The International Journal of Periodontics & Restorative

COPYRIGHT © 2002 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY.NO PART OF THIS ARTICLE MAY BE REPRO- DUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. 1–4 451 and clin- 9 9 and clinical stud- et, in all these studies, 5–11 olume 21, Number 5, 2001 Y V are now showing that early now showing that are literature discussing early load- literature For fixed rehabilitations, imme- For fixed rehabilitations, 12–14,16–18 19 12–19 eview of the experimental and immediate loading may lead to . A predictable r ical However, a growing number of number a growing However, experimental ing (< 3 months of healing) protocols in implant dentistry came to the con- clusion that early loading per se is for the lack of not responsible osseointegration; the latter is rather of excessive due to the presence during the healing micromotion phase. The authors showed that implant design, surface state, load- rehabilita- ing mode, and prosthetic tion type dictate the bone response the tradi- to implants loaded before tional 3 months of healing. diate loading with various implant systems has been studied, and high success rates have been report- ed. The original Brånemark protocol rec- The original Brånemark protocol healing ommended long stress-free periods to achieve the osseointe- gration of dental implants. ies the number of enrolled patients did the number of enrolled not exceed 10 individuals per study. (Int J and Institute of Stomatology, Plastic Surgery and Maxillo-facial Surgery, Plastic Surgery and Institute of Stomatology, Hospital, University of Paris VI, France. Salpetrière Reprint requests: Dr Tiziano Testori, Dipartimento di Medicina, Chirurgia e di Medicina, Chirurgia Dipartimento Testori, Dr Tiziano Reprint requests: Via Beldiletto 1/3, 20142 Milano, Odontoiatria, Cattedra di Parodontologia, e-mail: [email protected] Italy. Institute for Oral Health Care Sciences, London. Institute for Oral Health Care *Visiting Professor, Department of , University of Milano, Italy. University Department of Periodontology, *Visiting Professor, **Visiting Professor, Department of Periodontology, University of Milano, Italy; Department of Periodontology, Professor, **Visiting ***Researcher, Department of Periodontology, University of Milano, Italy. Department of Periodontology, ***Researcher, ****Department of Periodontology, University of Milano, Italy. ****Department of Periodontology, *****Research Fellow, Dental School, University of Chieti, Italy. Fellow, *****Research iziano Testori, MD, DDS*/Serge Szmukler-Moncler, DDS**/ Szmukler-Moncler, MD, DDS*/Serge iziano Testori, ******Professor, Dental School, University of Chieti, Italy; and Eastman Dental ******Professor, T BSc, PhD****/ Del Fabbro, Luca Francetti, MD, DDS***/Massimo Piattelli, MD, DDS******/ Antonio Scarano, DDS*****/Adriano MD, DDS******* Roberto L. Weinstein, of Occlusal Loading of Occlusal Histologic Analysis After 4 Months Analysis After 4 Months Histologic Implants: A Case Report and Report A Case Implants: Immediate Loading of Osseotite Loading Immediate *** ** * **** ****** ***** Periodontics Restorative Dent 2001;21:451–459.) A growing number of clinical reports show that early and immediate loading of show number of clinical reports A growing these osseointegration; however, endosseous implants may lead to predictable mostly short- to mid-term and based only on clinical mobility studies provide results needed to detect the possible pres- are radiographic observation. Other methods in the course of time interposition of tissue that could increase ence of a thin fibrous A histologic evaluation was performed on two immedi- and lead to clinical mobility. one after 4 months of function from ately loaded Osseotite implants retrieved a total of 12 implants in the mandible, of which six were patient. He had received Clinical and his- way. left to heal in a submerged immediately loaded and six were imme- achieved for both of the retrieved tologic osseointegration was consistently on the Osseotite sur- bone remodeling diately loaded implants. Osteogenesis and not impeded by immediate loading as shown by histomorphometric face were high levels of bone-to-implant contact ranging from evaluation, which revealed involving bilateral splinting of six 78% to 85%. This immediate loading protocol to be successful after 4 months of load- Osseotite implants in the mandible proved introducing ing. Further long-term needed before histologic studies are clinical and in implant therapy. procedure as a routine this immediate loading protocol ******* *******Professor and Chair, Department of Periodontology, University of Milano, Italy. Department of Periodontology, and Chair, *******Professor

