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RESEARCH REPORT |
1 Department of Orthodontics, Okayama University Graduate School of Medicine and Dentistry, 2-5-1, Shikata-cho, Okayama, 700, Japan;
2 Kanomi Dental Clinic, 30-1-MD Minamiekimae-cho Himeji, 670, Japan;
3 Department of Oral Facial Development, Indiana University School of Dentistry, 1121 West Michigan Street, Indianapolis, IN 46202; and
4 Department of Cellular/Integrative Physiology, Indiana University School of Medicine, 635 Barnhill Drive, Indianapolis, IN 46202;
* corresponding author, lgaretto{at}iupui.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: implant • orthodontic • anchorage • dog
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Kanomi (1997) introduced a miniature implant (5.0 mm x Ø1.0 mm titanium screw, Leibinger®, Freiburg, Germany) that is a variation of a mini-bone screw used to fix bone plates in plastic and reconstructive surgery. For orthodontists, the potential advantage to such a small implant is that it increases the number of sites where anchorage implants can be placed. A preliminary study demonstrated that similar mini-implants (4.0 mm x Ø1.0 mm, 99.5% titanium, Sankin®, Tokyo, Japan) in dog mandibles were successfully used to intrude premolars (Ohmae et al., 2001). However, the bone healing reaction and response to applied loads are unknown.
The purpose of this study was to assess, histomorphometrically, the osseous support of small titanium screws and to determine clinical guidelines for healing prior to orthodontic loading.
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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) were equally divided among 8 eight-month-old male dogs. Within each jaw, both force-applied (FA) and healing control (HC) implants were further divided into 3 groups (three-, six-, 12-week), with 8 implants per group (Fig. 1b). It is important to note that the HC implants were placed in the jaw for 3, 6, or 12 wks prior to termination of the experiment so that bone could be assessed at the initiation of loading (Fig. 1c). The FA implants remained in the jaw for an additional 12 wks of force application. In the FA, a force of 200–300 g was applied for 12 wks with an elastomeric chain attached from the implant to a hook on the crowns of the premolars. Every 4 wks, the force was checked with a force gauge and adjusted to be maintained within the 200- to 300-g range. The study protocol was reviewed and approved by the Indiana University Review Committee for animal care and use.
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).
Tissue Preparation
The maxillary and mandibular block specimens were harvested and dehydrated in an ascending series of ethyl alcohols, and cleared in xylene. The specimens were infiltrated with methylmethacrylate (MM), containing 3% dibutyl phthalate, in a Shandon Hypercenter XPTM automatic tissue processor (Shandon, Pittsburgh, PA, USA). The embedded specimens were serially sectioned at 110–120 µm in the sagittal plane with a Leica 1600 Saw MicrotomeTM (Deerfield, MA, USA) or an ExaktTM cutting/grinding system (Exakt Medical Instruments, Oklahoma City, OK, USA) and polished to approximately 100 µm for the bright-field and fluorescent microscopic examination.
Histomorphometric Analysis
Histomorphometric analysis was performed on a Nikon FXA epifluorescent microscope (Nikon Inc., Melville, NY, USA) with stereological point-hit and linear intercept methods at magnifications of X100 with a 10 x 10 point ocular square grid (Kimmel and Jee, 1983). The measurements and calculations followed standard nomenclature and formulae (Parfitt, 1983). Measurements were performed on bone within 1 mm of the implant. Microradiographic images were produced by means of a FaxitronTM (Hewlett-Packard, Beaverton, OR, USA). Static variables [bone-implant contact, woven bone volume (WV/TV%), and bone volume (BV/TV%)] and dynamic variables [bone formation rate (BFR%/year), mineralizing surface relative to bone surface (MS/BS%), and the mineral appositional rate (MAR µm/day)] were calculated. Double-label and osteon wall thickness, as well as direct measurement of the wall thickness, were measured at X250 magnification.
