Periodontal Disease Impairs Muscle Recovery by Modulating the Recruitment of Leukocytes

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Abstract

The purpose of this study is to analyze the impact of periodontal disease (PD) associated with physical exercise on inflammatory mediators and muscle repair. Twenty-four Wistar rats were divided into four groups: control (SH), healthy trained (TH), sedentary with PD (SP), and trained with PD (TP). PD was induced in groups SP and TP while the trained groups performed treadmill exercises for 8 weeks. For the analysis of IL-6, IL-10, TNF-α, and leukocyte count, we collected blood samples. Cryolesions were induced in the tibialis anterior and gastrocnemius, which were analyzed for morphological changes. The presence of PD modified leukocyte counts, while exercise showed an additive role. PD increased levels of IL-6, IL-10, and TNF-α, and physical exercise changed only values of IL-10. The association between physical exercise and PD was responsible for an increased concentration of leukocytes in the region of the inflammation. Serum levels of inflammatory markers were modified by PD and, when combined with exercise, may negatively modulate inflammation. The association between PD and physical exercise showed the most significant changes in the number of inflammatory cells and may negatively influence the process of muscle repair.

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  • 11 September 2020

    The original version of this article contained mistakes, and the authors would like to correct them.

References

  1. 1.

    Lasserre, J.F., M.C. Brecx, and S. Toma. 2018. Oral Microbes, Biofilms and Their Role in Periodontal and Peri-implant Diseases. Materials (Basel) 11: E1802.

    Google Scholar 

  2. 2.

    Irfan, U.M., D.V. Dawson, and N. Bissada. 2001. Epidemiology of periodontal disease: a review and clinical perspectives. Journal of the International Academy of Periodontology 3: 14–21.

    CAS  PubMed  Google Scholar 

  3. 3.

    Teles, R.P., V. Likhari, S.S. Socransky, and A.D. Haffajee. 2009. Salivary Cytokine Levels in Chronic Periodontitis and Periodontally Healthy Subjects. A cross-sectional Study. Journal of Periodontal Research 44: 411–417.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Keelan, J.A., P.M. Wong, P.S. Bird, and M.D. 2010. Mitchell. Innate inflammatory responses of human decidual cells to periodontopathic bacteria. American Journal of Obstetrics and Gynecology 202: 1–11.

    Google Scholar 

  5. 5.

    Eming, S.A., M. Hammerschmidt, T. Krieg, and U. Roers. 2009. Interrelation of immunity and tissue repair or regeneration. Seminars in Cell & Developmental Biology 20: 517–527.

    CAS  Google Scholar 

  6. 6.

    Panezai, J., A. Ghaffar, M. Altamash, K.G. Sundqvist, P.E. Engström, and A. Larsson. 2017. Correlation of serum cytokines, chemokines, growth factors and enzymes with periodontal disease parameters. PLoS One 12: e0188945.

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Kampits, C., M.M. Montenegro, I.W. Ribeiro, M.V. Furtado, C.A. Polanczyk, C.K. Rösing, and A.N. Haas. 2016. Periodontal disease and inflammatory blood cytokines in patients with stable coronary artery disease. Journal of Applied Oral Science 24: 352–358.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Seymour, G.J., P.J. Ford, M.P. Cullinan, S. Leishman, and K. Yamazaki. 2007. Relationship between periodontal infections and systemic disease. Clinical Microbiology and Infection 13: 3–10.

    CAS  PubMed  Google Scholar 

  9. 9.

    Leite, M.A., T.M. de Mattia, C.M.M. Kakihata, B.M. Bortolini, P.H. de Carli Rodrigues, G.R.F. Bertolini, R.M.C. Brancalhão, L.F.C. Ribeiro, C.A. Nassar, and P.O. Nassar. 2017. Experimental Periodontitis in the Potentialization of the Effects of Immobilism in the Skeletal Striated Muscle. Inflammation 40: 2000–2011.

