UNIVERSIDADE ESTADUAL DE CAMPINAS FACULDADE DE ODONTOLOGIA DE PIRACICABA
FÁBIO VIEIRA DA SILVA
EFEITO DA EXTRAÇÃO DENTAL NA REMODELAÇÃO ÓSSEA
CONDILAR DE RATOS
EFFECT OF DENTAL EXTRACTION ON CONDILAR BONE
REMODELING OF RATS
Piracicaba 2019
FÁBIO VIEIRA DA SILVA
EFEITO DA EXTRAÇÃO DENTAL NA REMODELAÇÃO ÓSSEA
CONDILAR DE RATOS
EFFECT OF DENTAL EXTRACTION ON CONDILAR BONE
REMODELING OF RATS
Dissertação apresentada à Faculdade de Odontologia de Piracicaba da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do título de
Mestre em Biologia Buco-Dental,
na Área de Anatomia.
Dissertation presented to the Piracicaba Dental School of the University of Campinas in partial fulfillment of the requirements for the degree of Master in Oral Biology, in Anatomy area
Orientador: Prof. Dr. Felippe Bevilacqua Prado ESTE EXEMPLAR CORRESPONDE A VERSÃO FINAL DA DISSERTAÇÃO DEFENDIDA PELO
ALUNOFÁBIOVIEIRADASILVA
ORIENTADA PELO PROF.DR. FELIPPE BEVILACQUA PRADO.
Piracicaba 2019
RESUMO
O estresse mecânico é reconhecido como um fator importante afetante do metabolismo ósseo. Para entender mais detalhadamente o mecanismo do processo de adaptação funcional em resposta a mudanças na distribuição das tensões mecânicas, no presente estudo, a histomorfometria foi utilizada para investigar a influência da extração dental anterior unilateral e a morfologia óssea do côndilo mandibular em ratos. MATERIAIS E MÉTODOS: Foram utilizados 24 ratos machos (Rattus norvegicus albinus) da linhagem Wistar, com 2 meses de idade. No final dos 2 meses de idade, o dente incisivo central superior foi extraído (lado direito), e a eutanásia ocorreu nos períodos 5 (n = 6), 7 (n = 6) e 14 (n = 6) dias após o Dia 0. No grupo controle (n = 6), a dentição foi mantida sem extração dentária. A eutanásia ocorreu no período de 14 dias após o dia 0. Após a eutanásia, os ratos de todos os grupos tiveram sua mandíbula esquerda removida e separada ao meio. As peças foram submetidas a processamento histológico de rotina em HE, e foi avaliado qualitativamente a morfologia óssea do côndilo mandibular por meio do software Image J. Para a avaliação da distribuição paramétrica dos dados foi utilizado o teste de Shapiro-Wilk. Os dados foram submetidos ao teste ANOVA para verificar a diferença entre os valores de área obtidos e o teste post-hoc de Dunnet para detectar as diferenças na comparação entre os grupos (Software GraphPAD Prism, EUA). O nível de significância de p <0,05 foi considerado. RESULTADOS E CONCLUSÃO: Houve associação entre a extração dentaria e a deformação mecânica morfológica do côndilo mandibular de ratos. A extração do dente incisivo central superior direito interfere na morfologia condilar mandibular. Os dados do presente estudo poderão ser utilizados como suporte para futuras pesquisas baseadas em microtomografia computadorizadas tridimensional (Microct-3D) bem como análises imunohistoquimicas.
