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Primary loading of palatal implants for orthodontic anchorage – A pilot animal study
Journal of Cranio-Maxillofacial Surgery (2008) 36, 21e27 Ó 2007 European Association for Cranio-Maxillofacial Surgery doi:10.1016/j.jcms.2007.07.006, available online at http://www.sciencedirect.com
Primary loading of palatal implants for orthodontic anchorage e A pilot animal study Pe´ter BORBE´LY1, Miklo´s P. DUNAY2, Britta A. JUNG3, Heinrich WEHRBEIN3, Wilfried WAGNER4, Martin KUNKEL4 Fogszaba´lyoza´si Stu´dio´, Private Practice, Budapest, Hungary; 2 Department of Surgery (Chair: Prof. Dr. Tibor Nemeth) Szent Istva´n University, Faculty of Veterinary Science, Budapest, Hungary; 3 Department of Orthodontics (Chair: Prof. Dr. Dr. H. Wehrbein); 4 Department of Oral and Maxillofacial Surgery (Chair: Prof. Dr. Dr. W. Wagner) University of Mainz, Germany
1
Objectives: This study aimed at evaluating the clinical performance and osseointegration of short orthodontic implants immediately loaded with orthodontic forces. Material and methods: The investigation was designed as an experimental animal study. Eight palatal implants of the Ortho-systemÒ were immediately loaded with 100 cN after palatal insertion in 4 female german shepherd dogs. Xylene orange and calcein green were used for polychrome sequential labelling. Histological preparation utilized the cutting and grinding technique. Outcome variables were clinical implant success, histological osseointegration and bone-to-implant contact rates. Results: All (8/8) implants were clinically successful and stable when the animals were sacrificed. One implant showed fibrous encapsulation and was histologically classified as ‘‘failed’’ for ‘‘osseointegration’’. Upon morphometrical analysis, bone to implant contact rates for newly formed or remodelled bone were 19% at 4 weeks and 26% at 6 months. The fluorochrome labelling indicated substantial mineral apposition on the surface of the implants at the end of the first and the second postoperative months. Conclusion: This study revealed borderline reliability of osseointegration for immediately loaded palatal implants but reasonable bone formation at the 4th postoperative week. Thus, two clinical concepts are both supported: early orthodontic loading after 4 weeks as well as improvement of primary stability to provide a biomechanical basis for immediate orthodontic loading. Ó 2007 European Association for Cranio-Maxillofacial Surgery
SUMMARY.
Keywords: palatal implant, Ortho-systemÒ, Ortho implantÒ, orthodontic loading, osseointegration, dental implants, animal study, polychrome sequential labelling, orthodontic anchorage, early loading, morphometry
introduced for orthodontic loading in the last decade. Today, there is evidence, that osseointegrated implants remain positionally stable under typical orthodontic loading conditions (Wehrbein & Diedrich, 1993; Wehrbein et al., 1996a, 1996b, 1999; Bernhart et al., 2001; Freudenthaler et al., 2001; Fortini et al., 2004). The use of palatal implants of the Ortho-systemÒ (Straumann, Basel, Switzerland) has been extensively investigated and can be regarded as a classic for orthodontic skeletal anchorage (Wehrbein & Diedrich, 1993; Wehrbein, 1994; Wehrbein et al., 1996a, 1996b, 1998, 1999; Cously, 2005). However, a relevant drawback of this system is, at least according to the present manufacturers instructions, that the healing period has to be at least 3 months. Encouraged by recent research progress in implantology (Cochran et al., 2004; Nkenke and Fenner, 2006) demonstrating high success rates for immediate and early loading in prosthetic implants, it was the aim of this pilot study to evaluate, whether immediate loading could also be applied for short orthodontic implants. Therefore, an experimental animal study was initiated, to investigate the feasibility of immediate loading for palatal implants of the OrthoÒ- system.
INTRODUCTION Anchorage, defined as the ‘‘resistance to unwanted tooth movement’’ is a fundamental orthodontic problem and a major determinant of success in the treatment of dental and skeletal dysgnathia (Diedrich, 1993; Willems et al., 1999). Loading of an anchorage unit in orthodontic treatment is possible on the conditions of a static equilibrium of forces (action ¼ reaction). Hence, if teeth are used for anchorage, their reaction to quantity, type and duration of the forces and moments applied through the orthodontic biomechanics is critical for active movement of other teeth. Anchorage can be enhanced to a limited degree by connecting several teeth using rigid steel wires or heavy ligatures. Supportive appliances such as ‘‘external’’ headgear and inter-maxillary elastics can provide additional stability. However, these pose considerable inconveniences, are visible, and even bear the risk of potential injury (Booth-Mason and Birnie, 1988; BlumHareuveni et al., 2004). Moreover, patients acceptance is crucial and compliance is another limiting factor (Diedrich, 1993). To overcome the limits of dental orthodontic anchorage, numerous skeletal anchorage devices have been 21
22 Journal of Cranio-Maxillofacial Surgery
