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Table of Contents   
ORIGINAL RESEARCH  
Year : 2012  |  Volume : 23  |  Issue : 4  |  Page : 501-505
Distraction-like phenomena in maxillary bone due to application of orthodontic forces in ovariectomized rats


1 Department of Orthodontics, School of Dentistry, University of Athens, Greece, and Adjunct Associate Professor, Department of Orthodontics, School of Dental Medicine, Case Western Reserve University, Cleveland, Ohio, USA
2 Department of Pathology, Amalia Fleming Hospital, Athens, Greece, and Laboratory for Research of the Musculoskeletal System, School of Medicine, University of Athens, Greece
3 Department of Orthodontics, School of Dentistry, University of Athens, Greece
4 Laboratory for Research of the Musculoskeletal System, School of Medicine, University of Athens, Greece, and Laboratory of Experimental Surgery and Surgical Research, School of Medicine, University of Athens, Greece

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Date of Web Publication20-Dec-2012
 

   Abstract 

Background: Orthodontic forces may not only influence the dentoalveolar system, but also the adjacent and surrounding cortical bone.
Aim: Since there is very limited information on this issue, we aimed to study the possible changes in maxillary cortical bone following the application of heavy orthodontic forces in mature normal and osteoporotic rats.
Materials and Methods: Twenty-four 6-month-old female rats were selected and divided into an ovariectomized group and a normal group. In both groups, the rats were subjected to a 60 gr* orthodontic force on the upper right first molar for 14 days.
Results: In both groups, histological sections showed that the application of this force caused hypertrophy and fatigue failure of the cortical maxillary bone. The osteogenic reaction to distraction is expressed by the formation of subperiosteal callus on the outer bony side, resembling that seen in distracted bones.
Conclusion: From this study we concluded that heavy experimental orthodontic forces in rats affect the maxillary cortical bone. The osteogenic reaction to these forces, expressed histologically by subperiosteal callus formation, is similar to that seen in distraction osteogenesis models.

Keywords: Bone, distraction, orthodontic forces, osteoporosis, ovariectomy, rats

How to cite this article:
Tsolakis AI, Khaldi L, Bitsanis I, Makou M, Dontas IA. Distraction-like phenomena in maxillary bone due to application of orthodontic forces in ovariectomized rats. Indian J Dent Res 2012;23:501-5

How to cite this URL:
Tsolakis AI, Khaldi L, Bitsanis I, Makou M, Dontas IA. Distraction-like phenomena in maxillary bone due to application of orthodontic forces in ovariectomized rats. Indian J Dent Res [serial online] 2012 [cited 2018 Aug 17];23:501-5. Available from: http://www.ijdr.in/text.asp?2012/23/4/501/104958
Current clinical practice in dentofacial orthopedics aims, by loading teeth, not only to influence the dentoalveolar system but also to transmit therapeutic forces onto the adjacent bone and surrounding tissue. [1] Various dentofacial orthopedic appliances are used in everyday clinical practice in order to enhance or retard maxillary growth. However, there is still no satisfactory scientific evidence on the biologic mechanisms that contribute to cortical bone modeling and remodeling in adjacent and distal areas following the application of heavy orthodontic forces.

So far, the clinical changes that occur in the anterior maxillary region following the application of a distal headgear to the upper molars have not been interpreted in the light of present knowledge of bone biology. Also, the effects of the application of a facial mask or reverse headgear on the maxillary bone demand a biologic scheme to be interpreted. Our hypothesis considers bone damage distal to the loading area as a possible mechanism for bone generation due to the applied forces. Since the spongiosa provides mechanical support for teeth and transfers loads from teeth to cortical bone and vice versa, [2] heavy forces applied to the dentoalveolar complex may influence adjacent and distal cortical bone. Thus, strains applied to teeth act as a mechanical stimulus to the underlying cortical bone and may influence bone modeling and/or remodeling patterns.

Additionally, it is well known that the jaws are also affected by systemic osteoporosis, both in pre- and postmenopausal women. [3],[4] Studies in rats have shown a decrease in mandibular cortical thickness, [5] as well as deterioration of the alveolar bone, in experimentally induced osteoporosis. [6]

The purpose of the present study was to test our aforementioned hypothesis, and to investigate the morphological changes in cortical maxillary bone following the application of heavy orthodontic forces in mature normal and ovariectomized female rats.