ABSTRACT
Mechanical stress is recognized as an important factor affecting bone metabolism. To further understand the mechanism of the functional adaptation process in response to changes in the distribution of mechanical stresses, in the present study, histomorphometry was used to investigate the influence of unilateral anterior dental extraction and mandibular condyle bone morphology in rats. MATERIALS AND METHODS: Twenty-four male rats (Rattus norvegicus albinus) of the Wistar line, 2 months old, were used. At the end of 2 months of age, the upper central incisor tooth was extracted (right side), and euthanasia occurred in periods 5 (n = 6), 7 (n = 6) and 14 (n = 6) days after Day 0. In the control group (n = 6), the dentition was maintained without dental extraction. Euthanasia occurred within 14 days after day 0. After euthanasia, the rats of all groups had their left jaw removed and separated in half. The pieces were submitted to routine histological processing in HE, and the bone morphology of the mandibular condyle was evaluated qualitatively through the Image J. software. The Shapiro-Wilk test was used to evaluate the parametric distribution of the data. The data were submitted to the ANOVA test to verify the difference between the area values obtained and the Dunnet post-hoc test to detect the differences in the comparison between the groups (Software GraphPAD Prism, USA). The level of significance of p <0.05 was considered. RESULTS AND CONCLUSION: There was an association between tooth extraction and mechanical morphological deformation of the mandibular condyle of rats. The extraction of the right upper central incisor tooth interferes with mandibular condylar morphology. The data of the present study could be used as support for future researches based on three-dimensional computerized microtomography (Microct-3D) as well as immunohistochemical analyzes.
SUMÁRIO
1 INTRODUÇÃO ... 8
2 Artigo: EFFECT OF DENTAL EXTRACTION ON CONDILAR BONE REMODELING OF RATS ... 10
3 Conclusão ... 21
Referencias ... 22
Anexo 1- Comprovante de submissão na revista...24
Anexo 2- Comprovante do Comitê de Ética – CEUA/UNICAMP...25
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1 INTRODUÇÃO
O estresse mecânico é reconhecido como um fator importante afetando o metabolismo do osso (Zernicke et al., 2006; Skerry, 2008). A redução da estimulação mecânica pode diminuir significativamente a massa óssea (LeBlanc et al., 2007) enquanto o exercício habitual aumenta ou mantém a massa óssea (Bassey et al., 1994). Essas mudanças na distribuição de tensão mecânica levam à adaptação funcional no tecido ósseo (Zernicke et al., 2006; Skerry, 2008). Similarmente, durante o período de crescimento do côndilo mandibular, mudanças ocorrem na espessura do osso cortical e na arquitetura tridimensional das trabéculas ósseas da articulação temporomandibular (ATM) (Nagahara et al., 1999; Springe et al., 2002).
Pesquisas envolvendo o método dos elementos finitos mostraram que à medida que o crescimento ocorre, as mudanças na estrutura óssea e aumento da mineralização do osso trabecular impedem a deformação excessiva (Van Ruuven et al., 2003; Mulder et al., 2007; Pileicikiene et al., 2007).
Estudos em humanos sugerem que mudanças ocorrem no tecido ósseo do côndilo mandibular em resposta a novas distribuições de carga funcional causadas por alterações oclusais (Parker, 1993; Huja et al., 2008). Estes fenômenos são importantes porque afetarão a adaptação funcional dos côndilos mandibulares (De Boever et al., 2000; Ueki et al., 2006). No entanto, o mecanismo exato desses efeitos não foi completamente elucidado.
O metabolismo ósseo é constantemente equilibrado pela remodelação através da formação e reabsorção ósseas. Quando ocorre a adaptação funcional no tecido ósseo, as atividades celulares do osso e as células de reabsorção óssea devem mudar. Um modelo experimental animal demonstrou que o hipocrescimento da mandíbula com um aumento significativo nas trabéculas ósseas mandibulares ocorreu no lado onde molares foram extraídos como resultado de uma mudança na posição do côndilo mandibular causada pela perda unilateral da oclusão de suporte (Endo et al., 1998; Huang et al., 2002). Este resultado indica que o metabolismo ósseo é um indicador importante durante o processo de adaptação funcional do tecido ósseo em resposta a alterações oclusais como a perda dental. No entanto, nenhuma pesquisa avaliou a dinâmica do metabolismo ósseo dos côndilos mandibulares como resultado da mudança de cargas funcionais provenientes da extração do dente incisivo em ratos.
