Bone changes and microct in maxillo-facial diseases

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1 Bone changes and microct in maxillo-facial diseases J.D. Kün-Darbois 1, 2, D. Chappard 1 1 GEROM Groupe d Etude Remodelage Osseux et biomatériaux, LHEA, IRIS-IBS, Université d Angers, 4 rue Larrey, Anger Cedex France 2 Service de chirurgie maxillo-faciale et stomatologie, CHU d Angers, 4 rue Larrey, Anger Cedex France Aims MicroCT has been extensively used to study long bones in laboratory animals. However, the method has been seldom used in maxillo-facial pathology. The presence of teeth anchored in the jaw bone creates additional problems that need the development of new techniques and microct can bring new interesting solutions. The aims of this study were to evaluate the interest of microct in maxillo-facial pathology. 1) Botulinum toxin (BTX) injection is known to induce bone loss due to immobilization: this represents an animal model of disuse osteoporosis. BTX is a bacterial neurotoxin that leads to a transient muscle paralysis. In human clinical practice, BTX injection in masticatory muscles is frequently used. We have analyzed bone changes at the mandible following a unilateral BTX injection in masticatory muscles of adult rats. 2) Bisphosphonates (BPs) are molecules used to treat bone diseases associated with increased osteolysis in humans. Bisphosphonate-related osteonecrosis of the jaws (BRONJ) is a major adverse event due to BPs. The pathogenesis of BRONJ is not fully explained and seems multifactorial. An antiangiogenic effect of some BPs (e.g., zoledronic acid ZA) on jaw bone vascularization has been advocated. We induced BRONJ in the rat and analyzed the bone and alveolar vascularization of the mandible by microct. Methods 1) Adult male rats were randomized into 2 groups: control (CTRL, n=6) and BTX (n=9). Rats of the BTX group received a single injection of BTX into the right masticatory muscles. Rats of the CTRL group were similarly injected with saline. Rats were sacrificed 4 weeks after injections. Microcomputed tomography (microct) was performed with a Skyscan 1172 microct. Analysis of mandibular porosity by a vector projection algorithm was done on the 2D microct sections. 2) Other adult male rats were randomized into 2 groups: control (CTRL, n=11) and ZA (n=27). Rats of the ZA group received a weekly intravenous injection of ZA during 10 weeks. Rats of the CTRL group were similarly injected with equivalent volume of saline. After 6 weeks, right mandibular extraction of the 3 molars was performed in all rats (triggering factor). Rats were sacrificed 14 weeks after the first ZA injection. MicroCT was used to study bone lesions. Vascularization analysis was performed after intravascular injection of a radio-opaque material and 3D analysis by microct was done with CtVox. Results 1) MicroCT analysis showed significant bone loss in the right alveolar and condylar areas in BTX rats. Decrease in bone volume reached 20% for right alveolar bone and 35% at the right condylar bone. A hypertrophic bone outgrowth at the digastric muscle insertion was found on every right hemimandible in the BTX group and none in the CTRL group (Fig. 1). Analysis of porosity by vector analysis on microct sections revealed a higher bone porosity of the right alveolar bone (Fig. 2) (1). 2) MicroCT analysis revealed numerous signs of BRONJ at the right molar area in the ZA group (cortical erosion, periosteal reaction and bone sequestration). None of this signs were found at the left hemimandible in the ZA group and in both hemimandibles of the CTRL group

2 (Fig. 3). Vascular density of the molar area was found reduced at the right side in the ZA group due to tooth extraction but was not suppressed (Fig. 4). Figure 1: MicroCT analysis of bone loss as seen on 2D sections: A) Frontal sections of right (R) and left (L) hemimandibles in a rat of the CTRL group showing no difference at the alveolar bone and at the right digastric muscle enthesis. B) Frontal sections of right (R) and left (L) hemimandibles in a rat of the BTX group. Note the alveolar bone loss on the right side and the occurrence of a hypertrophic bone proliferation at the digastric muscle enthesis (arrow). C) Frontal sections of the mandibular condylar heads in a rat of the CTRL group showing no difference between each side. D) Frontal sections of the mandibular condylar heads in a rat of the BTX group showing a marked trabecular bone loss. For each image R and L identify respectively the right, and the left side.

3 Figure 2: MicroCT analysis of the hemimandibles of rat with BTX paralysis of Mus Masseter and Mus Temporalis on the right side. A) General view from the lingual side of the left hemimandible. B) Similar view of the right hemimandible. The green arrow identifies the hypertrophic bone proliferation at the digastric muscle enthesis. Analysis of porosity by vector analysis on microct sections in the molar region of the same bones C) left hemimandible, D) right hemimandible. The red pseudo color of alveolar bone indicates higher bone porosity according to a look up table. Note the considerable increase in hot colors (red orange yellow) in the alveolar area of the right side.

4 Figure 3: MicroCT analysis of alveolar bone changes. (A) a 3D model of a CTRL left hemimandible, (B) a CTRL right hemimandible with teeth removal (C) a ZA right hemimandible with teeth removal showing signs of BRONJ (cortical osteolysis (black arrow) and periosteal reaction (withe arrow). 2D frontal sections of right (D) and left (E) hemimandibles of a ZA rat showing periosteal reaction on the right side after teeth removal (arrows).

5 Figure 4: 3D models of vascular reconstructions of the molar area (arrows) of a CTRL rat (A) and a ZA rat (B) showing reduced vascular density at the right side in the ZA group due to teeth extraction. Conclusion 1) BTX injection in masticatory muscles leads to a significant and major mandible bone loss. These alterations can represent a risk factor for fractures in human. The occurrence of a hypertrophic bone metaplasia at the digastric muscle insertion may constitute an etiological factor for tori, a benign bone tumor frequently observed at the jaw. 2) In a rat model of BRONJ with mandibular tooth extraction, microct evidenced signs of osteonecrosis. However, vascularization was not suppressed by ZA but reduced due to the tooth extraction. MicroCT appears a powerful tool in the evaluation of bone and bone vessels changes in animal models of bone diseases in maxillo-facial pathology. 1. Kun-Darbois JD, Libouban H, Chappard D. "Botulinum toxin in masticatory muscles of the adult rat induces bone loss at the condyle and alveolar regions of the mandible associated with a bone proliferation at a muscle enthesis". Bone. 2015;77:75-82.

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