MATERIAL AND METHODS Animals Four female german shepherd dogs (age 1 year) were operated upon under general anaesthesia. The study protocol was approved by the review board of the Hungarian ¨ . e´s E´ell. All. Ministry of Agriculture (Ref. Nr. FTv. Aeu 271/2003/2004). Following sedation by subcutaneous application of 0.1 mg/kg (body weight) acepromazine (Vetranquil 1%: Ceva-Sante Animale, La Ballastiere, France), the animals were anaesthesized by an intra-venous bolus of xylazine (Primazin 2%: Alfasan International, Woerden, Netherlands) 1 mg/kg and ketamine (Calypsol: Richter, Budapest, Hungary) 10 mg/kg. For peri-operative prophylaxis the animals received 30 mg/kg amoxicillin and 7.5 mg/kg clavulanic acid (Synulox RTU: Pfizer, Sandwich, UK). Prior to intraoral surgery, a polividone iodine mouth-rinse (Betadine: Egis, Budapest, Hungary) was applied for local disinfection. Meloxicam 0.2 mg/kg (Metacam 0.5%: Labania Life Science, Barcelona, Spain) was given subcutaneously for peri- and post-operative analgesia. Palatal implants of the Ortho-systemÒ (Straumann, Basel, Germany) of 3.36 mm with a sandblasted large grit acid etched (SLA) surface were inserted according to the manufacturers instructions in the midsagittal plane at the depression of the 3rd and 5th palatal mucosal fold, corresponding to the position of 1st and 3rd premolars. This was chosen to ensure minimal per-implant thickness of palatal mucosa. Briefly, the palatal mucosa was removed at the prospective site of implant placement with a rotating mucosal trephine. Using a round bur, a slight bony indentation was created in the midline. Thereafter the implant site was prepared using the OrthoÒ profile drill to a depth of 6 mm. All drilling procedures were performed under copious irrigation with sterile physiological saline. Then the implants were inserted using the appropriate ratchet. All implants were clinically stable at the time of insertion. Steel tubes soldered to steel OrthoÒ-caps served as attachments for coil springs. The OrthoÒ-caps were inserted and fixation screws were placed using cyanoacrylate glue (Loctite 496, Loctite, Munich, Germany) to protect the screws from loosening. For immediate loading, NieTi coil springs of 100 cN were placed between the implants and fixed with 0.3 mm stainless steel wires (Fig. 1). To prevent soft tissue irritation due to sharp edges, wires and tubes were encapsulated by using a light-cured orthodontic adhesive (TransbondTM XT, 3M-Unitek, Puchheim, Germany). Lateral and axial radiographic checks were performed immediately after implant placement and at the time of harvesting the specimens. The animals were kept on a strict soft diet (Pedigree Adult for Medium Dogs, Masterfood, Csongrad, Hungary) with water ad libitum. For polychrome sequential labelling, two substances were administered: 15 mg/kg calceine green: 1% buffered in hydrogen carbonate solution 2% after the first post-operative week, 90 mg/kg xylene orange: 6% buffered in hydrogen carbonate solution 2% after the
Fig. 1 e Palatal implants immediately postoperately. Coil-spring attached to small tubes soldered to OrthoÒ-caps. Light curing resin added later. Inset: lateral view of the implants after harvesting and sectioning the maxilla.
first post-operative month and again 15 mg/kg calceine green: 1% buffered in hydrogen carbonate solution 2% after the second post-operative month. Specimens and histological processing After 4 weeks 2 dogs and after 6 months the other 2 dogs were sacrificed. The maxillae were dissected out and fixed by immersion in 50% ethanol for 10 days. For histological preparation, the cutting and grinding technique according to Donath and Breuner (1982) was used. In brief, after fixation, the bones were immersed into ascending concentrations up to absolute ethanol over 2 weeks and then embedded in a mixture of glycol methacrylate (Technovit 7200 VLCÒ, Kulzer, Wehrheim, Germany). Polymerisation was obtained by light curing with a light source of 450 nm wave length. From each specimen, sections were cut in the sagittal plane parallel to the implant’s longitudinal axis, using a diamond band saw. This allowed for the definition of implant surface orientation as either in the direction of the force or opposite to the force direction. Thereafter, the sections were ground and polished on a micro-grinding system (EXACT, Norderstedt, Germany) to a final thickness of 20 mm. The sections were stained by haematoxylin/eosin for light microscopy after fluorescence microscopy. Evaluation of stained sections All histological examinations were performed on a LeicaÒ DM/RBE microscope equipped with the digital image system IM50Ò. To evaluate the bone-to-implant contact rate, the contour of each implant was scanned by a series of microphotographs (Matrix 25601920) with an original magnification of 100. The entire implant surface was displayed by merging these 14e18 digital images. For morphometrical analysis, a grid of 50 mm was placed over the implant. Thus the surface was represented by 339e416 fields of 50 mm50 mm per implant.
Primary loading of palatal implants 23
Each field was classified according to one of the following four categories: d Fibrous connective tissue or bone marrow, d Bony debris, d Primary bone-to-implant contact: bone without signs of remodelling, d Secondary bone-to-implant contact: newly formed or remodelled bone. The rate of primary-to-secondary contact was calculated as the proportion of fields showing direct bone contact for the complete surface of the implant. In addition, the same was listed for both implant sides, the implant side in the direction of and the one opposite to the force direction. All results were given as the percentage of bone contact divided by the total whole implant surface. Statistical analysis Until now, success criteria as used in dental implantology have not been established in the field of orthodontic anchorage devices. Thus two endpoints were defined in order to measure success or failure of the implants. The primary endpoint was ‘‘clinical stability’’. An implant was classified as clinically stable, if there was no loss of the implant under orthodontic loading. The second endpoint was ‘‘osseointegration’’. In this pilot study, gross fibrous encapsulation and a bone to implant contact of less than 10% was considered as a failure. According to these definitions, success rates are given separately for each of the two endpoints. The bone-to-implant contact rates were compared for the implants retrieved at 4 weeks and at 6 months using the non-parametric U-Test for independent samples according to Mann and Whitney. To compare the boneto-implant contact rates of the traction (opposite to force direction) and the pressure sides (in force direction) of the implant, the Wilcoxon test for paired samples was applied. For graphic description, box plots are given. All calculations were carried out using SPSS for Windows, Version 11 (SPSS Inc., Chicago, USA).