Para entender mais detalhadamente o mecanismo do processo de adaptação funcional em resposta a mudanças na distribuição das tensões mecânicas, no presente estudo, a histomorfometria foi utilizada para avaliar a dinâmica dos metabolismo dos côndilos mandibulares de ratos que foram submetidos a extração do incisivo superior no lado direito.
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Assim, O objetivo deste estudo foi investigar a influência da extração dental anterior unilateral e a morfologia óssea do côndilo mandibular em ratos.
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2 ARTIGO: EFFECT OF DENTAL EXTRACTION ON CONDILAR BONE REMODELING OF RATS
Artigo submetido ao periódico Brazilian Dental Journal (ANEXO 1).
Authors: Fábio Vieira da Silva1, Alexandre Rodrigues Freire1, Beatriz Carmona Ferreira1, Ana Cláudia Rossi1, Felippe Bevilacqua Prado1
1Department of Biociences, Anatomy Division, Piracicaba Dental School, University of Campinas, Piracicaba, São Paulo, Brazil.
Corresponding author’s email address: Prof. Dr. Felippe Bevilacqua Prado
Avenida Limeira, n / 901 – Areião. Piracicaba, São Paulo – Brazil. Tel: +55 19 21065721 Postal Code: 13414-903
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ABSTRACT
Mechanical stress is recognized as an important factor affecting bone metabolism. To further understand the mechanism of the functional adaptation process in response to changes in the distribution of mechanical stresses, in the present study, histomorphometry was used to investigate the influence of unilateral anterior dental extraction and mandibular condyle bone morphology in rats. MATERIALS AND METHODS: Twenty-four male rats (Rattus norvegicus albinus) of the Wistar line, 2 months old, were used. At the end of 2 months of age, the upper central incisor tooth was extracted (right side), and euthanasia occurred in periods 5 (n = 6), 7 (n = 6) and 14 (n = 6) days after Day 0. In the control group (n = 6), the dentition was maintained without dental extraction. Euthanasia occurred within 14 days after day 0. After euthanasia, the rats of all groups had their left jaw removed and separated in half. The pieces were submitted to routine histological processing in HE, and the bone morphology of the mandibular condyle was evaluated qualitatively through the Image J. software. The Shapiro-Wilk test was used to evaluate the parametric distribution of the data. The data were submitted to the ANOVA test to verify the difference between the area values obtained and the Dunnet post-hoc test to detect the differences in the comparison between the groups (Software GraphPAD Prism, USA). The level of significance of p <0.05 was considered. RESULTS AND CONCLUSION: There was an association between tooth extraction and mechanical morphological deformation of the mandibular condyle of rats. The extraction of the right upper central incisor tooth interferes with mandibular condylar morphology. The data of the present study could be used as support for future researches based on three-dimensional computerized microtomography (Microct-3D) as well as immunohistochemical analyzes.
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INTRODUCTION
Mechanical stress is recognized as an important factor affecting bone metabolism (Zernicke et al., 2006; Skerry, 2008). The reduction of mechanical stimulation can significantly decrease bone mass (LeBlanc et al., 2007) while habitual exercise increases or maintains bone mass (Bassey et al., 1994). These changes in the mechanical stress distribution lead to functional adaptation in the bone tissue (Zernicke et al., 2006; Skerry, 2008). Similarly, during the period of growth of the mandibular condyle, changes occur in the thickness of the cortical bone and in the three-dimensional architecture of the temporomandibular joint (TMJ) bone trabeculae (Nagahara et al., 1999; Springe et al., 2002).
Studies in humans suggest that changes occur in the bone tissue of the mandibular condyle in response to new distributions of functional load caused by occlusal changes (Parker, 1993; Huja et al., 2008). These phenomena are important because they will affect the functional adaptation of the mandibular condyles (De Boever et al., 2000; Ueki et al., 2006). However, the exact mechanism of these effects has not been fully elucidated.
