student unpaired t tests were performed to determine Germany. any differences between mandibular and maxillary i Protemp, Espe, Seefeld, Germany. peri-implant soft tissue variables. A P value <0.05 ¶ Axiolab, Zeiss, Oberchen, Germany. # FinePix S2 Pro, Fuji Photo Film, Minato-Ku, Japan. was considered statistically significant. Statistical ** Zeiss Axiovert 200 M with the 510 META scanning module, Carl Zeiss, Jena, Germany. analyses were performed by means of a computerized †† Image J, version 1.39f, National Institutes of Health, Bethesda, MD. statistical package.‡‡ ‡‡ Sigma Stat 3.0, SPSS, Erkrath, Germany.72
  4. 4. J Periodontol • January 2010 Romanos, Traini, Johansson, Piattelli sites and irrespective of location (mandible or max- illa), the collagen bundles were in contact with the outer margin of the implant shoulder (Figs. 3A and 3B). In general, the CT was composed of two different layers of collagen bundles: a first layer (yellow in Fig. 3A) of thin collagen bundles (constituting the lamina propria of the JE) of 80 to 170 mm in thickness run- ning parallel to the abutment surface and a second layer (blue in Fig. 3A) of thick collagen bundles run- ning circularly around the abutments. In the second layer of the CT, from the bottom (below the implant platform) to the top (below the oral epithelium), col- lagen bundles had a direction parallel to the implant surface 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 in an apico-coronal direction forming the lamina propria of 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, it was possible to observe collagen bundles of the CT oriented in an S-shape fashion around these implants. In some areas, it was possible to see collagen fibers and bundles oriented perpendicularly or obliquely to the section plane. Few scattered monocytes and mac- rophages were present. Some elongated fibroblasts were present. The mean of the BW measured in the Figure 1. maxilla (n = 19) was 6.5 – 2.5 mm, whereas the mean A) CSLM image of undecalcified cut and ground section with peri-implant of the BW in the mandible (n = 17) was 4.8 – 1.3 mm. A soft tissue. B) Magnification of the square area (*) in A. Note the statistically significant difference was obtained be- presence of a parakeratinized epithelial multicell layer. (Toluidine blue stain; original magnification: A, ·50; B, ·630.) tween the dimensions of the two BW (P = 0.017) (Fig. 4; Table 1). The SE and CT extensions increased in the maxilla, contributing significantly to the differ-apico-coronal direction below the level of the outer ence, whereas the JE remained constant.angle of the implant shoulder (platform) (Fig. 3A). At the level of the implant shoulder, the collagen DISCUSSIONbundles showed a perpendicular direction from the The present study overcame the limitations of a one-bone toward the abutment surface. In the majority case report because it is unique, to our knowledge, inof the measured regions (n = 16) of the 38 measured that it presents histologic human data on peri-implantTable 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. 73
  5. 5. Biologic Width Around Immediately Loaded Implants Volume 81 • Number 1 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 arrow indicates 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 thickness showing two thick areas (coronal and apical) separated by a very thin cell layer of five to six cells. C) Low magnification of the peri-implant soft tissue. C1) High magnification of epithelial cells tightly adherent to the surface of the abutment and coronally spread. C2) High magnification of the JE adherent to the surface of 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 colors due 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 the section plane (circularly around the implant-abutment unit). B) Map reconstruction of the soft tissue around a mandibular implant under a circularly polarized light microscope. The pale yellow color indicates the collagen fibers parallel to the long axis of the implant–abutment unit, whereas the blue color shows the collagen fibers that ran circularly around the implant–abutment unit. C) Schematic diagrams illustrating the main results on the orientation of the collagen bundles 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 turn toward the abutment surface adjacent to the outer angle of the implant shoulder. In C, they became parallel to the abutment surface in an apico-coronal direction, 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 of collagen bundles that, just