Clinical Oral Investigations

, Volume 22, Issue 3, pp 1197–1208 | Cite as

Influence of obesity on experimental periodontitis in rats: histopathological, histometric and immunohistochemical study

  • Elizangela Partata Zuza
  • Valdir Gouveia Garcia
  • Letícia Helena Theodoro
  • Edilson Ervolino
  • Luiz Fernando Veloso Favero
  • Mariéllen Longo
  • Fernando Salimon Ribeiro
  • Alex Tadeu Martins
  • Luís Carlos Spolidorio
  • José Antônio Sampaio Zuanon
  • Benedicto Egbert Corrêa de Toledo
  • Juliana Rico Pires
Original Article

Abstract

Objectives

This study assessed the influence of obesity on the progression of ligature-induced periodontitis in rats.

Materials and methods

Forty-eight adult Wistar rats were randomly divided into two groups: the HL group (n = 24) was fed high-fat animal food to induce obesity, and the NL group (n = 24) was fed normolipidic animal food. Obesity was induced within a period of 120 days, and the induction of experimental periodontitis (EP) was subsequently performed for 30 days. The animals were euthanized after 7, 15, and 30 days, and the jaws were removed for histopathological, histometric, and immunohistochemical analyses. Tartrate-resistant acid phosphatase (TRAP), receptor activator of nuclear factor kappa beta ligand (RANKL), and osteoprotegerin (OPG) were analyzed via immunolabeling.

Results

Histological findings indicated that the inflammation was more extensive and lasted longer in the HL⁄EP; however, advanced destruction also occurred in the NL/EP. Greater bone loss was verified in the HL/EP group (2.28 ± 0.35) in the period of 7 days than in the NL/EP group (1.2 ± 0.29). High immunolabeling was identified in the HL/EP group in the initial periods for RANKL and TRAP, whereas the NL⁄EP group presented with moderate immunolabeling for both factors. The HL/EP and NL/EP groups showed low immunolabeling for OPG.

Conclusions

Obesity induced by a high-fat diet influenced alveolar bone metabolism when associated with experimental periodontitis and caused a more severe local inflammatory response and alveolar bone loss.

Clinical relevance

Obesity is related to greater alveolar bone loss and an accentuated local inflammatory response, which may be reflected in the clinical severity of periodontitis and dental loss.

Keywords

Periodontitis Alveolar bone loss Obesity Body weight Rats Inflammation 

Notes

Acknowledgements

We thank the vivarium technician Darcy Thomaz de Aquino (in memoriam) and Professor Patrícia Rodella for the laboratory analyses at UNIFEB.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Informed consent

For this type of study, formal consent is not required.

Supplementary material

784_2017_2207_MOESM1_ESM.docx (15 kb)
Table 1 (DOCX 15 kb)

