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Healing of Osseotite Implants Under Submerged and Immediate Loading Conditions in a Single Patient: A Case Report and Interface Analysis After 2 Months

Tiziano Testori, MD, DDS*/Serge Szmukler-Moncler, DDS, PhD**/ Textured surfaces have been shown Luca Francetti, MD, DDS***/Massimo Del Fabbro, BSc, PhD****/ to induce a distinct osteophilic bone Paolo Trisi, DDS, PhD*****/Roberto L. Weinstein, MD, DDS****** response to implant placement A growing number of clinical studies show that early (2 months) and immediate loading when compared to machined sur- protocols may be predictable. However, they are based on clinical stability only. The faces. Higher percentages of direct aim of this case report was to document the status of two Osseotite bone apposition,1–3 stronger anchor- implants after 2 months of healing in soft bone corresponding to type IV and subjected age in bone,4–6 and increased toler- to two distinct mechanical environments. A completely edentulous patient received a ance threshold to micromotion7 total of 11 Osseotite implants in the mandible. Six were immediately loaded to support have been repeatedly measured in a provisional fixed partial denture, and five were left submerged. After 2 months, two animal experiments. High levels of submerged and one immediately loaded implants were retrieved and processed for histologic analysis. All immediately loaded implants were clinically stable. One histo- predictability for machine-surfaced 8–10 logic section per implant was obtained. All implants achieved osseointegration. The implants and evidence of faster bone-implant contact was 38.9% for the submerged implant and 64.2% for the imme- bone apposition at textured sur- diately loaded one. In the marrow space, both implants were covered by thin, neo- faces1–3 led to the clinical application formed bone trabeculae. Osseointegration can be achieved after 2 months by of healing periods shorter than the 3 Osseotite implants placed in soft bone in the mandible either when immediately to 4 months and 6 to 8 months advo- loaded and splinted into a provisional denture retained on six implants, or when sub- cated in the mandible and maxilla, merged and unloaded. (Int J Periodontics Restorative Dent 2002;22:345–353.) respectively, for machined surfaces by Brånemark and collaborators.11–14 ******Visiting Professor, Department of Odontology, Section of Implant Dentistry and Oral Rehabilitation, Galeazzi Orthopedic Institute, University of Milan, Italy. Two methods have been sug- ******Visiting Professor, Department of Odontology, Section of Implant Dentistry and Oral gested to shorten implant ther- Rehabilitation, Galeazzi Orthopedic Institute, University of Milan, Italy; and Institute of apy.15,16 One is to reduce the tra- Stomatology, Plastic Surgery and Maxillo-facial Surgery, Salpetrière Hospital, University of Paris VI, France. ditional healing periods for single ******Researcher, Department of Odontology, Section of Implant Dentistry and Oral crowns and short-span fixed par- Rehabilitation, Galeazzi Orthopedic Institute, University of Milan, Italy. ******Department of Odontology, Section of Implant Dentistry and Oral Rehabilitation, tial dentures (FPD) to less than 3 Galeazzi Orthopedic Institute, University of Milan, Italy. months. The second is to identify ******Biomaterials Clinical Research Association, Pescara, Italy. immediate loading protocols that ******Professor and Chair, Department of Odontology, Galeazzi Orthopedic Institute, University of Milan, Italy. are capable of maintaining micro- motion within the tolerated thresh- ******Reprint requests: Dr Tiziano Testori, Department of Odontology, Galeazzi Orthopedic Institute, University of Milan, Via Riccardo Galeazzi 4, 20161 Milano, Italy. e-mail old. Following the first path, Laz- [email protected] zara et al17 published the first large