over the bone tissue, ran toward the implant surface, whereas, just under the SE, they turned back forming an S shape. (Original magnification: A, ·100; B, ·50.) soft tissue extensions around 12 immediately loaded significantly as a result of the site of insertion (mandi- implants with PS. The implants, placed in upper and ble versus maxilla). The analysis of each single lower jaws in a single surgical stage were retrieved parameter comprising the BW showed an interdepen- after 7 months of loading. All of the implants had dence among CT, SE, and BW dimensions, which abutments with machined surfaces connected to tended to increase in the maxilla more than in the the implant by a Morse taper conical connection. mandible. Surprisingly, the JE dimension did not sig- The most significant finding was that the BW changed nificantly contribute to the BW dimension (Fig. 4).74
  6. 6. J Periodontol • January 2010 Romanos, Traini, Johansson, Piattelli A more accurate measuring method for the BW will be ad- dressed in future studies. The features of the peri-im- plant soft tissues were similar to those reported in previous human and animal studies13,15,18,33,43 (Fig. 5). Nevertheless, they were not completely comparable be- cause no data were found in the literature regarding peri-implant soft 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 the middle level, whereas it increased again from the middle level to the apical portion (Fig. 2B). This fact might be explained by the pres- ence of the PS, which gave a lat- Figure 4. Histometric data of the peri-implant soft tissues around maxillary and mandibular immediately loaded eral dimension to the BW. In these implants. The least-square regression procedure assumed an association between the variable BW specimens, the abutments were (independent) and the variables SE, JE, and CT (explanatory). In the maxilla, the JE did not significantly not removed; no violation of the contribute to the BW dimension as did the SE and CT. BW due to removal of the pros- thetic components was present.Additionally, at the bottom of the SE, a pocket of ep- Significantly different dimensions for the BW, CT,ithelial cells, coronally spread in a creeping attach- and SE, but not for JE, were present. Clinically, thement fashion, were tightly adherent to the surface of length of the SE in the maxilla (2.7 – 0.8 mm) indi-the abutment (Figs. 2C and 2C1). cated the presence of a peri-implant pocket. This fact The BW appeared to be independent of the pres- could explain the presence of an inflammatory infil-ence/absence of a microgap because the implant sys- trate in the lamina propria of the SE. Nevertheless,tem used in the present study had virtually no gap due the inflammation was limited, and the normal archi-to the Morse taper connection; nevertheless, the BW tecture of the CT was not disrupted.was significantly different in the upper and lower jaws. The dimensions of the JE around implants inIn the maxilla, it was 6.5 – 2.5 mm, whereas in the animal studies6,7,18,36 were between 1.16 and 1.90mandible, it was 4.8 – 1.3 mm. The quality of the bone mm. Higher values were reported in human studies.seemed to be a determinant factor considering that In an autopsy report, the length of the JE was foundthe maxillary bone was almost trabecular with wide to be 3.00 mm.33 In a study on retrieved microim-bone-marrow spaces, whereas the mandibular bone plants, Glauser et al.13 found different lengths de-was much more compact. The presence of a mild pending on the surface structures of the abutments.inflammatory infiltrate in the CT underlying the SE, They found lengths of 1.8 mm in oxidized abutments,found in some maxillary specimens (much lower in 1.9 mm in acid-etched abutments, and 3.4 mm in ma-the mandibular specimens), might be another factor chined abutments. The length of the JE in the presentthat could explain the differences in the BW due to report was slightly less than those reported in thesepocket formation. The dimension of the CT was signif- human studies. In addition, the loading conditions oficantly increased in the maxilla. Part of the differences the implants can probably influence the length ofin the BW dimensions was due to a measurement bias. the JE: Hermann et al.17 reported lengths of 1.16 As actually postulated, the BW dimension was cal- mm for unloaded implants, 1.44 mm for implantsculated measuring the distance from the top of the loaded for a 3-month period, and 1.88 mm for im-gingival margin to the first bone-to-implant contact plants loaded for 12 months. The apical migrationpoint. However, this aspect is questionable, particu- of the JE could be influenced by the presence of a mi-larly in the trabecular bone (maxillary bone) where crogap and its vertical positioning.13 The epitheliumthe bone marrow spaces between two trabeculae tended to migrate beyond the damaging agent in anwere sometimes erroneously considered a BW dimen- attempt to isolate it.38 In the present study, as alreadysion when they were part of the healthy bone tissue. reported in an animal study36 using the same implant 75