    PubMed  Google Scholar 

  10. 10.

    Souza, B.C., M.E. Ribas, A.R. Oliveira, J.B. Burzlaff, and A.N. Haas. 2012. Impact of periodontal inflammation on changes of a marker of muscle injury in young soccer players during training. Revista Odonto Ciencia 27: 294–299.

    Google Scholar 

  11. 11.

    Souza, B.C., M.E. Ribas, A.L. Lopes, B.C. Teixeira, and M.L. Lamers. 2017. Periodontal disease influences the recovery processes in the muscles in trained mice. Journal of Physical Education and Sport 17: 572–581.

    Google Scholar 

  12. 12.

    Lieber, R.L., S. Shah, and J. Fridén. 2002. Cytoskeletal disruption after eccentric contraction-induced muscle injury. Clinical Orthopaedics 403: S90–S99.

    Google Scholar 

  13. 13.

    Paschalis, V., Y. Koutedakis, A.Z. Jamurtas, V. Mougios, and V. Baltzopoulos. 2005. Equal volumes of high and low intensity of eccentric exercise in relation to muscle damage and performance. Journal of Strength and Conditioning Research 19: 121–125.

    Google Scholar 

  14. 14.

    Paulsen, G., U.R. Mikkelsen, T. Raastad, and J.M. Peake. 2012. Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exercise Immunology Review 18: 42–97.

    PubMed  Google Scholar 

  15. 15.

    Soehnlein, O., and L. Lindbom. 2010. Phagocyte partnership during the onset and resolution of inflammation. Nature Reviews. Immunology 10: 427–439.

    CAS  PubMed  Google Scholar 

  16. 16.

    Malm, C. 2001. Exercise-induced muscle damage and inflammation: fact or fiction? Acta Physiologica Scandinavica 171: 233–239.

    CAS  PubMed  Google Scholar 

  17. 17.

    Tidball, J.G. 2005. Mechanical signal transduction in skeletal muscle growth and adaptation. Journal of Applied Physiology 98: 1900–1908.

    CAS  PubMed  Google Scholar 

  18. 18.

    Clarkson, P.M., and M.J. Hubal. 2002. Exercise-induced Muscle Damage in Humans. Am J Phys Rehabil 81: S52–S69.

    Google Scholar 

  19. 19.

    Proske, U., and D.L. Morgan. 2001. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. The Journal of Physiology 537: 333–345.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Cheung, K., P. Hume, and L. Maxwell. 2003. Delayed onset muscle soreness—treatment strategies and performance factors. Sports Medicine 33: 145–164.

    PubMed  Google Scholar 

  21. 21.

    Kimura, S., A. Nagai, T. Onitsuka, T. Koga, T. Fujiwara, H. Kaya, and S. Hamada. 2000. Induction of experimental periodontitis in mice with Porphyromonas gingivalis-adhered ligatures. Journal of Periodontology 71: 1167–1173.

    CAS  PubMed  Google Scholar 

  22. 22.

    Bak, E.J., H.G. Park, M. Kim, S.W. Kim, S. Kim, S.H. Choi, J.H. Cha, and Y.J. Yoo. 2010. The effect of metformin on alveolar bone in ligature-induced periodontitis in rats: a pilot study. Journal of Periodontology 81: 412–419.

    CAS  PubMed  Google Scholar 

  23. 23.

    Miyabara, E.H., M.S. Aoki, A.G. Soares, and A.S. Moriscot. 2005. Expression of tropism-related genes in regenerating skeletal muscle of rats treated with cyclosporin-A. Cell and Tissue Research 319: 479–489.

    CAS  PubMed  Google Scholar 

  24. 24.

    Gulati, G., J. Song, A.D. Florea, and J. Gong. 2013. Purpose and criteria for blood smear scan, blood, smear examination, and blood smear review. Annals of Laboratory Medicine 33: 1–7.

