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Erschienen in: Inflammation 6/2017

18.08.2017 | ORIGINAL ARTICLE

Experimental Periodontitis in the Potentialization of the Effects of Immobilism in the Skeletal Striated Muscle

verfasst von: Marcela Aparecida Leite, Tatiane Morgenstern de Mattia, Camila Mayumi Martin Kakihata, Bruna Martinazzo Bortolini, Pedro Henrique de Carli Rodrigues, Gladson Ricardo Flor Bertolini, Rose Meire Costa Brancalhão, Lucinéia de Fátima Chasko Ribeiro, Carlos Augusto Nassar, Patrícia Oehlmeyer Nassar

Erschienen in: Inflammation | Ausgabe 6/2017

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Abstract

This study aims to evaluate if ligature-induced periodontitis can potentiates the deleterious effects of immobilization in the skeletal striated muscle, contributing to the development of muscle atrophy due to disuse. Forty Wistar rats were divided into four groups: (1) Control Group (CG), (2) Periodontal Disease (PDG), (3) Immobilized (IG), and (4) Immobilized with Periodontal Disease (IPDG). Periodontal disease was induced for 30 days, with ligature method, and the immobilization was performed with cast bandage for 15 days. Prior to euthanasia, nociceptive threshold and muscular grasping force were evaluated. Afterwards, the soleus muscle was dissected and processed for sarcomere counting and morphological/morphometric analysis. For data analysis, was used the one-way ANOVA and post-test Tukey (p < 0.05). The IG and IPDG presented lower muscle weight, lower muscular grip strength, and less number of sarcomeres compared to CG. The PDG showed reduction of muscle strength and nociceptive threshold after 15 days of periodontal disease and increased connective tissue compared to CG. The IPDG presented lower muscle length and nociceptive threshold. The IG presented reduction in cross-sectional area and smaller diameter, increase in the number of nuclei and a nucleus/fiber ratio, decrease in the number of capillaries and capillary/fiber ratio, with increase in connective tissue. The IPDG had increased nucleus/fiber ratio, decreased capillaries, and increased connective tissue when compared to the IG. The IPDG presented greater muscle tissue degeneration and increased inflammatory cells compared to the other groups. Ligature-induced periodontitis potentiated the deleterious effects of immobilization of the skeletal striated muscle.
Literatur
1.
Zurück zum Zitat Garlet, G.P., A.M.F. Aranha, E.M. Silveira, A.E. Vieira, C.M. Queiroz-Junior, M.F.M. Madeira, S.Y. Fukada, and T.A. Silva. 2012. The role of chemokines and cytokines in the pathogenesis of periodontal and periapical lesions: current concepts. In Cell and molecular biology, immunology and clinical basis, ed. InTech, 219–264. Rijeka: Croatia. doi:10.5772/27252. Garlet, G.P., A.M.F. Aranha, E.M. Silveira, A.E. Vieira, C.M. Queiroz-Junior, M.F.M. Madeira, S.Y. Fukada, and T.A. Silva. 2012. The role of chemokines and cytokines in the pathogenesis of periodontal and periapical lesions: current concepts. In Cell and molecular biology, immunology and clinical basis, ed. InTech, 219–264. Rijeka: Croatia. doi:10.​5772/​27252.
2.
Zurück zum Zitat Vettore, M.V., R.A.A. Marques, and M.A. Peres. 2010. Desigualdades sociais e doença periodontal no estudo SBBrasil 2010: abordagem multinível. Revista Saúde Pública 47 (Supl3): 29–39. Vettore, M.V., R.A.A. Marques, and M.A. Peres. 2010. Desigualdades sociais e doença periodontal no estudo SBBrasil 2010: abordagem multinível. Revista Saúde Pública 47 (Supl3): 29–39.
3.
Zurück zum Zitat Craig, R.G., A.M. Pernat, R. Pecoits-Filho, N.W. Levin, and P. Kotanko. 2013. Periodontal diseases and systemic inflammation. Seminars in Dialysis 26 (1): 16–39.CrossRef Craig, R.G., A.M. Pernat, R. Pecoits-Filho, N.W. Levin, and P. Kotanko. 2013. Periodontal diseases and systemic inflammation. Seminars in Dialysis 26 (1): 16–39.CrossRef
4.
Zurück zum Zitat Khalaf, H., J. Lönn, and T. Bengtsson. 2014. Cytokines and chemokines are differentially expressed in patients with periodontitis: possible role for TGF-β1 as a marker for disease progression. Cytokine 67 (1): 29–35.CrossRefPubMed Khalaf, H., J. Lönn, and T. Bengtsson. 2014. Cytokines and chemokines are differentially expressed in patients with periodontitis: possible role for TGF-β1 as a marker for disease progression. Cytokine 67 (1): 29–35.CrossRefPubMed
5.
Zurück zum Zitat Leishman, S.J., G.J. Seymour, and P.J. Ford. 2013. Local and systemic inflammatory responses to experimentally induced gingivitis. Disease Markers 35 (5): 543–549.CrossRefPubMedPubMedCentral Leishman, S.J., G.J. Seymour, and P.J. Ford. 2013. Local and systemic inflammatory responses to experimentally induced gingivitis. Disease Markers 35 (5): 543–549.CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Ramseier, C.A., J.S. Kinney, A.E. Herr, T. Braun, J.V. Sugai, C.A. Shelburne, L.A. Rayburn, H.M. Tran, A.K. Singh, and W.V. Giannobile. 2009. Identification of pathogen and host-response markers correlated with periodontal disease. Journal of Periodontology 80 (3): 436–446.CrossRefPubMed Ramseier, C.A., J.S. Kinney, A.E. Herr, T. Braun, J.V. Sugai, C.A. Shelburne, L.A. Rayburn, H.M. Tran, A.K. Singh, and W.V. Giannobile. 2009. Identification of pathogen and host-response markers correlated with periodontal disease. Journal of Periodontology 80 (3): 436–446.CrossRefPubMed
7.