   Materials and Methods Top


Laboratory animals

Twenty-four 6-month-old Wistar female rats (mean weight 230 g), obtained from the Hellenic Pasteur Institute, were used in this study. The experiments took place in the Laboratory of Experimental Surgery and Surgical Research, School of Medicine, and in the Laboratory of Orthodontics, School of Dentistry, University of Athens, Greece. The animals were housed four to a cage according to national regulations and in conformance with the EU Directive 86/609 (permit no. Κ/3816/5-7-05) in a room with regulated light cycle (12-hour dark/12-hour light), temperature (20±2°C), and relative humidity (55±5%) and were fed a normal balanced rat pellet diet; the pellets were administered in pulverized form after the application of tooth forces. The animals were divided into two groups of 12 animals each. Group A included 12 rats that were subjected only to orthodontic movement of the upper right first molars. Group B included 12 rats that were also subjected to orthodontic movement of the upper right first molars, but these rats underwent bilateral ovariectomy 60 days before the application of the orthodontic appliance. Bilateral ovariectomies were performed via the ventral approach under general anesthesia. The animals in both groups were observed daily and their clinical appearance and food consumption was recorded.

Orthodontic appliance

Orthodontic rat molar movement was achieved by the application, under general anesthesia, of a closed nickel-titanium coil spring (0.010 × 0.045 inches) extending from the upper right first molar to the upper right incisor. Postoperatively, the animals received oral paracetamol as an analgesic for 2 days. The coil spring was 1 cm in length, and its elongation for 0.25 cm produced a force of 60 gr*, which was measured with the Haldex™ precision force gauge. The orthodontic force was applied for 14 days. At the end of this period, the animals were euthanized and the upper jaw was dissected from the rest of the skull and the spring was removed carefully.

Histology

The upper jaw specimens were fixed in 10% buffered formalin for 18 hours and then decalcified in EDTA buffer for 6-8 weeks. Following this, 5-mm-thick slices of the upper jaw were cut sagittally, including the apical region from the central incisor to the third molar. The specimens were dehydrated with ethanol and embedded in paraffin; 5-μm-thick sections were then obtained, stained with hematoxylin and eosin, and observed under transmitted-light microscopy.


   Results Top


Clinical findings

The rats of both groups showed no adverse effects that could be related to anesthesia or food consumption. Edema of the gingiva was observed postoperatively after the application of the spring in 30% of the animals but this disappeared after 3 days. Clinical symptoms of inflammation were not observed.

Histological findings

Normal rats: The cortical bone at the apical region at the site of retraction, between the first and second molars revealed extensive structural distortion; however, there was no obvious bone rupture. The cortical bone at that site showed marked hypertrophy of non-lamellar bone, with irregular cement lines and formation of a large subperiosteal callus, which extended from the first molar up to the third molar and along the curvature of the upper jaw [Figure 1]. The bone at the apical region, distal to the retracted molar, showed cortical thinning of lamellar structure, with marked cement lines and visible vessels [Figure 2]. In comparison, on the nonretracted side, the cortical bone at the apical region, from the first molar up to the third molar, showed no changes and the bone structure remained intact [Figure 3].
Figure 1: Retracted side of normal rats. Subperiosteal callus extending from the first molar up to the curvature of the upper jaw (black arrow). Area of distortion of cortical bone within black lines (yellow arrow) (H and E, ×4 objective)

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Figure 2: Retracted side of normal rats. Cortical thinning of the apical region, subperiosteal callus (black arrow), and obvious vessels (H and E, ×4 objective)

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Figure 3: Nonretracted side of normal rats. No changes of bone structure; intact cortical bone (arrow) (H and E, ×4 objective)

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Ovariectomized rats: The cortical bone at the apical region at the site of retraction, between the first and second molars, presented ruptures (fatigue failure) at more than one point and showed increased porosity. Bone hypertrophy was less than in the normal rats and the subperiosteal callus was conspicuously smaller [Figure 4]. The cortical bone at the level of the third molar and along the curvature of the upper jaw was significantly thinner and was ruptured at multiple points and inflamed at others. The bone callus was extensive and large and the vessels were less apparent [Figure 5]. On the opposite (nonretracted) side, from the third molar through the curvature of the upper jaw, the cortical bone at the apical region was intact but showed obvious cement lines at the cortical bone-tooth interface [Figure 6].
Figure 4: Retracted side of ovariectomized rats. Rupture of cortical bone in the area between first and second molars (line); small subperiosteal callus (arrow) (H and E, ×4 objective)