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clinical study involving a healing Osseotite implants supporting a pro- Method and materials period less than the traditionally visional FPD. After 4 months of accepted 3 to 6 months. In that occlusal function, all implants were Case report report, 429 Osseotite implants (3i) clinically stable, and two of these six supporting 212 single and short- implants were retrieved. Histologic A nonsmoking, healthy 52-year-old span rehabilitations in the man- analysis showed that the two imme- male patient consulted for replace- dible and maxilla were subjected to diately loaded implants displayed ment of an unstable mandibular a mean healing period of 2.1 ± 0.7 osseointegration. Immediate load- overdenture by an implant-sup- months. A cumulative implant sur- ing did not impede osteogenesis, ported FPD. As he wore an over- vival rate of 98.6% was obtained at and bone remodeling occurred in a denture in the maxilla, the patient 1 year of follow-up, showing that comparable way to nonloaded requested a fixed appliance and the Osseotite surface obtained by implants. As these recipient sites wished to finish his treatment as dual thermoetching is highly pre- proved to be of normal bone with soon as possible. An immediate dictable even under early loading good density corresponding to type loading protocol according to (2 months) conditions. II,25 the question of whether a simi- Schnitman et al18 was proposed, Immediate loading protocols lar histologic response would be involving simultaneous placement that reduce implant treatment have obtained in poorer quality bone of submerged and immediately been mostly applied to the rehabil- arose. Histologically, Osseotite loaded implants in the edentulous itation of completely edentulous implants showed greater bone for- mandible. The immediately loaded patients in the mandible. The results mation on the surface in poor-qual- implants were intended to sustain a of these clinical pilot trials look at ity bone compared to denser bone.2 provisional FPD, while the sub- immediately loaded, bilaterally In addition, as Osseotite implants merged implants were left to heal in splinted FPDs as a viable therapeu- have been shown to achieve clinical the traditional way. The rationale was tic alternative for the edentulous osseointegration and prosthetic pre- that should every immediately patient in the mandible.16,18–23 The dictability after 2 months even when loaded implant fail, a sufficient num- outcomes of these clinical studies placed in soft bone,17 it appeared ber of submerged implants would have been based on evidence of interesting to document the osseoin- be left to support the final prosthe- clinical implant immobility. However, tegration status of Osseotite im- sis. clinical stability alone is insufficient to plants after 2 months of healing As the patient displayed rather prove the reality of osseointegra- when submitted to the submerged spongy bone, it was proposed that tion. The possibility of a thin fibrous and immediately loaded modes. he receive additional implants, with capsule must be excluded, because This article reports on the histo- the aim of obtaining biopsies at sub- it can grow with time and lead to logic findings after 2 months of heal- merged and immediately loaded implant mobility in the longer ing of an Osseotite implant left to implants. According to the number term.12,16 heal in a submerged fashion and on of clinically stable immediately Considering the specificity of another one subjected to immediate loaded implants found after 2 the human occlusal loading scheme, occlusal function. months of healing, one to two imme- it has been suggested that human diately loaded and one to two sub- biopsy of immediately loaded merged implants would be re- implants is the most relevant route to trieved. Ultimately, a minimum of ascertain occurrence of osseointe- eight implants would retain his final gration.24 In a previous paper,24 the reconstruction. The patient volun- authors reported on a patient who teered for the protocol and an received six immediately loaded informed consent form was signed in

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Fig 1a Preoperative situation without Fig 1b Situation after implant place- Fig 1c Provisional restoration delivery, 4 abutments. ment. hours after implant placement.

Fig 2a Postoperative orthopantomogram. Fig 2b Orthopantomogram obtained 24 months after biopsy retrieval. Note that the biopsied sites healed completely.

accordance with the Helsinki decla- according to the manufacturer’s implants and around the six pro- ration of 1975, as revised in 1983. instructions. All implants were placed truding abutments. Four hours fol- Subsequently, 11 Osseotite with 32-Ncm torque and achieved lowing implant placement, a screw- implants were placed, six implants to primary stability. Normal and spon- retained resin metal–reinforced support an immediately loaded pro- gious bone was recorded (Table 1). provisional FPD was seated on the visional FPD and five submerged The immediately loaded implants six abutments (Figs 1c and 2a). Table implants to retain the definitive pros- received a 4-mm-high standard 1 illustrates the clinical situation dur- thesis (Figs 1 and 2). Self-tapping abutment, and the soft tissues were ing the provisional period and at final Osseotite implants were placed sutured over the five submerged prosthesis delivery.