months. At the time when the animals were sacrificed, there was no exposure of the implants on the side of the nasal cavity (Table 1). Upon histological evaluation, however 1 implant (anterior implant, 6 months animal) showed almost complete fibrous encapsulation with only minimal bone-to-implant contact of less than 4%. This implant was classified as ‘‘failed’’ for the endpoint ‘‘osseointegration’’. Histological evaluation of osseointegration After 4 weeks, all 4 implant sites showed considerable deposits of bony debris (12e23% of the implant surface) resulting from the drilling and insertion procedure (Fig. 2). However, all implants had zones of primary bone contact without apparent signs of remodelling (12e21%; mean 16% (^5) of the implant surface). Besides this, the specimens showed distinct sites of new bone formation either as pseudopodial and finger-like contacts or as linear bone formation along the implant surface. In these areas, covering 6e29% (mean 19% ^12) of the implant surface, high-power magnification (1000) displayed osteocytes in close vicinity to the implant surface (Fig. 3). After 6 months of implant loading, complete remodelling has taken place (primary bone contact \2%) and the deposits of abraded, non-vital bone had vanished. The overall secondary bone to implant contact ratio remained at a rather low level (mean 20% (^13) with one (anterior) implant being almost completely encapsulated by fibrous tissue (Fig. 4). Excluding this implant whose osseointegration was classified as ‘‘failed’’, the mean overall bone-to-implant contact rate of the 3 osseointegrated implants was 26% (^9). Although the immediate
RESULTS Clinical implant success The implants, OrthoÒ-caps and the coil springs were well tolerated by the animals. Except for the symptomless loosening of the covering resin in 1 animal, the orthodontic loading set-up was kept for the duration of the study in all animals. All implants of this series (8 out of 8) remained clinically stable under constant linear loading conditions with 100 cN for 4 weeks and for 6
Fig. 2 e Specimen harvested after 4 weeks. Substantial deposits of bony debris (deep blue) discernible along the implants surface (HE; 100).
Table 1 e Implant success and bone-to-implant contact rates Time of evaluation
Implants clinically stable
Implants osseointegrated
Primary bone to implant contact
Secondary bone to implants contact
4 weeks 6 months
4 out of 4 4 out of 4
4 out of 4 3 out of 4
16% (^5) 2% (^3)
19% (^12) 26% (^9)*
* Failed implant excluded.
24 Journal of Cranio-Maxillofacial Surgery
bone-to-implant contacts were still predominantly of a pseudopodial type with numerous gaps and extended zones of fibrous tissue, the surrounding bone appeared condensed with only few marrow spaces remaining. In Figure 4, the bone to implant contact zones are highlighted in green for the specimens of a 6 months animal in which one implant was histologically classified as a failure. Only punctate contacts remained in this failed anterior implant, whilst there was about 34% bone-toimplant contact rate in the successful posterior implant of this animal. The box plots in Fig. 5 represent the primary and secondary bone contact rates at 4 weeks and at 6 months. In spite of a moderate increase of the secondary bone con-
tact rate, there was no significant difference of bone contact between the specimens retrieved at 4 weeks when compared with the 6 months group (p ¼ 0.343; ManneWhitney U-Test, n.s.; Table 1). There was no significant difference between the ‘‘traction’’ and the ‘‘pressure’’ side of the implants (p ¼ 0.345e0.889; Wilcoxon matched pairs test) regarding the bone to implant contact rates. Polychrome sequential labelling In the specimens retrieved after 4 weeks, the first calceingreen labelling, administered at postoperative day 7, resulted in only diffuse green fluorescence at the sites of abraded bone chips displaced into marrow spaces and towards the tip of the implants. There was only minor labelling of the bone in the immediate vicinity of the surface of the implant at this time. The intense green fluorescence in Fig. 6 (/) represents such a zone of bony debris. Comparably minor bone apposition (i.e. fluorochrome marking) could be detected close to a thread in this specimen (*). In the 6 months specimens the diffuse fluorescence areas of the first dose of calcein-green had completely vanished. The fluorochromes administered after the first and second post-operative months were easily identified as well-defined fluorescent bands. At this time, fluorochrome incorporation was mainly seen in the surrounding bone and only to a minor extent at the immediate surface of the implants (Figs 7a and b). DISCUSSION
Fig. 3 e Detail of the new bone found after 4 weeks. Osteocytes (/) of typical morphology in close contact to the implant surface (HE; 1000).
In the last few years, a large body of clinical and experimental evidence has challenged the classic paradigm of
Fig. 4 e Bone to implant contacts in a ‘‘failed’’ (A: animal 3, anterior) and a ‘‘successful’’ (B: animal 3, posterior) implant (HE; original magnification 100; 17(in A)/14 (in B) microphotographs merged). Actual contact zones, evaluated in increments of 50 mm, are highlighted in green.
Primary loading of palatal implants 25
undisturbed bone healing for the osseointegration of dental implants (Adell et al., 1981; Albrektsson et al., 1981). Numerous studies demonstrated the principal value of immediate and early loading and consensus statements have been published (Cochran et al., 2004). Numerous criteria regarding implant design, bone quality and functional conditions have been postulated for segregating cases 0.5
0.4
Primary bone to implant contact
Bone to implant contact
Secondary bone to implant contact
0.3
0.2
0.1
0.0 N=
4 4 weeks
4
3
3
6 months
Fig. 5 e Bone contact rates after 4 weeks and 6 months (failed implant excluded). The boxplot represent the primary bone contact and new bone formation/remodelling rates. (Heavy line: median, box covers 25e 75% percentiles, whiskers mark maximum and minimum values).
Fig. 6 e Fluorescence microphotograph after 4 weeks (50). Rather diffuse incorporation of the fluorochrome administered at postoperative day 7, predominantly around the bone adjacent to the drilling site.