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Figure 5: Retracted side of ovariectomized rats. Significant cortical thinning of the apical region (two-headed yellow arrow); huge subperiosteal callus (arrow). Rupture of cortical bone in the area of the third molar (black frame) (H and E, ×4 objective)

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Figure 6: Nonretracted side of ovariectomized rats. Obvious cement lines at the cortical bone-tooth interface (H and E, ×4 objective)

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   Discussion Top


The rat animal model for orthodontic tooth forces has been used successfully in dental research in the past. [1] In addition, mature ovariectomized rats are the model of choice for the study of postmenopausal osteoporosis. The choice of 6-month-old rats was based on the knowledge that in order to simulate the results of postmenopausal osteoporosis, the animals should not be younger than 6 months of age. [7]

Distraction osteogenesis is the process of new bone regeneration in the gap between vascularized bony ends that are separated by gradual mechanical disruption. Distraction osteogenesis was extensively used and described by Ilizarov et al. for the treatment of shortened extremities and was first applied for the lengthening of long bones. [8] McCarthy et al. have reported successful application of this technique on bones in the craniofacial region. [9] Histologically, in distraction applied following osteotomy, the gap is first filled with blood clot, fibrous tissue, and inflammatory cells. [10],[11] As distraction progresses, the fibrous tissue presents a longitudinal orientation following the stress vector of gradual bone tension. During the distractive process, the following four zones have been observed:

  • a fibrous center with parallel collagen fibers,
  • a transitional zone with premature bone formation,
  • a zone showing bone remodeling, and
  • a zone with mature bone at the gap ends. Bone formation advances from the bony edges to the fibrous bridge. [11]
It has been considered that the processes involved in orthodontic tooth movement may be a type of distraction osteogenesis in the periodontal ligament. [12] In cases of rapid orthodontic tooth movement, the process of osteogenesis on the tension side is similar to distraction osteogenesis and intrabony defects are avoided. [11]

According to Roberts and Hartsfield, one of the fundamental genetic mechanisms influencing bone morphology is mechanically-induced inflammation; this can be modified by mechanical loading, which activates modeling and remodeling. [13] Orthodontic movement with the application of forces that exceed 4000 με has been described to result in hypertrophy and fatigue failure of the relevant bone tissue. The periodontal ligament at the zone of maximal compression may become necrotic and the adjacent bone exposed to high peak loads, resulting in mechanical fatigue and inflammation. [14]

In the present study, the applied orthodontic force of 60 gr* is considered a heavy force, as its application produces bone rupture due to fatigue failure and probably exceeds 4000 με. It was shown to distract the periodontal ligament and the adjacent bone, and it also influenced the bone distal to the point of application and extended into the curvature of the upper rat jaw. In the rats of our experiment, the osteogenic reaction to these forces was similar to that seen in the bone distraction phenomenon and was expressed by the formation of subperiosteal callus on the outer bony side, thus cushioning and splinting the affected bone. Microscopically, the formed callus consisted of fibro-osseous tissue that was the result of an intramembranous rather than endochondral ossification process. In the normal rats the callus was located distal to the applied force and appeared smaller in comparison to that in osteoporotic rats, where the callus was evident in two locations: one at the first molar (small) and the other at the level of the third molar and along the curvature of the upper jaw (large and extensive).

Similarly, Reitan and Kvam have also reported thick bone deposition at a certain distance from the undermining bone resorption site, along the curvature of the upper jaw. [15] In their experiments that lasted 2-14 days, the formed maxillary thick bone layers appeared even with forces of 4, 12, and 30 gr*. The bone tissue that develops distal to the point of application of orthodontic forces in rats resembles that seen in distracted bones and, therefore, this process may be considered a bone distraction-like phenomenon. This phenomenon constitutes a protective mechanism to preserve the integrity of the jaw when disruptive mechanical stresses are applied during orthodontic movement. Earlier, Glickman and Smulow reported rapid formation of compensatory bone layers as a 'buttressing bone formation' phenomenon, as a result of increasing pressure during tooth movement due to the alteration of occlusal contacts. [16]

This process can explain the increase of the apical base of the upper jaw in areas distal to applied forces in individuals treated with extraoral appliances. For example, the alteration in the direction of eruption of mesially impacted cuspids after the use of a headgear appliance may be due to a bone distraction-like phenomenon in the maxillary cuspid area. Furthermore, the increase in maxillary length and in bone remodeling at the posterior maxillary region following the application of a reverse headgear appliance may be, to some extent, the result of a bone distraction-like phenomenon in the distal maxillary region. The originality of this study lies in the ascertainment of a distraction-like phenomenon occurring distal to applied heavy orthodontic forces. Further research is needed to clarify the level of exerted orthodontic forces below which the bone distraction-like phenomenon will not occur, and also to unravel the mechanism that produces this phenomenon.