    PubMed  Google Scholar 

  25. 25.

    Ghermati, A., L. Corbin, G. Chabanne, C. Auger, J.P. Magnol, C. Fournel, J.C. Monier, J.L. Darlix, and D. Rigal. 2000. Canine large granular lymphocyte leukemia and its derived cell line produce infectious retroviral particles. Veterinary Pathology 37: 310–317.

    Google Scholar 

  26. 26.

    Battlehner, C.N., E.G. Caldini, J.C. Pereira, E.H. Luque, and G.S. Montes. 2003. How to measure the increase in elastic system fibres in the lamina propria of the uterine cervix of pregnant rats. Journal of Anatomy 203: 405–418.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Morath, V., M. Keuper, M. Rodriguez-Franco, S. Deswal, G. Fiala, B. Blumenthal, D. Kaschek, J. Timmer, G. Neuhaus, S. Ehl, O. Ronneberger, and W.W. Schamel. 2013. Semi-automatic determination of cell surface areas used in systems biology. Frontiers in Bioscience 5: 533–545.

    Google Scholar 

  28. 28.

    Howes, M.T., M. Kirkham, J. Riches, K. Cortese, P.J. Walser, F. Simpson, M.M. Hill, A. Jones, R. Rundmark, M.R. Lindsay, D.J. Hernandez-Deviez, G. Hadzic, R. McCluskey, L. Bashir, P. Liu, H. Pilch, P.J. McMahon, J.F. Robinson, S. Prefeito Hancock, and R.G. Parton. 2010. Clathrin-independent carriers form a high capacity endocytic sorting system at the leading edge of migrating cells. JCB 190: 675–691.

    CAS  PubMed  Google Scholar 

  29. 29.

    Sarjan, H.N., and H.N. Yajurvedi. 2019. Duration dependent effect of chronic stress on primary and secondary lymphoid organs and their reversibility in rats. Immunobiology 224: 133–141.

    Google Scholar 

  30. 30.

    Raica, M., S. Encică, A. Motoc, A.M. Cîmpean, T. Scridon, and M. Bârsan. 2006. Structural heterogeneity and immunohistochemical profile of Hassall corpuscles in normal human thymus. Annals of Anatomy 188: 345–352.

    PubMed  Google Scholar 

  31. 31.

    Villalta, S.A., C. Rinaldi, B. Deng, G. Liu, B. Fedor, and J.G. Tidball. 2011. Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Human Molecular Genetics 20: 790–805.

    CAS  PubMed  Google Scholar 

  32. 32.

    Tidball, J.G., and S.A. Villalta. 2010. Regulatory interactions between muscle and the immune system during muscle regeneration. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 298: 1173–1187.

    Google Scholar 

  33. 33.

    Noh, M.K., M. Jung, S.H. Kim, S.R. Lee, K.H. Park, D.H. Kim, H.H. Kim, and Y.G. Park. 2013. Assessment of IL-6, IL-8 and TNF-α levels in the gingival tissue of patients with periodontitis. Experimental and Therapeutic Medicine 6: 847–851.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Lomba, K.S.B., T.F.C. de Souza Breves Beiler, M.R.C. Sete, F.R. Pires, and C.M. da Silva Figueredo. 2015. Use of minimally invasive gingival biopsies in the study of inflammatory mediators expression and their correlation with gingival fluid in patients with chronic periodontitis. Indian Journal of Dental Research 26: 126–130.

    PubMed  Google Scholar 

  35. 35.

    Hoare, A., C. Soto, V. Rojas-Celis, and D. Bravo. 2019. Chronic Inflammation as a Link between Periodontitis and Carcinogenesis. Mediators of Inflammation 1029857.

  36. 36.

    Dias, I.H.K., I.L.C. Chapple, M. Milward, M.M. Grant, E. Hill, J. Brown, and H.R. Griffiths. 2013. Sulforaphane restores cellular glutathione levels and reduces chronic periodontitis neutrophils hyperactivity in vitro. PLoS One 8: e66407.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Chapple, L.C., and J.B. Matthews. 2007. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 (43): 160–232.