Zurück zum Zitat Winkelman, C. Inactivity and inflammation: selected cytokines as biologic mediators in muscle dysfunction during critical illness. AACN Clinical Issues 15 (1): 74–82. Winkelman, C. Inactivity and inflammation: selected cytokines as biologic mediators in muscle dysfunction during critical illness. AACN Clinical Issues 15 (1): 74–82.
8.
Zurück zum Zitat Haddad, F., F. Zaldivar, D.M. Cooper, and G.R. Adams. 2005. IL-6-induced skeletal muscle atrophy. Journal of Applied Physiology (1985) 98 (3): 911–917.CrossRef Haddad, F., F. Zaldivar, D.M. Cooper, and G.R. Adams. 2005. IL-6-induced skeletal muscle atrophy. Journal of Applied Physiology (1985) 98 (3): 911–917.CrossRef
9.
Zurück zum Zitat Lang, C.H., R.A. Frost, and T.C. Vary. 2007. Regulation of muscle protein synthesis during sepsis and inflammation. American Journal of Physiology 293 (2): E453–E459.PubMed Lang, C.H., R.A. Frost, and T.C. Vary. 2007. Regulation of muscle protein synthesis during sepsis and inflammation. American Journal of Physiology 293 (2): E453–E459.PubMed
10.
Zurück zum Zitat Poulsen, J.B. 2012. Impaired physical function, loss of muscle mass and assessment of biomechanical properties in critical ill patients. Danish Medical Journal 59 (11): B4544.PubMed Poulsen, J.B. 2012. Impaired physical function, loss of muscle mass and assessment of biomechanical properties in critical ill patients. Danish Medical Journal 59 (11): B4544.PubMed
11.
Zurück zum Zitat Tsujinaka, T., J. Fujita, C. Ebisui, M. Yano, E. Kominami, K. Suzuki, K. Tanaka, A. Katsume, Y. Ohsugi, H. Shiozaki, and M. Monden. 1996. Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. The Journal of Clinical Investigation 97 (1): 244–249.CrossRefPubMedPubMedCentral Tsujinaka, T., J. Fujita, C. Ebisui, M. Yano, E. Kominami, K. Suzuki, K. Tanaka, A. Katsume, Y. Ohsugi, H. Shiozaki, and M. Monden. 1996. Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice. The Journal of Clinical Investigation 97 (1): 244–249.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Zamir, O., P.O. Hasselgren, S.L. Kunkel, J. Frederick, T. Higashiguchi, and J.E. Fischer. 1992. Evidence that tumor necrosis factor participates in the regulation of muscle proteolysis during sepsis. Archives of Surgery 127 (2): 170–174.CrossRefPubMed Zamir, O., P.O. Hasselgren, S.L. Kunkel, J. Frederick, T. Higashiguchi, and J.E. Fischer. 1992. Evidence that tumor necrosis factor participates in the regulation of muscle proteolysis during sepsis. Archives of Surgery 127 (2): 170–174.CrossRefPubMed
13.
Zurück zum Zitat De Letter, M.A., P.I. Schmitz, L.H. Visser, F.M. Verheul, R.L.L.A. Schellens, D.A.W. Op De Coul, and F.G.M. Van Der Meché. 2001. Risk factors for the development of polyneuropathy and myopathy in critically ill patients. Critical Care Medicine 29 (12): 2281–2286.CrossRefPubMed De Letter, M.A., P.I. Schmitz, L.H. Visser, F.M. Verheul, R.L.L.A. Schellens, D.A.W. Op De Coul, and F.G.M. Van Der Meché. 2001. Risk factors for the development of polyneuropathy and myopathy in critically ill patients. Critical Care Medicine 29 (12): 2281–2286.CrossRefPubMed
14.
Zurück zum Zitat Langhans, C., S. Weber-Carstens, F. Schmidt, J. Hamati, M. Kny, X. Zhu, T. Wollersheim, S. Koch, M. Krebs, H. Schulz, D. Lodka, K. Saar, S. Labeit, C. Spies, N. Hubner, J. Spranger, S. Spuler, M. Boschmann, G. Dittmar, G. Butler-Browne, V. Mouly, and J. Fielitz. 2014. Inflammation-induced acute phase response in skeletal muscle and critical illness myopathy. PloS One 9 (3): e92048.CrossRefPubMedPubMedCentral Langhans, C., S. Weber-Carstens, F. Schmidt, J. Hamati, M. Kny, X. Zhu, T. Wollersheim, S. Koch, M. Krebs, H. Schulz, D. Lodka, K. Saar, S. Labeit, C. Spies, N. Hubner, J. Spranger, S. Spuler, M. Boschmann, G. Dittmar, G. Butler-Browne, V. Mouly, and J. Fielitz. 2014. Inflammation-induced acute phase response in skeletal muscle and critical illness myopathy. PloS One 9 (3): e92048.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Ochala, J., A. Gustafson, M.L. Diez, G. Renaud, M. Li, S. Aare, R. Qaisar, V.C. Banduseela, Y. Hedstrom, X. Tang, B. Dworkin, G.C. Ford, K.S. Nair, S. Perera, M. Gautel, and L. Larsson. 2011. Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. The Journal of Physiology 15 (589): 2007–2026.CrossRef Ochala, J., A. Gustafson, M.L. Diez, G. Renaud, M. Li, S. Aare, R. Qaisar, V.C. Banduseela, Y. Hedstrom, X. Tang, B. Dworkin, G.C. Ford, K.S. Nair, S. Perera, M. Gautel, and L. Larsson. 2011. Preferential skeletal muscle myosin loss in response to mechanical silencing in a novel rat intensive care unit model: underlying mechanisms. The Journal of Physiology 15 (589): 2007–2026.CrossRef
16.