  7. 7. Biologic Width Around Immediately Loaded Implants Volume 81 • Number 1 Figure 5. Histometric data of soft tissue around dental implants in humans and animals for comparison. system, the most apical epithelial cells of the JE were monkeys. Nevertheless, comparing these data to always located above the alveolar crest. Moreover, the results obtained in the present study in the man- a pocket of cells, coronally spread to form an epithe- dibular bone, we had relatively similar results for the lial cell barrier in a creeping attachment fashion on the SE and CT but much less length for the JE (3.0 – surface of the abutment, was noted at the base of the 0.4 mm as reported by Piattelli et al.33 versus 1.5 – peri-implant sulcular space. This unique aspect could 0.5 mm as measured in the present study) and for be related to the one-stage surgery procedure that BW (6.9 mm as reported by Piattelli et al.33 versus formed and stabilized the epithelial attachment with- 4.8 – 1.3 mm as measured in the present study). In out any disturbance as occurs in two-stage proce- a human study on one-piece dental implants mea- dures. The orientation of the basal and suprabasal sured after 2 months of loading, Glauser et al.13 found cells of the JE was parallel to the implant surface. less epithelial downgrowth and a longer CT seal The dimension of the CT was reported to be com- around oxidized and acid-etched surfaces than ma- prised between 1.01 and 2.01 mm in animal stud- chined surfaces. In the present study, we used only ies16,18,36 for implants placed in mandibles. In an machined surfaces without any evidence of epithelial implant system with a PS, it was reported that the CT downgrowth. This is probably due to the presence of was wider and longer.18 The present findings are con- a PS. Regarding the collagen fiber orientation, the sistent with these data. The soft tissue changes were re- present results are generally consistent with the find- lated to the occlusal forces acting on implants; in fact, ings of Schierano et al.34 and Glauser et al.,13 even Hermann et al.18 reported an influence of the load on though a difference concerning the adaptation of cir- the length of SE, JE, and CT, but not on the BW, around cular collagen bundles to the PS abutment, which pro- implants placed in the canine mandible. In a monkey duced the S shape, was found. Compared to standard study, Siar et al.15 evaluated the influence of a loading abutments, this latter aspect meant that there was protocol on the SE, JE, CT, and BW dimensions, report- a higher quantity of space that was able to be occu- ing no statistically significant differences among the pied by collagen bundles in the PS abutments. Clini- parameters evaluated for the immediate- or de- cally, this was particularly important in the case of layed-loading protocol. In the present study, statis- two adjacent implants. Moreover, very few inflamma- tically significantly different values for the BW in the tory cells inside the CT were found in the present two jaws were present notwithstanding the same study instead, as reported by Quirynen et al.44 for loading regimen. In addition, the surface topography two-stage implants with a screwed implant–abutment of the abutment seemed to have a significant role in connection with an interface at the level of the alveo- the peri-implant soft tissue organization. lar bone was found an association with a significant In a human autopsy case report, Piattelli et al.33 re- inflammatory cell infiltrate. ported the SE, JE, CT, and BW dimensions around Immediate loading of dental implants was reported three titanium plasma-sprayed implants placed in not to have untoward effects on the formation of min- the mandible. They concluded that the results were eralized bone at the interface.45-47 The bacteria-proof similar to those reported in studies using dogs and seal, the lack of micromovements due to the friction76