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Although clinical results seem to be Method and materials immediately loaded implants. These promising in regard to immediate would be retrieved after 4 months of loading with a fixed cross-arch pros- Case report function, at uncovering the sub- thesis, further long-term follow-ups merged implants. The patient vol- and larger numbers of patients are A healthy 61-year-old nonsmoking unteered for the protocol and required. Moreover, the above- man was examined for a failing fixed signed an informed consent form. It mentioned clinical studies provide partial denture (FPD) retained on five was therefore decided to place 12 mostly short- to mid-term results teeth and two implants. His teeth Osseotite implants, six implants to based only on clinical mobility and were in a state of advanced peri- support the immediately loaded radiographic observation. These odontal disease, one implant dis- provisional FPD and six submerged methods are not suitable to detect played noticeable bone loss be- implants to retain the final com- the possible presence of a thin cause of untreated periimplantitis, plete-arch rehabilitation of the fibrous interposition of tissue that and the second one was lingually mandible. The two implants des- can increase over the course of time angled. It was decided to extract all tined to be retrieved were chosen to and lead to clinical mobility.9,19 of the remaining teeth and remove allow for adequate prosthetic sup- While several animal experi- the preexisting dental implants. As port by the remaining implants. ments dealing with early and imme- the patient wore an overdenture in instructions were diate loading protocols have been the maxilla, he could not cope psy- given, and before surgery the published,5–11 extrapolation from chologically with another denture or patient was scheduled for proce- the animal model to the clinical with any other kind of partially dures to control his inflammatory application is not fully reliable removable appliance and therefore disease. Subgingival scaling and because of the distinct loading requested an immediate fixed root planing were performed. schemes and exerted stresses. restoration. An immediate loading Augmentin (SmithKline Beecham) Retrievals of immediately loaded protocol according to Schnitman et and Flagyl (Pharmacia & Upjohn) implants displaying clinical stability al,12 involving simultaneous place- were administered 7 days before have been scarce20–24 and have ment of submerged and immedi- implant placement and were con- involved a limited number of im- ately loaded implants in the eden- tinued for 6 days. Teeth were gen- plants. As surface state7 and loading tulous mandible, was discussed with tly removed and the sockets de- mode9 play a determinant role in the patient. In this protocol, the granulated. The implants were healing under loading, demonstra- immediately loaded implants are explanted with a premolar forceps, tion of osseointegration by means of intended to sustain a provisional trephining was avoided to preserve histologic evidence is warranted for FPD, while the submerged implants bone quantity, and the implant bed each implant type differing in design are left to heal in the traditional way. was thoroughly cleaned to remove and/or surface. The rationale is that, should every any remaining soft tissue. Self-tap- The aim of the present article is immediately loaded implant fail dur- ping Osseotite implants were to report on two Osseotite implants ing the provisional period, a suffi- placed according to the manufac- (3i), retrieved from one patient, that cient number of submerged turer’s instructions (Fig 1a). All had been immediately loaded after implants would still support the final implants displayed a high degree S ARTICLE MAY BE REPRO- placement and were in function for fixed rehabilitation. of primary stability, requiring a ≥ 32 4 months in the mandible. It was proposed to the patient Ncm torque as tested with a torque- that he receive two additional control instrument. At a freshly immediately loaded implants to explanted implant site, congruence retain his provisional FPD, with the at the implant neck was not aim of obtaining biopsies of the obtained, and the resulting circular

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Fig 1a (left) Surgical template in situ dur- ing surgery.