suitable for early loading from those requiring unloaded osseointegration. Besides poor bone quality (type IV), short (length below 10 mm) and thin implants (diameter below 4 mm) have been considered to jeopardize success under prosthetic loading (Chiapasco et al., 1997; Tarnow et al., 1997; Horiuchi et al., 2000). These recommendations, however, were mainly derived from gross clinical experience rather than sound experimental evidence, leaving the critical bone properties and the exact critical length and diameter of immediately loaded implants as open issues. Although the loading conditions of palatal implants clearly set them apart from prosthetic loading conditions, there are multiple factors that might exclude early functional loading for these, i.e. the reduced length and the small diameter of these implants might not enable primary stability usually considered adequate for immediate loading. A final insertion torque of 32e40 N cm, is postulated to correlate with sufficient primary stability (Horiuchi et al., 2000; Malo et al., 2000), but cannot be achieved with the small amount of bone available in the midpalatal region. However, regarding the direction, duration and dimensions of orthodontic forces, it has to be questioned whether the strict limitations just mentioned should also be applied to implants used for orthodontic anchorage. Hence the need for this animal experiment. It might be argued, that orthodontic loading conditions are not fully reflected in this experiment which only applied constant ‘‘static’’ forces by means of coil springs. However, it is the most prominent characteristic of Nie Ti coil springs, that they exert quasi ‘‘static’’ traction forces over a wide range of linear axial deformation. Thus, the loading characteristics applied in this study seemed adequate to imitate orthodontic anchorage. The overall rather low bone-contact rates in this study impressed, as values of about 75e80% have already been described for implants with SLA-surfaces (Perrin et al., 2002; Buser et al., 2004). However, Aldikac¸ti et al. (2004) reported substantially lower rates (40%) in maxillary SLA-implants under loading conditions with orthodontic forces. Comparable rates (38%) could be calculated for the present study, when the apical portion of the implants, protruding towards the nasal cavity were excluded from the morphometrical analysis (data not shown). Although in this study all implants were kept in place and seem to support the principle of immediate loading in orthodontic palatal implants. However, the histological evaluation gave rise to doubts with respect to the safety of osseointegration. The almost absent bone contact in one of eight implants indicates, that the experimental protocol approached the borderline of a reliable clinical procedure. At least, the failure of osseointegration suggested that clinical failure of the implant would follow soon. The morphometrical analysis of bone to implant contact suggested, that at 4 weeks after insertions, the initial mechanical retention still provided a major contribution to the implant stability in the four implants tested (about 50% of the overall bone to implant contact). New bone formation had already been initiated, but the major proportion of remodelling occurred later. When looking at
26 Journal of Cranio-Maxillofacial Surgery
Fig. 7 e a: Fluorescence microphotograph after 6 months (50). Both fluorochromes administered at the first (xylene orange) and second (calcein green) postoperative months are incorporated as clearly defined bands. b: Fluorescence microphotograph after 6 months (100). Intense fluorochrome apposition in the bony trabeculae.
the final 26% bone to implant contact rate in the 3 (out of 4) implants clinically and histologically classified as successful after 6 months, it is intriguing to note, that there was only a small difference from the values measured after 4 weeks (19%). Extrapolating the data, one might conclude, that sufficient osseointegration as was required for stability against orthodontic forces, already existed 4 weeks after surgery. This corresponds well to the findings of the polychrome sequential labelling, where intense mineral deposition in the bony trabecula around the implant (indicating remodelling) was noted at 1 and 2 months after surgery. One further detail may be of interest: the fluorochrome bands representing mineralization at 1 month (red) and 2 months (green) postoperatively were only scarcely seen in direct contact to the implant surface. This suggests, that the genuine osseointegration process was almost complete at that time. CONCLUSION In this study, borderline reliability of osseointegration for immediately loaded palatal implants but reasonable bone formation until the fourth postoperative week was found histologically. Thus it seems likely that sufficient secondary stability for early orthodontic loading can be expected after 4 weeks. ACKNOWLEDGMENTS This work was supported in part by a grant of the Institute Straumann AG, CH-4437 Waldenburg, Switzerland to Martin Kunkel.
References Adell R, Lekholm U, Rockler B, Bra˚nemark PI: A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 10: 387e416, 1981 Albrektsson T, Bra˚nemark PI, Hansson HA, Lindstrom J: Osseointegrated titanium implants. Requirements for ensuring a long-lasting, direct bone-to-implant contact in man. Acta Orthop Scand 52: 155e170, 1981 Aldikac¸ti M, Ac¸ikgo¨z G, Tu¨rk T, Trisi P: Long-term evaluation of sandblasted and acid-etched implants used as orthodontic anchors in dogs. Am J Orthod Dentofac Orthop 125: 139e147, 2004 Bernhart T, Freudenthaler JW, Do¨rtbudak O, Bantleon HP, Watzek G: Short epithetic implants for orthodontic anchorage in the paramedian region of the palate. A clinical study. Clin Oral Impl Res 12: 624e631, 2001 Blum-Hareuveni T, Rehany U, Rumelt S: Blinding endophthalmitis from orthodontic headgear. N Engl J Med 351: 2774e2775, 2004 Booth-Mason S, Birnie D: Penetrating eye injury from orthodontic headgearda case report. Eur J Orthod 10: 111e114, 1988 Buser D, Broggini N, Wieland M, Schwenk RK, Denzer AJ, Cochran DL, Hoffmann B, Lussi A, Steinemann SG: Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res 83: 529e533, 2004 Chiapasco M, Gatti C, Rossi E, Haeflinger W, Markwalder TH: Implant-retained mandibular overdentures with immediate loading. A retrospective multicenter study on 226 consecutive cases. Clin Oral Impl Res 8: 48e57, 1997 Cochran DL, Morton D, Weber HP: Consensus statement and recommended clinical procedures regarding loading protocols for endosseous dental implants. Int J Oral Maxillofac Impl 19(Suppl 1): 103e108, 2004 Cously R: Critical aspects in the use of orthodontic palatal implants. Am J Orthod Dentofacial Orthop 127: 723e729, 2005