Zurück zum Zitat Fink, H., M. Helming, C. Unterbuchner, A. Lenz, F. Neff, J.A.J. Martyn, and M. Blobner. 2008. Systemic inflammatory response syndrome increases immobility-induced neuromuscular weakness. Critical Care Medicine 36 (3): 910–916.CrossRefPubMed Fink, H., M. Helming, C. Unterbuchner, A. Lenz, F. Neff, J.A.J. Martyn, and M. Blobner. 2008. Systemic inflammatory response syndrome increases immobility-induced neuromuscular weakness. Critical Care Medicine 36 (3): 910–916.CrossRefPubMed
17.
Zurück zum Zitat Poulsen, J.B., K. Moller, C.V. Jensen, S. Weisdorf, H. Kehlet, and A. Perner. 2011. Effect of transcutaneous electrical muscle stimulation on muscle volume in patients with septic shock. Critical Care Medicine 39 (3): 456–461.CrossRefPubMed Poulsen, J.B., K. Moller, C.V. Jensen, S. Weisdorf, H. Kehlet, and A. Perner. 2011. Effect of transcutaneous electrical muscle stimulation on muscle volume in patients with septic shock. Critical Care Medicine 39 (3): 456–461.CrossRefPubMed
18.
Zurück zum Zitat Nassar, P.O., C.A. Nassar, M.R. Guimarães, S.G. Aquino, D.C. Andia, M.N. Muscara, D.M.P. Spolidorio, C. Rossa Jr., and L.C. Spolidorio. 2009. Simvastatin therapy in cyclosporine A-induced alveolar bone loss in rats. Journal of Periodontal Research 44 (4): 479–488.CrossRefPubMed Nassar, P.O., C.A. Nassar, M.R. Guimarães, S.G. Aquino, D.C. Andia, M.N. Muscara, D.M.P. Spolidorio, C. Rossa Jr., and L.C. Spolidorio. 2009. Simvastatin therapy in cyclosporine A-induced alveolar bone loss in rats. Journal of Periodontal Research 44 (4): 479–488.CrossRefPubMed
19.
Zurück zum Zitat Carvalho, C.M.M., A.C. Shimano, and J.B. Volpon. 2002. Efeitos da imobilização e do exercício físico em algumas propriedades mecânicas do músculo esquelético. Revista Brasileira de Engenharia Biomédica 18 (2): 65–73. Carvalho, C.M.M., A.C. Shimano, and J.B. Volpon. 2002. Efeitos da imobilização e do exercício físico em algumas propriedades mecânicas do músculo esquelético. Revista Brasileira de Engenharia Biomédica 18 (2): 65–73.
20.
Zurück zum Zitat Kunz, R.I., J.G. Coradini, L.I. Silva, G.R.F. Bertolini, R.M.C. Brancalhão, and L.F.C. Ribeiro. 2014. Effects of immobilization and remobilization on the ankle joint in Wistar rats. Brazilian Journal of Medical and Biological Research 47 (10): 842–849.CrossRefPubMedPubMedCentral Kunz, R.I., J.G. Coradini, L.I. Silva, G.R.F. Bertolini, R.M.C. Brancalhão, and L.F.C. Ribeiro. 2014. Effects of immobilization and remobilization on the ankle joint in Wistar rats. Brazilian Journal of Medical and Biological Research 47 (10): 842–849.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Marcioli, M.A.R., J.G. Coradini, R.I. Kunz, L.F.C. Ribeiro, R.M.C. Brancalhão, and G.R.F. Bertolini. 2013. Nociceptive and histomorphometric evaluation of neural mobilization in experimental injury of the median nerve. The Scientific World Journal 2013: 1–6.CrossRef Marcioli, M.A.R., J.G. Coradini, R.I. Kunz, L.F.C. Ribeiro, R.M.C. Brancalhão, and G.R.F. Bertolini. 2013. Nociceptive and histomorphometric evaluation of neural mobilization in experimental injury of the median nerve. The Scientific World Journal 2013: 1–6.CrossRef
22.
Zurück zum Zitat Vivancos, G.G., W.A. Verri Jr., T.M. Cunha, I.R.S. Schivo, C.A. Parada, F.Q. Cunha, and S.H. Ferreira. 2004. An electronic pressure-meter nociception paw test for rats. Brazilian Journal of Medical and Biological Research 37 (3): 391–399.CrossRefPubMed Vivancos, G.G., W.A. Verri Jr., T.M. Cunha, I.R.S. Schivo, C.A. Parada, F.Q. Cunha, and S.H. Ferreira. 2004. An electronic pressure-meter nociception paw test for rats. Brazilian Journal of Medical and Biological Research 37 (3): 391–399.CrossRefPubMed
23.