Statistical Methods
Analysis of variance models were used to examine the effects of healing and application of force on the histomorphometric indices of the maxilla and mandible. The model comparison, corrected for a random dog effect, was used to correlate all measurements from the same dog. In addition, the method analyzed fixed effects for HC and FA, healing period, location (maxilla or mandible), and all interactions. Comparisons were made by the Fisher’s Protected Least Significant Differences method to control the overall significance level at 5%. All data are presented as average ± the standard error of the mean (SEM).
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RESULTS |
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Bone and Implant Contact (%)
Mandibular implants had significantly higher bone-implant contact than maxillary implants (p = 0.0002). In the maxilla (Fig. 2a), the direct bone contact with the implant in the HC was 33.5 ± 3.2%, 24.5 ± 2.0%, and 21.9 ± 2.4% at 3, 6, and 12 wks, respectively. The three-week HC showed significantly higher bone-implant contact than either the six-week (p = 0.006) or 12-week (p = 0.0002) HC. In the FA, it was 32.9 ± 2.4%, 32.0 ± 6.0%, and 30.7 ± 4.2% at 3, 6, and 12 wks, respectively.
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), bone contact in the HC was 33.9 ± 3.3%, 32.4 ± 3.6%, and 30.2 ± 4.9% at 3, 6, and 12 wks, respectively. In the FA, it was 40.2 ± 4.1%, 35.2 ± 7.1%, and 36.3 ± 5.8% at 3, 6, and 12 wks, respectively.
Woven Bone Volume/Total Bone Volume (WV/TV%)
In the maxilla (Fig. 2c), WV/TV was 51.8 ± 3.2%, 26.8 ± 3.0%, and 22.7 ± 4.5% at 3, 6, and 12 wks, respectively, in the HC. In these groups, the three-week volume was significantly higher than the six-week (p = 0.0001) and the 12-week (p = 0.0001) volumes. In the FA, it was 26.1 ± 2.0%, 20.8 ± 2.1%, and 20.2 ± 3.3% at 3, 6, and 12 wks, respectively.
In the mandible (Fig. 2d), WV/TV was 50.8 ± 4.1%, 25.8 ± 2.8%, and 10.7 ± 2.6% at 3, 6, and 12 wks, respectively, in the HC. The three-week HC was significantly higher than the six-week (p = 0.0001) or the 12-week (p = 0.0001), and the six-week was also higher than that at 12 wks (p = 0.0007). In the FA, WV/TV was 18.0 ± 2.3%, 19.2 ± 3.3%, and 13.4 ± 1.1% at 3, 6, and 12 wks, respectively.
Bone Volume/Total Volume (BV/TV%)
In the maxilla (Fig. 2e), BV/TV in the HC was 55.6 ± 3.3%, 53.8 ± 2.9%, and 15.9 ± 3.0% in the three-, six-, and 12-week implants, respectively. The 12-week HC was significantly lower than that at 3 wks (p = 0.0001) and 6 wks (p = 0.0001). In the FA, BV/TV was 33.7 ± 2.9%, 36.7 ± 5.4%, and 44.5 ± 6.3% at 3, 6, and 12 wks, respectively.
In the mandible (Fig. 2f), BV/TV in the HC was 40.3 ± 2.9%, 49.2 ± 4.5%, and 45.0 ± 5.6% at 3, 6, and 12 wks, respectively. In the FA, it was 46.2 ± 1.6%, 41.1 ± 3.0%, and 53.9 ± 5.0% at 3, 6, and 12 wks, respectively.
Bone Formation Rate (BFR%/year)
When evaluated independently, MS/BS (mineralizing surface/bone surface; Figs. 3a, 3b) and MAR (mineral appositional rate; Figs. 3c, 3d) showed the same pattern as BFR. In the maxilla (Fig. 3e), BFR was 611.8 ± 73.7%, 210.9 ± 25.0%, and 189.9 ± 13.4% at 3, 6, and 12 wks, respectively, in the HC. In these groups, the three-week BFR was significantly higher than either the six-week (p = 0.0001) or the 12-week (p = 0.0001). In the FA, it was 167.9 ± 18.4%, 210.9 ± 25.0%, and 168.5 ± 36.3% at 3, 6, and 12 wks, respectively.