Bone metabolism is constantly balanced by remodeling through bone formation and resorption. When functional adaptation occurs in bone tissue, the cellular activities of bone and bone resorption cells must change. The bone metabolism is an important indicator during the process of functional adaptation of the bone tissue in response to occlusal alterations such as dental loss. However, no research has evaluated the dynamics of bone metabolism of the mandibular condyles as a result of the change in functional loads from the extraction of the incisive tooth in rats.
In the present study, the histomorphometry analysis was used to evaluate the dynamics of the mandibular condyle metabolism of rats submitted to upper incisor extraction on the right side. Thus, the purpose of this study was to investigate the influence of unilateral anterior dental extraction and mandibular condyle bone morphology in rats.
MATERIAL AND METHODS
All procedures performed on the animals were approved (protocol CEUA nº4674-1/2017-A) by the Animal Research Ethics Committee of the State University of Campinas (Anexo 2).
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Twenty-two male rats (Rattus norvegicus albinus), Wistar linage, 2 months old (200-250g) were used, from the Multidisciplinary Center for Biological Research in the Laboratory Animal Science area - CEMIB-UNICAMP. The rats were kept in the FOP / UNICAMP in collective cages (four animals / box), with temperature at 22 ± 2 ° C, controlled light cycle (12/12 h) and free access to water and feed.
Experimental draw
The rats were randomly assigned to different groups for the experiments:
- Control Group (n = 6): the normal dentition constituting the control group was maintained. Euthanasia occurred within 14 days after day 0 of the dental extraction surgery.
- Experimental group (n = 18): extraction of the upper central incisor tooth (right side) was performed, and euthanasia occurred in periods 5 (n = 6), 7 (n = 6) and 14 (n = 6) days after day 0 of the dental extraction surgery.
Dental extraction surgery
The procedure was performed under general anesthesia using ketamine solution (40-87 mg / kg) and muscle relaxant xilasin (5-13 mg / kg) intraperitoneally. Once sedation and signs of anesthesia were verified, antissepsis of the operative field with iodinated polyvinylpyrrolidone (Riodeine Indústria Química e Farmacêutica Rio Química, São José do Rio Preto, São Paulo, Brazil) was performed, and then the extraction surgery of the right upper incisor, using instruments specially adapted for this purpose (Okamoto and De Russo, 1973). The gingival mucosa was sutured with polyglactin 910 yarn (Vicryl 4.0 - Jhonson & Johnson, New Brunswick, NJ, USA).
Euthanasia
The euthanasia of the animals was performed in the periods previously proposed for both the control and the experimental group using excessive anesthetic dose, as recommended by the ethical principles for the use of laboratory animals of CEUA / UNICAMP. The head was disrupted from the body and dissected for block removal and fixed in 10% formalin solution and 0.1M phosphate buffer (pH 7.4) for 24h at 4 ° C.
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After euthanasia, the rats of all groups had their right and left temporomandibular joints (TMJs) removed and separated. TMJs were fixed in 10% formaldehyde and decalcified in 3.14% EDTA (Merck®, EMD Millipore Corporation, Germany). After the decalcification was verified, the pieces were placed in the histotechnical machine for dehydration (alcohol sequence), diaphanization (with xylol), infiltration and inclusion in Paraffin - Paraplast ® (Embedding Media, McCormick Scientific, USA). The obtained blocks were cut in microtome Lupetec MRP03 (Laboratory Equipment Technology for LTDA - ME, São Carlos - SP) in sections with 5 μm thickness and mounted on slides. The sections were sagittal (lateral to medial). The images of the slides were captured under light microscopy (LeicaR DMLB, Heerbrugg, Switzerland) coupled to the camera.
Qualitative analysis
Qualitative analysis of the mandibular condyle (both side) on each histological slide was performed on the 10x objective.
Quantitative analysis (Histomorphometry)
Quantitative analysis of the mandibular condyle (both side) on each histological slide was performed in ImageJ (National Institutes of Health) software. The method used was by marking the area (um2) of the mandibular condyle on the 10x objective.