Zurück zum Zitat Bertelli, J.A., and J.C. Mira. 1995. The grasping test: a simple behavioral method for objective quantitative assessment of peripheral nerve regeneration in the rat. Journal of Neuroscience Methods 58 (1–2): 151–155.CrossRefPubMed Bertelli, J.A., and J.C. Mira. 1995. The grasping test: a simple behavioral method for objective quantitative assessment of peripheral nerve regeneration in the rat. Journal of Neuroscience Methods 58 (1–2): 151–155.CrossRefPubMed
24.
Zurück zum Zitat Coradini, J.G., C.M.M. Kakihata, R.I. Kunz, T.K. Errero, M.L. Bonfleur, and G.R.F. Bertolini. 2015. Evaluation of grip strength in normal and obese Wistar rats submitted to swimming with overload after median nerve compression. Revista Brasileira de Reumatologia 55 (1): 43–47.CrossRef Coradini, J.G., C.M.M. Kakihata, R.I. Kunz, T.K. Errero, M.L. Bonfleur, and G.R.F. Bertolini. 2015. Evaluation of grip strength in normal and obese Wistar rats submitted to swimming with overload after median nerve compression. Revista Brasileira de Reumatologia 55 (1): 43–47.CrossRef
25.
Zurück zum Zitat Junqueira, L.C., and L.M.M. Junqueira. 1983. Técnicas básicas de citologia e histologia. São Paulo: Santos. Junqueira, L.C., and L.M.M. Junqueira. 1983. Técnicas básicas de citologia e histologia. São Paulo: Santos.
26.
Zurück zum Zitat Coutinho, E.L., A.R.S. Gomes, C.N. França, J. Oishi, and T.F. Salvini. 2004. Effect of passive stretching on the immobilized soleus muscle fiber morphology. Brazilian Journal of Medical and Biological Research 37 (12): 1853–1861.CrossRefPubMed Coutinho, E.L., A.R.S. Gomes, C.N. França, J. Oishi, and T.F. Salvini. 2004. Effect of passive stretching on the immobilized soleus muscle fiber morphology. Brazilian Journal of Medical and Biological Research 37 (12): 1853–1861.CrossRefPubMed
27.
Zurück zum Zitat Williams, P.E., T. Catanese, E.G. Lucey, and G. Goldspink. 1988. The importance of stretch and contractile activity in the prevention of connective tissue accumulation in muscle. Journal of Anatomy 158: 109–114.PubMedPubMedCentral Williams, P.E., T. Catanese, E.G. Lucey, and G. Goldspink. 1988. The importance of stretch and contractile activity in the prevention of connective tissue accumulation in muscle. Journal of Anatomy 158: 109–114.PubMedPubMedCentral
28.
Zurück zum Zitat Carvalho, M.M., W.R. Martins, J.C. Blackzick, C.A.C. Júnior, H.A. De Souza, S.A.S. Kückelhaus, and M.R. Mota. 2013. Análise morfométrica dos efeitos da imobilização sobre o músculo gastrocnêmio de ratos. Universitas: Ciências da Saúde 11 (2): 99–106. Carvalho, M.M., W.R. Martins, J.C. Blackzick, C.A.C. Júnior, H.A. De Souza, S.A.S. Kückelhaus, and M.R. Mota. 2013. Análise morfométrica dos efeitos da imobilização sobre o músculo gastrocnêmio de ratos. Universitas: Ciências da Saúde 11 (2): 99–106.
29.
Zurück zum Zitat Konno, E.A.B., E.P.B. Alves, G.R.F. Bertolini, C.H. Barbieri, and N. Mazzer. 2008. Remobilização por alongamento estático cíclico em músculo sóleo de ratos imobilizados em encurtamento. Revista Brasileira de Medicina do Esporte 14 (2): 122–125.CrossRef Konno, E.A.B., E.P.B. Alves, G.R.F. Bertolini, C.H. Barbieri, and N. Mazzer. 2008. Remobilização por alongamento estático cíclico em músculo sóleo de ratos imobilizados em encurtamento. Revista Brasileira de Medicina do Esporte 14 (2): 122–125.CrossRef
30.
Zurück zum Zitat Silva, L.I., A. Meireles, C.M. Nascimento, B.P. Rocha, C.T. Rosa, L.F.C. Ribeiro, R.M.C. Brancalhão, and G.R.F. Bertolini. 2013. Avaliação de parâmetros histomorfométricos em sóleos de ratos submetidos à remobilização por salto em meio aquático. Revista Brasileira de Medicina do Esporte 19 (3): 219–222.CrossRef Silva, L.I., A. Meireles, C.M. Nascimento, B.P. Rocha, C.T. Rosa, L.F.C. Ribeiro, R.M.C. Brancalhão, and G.R.F. Bertolini. 2013. Avaliação de parâmetros histomorfométricos em sóleos de ratos submetidos à remobilização por salto em meio aquático. Revista Brasileira de Medicina do Esporte 19 (3): 219–222.CrossRef
31.