Primary loading of palatal implants 27 Diedrich P: Verschiedene orthodontische Verankerungssystemedeine kritische Betrachtung. Fortschr Kieferorthop 54: 156e171, 1993 Donath K, Breuner G: A method for the study of undecalcified bones and teeth with attached soft tissues. J Oral Pathol 11: 318e326, 1982 Fortini A, Lupoli M, Lorenzo F: Dentoskeletal effects induced by rapid molar distalization with the first class appliance. Am J Orthod Dentofac Orthop 125: 697e705, 2004 Freudenthaler JW, Haas R, Bantleon HP: Bicortical titanium screws for critical orthodontic anchorage in the mandible: a preliminary report on clinical applications. Clin Oral Impl Res 12: 358e363, 2001 Horiuchi K, Uchida H, Yamamoto K, Sugimura M: Immediate loading of Branemark system implants following placement in edentulous patients: a clinical report. Int J Oral Maxillofac Impl 15: 824e830, 2000 Malo P, Rangert B, Dvarsater L: Immediate function of Branemark implants in the esthetic zone: a retrospective clinical study with 6 months to 4 years of follow-up. Clin Impl Dent Rel Res 2: 138e146, 2000 Nkenke E, Fenner M: Indications for immediate loading of implants and implant success. Clin Oral Impl Res 17(Suppl 2): 19e34, 2006 Perrin D, Szmuckler-Moncler S, Echikou C, Pointaire P, Bernard JP: Bone response to alteration of surface topography and surface composition of sandblasted and acid etched (SLA) implants. Clin Oral Impl Res 13: 465e469, 2002 Tarnow DP, Emtiaz S, Classi A: Immediate loading of threaded implants at stage I surgery in edentulous arches: ten consecutive case reports with 1 to 5 year data. Int J Oral Maxillofac Impl 12: 319e324, 1997 Wehrbein H: Endosseous titanium implants as orthodontic anchoring elements. Experimental studies and clinical application. J Orofac Orthop 55: 236e250, 1994
Wehrbein H, Diedrich P: Endosseous titanium implants during and after orthodontic load-an experimental study in the dog. Clin Oral Impl Res 4: 76e82, 1993 Wehrbein H, Merz BR, Diedrich P, Glatzmeier J: The use of palatal implants for orthodontic anchorage. Design and clinical application of the Orthosystem. Clin Oral Impl Res 7: 410e416, 1996a Wehrbein H, Glatzmaier J, Mundwiller U, Diedrich P: The orthosystem- a new implant system for orthodontic anchorage in the palate. J Orofac Orthop 57: 142e153, 1996b Wehrbein H, Merz BR, Ha¨mmerle CHF, Lang NP: Bone-to-implant contact of orthodontic implants in humans subjected to horizontal loading. Clin Oral Impl Res 9: 345e353, 1998 Wehrbein H, Feifel H, Diedrich P: Palatal implant anchorage reinforcement of posterior teeth: A prospective study. Am J Orthod Dentofac Orthop 116: 678e686, 1999 Willems G, Carels WG, Naert IE, van Steenberghe D: Interdisciplinary treatment planning for orthodontic-prosthetic implant anchorage in a partially edentulous patient. Clin Oral Impl Res 10: 331e337, 1999
Prof. Dr. Dr. M. KUNKEL Department of Oral and Maxillofacial Surgery University Hospital of Mainz Augustusplatz 2 55101 Mainz Tel.: 0049 6131 173191 Fax: 0049 6131 176602 E-mail: [email protected] Paper received 24 March 2006 Accepted 5 July 2007
Primary loading of palatal implants for orthodontic anchorage e A pilot animal study Pe´ter BORBE´LY1, Miklo´s P. DUNAY2, Britta A. JUNG3, Heinrich WEHRBEIN3, Wilfried WAGNER4, Martin KUNKEL4 Fogszaba´lyoza´si Stu´dio´, Private Practice, Budapest, Hungary; 2 Department of Surgery (Chair: Prof. Dr. Tibor Nemeth) Szent Istva´n University, Faculty of Veterinary Science, Budapest, Hungary; 3 Department of Orthodontics (Chair: Prof. Dr. Dr. H. Wehrbein); 4 Department of Oral and Maxillofacial Surgery (Chair: Prof. Dr. Dr. W. Wagner) University of Mainz, Germany
1
Objectives: This study aimed at evaluating the clinical performance and osseointegration of short orthodontic implants immediately loaded with orthodontic forces. Material and methods: The investigation was designed as an experimental animal study. Eight palatal implants of the Ortho-systemÒ were immediately loaded with 100 cN after palatal insertion in 4 female german shepherd dogs. Xylene orange and calcein green were used for polychrome sequential labelling. Histological preparation utilized the cutting and grinding technique. Outcome variables were clinical implant success, histological osseointegration and bone-to-implant contact rates. Results: All (8/8) implants were clinically successful and stable when the animals were sacrificed. One implant showed fibrous encapsulation and was histologically classified as ‘‘failed’’ for ‘‘osseointegration’’. Upon morphometrical analysis, bone to implant contact rates for newly formed or remodelled bone were 19% at 4 weeks and 26% at 6 months. The fluorochrome labelling indicated substantial mineral apposition on the surface of the implants at the end of the first and the second postoperative months. Conclusion: This study revealed borderline reliability of osseointegration for immediately loaded palatal implants but reasonable bone formation at the 4th postoperative week. Thus, two clinical concepts are both supported: early orthodontic loading after 4 weeks as well as improvement of primary stability to provide a biomechanical basis for immediate orthodontic loading. Ó 2007 European Association for Cranio-Maxillofacial Surgery
SUMMARY.
Keywords: palatal implant, Ortho-systemÒ, Ortho implantÒ, orthodontic loading, osseointegration, dental implants, animal study, polychrome sequential labelling, orthodontic anchorage, early loading, morphometry
introduced for orthodontic loading in the last decade. Today, there is evidence, that osseointegrated implants remain positionally stable under typical orthodontic loading conditions (Wehrbein & Diedrich, 1993; Wehrbein et al., 1996a, 1996b, 1999; Bernhart et al., 2001; Freudenthaler et al., 2001; Fortini et al., 2004). The use of palatal implants of the Ortho-systemÒ (Straumann, Basel, Switzerland) has been extensively investigated and can be regarded as a classic for orthodontic skeletal anchorage (Wehrbein & Diedrich, 1993; Wehrbein, 1994; Wehrbein et al., 1996a, 1996b, 1998, 1999; Cously, 2005). However, a relevant drawback of this system is, at least according to the present manufacturers instructions, that the healing period has to be at least 3 months. Encouraged by recent research progress in implantology (Cochran et al., 2004; Nkenke and Fenner, 2006) demonstrating high success rates for immediate and early loading in prosthetic implants, it was the aim of this pilot study to evaluate, whether immediate loading could also be applied for short orthodontic implants. Therefore, an experimental animal study was initiated, to investigate the feasibility of immediate loading for palatal implants of the OrthoÒ- system.