Statistical analysis
For the evaluation of the parametric distribution of the data the Shapiro-Wilk test was used. The data were submitted to the ANOVA test to verify the difference between the obtained area values and Dunnet's post-hoc test to detect the differences in the comparison between the groups (Software GraphPAD Prism, USA). The level of significance of p <0.05 was considered.
RESULTS
Qualitative analysis
The figures 1 and 2 showed the photomicrograph of the histological slides from a period of 5, 7 and 14 days after extraction surgery and control group in both sides, right and left. We observed in the most representative area of the cytoarchitecture of each group through a 10x objective, which allowed for analyzing if the control group had normal morphology of the
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mandibular condyle. In the images obtained from the groups after surgery extraction, it was possible to observe bone deformation and large intertrabecular spaces, mainly in 5 days. The slides of the animals of 14 days we verified a normalization of the histological characteristics, and it was possible to notice small areas of connective tissue with presented good histological characteristics.
Figure 1. Histological images of TMJ (right side) in the period of 5, 7 and 14 days after the tooth extraction of groups. C: Control group. Objective: 10x.
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Figure 2. Histological images of TMJ (left side) in the period of 5, 7 and 14 days after the tooth extraction of groups. C: Control group. Objective: 10x.
Quantitative analysis (Histomorphometry) Right side
For the right side, ANOVA showed a significant difference (P <0.0001) when all periods were compared with the control group (Figure 3).
Table 1 shows the values corresponding to the comparisons between groups 5, 7 and 14 days with the control group, and Dunnet's post-hoc test detected a significant difference for the comparison of all groups.
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Figure 3. ANOVA test showed a significant difference (P <0.0001) for the right side.
Table 1. Comparisons of all groups.
Dunnett's Multiple Comparison Test Mean Diff. q P value 95% CI of diff
Control vs 5d 884000 46,97 P < 0.001 834800 to 933100 Control vs 7d 886300 50,20 P < 0.001 840200 to 932400 Control vs 14d 834300 44,33 P < 0.001 785200 to 883500
Left side
For the left side, ANOVA showed a significant difference (P <0.0001) when all periods were compared with the control group (Figure 4).
Table 2 shows the values corresponding to the comparisons between groups 5, 7 and 14 days with the control group, and Dunnet's post-hoc test detected a significant difference for the comparison of all groups.
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Figure 4. ANOVA test showed a significant difference (P <0.0001) for the left side.
Table 2. Comparisons of all groups.
Dunnett's Multiple Comparison Test Mean Diff. q P value 95% CI of diff Control vs 5d 1138000 42,77 P< 0.001 1068000 to 1209000 Control vs 7d 115900 43,56 P<0.001 1089000 to 12130000 Control vs 14d 1113000 41,82 P<0.001 1042000 to 1183000
DISCUSSION
Our results suggest that tooth extraction, or the lack of a previous tooth, may lead to a worsening of the bone microstructure, reduction of osteogenesis and promotion of bone resorption. Wistar rats were used in the present study due to the short growth time and to the previous reports in which the functional masticatory loss was induced in rats by dental extraction and soft foods (Pirttiniemi et al., 2004; Hichijo et al., 2015).
The quantitative analysis of the mandibular condyle on the right side, that is, on the same side of the upper incisor, extraction surgery, showed a morphological difference in the mandibular condyle bone structure when compared to the control group in all periods (Figure2). When groups 5, 7 and 14 days were compared with the control group, gradual increases were also observed. The morphology of the mandibular condyle structure is essential for adaptation
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to increased mechanical stress, and the dynamics of bone metabolism can be an effective indicator with which to evaluate functional adaptation of these anatomic structure.