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down with the Precise 1 Automated Table 1 Clinical situation at each implant site System (Assing)26 and dehydrated Bone Implant Implant Biopsy or in an ascending series of alcohol Site* quality length (mm) status final prosthesis rinses, after which they were embed- 47 (31) Soft 13.0 Submerged Prosthesis ded in a glycolmethacrylate resin 46 (30) Soft 11.5 Immediately loaded Prosthesis (Technovit 7200 VLC, Heraeus 45 (29) Soft 13.0 Submerged Biopsy Kulzer). After polymerization, the 44 (28) Soft 13.0 Immediately loaded Prosthesis 43 (27) Soft 15.0 Immediately loaded Biopsy specimens were sectioned along the 42 (26) Normal 15.0 Submerged Prosthesis long axis with a high-precision dia- 32 (23) Normal 13.0 Submerged Biopsy mond disk at about 150 µm and 33 (22) Normal 15.0 Immediately loaded Prosthesis ground to about 50 µm. The slices 34 (21) Normal 13.0 Immediately loaded Prosthesis 35 (20) Soft 10.0 Submerged Prosthesis were stained with toluidine blue and 36 (19) Soft 11.5 Immediately loaded Prosthesis basic fuchsin and observed in normal *Fédération Dentaire Internationale tooth-numbering system (universal numbers are in parenthe- transmitted light. Histomorphometry ses).All sites healed. was performed by digitizing the images from the microscope via a JVC TK-C1380 color video camera (JVC Victor) and a frame grabber. Subsequently, they were analyzed by image-analysis software (IAS 2000, Delta Sistemi). No special diet recommenda- encountering the cortical tables. This tion was provided to the patient, reduced the amount of surrounding who was recalled after 1, 3, 4, and 8 bone around the retrieved implants. Results weeks. After 2 months of occlusal The biopsies were immediately loading, the provisional FPD was rinsed in a solution of NaCl 0.9% All immediately loaded implants unscrewed, and a gingival flap was and fixed. The soft tissue was achieved clinical osseointegration. raised. The submerged implants sutured, and standard prosthetic Consequently, they were added into received standard abutments, and procedures were carried out up to the final fixed prosthesis. The patient clinical mobility was checked at final prosthesis delivery. The has been uneventfully followed for every implant. All immediately trephined sites were checked clini- 24 months; an orthopantomogram loaded and submerged implants cally and radiographically after taken at that time (Fig 2b) confirmed achieved clinical osseointegration. implant retrieval until 24 months (Fig that the sites healed uneventfully Implants in the positions of the 2b). and were filled with bone. mandibular left lateral incisor (sub- Of the three retrieved implants, merged, placed in normal bone), two were submerged and one was right canine (immediately loaded, Histology preparation immediately loaded. Unfortunately, placed in soft bone), and right sec- the submerged implant placed in ond premolar (submerged, placed in The specimens were first rinsed in a normal bone was lost during pro- soft bone) were retrieved with a 5- saline solution and immediately cessing. One section from the sub- mm-diameter trephine (3i). Care was fixed in 4% paraformaldehyde and merged implant placed in soft bone taken to avoid altering the lingual 0.1% glutaraldehyde in a 0.15-M and one section from the immedi- and vestibular cortex at implant sites; cacodylate buffer at 4°C and a pH of ately loaded implant placed in soft the trephine was moved away when 7.4. Subsequently, they were ground bone were available for evaluation.

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Fig 3a (left) General overview of histo- logic section obtained at the submerged implant, mandibular right second premo- lar, shows poor bone quality. The vestibu- lar side is on the right (toluidine blue and basic fuchsin stain; original magnification 1.5).

Fig 3b (right) Higher magnification at the crestal part. Islands of dense bone are found mainly at the tip of the threads (tolui- dine blue and basic fuchsin stain; original magnification 10).

Fig 3c (left) Higher magnification at the spongious level. Discontinuous bone tra- beculae cover the Osseotite surface. Separation from implant surface is an arti- fact (toluidine blue and basic fuchsin stain; original magnification 10).

Fig 3d (right) Higher magnification of Fig 3c shows the discontinuous arrangement of the covering bone trabeculae. Separation from implant surface is an artifact (toluidine blue and basic fuchsin stain; original mag- nification 20).

Implant at mandibular right Osseointegration was achieved, and was in contact with implant collar, second premolar, submerged the measured bone-implant contact level with the cover screw. Coronally, healing for 2 months (BIC) was 38.9%. Bone contact with islands of dense bone were found, the Osseotite surface was observed. essentially at some thread tips (Figs The vestibular side of the section Poor bone quality with large marrow 3a and 3b). More apically, inter- and the upper half of the lingual spaces was found at the crestal and rupted thin bone trabeculae ran side were readable (Figs 3a and 3b). spongious areas (Fig 3). The crest along the implant surface, evoking