Fig 1b (right) Provisional restoration 4 hours after surgery. Standard abutments have been screwed on the six implants and immediately loaded.

Fig 1c (left) Final restoration, anterior view.

Fig 1d (right) Final restoration, occlusal view.

crestal bone defect of about 1 mm reinforced provisional FPD was that all of the immediately loaded was filled with bone chips collected seated on the six abutments (Fig 1b). and submerged implants had with a bone trap during surgery. No special diet was suggested achieved clinical osseointegration. Normal bone density was recorded for the patient, who was recalled Implants that were immediately at all implant sites. The immediately after 1 week, 3 weeks, and there- loaded in the positions of the

S ARTICLE MAY BE REPRO- loaded implants received 4-mm- after on a monthly basis. After 4 mandibular left second premolar high standard abutments. The soft months of occlusal function, the and right lateral incisor were re- tissues were sutured over the six provisional FPD was unscrewed, a trieved with a 5-mm-diameter submerged implants and around gingival flap was opened, and the trephine (3i). Care was taken to the six protruding abutments. Four previously submerged implants re- avoid altering the lingual and hours following implant placement, ceived standard abutments. Clini- vestibular cortex at the implant sites. a screw-retained, resin metal– cal mobility was assessed, revealing During drilling, the trephine was

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after which they were embedded in a glycolmethacrylate resin (Technovit 7200 VLC, Heraeus Kulzer). After polymerization, the specimens were sectioned along the long axis with a high-precision diamond disk at about 150 µm and ground to about 30 µm. Great attention was paid to cut the slide sections parallel to the long axis of the implant in an attempt to obtain three slices per specimen. The slices were stained with Paragon

Fig 2a Panoramic radiograph after provisional rehabilitation, 4 hours postsurgery. (Paragon C & C) and observed in normal transmitted light. Histomor- phometry was performed under a Laborlux-S light microscope (Leitz), using an Intel Pentium II 300 MMX computer, a video camera, and KS 100 Software (Zeiss). The acquired images were analyzed using the soft- ware system described.

Results

All of the immediately loaded im- plants achieved clinical osseointe- gration. Subsequently, they were Fig 2b Panoramic radiograph obtained 24 months after biopsy retrieval. Note that the biopsied sites healed completely. added into the final fixed prosthesis. The patient was followed after implant retrieval, and a radiograph taken 24 months later (Fig 2b) con- firmed that the trephined sites had tilted away from the cortical tables; Histology preparation healed without complications. this reduced the amount of avail- The implant at the mandibular able bone in some areas of the The specimens were first rinsed in a right lateral incisor was retrieved with retrieved biopsies. The flap was saline solution and immediately vestibular as well as buccal bone, sutured, and standard prosthetic fixed in 4% paraformaldehyde and and one histologic section was S ARTICLE MAY BE REPRO- procedures were carried out up to 0.1% glutaraldehyde in a 0.15-M obtained. Figure 4a gives an final restoration (Figs 1c and 1d). cacodylate buffer at 4°C and a pH of overview of the preparation; osseo- Radiographs were taken after 7.4. Subsequently, they were ground integration was achieved with close implant placement (Fig 2a), at down with the Precise 1 automated bone apposition as observed under retrieval, and 24 months later (Figs system (Assing)25 and dehydrated in the optical microscope (Fig 4b), and 2b and 3). an ascending series of alcohol rinses, bone-to-implant contact was 80%.

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Figs 3a to 3c Periapical radiographs of the final case show no radiolucency around the implants.