The opposite side to the upper incisor, that is, the left side, also showed significant morphological differences when comparing all periods with the control group (Figure 3) as well as between groups 5, 7 and 14 days with the control group. The histological results suggest that the dental extraction of the right upper central incisor affects the condylar morphology of both sides. Wolff's law states that "bone is formed and reabsorbed according to the dynamic environment, adjusting its shape and mass in a way that is adequate to maintain its strength" (Frost 1994). When we observed the mandibular condyle bone of the rats in the present study it seems that such changes occur in the trabecular bone in the extraction groups in both the right and left condyles probably due to the reduction of the masticatory stimulation exerted on the mandibular condyle as a result of the dental extraction.
CONCLUSION
We concluded that the dental extraction of the right upper central incisor interferes on the mandibular condylar morphology. The data of the present study could be used as support for future researches based on three-dimensional computerized microtomography (Microct-3D) as well as immunohistochemical analyzes.
REFERENCES
1. Bassey EJ, Ramsdale SJ. Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int. 1994; 4: 72–75.
2. Endo Y, Mizutani H, Yasue K, Senga K, Ueda M. Influence of food consistency and dental extractions on the rat mandibular condyle: a morphological, histological and immunohistochemical study. J Craniomaxillofac Surg 1998; 26: 185–190.
3. Frost HM. Wolff’s Law and Structural Adaptations of Bone to Mechanical Usage: An Overview for Clinicians. The Angle Orthodontist. 1994; 64: 175-188.
4. Hichijo N, Tanaka E, Kawai N, van Ruijven LJ, Langenbach GE. Effects of Decreased Occlusal Loading during Growth on the Mandibular Bone Characteristics. PLoS ONE. 2015; 10: e0129290.
5. Huang Q, Opstelten D, Samman N, Tideman H. Experimentally induced unilateral tooth loss: histochemical studies of the temporomandibular joint. J Dent Res 2002; 81: 209–213.
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6. Huja SS, Rummel AM, Beck FM. Changes in mechanical properties of bone within the mandibular condyle with age. J Morphol 2008; 269: 138–143. De Boever JA, Carlsson GE, Klineberg IJ. Need for occlusal therapy and prosthodontic treatment in the management of temporomandibular disorders. Part II: Tooth loss and prosthodontic treatment. J Oral Rehabil 2000; 27: 647–659.
7. LeBlanc AD, Spector ER, Evans HJ, Sibonga JD. Skeletal responses to space flight and the bed rest analog: a review. J Musculoskelet Neuronal Interact. 2007; 7: 33–47.
8. Mulder L, van Ruijven LJ, Koolstra JH, van Eijden TM. The influence of mineralization on intratrabecular stress and strain distribution in developing trabecular bone. Ann Biomed Eng. 2007; 35: 1668–1677.
9. Nagahara K, Murata S, Nakamura S, Tsuchiya T. Displacement and stress distribution in the temporomandibular joint during clenching. Angle Orthod. 1999; 69: 372–379.
10. Parker MW. The significance of occlusion in restorative dentistry. Dent Clin North Am 1993; 37: 341–351.
11. Pileicikiene G, Surna A, Barauskas R, Surna R, Basevicius A. Finite element analysis of stresses in the maxillary and mandibular dental arches and TMJ articular discs during clenching into maximum intercuspation, anterior and unilateral posterior occlusion. Stomatologija 2007; 9: 121–128.
12. Pirttiniemi P, Kantomaa T, Sorsa T. Effect of Decreased Loading on the Metabolic Activity of the Mandibular Condylar Cartilage in the Rat. European Journal of Orthodontics. 2004; 26: 1-5.
13. Skerry TM. The response of bone to mechanical loading and disuse: fundamental principles and influences on osteoblast/osteocyte homeostasis. Arch Biochem Biophys 2008; 473: 117–123.
14. Springer IN, Suhr M, Fleiner B. Adaptive adjustment of the adolescent porcine mandibular condyle. Bone 2002; 31: 230-235.
15. Ueki K, Nakagawa K, Takatsuka S, Yamamoto E. The change of stress distribution on the condyle after mandibular setback surgery. Eur J Orthod 2006; 28: 433–439.