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a flowing bone coverage of the tex- Discussion Osseotite surface has osteoconduc- tured surface (Figs 3c and 3d). tive properties.31 A similar observa- Detachment of the trabeculae from The present case report documents, tion in the posterior maxillae of the implant surface was likely an arti- for the first time, osseointegration humans2 was reported. In the softer fact created during biopsy retrieval of Osseotite implants placed in soft bone, the BIC for the Osseotite tex- and specimen preparation. bone after 2 months of healing, tured surface was 59.1% ± 25.3%, either unloaded or immediately compared to 6.5% ± 10.8% for the loaded. These findings are relevant machined surface. Implant at mandibular right because bone quality has been rec- The present human data were canine, healing under occlusal ognized to be a key parameter in obtained at a standard implant (3.75- function for 2 months the prognosis of both delayed27–29 mm diameter). They are in line with and immediately loaded proto- the bone response observed at mini- Only the vestibular side of this imme- cols.16,18,21 Osseointegration and the implants with a 2.00-mm diameter diately loaded implant was readable BIC (38.9%) measured at the sub- placed in the posterior maxilla.2 (Fig 4a). Osseointegration was merged implant support the clinical Therefore, the data might support achieved, the measured BIC was finding of Lazzara et al.17 Based on validation of the mini-implant model, 64.2%, and fibrous encapsulation 132 implants placed in soft bone, which was developed to optimize was not seen. Bone marrow occu- those authors demonstrated that the the response of human bone to spe- pied most of the crestal and spon- Osseotite implant might be pre- cific surface treatments. gious areas. The bone crest top was dictably loaded after 2 months of The efficacy of the thin isolated level with the first implant thread healing, even when placed in soft bone shell to resist mastication (Figs 4a and 4b), but the first BIC bone. forces may be questioned. However, occurred more apically at the level of In the spongious area, the pat- its participation appears to be effec- the third thread. The adjacent corti- tern of thin bone trabeculae cover- tive, since the same feature was cal bone was composed of newly ing the textured Osseotite surface found at the companion osseointe- formed bone, and remnants of the (Figs 3c and 3d) was consistent with grated immediately loaded implant. old bone were found embedded in the description obtained at human Rohrer et al32 observed similar thin this bone. Under the cortex, a single sites with soft bone.2 The arrange- trabeculae in human retrieved im- marrow space extended down to ment of new thin trabeculae sur- plants that had been successfully the ninth thread. In this spongious rounding the implant at the spon- loaded for 1 year. In a three-dimen- area, the implant’s textured surface gious area corresponds to the sional perspective, they noted that was covered by an almost continu- feature described as contact osteo- they were connected to a larger net- ous thin shell of newly formed bone genesis.30 The presence of thin tra- work of sustaining bone. in continuation with the crestal cor- beculae probably means that osteo- The present immediately tex (Figs 4b and 4c). More apically, progenitor cells were recruited loaded implant placed in soft bone bone was denser, with large marrow directly to the implant surface osseointegrated, as did other imme- spaces (Figs 4a and 4d). New bone instead of remaining at a distance. diately loaded implants inserted in contacted the metallic surface, inter- This could have resulted in a quicker normal bone.24 In contrast to the posing between the old bone and implant integration than is obtained companion submerged implant, the the interface. Epithelium down- at a machined surface. The thin bone crest stayed away from contacting growth was not observed. trabeculae were formed in the mar- the first two threads. Down to its row space after implant placement in first implant contact, the crest was an environment of few preexisting composed of new dense cortical trabeculae and suggest that the bone (Figs 4b and 4c) that seemed

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Fig 4a (left) General overview of histo- logic section obtained at the immediately loaded implant, mandibular right canine, shows the poor bone quality. The vestibu- lar side is on the right. Old bone is more purple (toluidine blue and basic fuchsin stain; original magnification 1.5).

Fig 4b (right) Higher magnification at the upper part. Note the large marrow space beneath the crestal bone and the thin shell of trabecular bone covering the implant surface (toluidine blue and basic fuchsin stain; original magnification 5).

Fig 4c (left) Higher magnification at the junction of the crestal and trabecular bone. In continuation with the crest, a thin bone trabecule covers the implant surface (tolui- dine blue and basic fuchsin stain; original magnification 15).

Fig 4d (right) Higher magnification at the apical implant part. Note that new bone appears to be flowing over the surface and is interposed between the old bone and implant surface. Bone remodeling and bone apposition happened despite heal- ing under loading (toluidine blue and basic fuchsin stain; original magnification 15).