    Google Scholar 

  38. 38.

    Matthews, J.B., H.J. Wright, A. Roberts, P.R. Cooper, and I.L. Chapple. 2007. Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clinical and Experimental Immunology 147: 255–264.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Hill, E.E., E. Zack, C. Battaglini, M. Viru, A. Viru, and A.C. Hackney. 2008. Exercise and circulating cortisol levels: the intensity threshold effect. Journal of Endocrinological Investigation 31: 587–591.

    CAS  PubMed  Google Scholar 

  40. 40.

    Jin, R.M., J. Warunek, and E.A. Wohlfert. 2018. Therapeutic administration of IL-10 and amphiregulin alleviates chronic skeletal muscle inflammation and damage induced by infection. Immunohorizons 2: 142–154.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Lockhart, N.C., and S.V. Brooks. 2008. Neutrophil accumulation following passive stretches contributes to adaptations that reduce contraction-induced skeletal muscle injury in mice. Journal of Applied Physiology 104: 1109–1115.

    PubMed  Google Scholar 

  42. 42.

    Pizza, F.X., J.M. Peterson, J.H. Baas, and T.J. Koh. 2005. Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. The Journal of Physiology 562: 899–913.

    CAS  PubMed  Google Scholar 

  43. 43.

    Gordon, S., and P.R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nature Reviews. Immunology 5: 953–964.

    CAS  PubMed  Google Scholar 

  44. 44.

    Lagrota-Candido, J., I. Canella, D.F. Pinheiro, L.P. Santos-Silva, R.S. Ferreira, F.J. Guimarães-Joca, J. Lannes-Vieira, and T. Quirico-Santos. 2010. Characteristic pattern of skeletal muscle remodelling in different mouse strains. International Journal of Experimental Pathology 91: 522–529.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Perdiguero, E., Y. Kharraz, A.L. Serrano, and P. Munoz-Canoves. 2012. MKP-1 coordinates ordered macrophage-phenotype transitions essential for stem cell-dependent tissue repair. Cell Cycle 11: 877–886.

    CAS  PubMed  Google Scholar 

  46. 46.

    Cantini, M., E. Giurisato, C. Radu, S. Tiozzo, F. Pampinella, D. Senigaglia, L. Zaniolo, F. Mazzoleni, and L. Vitiello. 2002. Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurological Sciences 23: 189–194.

    CAS  PubMed  Google Scholar 

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Correspondence to Bárbara Capitanio de Souza.

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The original version of this article was revised: The production made a mistake in the article title where the word “Periodontal” was changed to “Periodical”.

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Supplemental Fig. 1

Replacing the thymic parenchyma by adipose tissue. V=Pp/Ptx100% formula was used to calculate the volumetric density of adipose tissue present in the thymic parenchyma, where Pp is the number of points Pt on fat cells and the number of points of the test system (A). SH: control, SP: sedentary with periodontal disease, TH: trained without periodontal disease, TP: trained with periodontal disease. Hematoxylin-eosin staining. 200X magnification (JPG 310 kb)

Supplemental Fig. 2

Test system for analysis of inflammatory intensity. V=Pp/Ptx100% formula was used to calculate the volumetric density of inflammatory cells, where Pp is the number of points on Pt inflammatory cells and the number of points of the test system. Hematoxylin-eosin staining. 400X magnification (JPG 148 kb)

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de Souza, B.C., Matte, B.F., Lopes, A.L. et al. Periodontal Disease Impairs Muscle Recovery by Modulating the Recruitment of Leukocytes . Inflammation 43, 382–391 (2020). https://doi.org/10.1007/s10753-019-01128-5

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KEY WORDS

  • physical education and training
  • athletic performance
  • inflammation
  • muscular diseases
  • oral health