Zurück zum Zitat Miyachi, R., and T. Yamazaki. 2015. Effects of static interventions on disuse atrophy of the rat soleus muscle at different sites along its longitudinal axis. Journal of Physical Therapy Science 27 (7): 2317–2321.CrossRefPubMedPubMedCentral Miyachi, R., and T. Yamazaki. 2015. Effects of static interventions on disuse atrophy of the rat soleus muscle at different sites along its longitudinal axis. Journal of Physical Therapy Science 27 (7): 2317–2321.CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Zhong, H., R.R. Roy, B. Siengthai, and V.R. Edgerton. 2005. Effects of inactivity on fiber size and myonuclear number in rat soleus muscle. Journal of Applied Physiology (1985) 99 (4): 1494–1499.CrossRef Zhong, H., R.R. Roy, B. Siengthai, and V.R. Edgerton. 2005. Effects of inactivity on fiber size and myonuclear number in rat soleus muscle. Journal of Applied Physiology (1985) 99 (4): 1494–1499.CrossRef
33.
Zurück zum Zitat Kanazashi, M., Y. Okumura, S. Al-Nassan, S. Murakami, H. Kondo, F. Nagatomo, N. Fujita, A. Ishihara, R.R. Roy, and H. Fujino. 2013. Protective effects of astaxanthin on capillary regression in atrophied soleus muscle of rats. Acta Physiologica 207 (2): 405–415.CrossRefPubMed Kanazashi, M., Y. Okumura, S. Al-Nassan, S. Murakami, H. Kondo, F. Nagatomo, N. Fujita, A. Ishihara, R.R. Roy, and H. Fujino. 2013. Protective effects of astaxanthin on capillary regression in atrophied soleus muscle of rats. Acta Physiologica 207 (2): 405–415.CrossRefPubMed
34.
Zurück zum Zitat Kanazashi, M., M. Tanaka, S. Murakami, H. Kondo, F. Nagatomo, A. Ishihara, R.R. Roy, and H. Fujino. 2014. Amelioration of capillary regression and atrophy of the soleus muscle in hindlimb-unloaded rats by astaxanthin supplementation and intermittent loading. Experimental Physiology 99 (8): 1065–1077.CrossRefPubMed Kanazashi, M., M. Tanaka, S. Murakami, H. Kondo, F. Nagatomo, A. Ishihara, R.R. Roy, and H. Fujino. 2014. Amelioration of capillary regression and atrophy of the soleus muscle in hindlimb-unloaded rats by astaxanthin supplementation and intermittent loading. Experimental Physiology 99 (8): 1065–1077.CrossRefPubMed
35.
Zurück zum Zitat Pierre, N., Z. Appriou, A. Gratas-Delamarche, and F. Derbré. 2016. From physical inactivity to immobilization: dissecting the role of oxidative stress in skeletal muscle insulin resistance and atrophy. Free Radical Biology & Medicine 98: 197–207.CrossRef Pierre, N., Z. Appriou, A. Gratas-Delamarche, and F. Derbré. 2016. From physical inactivity to immobilization: dissecting the role of oxidative stress in skeletal muscle insulin resistance and atrophy. Free Radical Biology & Medicine 98: 197–207.CrossRef
36.
Zurück zum Zitat Talbert, E.E., A.J. Smuder, K. Min, O.S. Kwon, and S.K. Powers. 1985. Calpain and caspase-3 play required roles in immobilization-induced limb muscle atrophy. Journal of Applied Physiology 114 (10): 1482–1489.CrossRef Talbert, E.E., A.J. Smuder, K. Min, O.S. Kwon, and S.K. Powers. 1985. Calpain and caspase-3 play required roles in immobilization-induced limb muscle atrophy. Journal of Applied Physiology 114 (10): 1482–1489.CrossRef
37.
Zurück zum Zitat Huang, J., and N.E. Forsberg. 1998. Role of calpain in skeletal-muscle protein degradation. Proceedings of the National Academy of Sciences of the United States of America 95 (21): 12100–12105.CrossRefPubMedPubMedCentral Huang, J., and N.E. Forsberg. 1998. Role of calpain in skeletal-muscle protein degradation. Proceedings of the National Academy of Sciences of the United States of America 95 (21): 12100–12105.CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Nassar, C.A., R.C. De Moraes, M.B. Secundes, P. Bernardon, P.O. Nassar, and V. Camilotti. 2014. The effect of resin composites and polishing procedure on periodontal tissue parameters in patients with diabetes mellitus. The European Journal of Prosthodontics and Restorative Dentistry 22 (4): 146–151.PubMed Nassar, C.A., R.C. De Moraes, M.B. Secundes, P. Bernardon, P.O. Nassar, and V. Camilotti. 2014. The effect of resin composites and polishing procedure on periodontal tissue parameters in patients with diabetes mellitus. The European Journal of Prosthodontics and Restorative Dentistry 22 (4): 146–151.PubMed
39.
Zurück zum Zitat Brandelero, S., Jr., M.L. Bonfleur, R.A. Ribeiro, E.C. Vanzela, C.A. Nassar, P.O. Nassar, and S.L. Balbo. 2012. Decreased TNF-α gene expression in periodontal ligature in MSG-obese rats: a possible protective effect of hypothalamic obesity against periodontal disease? Archives of Oral Biology 57 (3): 300–306.CrossRefPubMed Brandelero, S., Jr., M.L. Bonfleur, R.A. Ribeiro, E.C. Vanzela, C.A. Nassar, P.O. Nassar, and S.L. Balbo. 2012. Decreased TNF-α gene expression in periodontal ligature in MSG-obese rats: a possible protective effect of hypothalamic obesity against periodontal disease? Archives of Oral Biology 57 (3): 300–306.CrossRefPubMed
40.