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to follow a defined orientation. This report). Further studies should osteoconductive properties and is indicates that after 2 months of func- address this intriguing issue. capable of contact osteogenesis. tion, the crestal bone adapted to The present case report, in addi- the functional load. New bone was tion to a previous one,24 docu- found interposed between the old mented that osseointegration of References bone and the metallic surface, sug- Osseotite implants can be achieved gesting that the load-bearing capac- despite immediate loading. As all 1. Buser D, Schenk RK, Steinemann SG, Fiorellini JP, Fox CH, Stich H. Influence of ity of the interface was maintained remaining immediately loaded surface characteristics on bone integra- over replacement of any necrotized implants maintained clinical osseoin- tion of titanium implants: A histomorpho- bone that occurred during implan- tegration over 14 months of func- metric study in miniature pigs. J Biomed Mater Res 1991;25:889–902. tation. Consequently, the exerted tion, it is at present reasonable to load did not interfere with the osteo- assume that they osseointegrated 2. Lazzara RJ, Testori T, Trisi P, Porter SS, Weinstein RL. A human histologic analysis 16 genesis as previously thought. as well. In fact, it seems that failure of of Osseotite and machined surfaces using It might also be that the func- nonintegrated or poorly integrated implants with 2 opposing surfaces. Int J tional loading stimulated bone immediately loaded implants mostly Periodontics Restorative Dent 1999;19: 3–16. apposition, because the BIC mea- occurs during the first 6 to 12 months sured at the immediately loaded of function.18,21,22,36–38 Immediate 3. Trisi P, Rao W, Rebaudi A. A histometric comparison of smooth and rough titanium implant (64.2%) was higher than that loading protocols are aimed to sim- implants in human low-density jawbone. measured at the submerged implant plify implant therapy and decrease Int J Oral Maxillofac Implants 1999;14: (38.9%). A similar bone stimulation the costs. This is achieved by reduc- 689–698. has been reported by Piattelli et al.33 ing the number of surgeries and the 4. Klokkevold PR, Nishimura RD, Adashi M, In a monkey model, mandibular and number of sessions required to Caputo AM. Osseointegration enhanced by chemical etching of the titanium sur- 24 maxillary rough implants were either deliver the final fixed prosthesis. face. A torque removal study in the rabbit. loaded 3 days after placement or All retrieved immediately loaded Clin Oral Implants Res 1997;8:442-447. left unloaded for 9 months. More implants were osseointegrated, and 5. Baker DA, London RM, O’Neil RB. Rate of bone with a more compact appear- all immediately loaded implants pull-out strength gain of dual-etched tita- ance was found at the mandibular maintained their clinical stability; nium implants: A comparative study in rabbits. Int J Oral Maxillofac Implants and maxillary immediately loaded therefore, it might be that six im- 1999;14:722–728. implants. BIC at the mandible for plants are sufficient to support an 6. Szmukler-Moncler S, Perrin D, Bernard JP, the immediately loaded and un- immediately loaded cross-arch pros- Pointaire P. Biological properties of titani- loaded implants was 72.3% ± 5.9% thesis in the mandible without any um acid etched surfaces: Effect of surface and 55.8% ± 6.5%, respectively. In additional submerged implants. composition and surface alteration. Influence of sandblasting on bony anchor- 34,35 contrast, others found that load- However, before this protocol can age [abstract]. Clin Oral Implants Res 1999; ing exerted during the healing be routinely applied, it should be 10:173. period led to less BIC. It might be documented with a sufficient num- 7. Szmukler-Moncler S, Reingewirtz Y, Weber that surface state plays a critical role ber of patients in the long term. H-P. Bone response to early loading: The when healing occurs under loading, The two Osseotite implants effect of surface state. In: Davidovitch Z, Norton LA (eds). Biological Mechanisms of as suggested by Szmukler-Moncler placed in soft bone osseointegrated Tooth Movement and Craniofacial et al.7 It should be stressed that the whether left submerged for 2 months Adaptation. Boston: Harvard Society for latter studies involved either or immediately loaded for 2 months. the Advancement of , 1996:611–616. machined35 or smooth34 implants, In the marrow space, a thin shell of whereas the implants that led to a new bone trabeculae was observed 8. Faehn O, Siddiqui AA, Lazzara RJ, Feldman SA. A four-year retrospective BIC increase were roughened either at both implants. This finding sug- study of 3i threaded implants. Aust physically33 or chemically (present gests that the Osseotite surface has Prosthodont J 1995;9:9–15.

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9. Lazzara RJ, Siddiqui AA, Binon P, et al. 19. Schnitman P, Wöhrle PS, Rubenstein JE, 28. Jaffin RA, Berman CL. The excessive loss Retrospective multicenter analysis of 3i DaSilva JD, Wang NH. Ten-year results for of Brånemark fixtures in type IV bone. A 5- endosseous dental implants placed over Brånemark implants immediately loaded year analysis. J Periodontol 1991;62:2–4. a five-year period. Clin Oral Implants Res with fixed prostheses at implant place- 29. Henry PJ, Tolman DE, Bolender C. The 1996;7:73–83. ment. Int J Oral Maxillofac Implants 1997; applicability of osseointegrated implants 12:495–503. 10. Esposito M, Hirsch J-M, Lekholm U, in the treatment of partially edentulous Thomsen P. Biological factors contribut- 20. Salama H, Rose LF, Salama M, Betts NJ. patients: 3-year results of a prospective ing to failures of osseointegrated oral Immediate loading of bilaterally splinted multicenter study. Quintessence Int implants. I. 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