The implant-bone interface con- of the threads. Again, epithelium providing short- to mid-term data. sisted of a combination of new and downgrowth was not found at the They are based on clinical mobility old bone. Bone was in contact with interface. Figure 5a shows that the and radiographic analysis and are the entire implant surface, including implant was placed in bone of nor- therefore not able to provide reli- the inner diameter of the screw mal quality. able information on the status of the threads, ie, the bottom part between implant-bone interface.26,27 Subse- the threads (Fig 4). Occasionally, quent human histologic investiga- bone was not present at the tip of Discussion tions are needed to demonstrate the some threads. On the vestibular side, actual implant osseointegration for the crest was situated above the first A 3- to 6-month healing period has each variety of immediate loading thread level; on the lingual, it was long been considered a prerequi- protocol and implant system.19 slightly above the second thread (Fig site for the achievement of osseoin- Four reasons might explain why 4a). Epithelium downgrowth was not tegration.1–4 However, the relevance early loading has been discour- found at the infracrestal areas con- of this concept has been recently aged19: (1) it may lead to fibrous tacting the implant surface. questioned in both the animal and integration; (2) the necrotic bone Only the vestibular part of the the clinical literature.9,19 The human at the implant bed border is not retrieved left second premolar im- histology data of the present study capable of load bearing and must plant was readable, and three histo- confirm that loading per se does not first be replaced by new bone; (3) logic sections were obtained. Figure impede osseointegration. Rather, rapid remodeling of the dead bone 5a gives an overview of one of the osseointegration of immediately layer compromises the strength of histologic preparations. Osseointe- loaded Osseotite implants has now the osseous tissue supporting the gration was achieved in all slices, been documented for the first time. bone-implant interface; and (4) the and the mean bone-to-implant con- These histologic data also strongly integrity of the periosteal margin

S ARTICLE MAY BE REPRO- tact was 81.5% (78% to 85%). Similar support the assumption that the may be threatened by undermin- to the previous implant, old and new other immediately loaded implants ing remodeling of adjacent bone bone was seen at the interface (Fig incorporated in this prosthesis during the late healing period. The 5b). The new bone was undergoing osseointegrated as well. present implants were loaded 4 remodeling, the implant surface was At present, only a limited num- hours after placement and were in contacted by bone, and no lacking ber of clinical immediate loading occlusal function for 4 months in bone patterns were found at the tip studies have been published, the mandible. At the interface, a

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Fig 4a (left) General overview of section from mandibular right lateral incisor implant shows that the recipient site was of good bone quality. Bone is reaching the internal core of the screw, between the threads. The vestibular side is on the left (Paragon stain; original magnification 1.5).

Fig 4b (right) Direct bone apposition at implant surface shows osseointegration and the presence of old (light stain) and new bone (darker stain). The vestibular side is on the left (Paragon stain; original magnification 25).

Fig 5a (left) Overview of section 1 of mandibular left second premolar implant shows that only the vestibular side, left, is readable. Bone quality at the recipient site was good; during surgery, it was identified as normal bone. On the vestibular side, bone reaches the internal core of the implant screw. The implant is well integrat- ed and presents a high level of osseointe- gration (Paragon stain; original magnifica- tion 1.5).

Fig 5b (right) Direct bone apposition at implant surface (section 2) shows osseoin- tegration and the presence of old and new bone (darker stain). Bone remodeling occurs as well at a distance (Paragon stain; original magnification 25). S ARTICLE MAY BE REPRO-