16. van Ruijven LJ, Giesen EB, Farella M, van Eijden TM. Prediction of mechanical properties of the cancellous bone of the mandibular condyle. J Dent Res 2003; 82: 819–823. 17. Zernicke R, MacKay C, Lorincz C. Mechanisms of boné remodeling during weight-bearing exercise. Appl Physiol Nutr Metab. 2006; 31: 655–660.
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3 CONCLUSÃO
A extração do dente incisivo central superior direito interfere na morfologia condilar mandibular.
Os dados do presente estudo poderão ser utilizados como suporte para futuras pesquisas baseadas em microtomografia computadorizadas tridimensional (Microct-3D) bem como análises imunohistoquimicas.
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REFERENCIAS*
1. Zernicke R, MacKay C, Lorincz C. Mechanisms of bone remodeling during weight bearing exercise. Appl Physiol Nutr Metab. 2006; 31: 655–660.
2. Skerry TM. The response of bone to mechanical loading and disuse: fundamental principles and influences on osteoblast/ osteocyte homeostasis. Arch Biochem Biophys. 2008; 473: 117– 123.
3. LeBlanc AD, Spector ER, Evans HJ, Sibonga JD. Skeletal responses to space flight and the bed rest analog: a review. J Musculoskelet Neuronal Interact. 2007; 7: 33–47.
4. Bassey EJ, Ramsdale SJ. Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int. 1994; 4: 72–75.
5. Nagahara K, Murata S, Nakamura S, Tsuchiya T. Displacement and stress distribution in the temporomandibular joint during clenching. Angle Orthod. 1999; 69: 372–379.
6. Springer IN, Suhr M, Fleiner B. Adaptive adjustment of the adolescent porcine mandibular condyle. Bone. 2002; 31: 230– 235.
7. Mulder L, van Ruijven LJ, Koolstra JH, van Eijden TM. The influence of mineralization on intratrabecular stress and strain distribution in developing trabecular bone. Ann Biomed Eng. 2007; 35: 1668–1677.
8. van Ruijven LJ, Giesen EB, Farella M, van Eijden TM. Prediction of mechanical properties of the cancellous bone of the mandibular condyle. J Dent Res. 2003; 82: 819–823.
9. Pileicikiene G, Surna A, Barauskas R, Surna R, Basevicius A. Finite element analysis of stresses in the maxillary and mandibular dental arches and TMJ articular discs during clenching into maximum intercuspation, anterior and unilateral posterior occlusion. Stomatologija. 2007; 9: 121–128.
*De acordo com as normas da UNICAMP/FOP, baseadas na padronização do International Committee of Medical Journal Editors – Vancouver Group. Abreviatura dos periódicos em conformidade com o PubMed.
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10. Parker MW. The significance of occlusion in restorative dentistry. Dent Clin North Am. 1993; 37: 341–351.
11. Huja SS, Rummel AM, Beck FM. Changes in mechanical properties of bone within the mandibular condyle with age. J Morphol. 2008; 269: 138–143.
12. De Boever JA, Carlsson GE, Klineberg IJ. Need for occlusal therapy and prosthodontic treatment in the management of temporomandibular disorders. Part II: Tooth loss and prosthodontic treatment. J Oral Rehabil. 2000; 27: 647–659.
13. Ueki K, Nakagawa K, Takatsuka S, Yamamoto E. The change of stress distribution on the condyle after mandibular setback surgery. Eur J Orthod. 2006; 28: 433–439.
14. Endo Y, Mizutani H, Yasue K, Senga K, Ueda M. Influence of food consistency and dental extractions on the rat mandibular condyle: a morphological, histological and immunohistochemical study. J Craniomaxillofac Surg. 1998; 26: 185–190.
15. Huang Q, Opstelten D, Samman N, Tideman H. Experimentally induced unilateral tooth loss: histochemical studies of the temporomandibular joint. J Dent Res. 2002; 81: 209–213.
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