In conclusion, heavy orthodontic forces applied to the dentoalveolar complex cause hypertrophy and fatigue failure of the cortical maxillary bone in both normal and ovariectomized rats, with a few differences. The osteogenic reaction to these forces is similar to that of distraction osteogenesis models and is expressed histologically by subperiosteal callus formation.


   Acknowledgment Top


The study was partly supported by a research grant from the Special Account for Research Grants, National and Kapodistrian University of Athens, Greece.

 
   References Top

1.Rygh P, Moyers RE. Force systems and tissue responses to forces in orthodontics and facial orthopedics. In: Moyers RE, Editor. Handbook of Orthodontics. 4th ed. Chicago: Year Book Medical Publishers; 1988. p. 306-31.  Back to cited text no. 1
    
2.Frost HM. Bone modeling, bone architecture, mechanical functions and effects. In: The Utah paradigm of skeletal physiology. Athens, Greece: International Society of Musculoskeletal and Neuronal Interactions; 2004. p. 75-95.  Back to cited text no. 2
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3.Horner K, Devlin H, Alsop CW, Hodgkinson IM, Adams JE. Mandibular bone mineral density as a predictor of skeletal osteoporosis. Br J Radiol 1996;69:1019-25.   Back to cited text no. 3
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4.von Wowern N. General and oral aspects of osteoporosis: A review. Clin Oral Invest 2001;5:71-82.  Back to cited text no. 4
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5.Yang J, Farnell D, Devlin H, Horner K, Graham J. The effect of ovariectomy on mandibular cortical thickness in the rat. J Dentistry 2005;33:123-9.  Back to cited text no. 5
    
6.Tanaka M, Ejiri S, Toyooka E, Kohno S, Ozawa H. Effects of ovariectomy on trabecular structures of rat alveolar bone. J Periodont Res 2002;37:161-5.  Back to cited text no. 6
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7.Jee WS, Yao W. Overview: Animal models of osteopenia and osteoporosis. J Muskuloskel Neuron Interact 2001;1:193-207.  Back to cited text no. 7
    
8.Ilizarov GA, Lediov VL, Shitin VP. The course of compact bone reparative regeneration in distraction osteosynthesis under different conditions of bone fragment fixation and experimental study (Russian). Exp Khir Anesteziol 1969;14:3-12.  Back to cited text no. 8
    
9.McCarthy JG, Schreiber J, Karp N, Thorne CH, Grayson BH. Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 1992;89:1-10.  Back to cited text no. 9
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10.Yen SL. Distraction Osteogenesis: Application to dentofacial orthopedics. Semin Orthod 1997;3:275-83.  Back to cited text no. 10
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11.Liou EJ, Figueroa AA, Polley JW. Rapid orthodontic tooth movement into newly distracted bone after mandibular distraction osteogenesis in a canine model. Am J Orthod Dentofacial Orthop 2000;117:391-8.  Back to cited text no. 11
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12.Liou EJ, Huang CS. Rapid canine retraction through distraction of the periodontal ligament. Am J Orthod Dentofacial Orthop 1998;114:372- 82.  Back to cited text no. 12
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13.Roberts WE, Hartsfield JK. Bone development and function: genetic and environmental mechanisms. Semin Orthod 2004;10:100-22.  Back to cited text no. 13
    
14.Roberts WE, Huja S, Roberts JA. Bone modeling: Biomechanics, molecular mechanisms, and clinical perspectives. Semin Orthod 2004;10:123-61.  Back to cited text no. 14
    
15.Reitan K, Kvam E. Comparative behaviour of human and animal tissue during experimental tooth movement. Angle Orthodontist 1971;41:1- 23.  Back to cited text no. 15
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16.Glickman I, Smulow JB. Buttressing bone formation in the periodontium. J Periodont 1965;36:365-70.  Back to cited text no. 16
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Correspondence Address:
Apostolos I Tsolakis
Department of Orthodontics, School of Dentistry, University of Athens, Greece, and Adjunct Associate Professor, Department of Orthodontics, School of Dental Medicine, Case Western Reserve University, Cleveland, Ohio, USA

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0970-9290.104958

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