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combination of remodeled mature a substantial anchorage to the fibrin apposition was found despite load- new bone and old bone was found, fibers of the clot. This suggests a ing 4 hours after surgery. The dif- similar to loaded implants that heal higher clot stability in case of micro- ference may be attributed to the in a traditional way.28,29 This proves motion and subsequently a higher surface features because they play a that the bone-healing sequence threshold of tolerance to deleterious key role in bone response.7 Indeed, was not disturbed by the stresses micromotion. In the present patient, in the dog study,6 bone interacted transmitted under this mechanical six implants arranged in a wide tri- with a smooth machined surface, environment. Moreover, the histol- pod were splinted 4 hours after whereas in the present study the ogy data demonstrate that both the implant placement. Implants were patient’s bone responded to the bone injured during drilling and the sufficient in number because Osseotite textured surface. The dif- remodeled necrotic bone provided Schnitman et al12 suggested that ference might be also due to the sufficient load-bearing capacity. In three implants arranged in a wide strain amplitude at the interface. In addition, the data show that the tripod might be enough to sustain the present patient six implants periosteal margins were not threat- a provisional FPD. The prosthesis were bilaterally splinted in a wide tri- ened by extensive remodeling. was conceived to allow full occlusal pod, whereas in the above experi- Implant design, surface state, loading, the most demanding load- mental study6 three implants were splinting, and the loading mode ing mode,9 under a mechanically splinted in a unilateral FPD. It should influence bone-implant interface disadvantageous crown:implant be stressed that the unilateral FPD status, ie, either osseointegration or ratio of 1.1:1.4; splinting was suffi- design allows for high moment in fibrous encapsulation.19 The present cient to decrease the amount of the vestibulolingual axis, while the screw design has been associated micromotion during mastication bilateral FPD configuration reduces with primary stability,30,31 which below the threshold of deleterious it.31 Furthermore, occlusion in this seems to be the paramount require- micromotion. patient was obtained in this region ment to achieve osseointegration, Sagara et al6 investigated the via an overdenture with resin con- whatever the loading conditions are. bone-healing response to three dis- tacts, whereas in the dog it was The Osseotite dual-etched textured tinct loading modes, the sub- obtained through a fixed metallic surface represents an improvement merged mode, the protruding bar connected to natural teeth in over the machined surface.32,33 mode (implant post protruding in the maxilla. Clinically, this has been assessed by the oral cavity, more than 3 mm An intriguing feature was ob- Testori et al34; they did not observe above the bone level; soft diet; served at both retrieved immediately any increased failure rate for short pressure exerted by tongue, cheeks, loaded implants. The first implant-to- Osseotite implants (≤ 10 mm), in and lips9), and the occlusal mode bone-contact occurred at a lower contrast to short-machined surface (crown on post, occlusion, and hard level with respect to the cortical implants.34–38 In addition, Lazzara et diet9), that started 7 days after crest, down to the upper flank of the al39 demonstrated that the surgery. Early loading in the occlusal third thread (Figs 4a and 5a). This Osseotite surface makes it possible mode led to incomplete bone region corresponds to the transition to predictably reduce the healing apposition, ie, bone did not grow zone between the turned and the

S ARTICLE MAY BE REPRO- period to 8 weeks, even for single down to the implant surface Osseotite textured surface. It could teeth and short-span FPDs, from the between the threads, but stayed at be that under immediate loading 12 to 24 weeks recommended for a distance from the implant surface.6 conditions, the bone that is under- machined surfaces. Furthermore, These authors attributed this to the going healing requires the presence Davies40 showed in vitro that the effect of early occlusal loading dur- of the Osseotite microtextured Osseotite surface, in contrast to a ing initial bone healing. In the pre- surface rather than the turned sur- machined surface, is able to ensure sent histology data, complete bone face to distribute adequately the