INTRODUCTION Anchorage, defined as the ‘‘resistance to unwanted tooth movement’’ is a fundamental orthodontic problem and a major determinant of success in the treatment of dental and skeletal dysgnathia (Diedrich, 1993; Willems et al., 1999). Loading of an anchorage unit in orthodontic treatment is possible on the conditions of a static equilibrium of forces (action ¼ reaction). Hence, if teeth are used for anchorage, their reaction to quantity, type and duration of the forces and moments applied through the orthodontic biomechanics is critical for active movement of other teeth. Anchorage can be enhanced to a limited degree by connecting several teeth using rigid steel wires or heavy ligatures. Supportive appliances such as ‘‘external’’ headgear and inter-maxillary elastics can provide additional stability. However, these pose considerable inconveniences, are visible, and even bear the risk of potential injury (Booth-Mason and Birnie, 1988; BlumHareuveni et al., 2004). Moreover, patients acceptance is crucial and compliance is another limiting factor (Diedrich, 1993). To overcome the limits of dental orthodontic anchorage, numerous skeletal anchorage devices have been 21
22 Journal of Cranio-Maxillofacial Surgery
MATERIAL AND METHODS Animals Four female german shepherd dogs (age 1 year) were operated upon under general anaesthesia. The study protocol was approved by the review board of the Hungarian ¨ . e´s E´ell. All. Ministry of Agriculture (Ref. Nr. FTv. Aeu 271/2003/2004). Following sedation by subcutaneous application of 0.1 mg/kg (body weight) acepromazine (Vetranquil 1%: Ceva-Sante Animale, La Ballastiere, France), the animals were anaesthesized by an intra-venous bolus of xylazine (Primazin 2%: Alfasan International, Woerden, Netherlands) 1 mg/kg and ketamine (Calypsol: Richter, Budapest, Hungary) 10 mg/kg. For peri-operative prophylaxis the animals received 30 mg/kg amoxicillin and 7.5 mg/kg clavulanic acid (Synulox RTU: Pfizer, Sandwich, UK). Prior to intraoral surgery, a polividone iodine mouth-rinse (Betadine: Egis, Budapest, Hungary) was applied for local disinfection. Meloxicam 0.2 mg/kg (Metacam 0.5%: Labania Life Science, Barcelona, Spain) was given subcutaneously for peri- and post-operative analgesia. Palatal implants of the Ortho-systemÒ (Straumann, Basel, Germany) of 3.36 mm with a sandblasted large grit acid etched (SLA) surface were inserted according to the manufacturers instructions in the midsagittal plane at the depression of the 3rd and 5th palatal mucosal fold, corresponding to the position of 1st and 3rd premolars. This was chosen to ensure minimal per-implant thickness of palatal mucosa. Briefly, the palatal mucosa was removed at the prospective site of implant placement with a rotating mucosal trephine. Using a round bur, a slight bony indentation was created in the midline. Thereafter the implant site was prepared using the OrthoÒ profile drill to a depth of 6 mm. All drilling procedures were performed under copious irrigation with sterile physiological saline. Then the implants were inserted using the appropriate ratchet. All implants were clinically stable at the time of insertion. Steel tubes soldered to steel OrthoÒ-caps served as attachments for coil springs. The OrthoÒ-caps were inserted and fixation screws were placed using cyanoacrylate glue (Loctite 496, Loctite, Munich, Germany) to protect the screws from loosening. For immediate loading, NieTi coil springs of 100 cN were placed between the implants and fixed with 0.3 mm stainless steel wires (Fig. 1). To prevent soft tissue irritation due to sharp edges, wires and tubes were encapsulated by using a light-cured orthodontic adhesive (TransbondTM XT, 3M-Unitek, Puchheim, Germany). Lateral and axial radiographic checks were performed immediately after implant placement and at the time of harvesting the specimens. The animals were kept on a strict soft diet (Pedigree Adult for Medium Dogs, Masterfood, Csongrad, Hungary) with water ad libitum. For polychrome sequential labelling, two substances were administered: 15 mg/kg calceine green: 1% buffered in hydrogen carbonate solution 2% after the first post-operative week, 90 mg/kg xylene orange: 6% buffered in hydrogen carbonate solution 2% after the
Fig. 1 e Palatal implants immediately postoperately. Coil-spring attached to small tubes soldered to OrthoÒ-caps. Light curing resin added later. Inset: lateral view of the implants after harvesting and sectioning the maxilla.
first post-operative month and again 15 mg/kg calceine green: 1% buffered in hydrogen carbonate solution 2% after the second post-operative month. Specimens and histological processing After 4 weeks 2 dogs and after 6 months the other 2 dogs were sacrificed. The maxillae were dissected out and fixed by immersion in 50% ethanol for 10 days. For histological preparation, the cutting and grinding technique according to Donath and Breuner (1982) was used. In brief, after fixation, the bones were immersed into ascending concentrations up to absolute ethanol over 2 weeks and then embedded in a mixture of glycol methacrylate (Technovit 7200 VLCÒ, Kulzer, Wehrheim, Germany). Polymerisation was obtained by light curing with a light source of 450 nm wave length. From each specimen, sections were cut in the sagittal plane parallel to the implant’s longitudinal axis, using a diamond band saw. This allowed for the definition of implant surface orientation as either in the direction of the force or opposite to the force direction. Thereafter, the sections were ground and polished on a micro-grinding system (EXACT, Norderstedt, Germany) to a final thickness of 20 mm. The sections were stained by haematoxylin/eosin for light microscopy after fluorescence microscopy. Evaluation of stained sections All histological examinations were performed on a LeicaÒ DM/RBE microscope equipped with the digital image system IM50Ò. To evaluate the bone-to-implant contact rate, the contour of each implant was scanned by a series of microphotographs (Matrix 25601920) with an original magnification of 100. The entire implant surface was displayed by merging these 14e18 digital images. For morphometrical analysis, a grid of 50 mm was placed over the implant. Thus the surface was represented by 339e416 fields of 50 mm50 mm per implant.