Zurück zum Zitat Do Nascimento, C.M., T. Cassol, F.S. Da Silva, M.L. Bonfleur, C.A. Nassar, and P.O. Nassar. 2013. Radiographic evaluation of the effect of obesity on alveolar bone in rats with ligature-induced periodontal disease. Diabetes, Metabolic Myndrome and Obesity 7 (6): 365–370. Do Nascimento, C.M., T. Cassol, F.S. Da Silva, M.L. Bonfleur, C.A. Nassar, and P.O. Nassar. 2013. Radiographic evaluation of the effect of obesity on alveolar bone in rats with ligature-induced periodontal disease. Diabetes, Metabolic Myndrome and Obesity 7 (6): 365–370.
41.
Zurück zum Zitat Toregeani, J.F., C.A. Nassar, P.O. Nassar, K.M. Toregeani, G.K. Gonzatto, R. Vendrame, J.S. Castilhos, L.S. Rotta, A.C. Reinheimer, A. Longoni, and M.W. Barcella. 2016. Evaluation of periodontitis treatment effects on carotid intima-media thickness and expression of laboratory markers related to atherosclerosis. General Dentistry 64 (1): 55–62.PubMed Toregeani, J.F., C.A. Nassar, P.O. Nassar, K.M. Toregeani, G.K. Gonzatto, R. Vendrame, J.S. Castilhos, L.S. Rotta, A.C. Reinheimer, A. Longoni, and M.W. Barcella. 2016. Evaluation of periodontitis treatment effects on carotid intima-media thickness and expression of laboratory markers related to atherosclerosis. General Dentistry 64 (1): 55–62.PubMed
42.
Zurück zum Zitat Oliveira, J.A.P., C.B. Hoppe, M.S. Gomes, F.S. Grecca, and A.N. Haas. 2015. Periodontal disease as a risk indicator for poor physical fitness: a cross-sectional observational study. Journal of Periodontology 86 (1): 44–52.CrossRefPubMed Oliveira, J.A.P., C.B. Hoppe, M.S. Gomes, F.S. Grecca, and A.N. Haas. 2015. Periodontal disease as a risk indicator for poor physical fitness: a cross-sectional observational study. Journal of Periodontology 86 (1): 44–52.CrossRefPubMed
43.
Zurück zum Zitat Eremenko, M., C. Pink, R. Biffar, C.O. Schmidt, T. Ittermann, T. Kocher, and P. Meisel. 2016. Cross-sectional association between physical strength, obesity, periodontitis and number of teeth in a general population. Journal of Clinical Periodontology 43 (5): 401–407.CrossRefPubMed Eremenko, M., C. Pink, R. Biffar, C.O. Schmidt, T. Ittermann, T. Kocher, and P. Meisel. 2016. Cross-sectional association between physical strength, obesity, periodontitis and number of teeth in a general population. Journal of Clinical Periodontology 43 (5): 401–407.CrossRefPubMed
44.
Zurück zum Zitat Caron, A.Z., G. Drouin, J. Desrosiers, F. Trensz, and G. Grenier. 2009. A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. Journal of Applied Physiology (1985) 106 (6): 2049–2059.CrossRef Caron, A.Z., G. Drouin, J. Desrosiers, F. Trensz, and G. Grenier. 2009. A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. Journal of Applied Physiology (1985) 106 (6): 2049–2059.CrossRef
45.
Zurück zum Zitat Liao, C.H., W. Fei, S.H. Shen, M.P. Yin, and C. Lu. 2014. Expression and distribution of TNF-α and PGE2 of periodontal tissues in rat periodontitis model. Asian Pacific Journal of Tropical Medicine 7 (5): 412–416.CrossRefPubMed Liao, C.H., W. Fei, S.H. Shen, M.P. Yin, and C. Lu. 2014. Expression and distribution of TNF-α and PGE2 of periodontal tissues in rat periodontitis model. Asian Pacific Journal of Tropical Medicine 7 (5): 412–416.CrossRefPubMed
46.
Zurück zum Zitat Da Costa, T. A., M .J .B. Silva, P. M. Alves, J. E. L. Chica, E. Z. Barcelos, M. A. A. Giani, G. P. Garlet, J. S. Silva, V. R. Júnior, D. B. R. Rodrigues, and C. R. B. Cardoso. 2015. Inflammation biomarkers of advanced disease in nongingival tissues of chronic periodontitis patients. Mediators of Inflammation 2015. Da Costa, T. A., M .J .B. Silva, P. M. Alves, J. E. L. Chica, E. Z. Barcelos, M. A. A. Giani, G. P. Garlet, J. S. Silva, V. R. Júnior, D. B. R. Rodrigues, and C. R. B. Cardoso. 2015. Inflammation biomarkers of advanced disease in nongingival tissues of chronic periodontitis patients. Mediators of Inflammation 2015.
47.
Zurück zum Zitat Reid, M.B., and Y.P. Li. 2001. Cytokines and oxidative signalling in skeletal muscle. Acta Physiolgica Scandinavica 171 (3): 225–232.CrossRef Reid, M.B., and Y.P. Li. 2001. Cytokines and oxidative signalling in skeletal muscle. Acta Physiolgica Scandinavica 171 (3): 225–232.CrossRef
48.