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stresses at the bone-implant inter- Osseointegration was consis- 5. Akagawa Y, Ichikawa Y, Nikai H, Tsuru H. face. Furthermore, the earliest tently achieved for both retrieved Interface histology of early loaded par- tially stabilized zirconia endosseous immediately loaded Osseotite stages of endosseous wound heal- implant in initial bone healing. J Prosthet ing have been proposed to be criti- implants. An immediate loading pro- Dent 1993;69:599–604. cally dependent on platelet activa- tocol involving bilateral splinting of 6. Sagara M, Akagawa Y, Nikai H, Tsuru H. tion and fibrin retention by the six Osseotite implants proved to be The effects of early occlusal loading on implant surface.40 These phenom- safe in this patient after 4 months of one-stage titanium implants in beagle dogs: A pilot study. J Prosthet Dent 1993; loading. Bone remodeling was not ena seem to be favored by a micro- 69:281–288. impeded by these immediate load- textured surface, as described in 7. Szmukler-Moncler S, Reingewirtz Y, recent papers by Davies and ing conditions. A high level of bone Weber H-P. Bone response to early load- coworkers,41,42 and precede and apposition was measured (78% to ing: The effect of surface state. In: accelerate osteogenic cell migration 85%), including growth down to the Davidovitch Z, Norton LA (eds). Biological Mechanisms of Tooth Movement and bottom of the threads. The interface toward the implant surface through Cranio-Facial Adaptation. Boston: a fibrin meshwork. Therefore, the was composed of a combination of Harvard Society for the Advancement of osteoconductive nature of a micro- mature new bone and old bone, as , 1996:611–616. textured implant surface like with unloaded implants. Load-bear- 8. Piattelli A, Corigliano M, Scarano A, Osseotite may increase the rate at ing capacity was ensured by the Quaranta M. Immediate loading of tita- nium plasma-sprayed implants: A histo- dynamic remodeling of the necrotic which new bone forms on the logic analysis in monkeys. J Periodontol implant, thereby reducing the inter- bone. Further clinical and histologic 1998;69:321–327. val necessary between implant studies are needed before a proto- 9. Szmukler-Moncler S, Salama S, placement and functional loading. col of five to six immediately loaded Reingewirtz Y, Dubruille JH. Timing of Therefore, when shortened proto- implants can be introduced on a reg- loading and effect of micromotion on bone- interface: Review of ular basis in implant therapy. cols are indicated, it might be advan- experimental literature. J Biomed Mater tageous to have a textured surface Res 1998;43:192–203. up to the implant collar to increase 10. Corso M, Sirota C, Fiorellini J, Rasool F, the healing potential of the most References Szmukler-Moncler S, Weber H-P. Clinical coronal part of the immediately and radiographic evaluation of early loaded free-standing dental implants with loaded implants. Further studies 1. Adell R, Lekholm U, Rockler B, Brånemark P-I. A 15-year study of osseointegrated various coatings in beagle dogs. J should address this issue. implants in the treatment of the edentu- Prosthet Dent 1999;82:428–435. The development of pre- lous jaw. Int J Oral Surg 1981;10:387–416. 11. Szmukler-Moncler S, Figueredo FR, Trisi P, dictable immediate loading proto- 2. Albrektsson T, Brånemark P-I, Hansson Legrand R, Ropen E. Immediate loading cols should be regarded as an effort HA, Lindström J. Osseointegrated titani- of single crowns retained by short im- plants. A histologic study with various to alleviate the psychologic burden um implants: Requirements for ensuring a long-lasting direct bone to implant anchor- surfaces in the canine mandible [abstr]. of patients switching from partial to age in man. Acta Orthop Scand 1981;52: Clin Oral Implants Res 2000;11:373. 12–14 total edentulism or facing sud- 155–170. 12. Schnitman PA, Wöhrle PS, Rubenstein JE. 18 den tooth loss. In addition, imme- 3. Brånemark P-I, Zarb GA, Albrektsson T. Immediate fixed interim prostheses sup- diate loading simplifies and eases Tissue-Integrated Prostheses: Osseointe- ported by two-stage threaded implants: Methodology and results. J Oral implant therapy, shortens it, and ren- gration in Clinical Dentistry. Chicago: S ARTICLE MAY BE REPRO- Quintessence, 1985. Implantol 1990;2:96–105. ders it more cost effective.14,16 4. Albrektsson T, Hansson HA, Lekholm U. 13. Schnitman PA, Wöhrle PS, Rubenstein JE, Simplification and reduction of treat- Osseointegrated dental implants. Dent DaSilva JD, Wang NH. Ten-year results for ment costs are achieved by reduc- Clin North Am 1986;30:151–174. Brånemark implants immediately loaded ing the numbers of surgeries and with fixed prostheses at implant place- ment. Int J Oral Maxillofac Implants 1997; the number of sessions required to 12:495–503. deliver the final fixed prosthesis.

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Volume 21, Number 5, 2001