Primary loading of palatal implants 23
Each field was classified according to one of the following four categories: d Fibrous connective tissue or bone marrow, d Bony debris, d Primary bone-to-implant contact: bone without signs of remodelling, d Secondary bone-to-implant contact: newly formed or remodelled bone. The rate of primary-to-secondary contact was calculated as the proportion of fields showing direct bone contact for the complete surface of the implant. In addition, the same was listed for both implant sides, the implant side in the direction of and the one opposite to the force direction. All results were given as the percentage of bone contact divided by the total whole implant surface. Statistical analysis Until now, success criteria as used in dental implantology have not been established in the field of orthodontic anchorage devices. Thus two endpoints were defined in order to measure success or failure of the implants. The primary endpoint was ‘‘clinical stability’’. An implant was classified as clinically stable, if there was no loss of the implant under orthodontic loading. The second endpoint was ‘‘osseointegration’’. In this pilot study, gross fibrous encapsulation and a bone to implant contact of less than 10% was considered as a failure. According to these definitions, success rates are given separately for each of the two endpoints. The bone-to-implant contact rates were compared for the implants retrieved at 4 weeks and at 6 months using the non-parametric U-Test for independent samples according to Mann and Whitney. To compare the boneto-implant contact rates of the traction (opposite to force direction) and the pressure sides (in force direction) of the implant, the Wilcoxon test for paired samples was applied. For graphic description, box plots are given. All calculations were carried out using SPSS for Windows, Version 11 (SPSS Inc., Chicago, USA).
months. At the time when the animals were sacrificed, there was no exposure of the implants on the side of the nasal cavity (Table 1). Upon histological evaluation, however 1 implant (anterior implant, 6 months animal) showed almost complete fibrous encapsulation with only minimal bone-to-implant contact of less than 4%. This implant was classified as ‘‘failed’’ for the endpoint ‘‘osseointegration’’. Histological evaluation of osseointegration After 4 weeks, all 4 implant sites showed considerable deposits of bony debris (12e23% of the implant surface) resulting from the drilling and insertion procedure (Fig. 2). However, all implants had zones of primary bone contact without apparent signs of remodelling (12e21%; mean 16% (^5) of the implant surface). Besides this, the specimens showed distinct sites of new bone formation either as pseudopodial and finger-like contacts or as linear bone formation along the implant surface. In these areas, covering 6e29% (mean 19% ^12) of the implant surface, high-power magnification (1000) displayed osteocytes in close vicinity to the implant surface (Fig. 3). After 6 months of implant loading, complete remodelling has taken place (primary bone contact \2%) and the deposits of abraded, non-vital bone had vanished. The overall secondary bone to implant contact ratio remained at a rather low level (mean 20% (^13) with one (anterior) implant being almost completely encapsulated by fibrous tissue (Fig. 4). Excluding this implant whose osseointegration was classified as ‘‘failed’’, the mean overall bone-to-implant contact rate of the 3 osseointegrated implants was 26% (^9). Although the immediate
RESULTS Clinical implant success The implants, OrthoÒ-caps and the coil springs were well tolerated by the animals. Except for the symptomless loosening of the covering resin in 1 animal, the orthodontic loading set-up was kept for the duration of the study in all animals. All implants of this series (8 out of 8) remained clinically stable under constant linear loading conditions with 100 cN for 4 weeks and for 6
Fig. 2 e Specimen harvested after 4 weeks. Substantial deposits of bony debris (deep blue) discernible along the implants surface (HE; 100).
Table 1 e Implant success and bone-to-implant contact rates Time of evaluation
Implants clinically stable
Implants osseointegrated
Primary bone to implant contact
Secondary bone to implants contact
4 weeks 6 months
4 out of 4 4 out of 4
4 out of 4 3 out of 4
16% (^5) 2% (^3)
19% (^12) 26% (^9)*
* Failed implant excluded.
24 Journal of Cranio-Maxillofacial Surgery
bone-to-implant contacts were still predominantly of a pseudopodial type with numerous gaps and extended zones of fibrous tissue, the surrounding bone appeared condensed with only few marrow spaces remaining. In Figure 4, the bone to implant contact zones are highlighted in green for the specimens of a 6 months animal in which one implant was histologically classified as a failure. Only punctate contacts remained in this failed anterior implant, whilst there was about 34% bone-toimplant contact rate in the successful posterior implant of this animal. The box plots in Fig. 5 represent the primary and secondary bone contact rates at 4 weeks and at 6 months. In spite of a moderate increase of the secondary bone con-
tact rate, there was no significant difference of bone contact between the specimens retrieved at 4 weeks when compared with the 6 months group (p ¼ 0.343; ManneWhitney U-Test, n.s.; Table 1). There was no significant difference between the ‘‘traction’’ and the ‘‘pressure’’ side of the implants (p ¼ 0.345e0.889; Wilcoxon matched pairs test) regarding the bone to implant contact rates. Polychrome sequential labelling In the specimens retrieved after 4 weeks, the first calceingreen labelling, administered at postoperative day 7, resulted in only diffuse green fluorescence at the sites of abraded bone chips displaced into marrow spaces and towards the tip of the implants. There was only minor labelling of the bone in the immediate vicinity of the surface of the implant at this time. The intense green fluorescence in Fig. 6 (/) represents such a zone of bony debris. Comparably minor bone apposition (i.e. fluorochrome marking) could be detected close to a thread in this specimen (*). In the 6 months specimens the diffuse fluorescence areas of the first dose of calcein-green had completely vanished. The fluorochromes administered after the first and second post-operative months were easily identified as well-defined fluorescent bands. At this time, fluorochrome incorporation was mainly seen in the surrounding bone and only to a minor extent at the immediate surface of the implants (Figs 7a and b). DISCUSSION
Fig. 3 e Detail of the new bone found after 4 weeks. Osteocytes (/) of typical morphology in close contact to the implant surface (HE; 1000).