Zurück zum Zitat Li, Y.P., Y. Chen, J. John, J. Moylan, B. Jin, D.L. Mann, and M.B. Reid. 2015. TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. Federation of American Societies for Experimental Biology Journal 19 (3): 362–370.CrossRef Li, Y.P., Y. Chen, J. John, J. Moylan, B. Jin, D.L. Mann, and M.B. Reid. 2015. TNF-α acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. Federation of American Societies for Experimental Biology Journal 19 (3): 362–370.CrossRef
49.
Zurück zum Zitat Lin, S.Y., Y.Y. Wang, Y.H. Chuang, and C.J. Chen. 2016. Skeletal muscle proteolysis is associated with sympathetic activation and TNF-α-ubiquitin-proteasome pathway in liver cirrhotic rats. Journal of Gastroenterology and Hepatology 31 (4): 890–896.CrossRefPubMed Lin, S.Y., Y.Y. Wang, Y.H. Chuang, and C.J. Chen. 2016. Skeletal muscle proteolysis is associated with sympathetic activation and TNF-α-ubiquitin-proteasome pathway in liver cirrhotic rats. Journal of Gastroenterology and Hepatology 31 (4): 890–896.CrossRefPubMed
50.
Zurück zum Zitat Quintana, H.T., J.A. Bortolin, N.T. Da Silva, F.A.P. Ribeiro, E.A. Liberti, D.A. Ribeiro, and F. De Oliveira. 2015. Temporal study following burn injury in young rats is associated with skeletal muscle atrophy, inflammation and altered myogenic regulatory factors. Inflammation Research 64 (1): 53–62.CrossRefPubMed Quintana, H.T., J.A. Bortolin, N.T. Da Silva, F.A.P. Ribeiro, E.A. Liberti, D.A. Ribeiro, and F. De Oliveira. 2015. Temporal study following burn injury in young rats is associated with skeletal muscle atrophy, inflammation and altered myogenic regulatory factors. Inflammation Research 64 (1): 53–62.CrossRefPubMed
51.
Zurück zum Zitat Ferreira, R., M.J. Neuparth, A. Ascensão, J. Magalhães, J. Duarte, and F. Amado. 2004. Atrofia muscular esquelética. Modelos experimentais, manifestações teciduais e fisiopatologia. Revista Portuguesa de Ciências do Desporto 4 (3): 94–111.CrossRef Ferreira, R., M.J. Neuparth, A. Ascensão, J. Magalhães, J. Duarte, and F. Amado. 2004. Atrofia muscular esquelética. Modelos experimentais, manifestações teciduais e fisiopatologia. Revista Portuguesa de Ciências do Desporto 4 (3): 94–111.CrossRef
52.
Zurück zum Zitat Slimani, L., D. Micol, J. Amat, G. Delcros, B. Meunier, D. Taillandier, C. Polge, D. Béchet, D. Dardevet, B. Picard, D. Attaix, A. Listrat, and L. Combare. 2012. The worsening of tibialis anterior muscle atrophy during recovery post-immobilization correlates with enhanced connective tissue area, proteolysis, and apoptosis. American Journal of Physiology Endocrinology and Metabolism 303 (11): E1335–E1347.CrossRefPubMed Slimani, L., D. Micol, J. Amat, G. Delcros, B. Meunier, D. Taillandier, C. Polge, D. Béchet, D. Dardevet, B. Picard, D. Attaix, A. Listrat, and L. Combare. 2012. The worsening of tibialis anterior muscle atrophy during recovery post-immobilization correlates with enhanced connective tissue area, proteolysis, and apoptosis. American Journal of Physiology Endocrinology and Metabolism 303 (11): E1335–E1347.CrossRefPubMed
53.
Zurück zum Zitat Fernandes, K.C.B.G., M.L.O. Polacow, R.R. Guirro, G.E.R. Campos, M.C. Somazz, V.F. Pinto, C.B. Fuentes, and R.M. Teodori. 2005. Análise morfométrica dos tecidos muscular e conjuntivo após desnervação e estimulação elétrica de baixa frequência. Revista Brasileira de Fisioterapia 9 (2): 235–241. Fernandes, K.C.B.G., M.L.O. Polacow, R.R. Guirro, G.E.R. Campos, M.C. Somazz, V.F. Pinto, C.B. Fuentes, and R.M. Teodori. 2005. Análise morfométrica dos tecidos muscular e conjuntivo após desnervação e estimulação elétrica de baixa frequência. Revista Brasileira de Fisioterapia 9 (2): 235–241.
54.
Zurück zum Zitat Chuganji, S., J. Nakano, Y. Sekino, Y. Hamaue, J. Sakamoto, and M. Okita. 2015. Hyperalgesia in an immobilized rat hindlimb: effect of treadmill exercise using non-immobilized limbs. Neuroscience Letters 584: 66–70.CrossRefPubMed Chuganji, S., J. Nakano, Y. Sekino, Y. Hamaue, J. Sakamoto, and M. Okita. 2015. Hyperalgesia in an immobilized rat hindlimb: effect of treadmill exercise using non-immobilized limbs. Neuroscience Letters 584: 66–70.CrossRefPubMed
55.