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), BFR was 553.0 ± 39.8%, 266.5 ± 49.1%, and 174.7 ± 29.0% at 3, 6, and 12 wks, respectively, for the HC. Among these groups, the three-week group was significantly higher than the six-week (p = 0.0001) or the 12-week group (p = 0.0001), and the six-week group was significantly higher than the 12-week group (p = 0.0453). In the FA, it was 228.7 ± 34.1%, 233.7 ± 50.9%, and 169.0 ± 14.7% at 3, 6, and 12 wks, respectively.
Histological Appearance
Consistent with the quantitative analysis of WB/TV, at the light-microscopic level, the fluorochrome labels observed in the three-week HC (Fig. 4a) were predominantly diffuse, indicating active woven bone mineralization. Polarized light microscopy (Fig. 4b) demonstrated that woven bone was the predominant type of mineralized tissue located within 1.0 mm of the implant surface. However, in the six- and 12-week HC, fewer labels (Fig. 4c) were observed, and lamellar bone predominated (Fig. 4d). The three-week healing interval FA also showed fewer and narrower labels (Fig. 4e), indicating a much lower rate of bone turnover. The predominant type of bone observed around the implants for all loaded groups was lamellar (Fig. 4f).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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All three implant failures occurred in the mandible. Two of the three failures occurred in the same group. Both of these implants were intentionally placed between the roots of the first and second premolars. In retrospect, this was the narrowest of all the surgical sites. The reason for the failure of these implants is not clear, but may be associated with a surgical problem related to penetration of or contact with the roots of the teeth.
Static Histomorphometry
The present bone-implant contact data are consistent with previous reports (Roberts et al., 1989; Parr et al., 1996). In the present study, implants with as little as 5% bone contact at the bone-implant interface successfully resisted orthodontic force. Mandibular implants consistently had more bone-implant contact than the maxillary ones. This probably relates to the higher ratio of cortical to trabecular bone in the mandible. There were no significant differences for bone-implant contact between the FA and HC. However, significantly greater bone contact was noted in the three-week group in the maxilla of the HC. Since the type of bone at the interface at 3 wks was predominantly of the immature woven type, high bone contact at 3 wks is a transient healing reaction.
Biomechanical resistance of a rigid implant to orthodontic loads is related to both the quality and quantity of the integrated interface (Albrektsson et al., 1981; Roberts et al., 1984). Analysis of the data from microradiographs indicated that three-week HC showed significantly higher woven bone volume than at 6 and 12 wks. Thus, the lower bone-implant contact in the six- and 12-week HC is an indication of the change in quality from woven to lamellar bone. A similar pattern was also seen in BV/TV in the 12-week group for the HC in the maxilla.
Dynamic Histomorphometric Parameters
The rate of remodeling is known to increase to as much as 400%/yr (Garetto et al., 1995) as the healing interface matures. In the present study, at 3 wks there was intense formation of woven bone around the endosseous implants. The high rate in the three-week group was due to increases in both MAR and MS/BS, reflecting an elevation in the overall rate of bone activity. The bone formation rate was significantly higher in the three-week HC relative to other groups (about 600%/yr). Because of the short time-course of the experiment, the increased bone formation at the three-week period is indicative of intense bone modeling and remodeling of the initial healing reaction. While all other sampling times showed a lower rate of bone formation, it is important to note that these levels were still much higher (three-fold increase) compared with normal BFR in the untreated mandible (Garetto and Tricker, 2002). The only other significant difference observed was a higher MS/BS in the maxillary six-week FA compared with the three-week animals. These results are not consistent with previous data for long-term maintenance of osseointegration (Garetto et al., 1995; Roberts, 2002). It is unclear if these data reflect an unrecognized variable in the present experiment or are due to the lower n-value in the six-week group.