  8. 8. J Periodontol • January 2010 Romanos, Traini, Johansson, Piattelligrip of the conical connection, and the minimal trauma 3. Newman MG, Fleming TF. Periodontal considerationsto the periosteal tissues during second-stage surgery of implants and implant associated microbiota. J Dentalso helped prevent peri-implant bone loss.48 The lack Educ 1988;52:737-744. 4. Listgarten MA, Lang NP, Schroeder HE, Schroederof the removal of the abutment in this implant system A. Periodontal tissues and their counterparts aroundhas certainly an importance in the results of the present endosseous implants. Clin Oral Implants Res 1991;study. In fact, it was reported that the removal and re- 2:1-19.connection of the abutment created a wound within the 5. Schou S, Holmstrup P, Hjorting-Hansen E, Lang NP.soft tissues with subsequent bone resorption due to the Plaque-induced marginal tissue reactions of osseoin- tegrated oral implants. A review of the literature. Clinattempt made by the soft tissues to establish a proper Oral Implants Res 1992;3:149-161.biologic dimension of the mucosal barrier attachment 6. Ericsson I, Berglundh T, Marinello C, Liljenberg B,to a stable implant surface.49 Moreover, the lack of com- Lindhe J. Long-standing plaque and gingivitis atplications of the hard and soft tissues for this implant implants and teeth in the dog. Clin Oral Implants Ressystem can be attributed to the thick deposition of soft 1992;3:99-103.tissues in the narrowed neck of the abutment.48,50 This 7. Hurzeler MB, Quinones CR, Schupbach P, Vlassis JH, Strub JR, Caffesse RG. Influence of the superstructurecollar of soft tissue, which appeared wedge shaped in on the peri-implant tissues in beagle dogs. Clin Oralcross-section, seemed to provide a supplementary Implants Res 1995;6:139-148.protective function for the peri-implant bone.50 Our ¨ 8. Abrahamsson I, Berglundh T, Wennstrom J, Lindhe J.results are consistent with that of other studies.48,50 The peri-implant hard and soft tissues at different implant systems. A comparative study in the dog. ClinCONCLUSIONS Oral Implants Res 1996;7:212-219. 9. Weber HP, Buser D, Donath K, et al. Comparison ofIn the present human study, we observed: healed tissues adjacent to submerged and non-sub- A statistically significant difference between the merged unloaded titanium dental implants. A histo-BW of the maxilla and mandible (6.5 – 2.5 mm versus metric study in beagle dogs. Clin Oral Implants Res4.8 – 1.3 mm, respectively), due to the increase of CT 1996;7:11-19.and SE lengths, whereas the dimension of the JE re- 10. Abrahamsson I, Berglundh T, Lindhe J. Soft tissue response to plaque formation at different implantmained almost constant. systems. A comparative study in the dog. Clin Oral An SE significantly longer in the maxillary implants Implants Res 1998; which either a mild inflammatory infiltrate or trabec- ¨ 11. Romanos GE, Schroter-Kermani C, Weingart D, Strubular bone was present. JR. Health human periodontal versus peri-implant A JE attached to the machined abutment surface gingival tissues: An immunohistochemical differentia- tion of the extracellular matrix. Int J Oral Maxillofacwith a pocket of cells at the bottom of the SE and Implants 1995; epithelial downgrowth to the alveolar crest. ¨ 12. Romanos GE, Schroter-Kermani C, Strub JR. Inflamed A CT with collagen fibers separated into two differ- human periodontal versus peri-implant gingival tis-ent layers of different orientation and a second, thicker sues: An immunohistochemical differentiation of thelayer of collagen bundles running circularly around the extracellular matrix. Int J Oral Maxillofac Implantsabutment that lined a first layer of 100 to 150 mm in 1996;11:605-611. ¨ 13. Glauser R, Schupbach P, Gottlow J, Hammerle CH. ¨thickness made by thin collagen bundles parallel to Periimplant soft tissue barrier at experimental one-the abutment surface. Because of the spatial variation piece mini-implants with different surface topographygenerated by the PS abutments, circular collagen bun- in humans: A light microscopic overview and histo-dles, oriented in an S-shape fashion, were present. metric analysis. Clin Implant Dent Relat Res 2005; 7(Suppl. 1):S44-S51.ACKNOWLEDGMENTS 14. Quirynen M, van Steenberghe D. Bacterial coloniza- tion of the internal part of two-stage implants. An inDrs. Romanos and Traini contributed equally to this vivo study. Clin Oral Implants Res 1993; Drs. Romanos and Piattelli have received lec- 15. Siar CH, Toh CG, Romanos G, et al. Peri-implant softture fees from DENTSPLY Friadent. 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