Zurück zum Zitat Guo, T.Z., T. Weia, W.W. Lia, X.Q. Li, J.D. Clarkc, and W.S. Kingerya. 2014. Immobilization contributes to exaggerated neuropeptide signaling, inflammatory changes, and nociceptive sensitization after fracture in rats. The Journal of Pain 15 (10): 1033–1045.CrossRefPubMedPubMedCentral Guo, T.Z., T. Weia, W.W. Lia, X.Q. Li, J.D. Clarkc, and W.S. Kingerya. 2014. Immobilization contributes to exaggerated neuropeptide signaling, inflammatory changes, and nociceptive sensitization after fracture in rats. The Journal of Pain 15 (10): 1033–1045.CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Abramova, A.Y., A.Y. Kozlov, and S.S. Pertsov. 2014. Dynamics of changes in nociceptive reactions of rats after peripheral administration of lipopolysaccharide. Bulletin of Experimental Biology and Medicine 157 (4): 413–415.CrossRefPubMed Abramova, A.Y., A.Y. Kozlov, and S.S. Pertsov. 2014. Dynamics of changes in nociceptive reactions of rats after peripheral administration of lipopolysaccharide. Bulletin of Experimental Biology and Medicine 157 (4): 413–415.CrossRefPubMed
57.
Zurück zum Zitat Teixeira, M.J. Fisiopatologia da nocicepção e da supressão da dor. Jornal Brasileiro de Oclusão 1 (4): 329–334. Teixeira, M.J. Fisiopatologia da nocicepção e da supressão da dor. Jornal Brasileiro de Oclusão 1 (4): 329–334.
58.
Zurück zum Zitat Voisin, L., D. Breuillé, L. Combaret, C. Pouyet, D. Taillandier, E. Aurousseau, C. Obled, and D. Attaix. 1996. Muscle wasting in a rat model of long-lasting sepsis results from the activation of lysosomal, Ca21-activated, and ubiquitin-proteasome proteolytic pathways. The Journal of Clinical Investigation 97 (7): 1610–1617.CrossRefPubMedPubMedCentral Voisin, L., D. Breuillé, L. Combaret, C. Pouyet, D. Taillandier, E. Aurousseau, C. Obled, and D. Attaix. 1996. Muscle wasting in a rat model of long-lasting sepsis results from the activation of lysosomal, Ca21-activated, and ubiquitin-proteasome proteolytic pathways. The Journal of Clinical Investigation 97 (7): 1610–1617.CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat Breuille, D., M. Arnal, F. Rambourdin, G. Bayle, D. Levleux, and C. Obled. 1998. Sustained modifications of protein metabolism in various tissues in a rat model of long-lasting sepsis. Clinical Science 94 (4): 413–423.CrossRefPubMed Breuille, D., M. Arnal, F. Rambourdin, G. Bayle, D. Levleux, and C. Obled. 1998. Sustained modifications of protein metabolism in various tissues in a rat model of long-lasting sepsis. Clinical Science 94 (4): 413–423.CrossRefPubMed
60.
Zurück zum Zitat Rossignol, B., G. Gueret, J. Pennec, J. Morel, F. Rannou, M. Giroux-Metges, H. Talarmin, M. Gioux, and C.C. Arvieux. 2008. Effects of chronic sepsis on contractile properties of fast twitch muscle in an experimental model of critical illness neuromyopathy in the rat. Critical Care Medicine 36 (6): 1855–1863.CrossRefPubMed Rossignol, B., G. Gueret, J. Pennec, J. Morel, F. Rannou, M. Giroux-Metges, H. Talarmin, M. Gioux, and C.C. Arvieux. 2008. Effects of chronic sepsis on contractile properties of fast twitch muscle in an experimental model of critical illness neuromyopathy in the rat. Critical Care Medicine 36 (6): 1855–1863.CrossRefPubMed
61.
Zurück zum Zitat Ahlbeck, K., K. Fredriksson, O. Rooyackers, G. Maback, S. Remahl, T. Ansved, L. Eriksson, and P. Radell. 2009. Signs of critical illness polyneuropathy and myopathy can be seen early in the ICU course. Acta Anaesthesiologica Scandinavica 53 (6): 717–723.CrossRefPubMed Ahlbeck, K., K. Fredriksson, O. Rooyackers, G. Maback, S. Remahl, T. Ansved, L. Eriksson, and P. Radell. 2009. Signs of critical illness polyneuropathy and myopathy can be seen early in the ICU course. Acta Anaesthesiologica Scandinavica 53 (6): 717–723.CrossRefPubMed
62.
Zurück zum Zitat Z’graggen, W.J., L. Brander, D. Tuchscherer, O. Scheidegger, J. Takala, and H. Bostock. 2011. Muscle membrane dysfunction in critical illness myopathy assessed by velocity recovery cycles. Clinical Neurophysiology 122 (4): 834–841.CrossRefPubMed Z’graggen, W.J., L. Brander, D. Tuchscherer, O. Scheidegger, J. Takala, and H. Bostock. 2011. Muscle membrane dysfunction in critical illness myopathy assessed by velocity recovery cycles. Clinical Neurophysiology 122 (4): 834–841.CrossRefPubMed
Metadaten
Titel
Experimental Periodontitis in the Potentialization of the Effects of Immobilism in the Skeletal Striated Muscle
verfasst von
Marcela Aparecida Leite
Tatiane Morgenstern de Mattia
Camila Mayumi Martin Kakihata
Bruna Martinazzo Bortolini
Pedro Henrique de Carli Rodrigues
Gladson Ricardo Flor Bertolini
Rose Meire Costa Brancalhão
Lucinéia de Fátima Chasko Ribeiro
Carlos Augusto Nassar
Patrícia Oehlmeyer Nassar
Publikationsdatum
18.08.2017
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 6/2017
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-017-0640-3

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