In the present study, we chose to evaluate different healing durations prior to implant loading. It is possible that the present implants may be able to withstand immediate loading if they are carefully placed in good-quality bone; however, that issue should be investigated in a specific experiment. Roberts et al. (1984) suggested that a six-week healing period in rabbits (equivalent to approximately 12 wks in dogs and 4 to 5 mos in humans) is adequate for the implants to resist orthodontic forces. An important observation in the present study is that implants were able to resist orthodontic loads despite an intense healing reaction when the surrounding bone was mainly of the immature woven type.
It is interesting to note that there were no significant differences between three- and 12-week FA, indicating that a three-week healing period is sufficient for orthodontic loading in dogs. This interval relates to about 4–5 wks of healing in humans because of the slower bone remodeling rate in man (Takahashi et al., 1980). Thus, as long as there is adequate bone support, small titanium screws can successfully resist loads following a relatively short period of healing. Although the present study demonstrates that a short interval of healing is all that is necessary, the lack of failure of loaded implants that healed for only 3 wks indicates that the critical healing time is actually shorter. If the implants are well-placed in good-quality bone, is it detrimental to load them immediately? Answering this important question requires additional research.
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ACKNOWLEDGMENTS |
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Received July 12, 2002; Last revision December 12, 2002; Accepted February 3, 2003
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Garetto LP, Tricker ND (2002). Bone remodeling surrounding implants. In: Bridging the gap between dental and orthopaedic implants. Garetto LP, Turner CH, Duncan RL, Burr DB, editors. Indianapolis: Indiana University School of Dentistry, pp. 89–99.
Garetto LP, Chen J, Parr JA, Roberts WE (1995). Remodeling dynamics of bone supporting rigidly fixed titanium implants: a histomorphometric comparison in four species including humans. Implant Dent 4:235–243.[Medline]
Kanomi R (1997). Mini-implant for orthodontic anchorage. J Clin Orthod 31:763–767.[Medline]
Kimmel DB, Jee WSS (1983). Measurements of area, perimeter, and distance: details of data collection in bone histomorphometry. In: Bone histomorphometry. Techniques and interpretation. Recker RR, editor. Boca Raton, FL: CRC Press, pp. 89–108.
Ohmae M, Saito S, Morohashi T, Seki K, Qu H, Kanomi R, et al. (2001). A clinical and histological evaluation of titanium mini-implants as anchors for orthodontic intrusion in the beagle dog. Am J Orthod Dentofacial Orthop 119:489–497.[ISI][Medline]
Parfitt AM (1983). Stereologic basis of bone histomorphometry: theory of quantitative microscopy and reconstruction in the third dimension. In: Bone histomorphometry. Techniques and interpretations. Recker RR, editor. Boca Raton, FL: CRC Press, pp. 53–88.
Parr JA, Young T, Dunn-Jena P, Garetto LP (1996). Histomorphometrical analysis of the bone-implant interface: comparison of microradiography and brightfield microscopy. Biomaterials 17:1921–1926.[Medline]
Roberts WE (2002). When planning to use an implant for anchorage, how long do you have to wait to apply force after implant placement? (letter) Am J Orthod Dentofacial Orthop 121:14A.
Roberts WE, Smith RK, Zilberman Y, Mozsary PG, Smith RS (1984). Osseous adaptation to continuous loading of rigid endosseous implants. Am J Orthod 86:95–111.[Medline]
Roberts WE, Helm FR, Marshall KJ, Gongloff KR (1989). Rigid endosseous implants for orthodontic and orthopedic anchorage. Angle Orthod 59:247–256.[Medline]
Roberts WE, Marshall KJ, Mozsary PG (1990). Rigid endosseous implant utilized as anchorage to close an atrophic extraction site. Angle Orthod 60:135–152.[Medline]
Takahashi H, Norimatsu H, Watanabe G, Konno T, Inoue J, Fukuda M (1980). The remodeling period (sigma) in canine and human trabecular bone. In: Calcium endocrinology. Yoshitoshi U, Fujita T, editors. Tokyo: Chugai Igaku Co., pp. 13–31.
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