In the last few years, a large body of clinical and experimental evidence has challenged the classic paradigm of
Fig. 4 e Bone to implant contacts in a ‘‘failed’’ (A: animal 3, anterior) and a ‘‘successful’’ (B: animal 3, posterior) implant (HE; original magnification 100; 17(in A)/14 (in B) microphotographs merged). Actual contact zones, evaluated in increments of 50 mm, are highlighted in green.
Primary loading of palatal implants 25
undisturbed bone healing for the osseointegration of dental implants (Adell et al., 1981; Albrektsson et al., 1981). Numerous studies demonstrated the principal value of immediate and early loading and consensus statements have been published (Cochran et al., 2004). Numerous criteria regarding implant design, bone quality and functional conditions have been postulated for segregating cases 0.5
0.4
Primary bone to implant contact
Bone to implant contact
Secondary bone to implant contact
0.3
0.2
0.1
0.0 N=
4 4 weeks
4
3
3
6 months
Fig. 5 e Bone contact rates after 4 weeks and 6 months (failed implant excluded). The boxplot represent the primary bone contact and new bone formation/remodelling rates. (Heavy line: median, box covers 25e 75% percentiles, whiskers mark maximum and minimum values).
Fig. 6 e Fluorescence microphotograph after 4 weeks (50). Rather diffuse incorporation of the fluorochrome administered at postoperative day 7, predominantly around the bone adjacent to the drilling site.
suitable for early loading from those requiring unloaded osseointegration. Besides poor bone quality (type IV), short (length below 10 mm) and thin implants (diameter below 4 mm) have been considered to jeopardize success under prosthetic loading (Chiapasco et al., 1997; Tarnow et al., 1997; Horiuchi et al., 2000). These recommendations, however, were mainly derived from gross clinical experience rather than sound experimental evidence, leaving the critical bone properties and the exact critical length and diameter of immediately loaded implants as open issues. Although the loading conditions of palatal implants clearly set them apart from prosthetic loading conditions, there are multiple factors that might exclude early functional loading for these, i.e. the reduced length and the small diameter of these implants might not enable primary stability usually considered adequate for immediate loading. A final insertion torque of 32e40 N cm, is postulated to correlate with sufficient primary stability (Horiuchi et al., 2000; Malo et al., 2000), but cannot be achieved with the small amount of bone available in the midpalatal region. However, regarding the direction, duration and dimensions of orthodontic forces, it has to be questioned whether the strict limitations just mentioned should also be applied to implants used for orthodontic anchorage. Hence the need for this animal experiment. It might be argued, that orthodontic loading conditions are not fully reflected in this experiment which only applied constant ‘‘static’’ forces by means of coil springs. However, it is the most prominent characteristic of Nie Ti coil springs, that they exert quasi ‘‘static’’ traction forces over a wide range of linear axial deformation. Thus, the loading characteristics applied in this study seemed adequate to imitate orthodontic anchorage. The overall rather low bone-contact rates in this study impressed, as values of about 75e80% have already been described for implants with SLA-surfaces (Perrin et al., 2002; Buser et al., 2004). However, Aldikac¸ti et al. (2004) reported substantially lower rates (40%) in maxillary SLA-implants under loading conditions with orthodontic forces. Comparable rates (38%) could be calculated for the present study, when the apical portion of the implants, protruding towards the nasal cavity were excluded from the morphometrical analysis (data not shown). Although in this study all implants were kept in place and seem to support the principle of immediate loading in orthodontic palatal implants. However, the histological evaluation gave rise to doubts with respect to the safety of osseointegration. The almost absent bone contact in one of eight implants indicates, that the experimental protocol approached the borderline of a reliable clinical procedure. At least, the failure of osseointegration suggested that clinical failure of the implant would follow soon. The morphometrical analysis of bone to implant contact suggested, that at 4 weeks after insertions, the initial mechanical retention still provided a major contribution to the implant stability in the four implants tested (about 50% of the overall bone to implant contact). New bone formation had already been initiated, but the major proportion of remodelling occurred later. When looking at
26 Journal of Cranio-Maxillofacial Surgery
Fig. 7 e a: Fluorescence microphotograph after 6 months (50). Both fluorochromes administered at the first (xylene orange) and second (calcein green) postoperative months are incorporated as clearly defined bands. b: Fluorescence microphotograph after 6 months (100). Intense fluorochrome apposition in the bony trabeculae.
the final 26% bone to implant contact rate in the 3 (out of 4) implants clinically and histologically classified as successful after 6 months, it is intriguing to note, that there was only a small difference from the values measured after 4 weeks (19%). Extrapolating the data, one might conclude, that sufficient osseointegration as was required for stability against orthodontic forces, already existed 4 weeks after surgery. This corresponds well to the findings of the polychrome sequential labelling, where intense mineral deposition in the bony trabecula around the implant (indicating remodelling) was noted at 1 and 2 months after surgery. One further detail may be of interest: the fluorochrome bands representing mineralization at 1 month (red) and 2 months (green) postoperatively were only scarcely seen in direct contact to the implant surface. This suggests, that the genuine osseointegration process was almost complete at that time. CONCLUSION In this study, borderline reliability of osseointegration for immediately loaded palatal implants but reasonable bone formation until the fourth postoperative week was found histologically. Thus it seems likely that sufficient secondary stability for early orthodontic loading can be expected after 4 weeks. ACKNOWLEDGMENTS This work was supported in part by a grant of the Institute Straumann AG, CH-4437 Waldenburg, Switzerland to Martin Kunkel.
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Prof. Dr. Dr. M. KUNKEL Department of Oral and Maxillofacial Surgery University Hospital of Mainz Augustusplatz 2 55101 Mainz Tel.: 0049 6131 173191 Fax: 0049 6131 176602 E-mail: [email protected] Paper received 24 March 2006 Accepted 5 July 2007