References

  1. 1.
    Williams RC (1990) Periodontal disease. N Engl J Med 322:373–382CrossRefPubMedGoogle Scholar
  2. 2.
    Graves DT, Li J, Cochran DL (2011) Inflammation and uncoupling as mechanisms of periodontal bone loss. J Dent Res 90:143–153CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Zuza EP, Barroso EM, Carrareto ALV, Pires JR, Carlos IZ, Theodoro LH, Toledo BE (2011) The role of obesity as a modifying factor in patients undergoing non-surgical periodontal therapy. J Periodontol 82:676–682CrossRefPubMedGoogle Scholar
  4. 4.
    Ritchie CS (2007) Obesity and periodontal disease. Periodontol 2000(44):154–163CrossRefGoogle Scholar
  5. 5.
    Boesing F, Patiño JSR, da Silva VRG, Moreira EAM (2009) The interface between obesity and periodontitis with emphasis on oxidative stress and inflammatory response. Obes Rev 10:290–297CrossRefPubMedGoogle Scholar
  6. 6.
    Pischon N, Heng N, Bernimoulin J-P, Kleber B-M, Willich SN, Pischon T (2007) Obesity, inflammation, and periodontal disease. J Dent Res 86:400–409CrossRefPubMedGoogle Scholar
  7. 7.
    Chaffee BW, Weston SJ (2010) Association between chronic periodontal disease and obesity: a systematic review and meta-analysis. J Periodontol 81:1708–1724CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Suvan J, D'Aiuto F, Moles DR, Petrie A, Donos N (2011) Association between overweight/obesity and periodontitis in adults. A systematic review. Obes Rev 12:381–404CrossRefGoogle Scholar
  9. 9.
    Amar S, Zhou Q, Shaik-Dasthagirisaheb Y, Leeman S (2007) Diet-induced obesity in mice causes changes in imune responses and bone loss manifested by bacterial challenge. Proc Natl Acad Sci U S A 104:20466–20471CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Nascimento CM, Cassol T, Silva FS, Bonfleur ML, Nassar CA, Nassar PO (2013) Radiographic evaluation of the effect of obesity on alveolar bone loss in rats with ligature-induced periodontal disease. Diabetes Metab Syndr Obes 6:365–370PubMedPubMedCentralGoogle Scholar
  11. 11.
    Simch RP, Gaio EJ, Rösing CK (2008) Effect of body weight in the pathogenesis of ligature-induced periodontal disease in Wistar rats. Acta Odontol Scand 66:130–134CrossRefPubMedGoogle Scholar
  12. 12.
    Endo Y, Tomofuji T, Ekuni D, Irie K, Azuma T, Tamaki N, Yamamoto T, Morita M (2010) Experimental periodontitis induces gene expression of proinflammatory cytokines in liver and white adipose tissues in obesity. J Periodontol 81:520–526CrossRefPubMedGoogle Scholar
  13. 13.
    Verzeletti GN, Gaio EJ, Linhares DS, Rösing CK (2012) Effect of obesity on alveolar bone loss in experimental periodontitis in Wistar rats. J Appl Oral Sci 20:218–221CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Cabeço LC, Akiba M, Calsa MS, Sartori DRS, Vicentini-Paulino MLM, Pinheiro DF (2010) High-fat diet with soy flour as protein source: use in selection of mice prone and obesity resistant (in Portuguese). Rev Nutr 23:417–424CrossRefGoogle Scholar
  15. 15.
    Dong H, Altomonte J, Morral N, Meseck M, Thung SN, Woo SL (2002) Basal insulin gene expression significantly improves conventional insulin therapy in type 1 diabetic rats. Diabetes 51:130–138CrossRefPubMedGoogle Scholar
  16. 16.
    Almeida JM, Theodoro LH, Bosco AF, Nagata MJH, Bonfante S, Garcia VG (2008) Treatment of experimental periodontal disease by photodinamic therapy in rats with diabetes. J Periodontol 79:2156–2165CrossRefPubMedGoogle Scholar
  17. 17.
    Garcia VG, Longo M, Gualberto Júnior EC, Bosco AF, Nagata MJ, Ervolino E, Theodoro LH (2014) Effect of the concentration of phenothiazine photosensitizers in antimicrobial photodynamic therapy on bone loss and the immune inflammatory response of induced periodontitis in rats. J Periodontal Res 49:584–594CrossRefPubMedGoogle Scholar
  18. 18.
    Gomes DA, Pires JR, Zuza EP, Muscara MN, Herrera BS, Spolidorio LC, Toledo BE, Spolidorio DM (2009) Myeloperoxidase as inflammatory marker of periodontal disease: experimental study in rats. Immunol Investig 38:117–122CrossRefGoogle Scholar
  19. 19.
    Gomes DA, Spolidorio DM, Pepato MT, Zuza EP, de Toledo BE, Gonçalves A, Spolidorio LC, Pires JR (2009) Effect of induced diabetes mellitus on alveolar bone loss after 30 days of ligature-induced periodontal disease. J Int Acad Periodontol 11:188–192PubMedGoogle Scholar
  20. 20.
    Lisboa MR, Gondim DV, Ervolino E et al (2015) Effects of electroacupuncture on experimental periodontitis in rats. J Periodontol 86:801–811CrossRefPubMedGoogle Scholar
  21. 21.
    Kim YD, Kim SS, Hwang DS et al (2007) Effect of low-level laser treatment after installation of dental titanium implant-immunohistochemical study of RANKL, RANK, OPG: an experimental study in rats. Lasers Surg Med 39:441–450CrossRefPubMedGoogle Scholar
  22. 22.
    Felipetti FA, Silva EO, Rangel ALCA et al (2014) Evaluation of alveolar bone mandibular of rats obese induced at monosodium glutamate undergoing modified duodenal-jejunal bypass surgery. J Endocrinol Metab 14:93–100Google Scholar
  23. 23.
    Fujita Y, Maki K (2016) High-fat diet-induced obesity triggers alveolar bone loss and spontaneous periodontal disease in growing mice. BMC Obes 3:1CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Perlstein MI, Bissada NF (1977) Influence of obesity and hypertension on the severity of periodontitis in rats. Oral Surg Oral Med Oral Pathol 43:707–719CrossRefPubMedGoogle Scholar
  25. 25.
    Akram Z, Abduljabbar T, Abu Hassan MI, Javed F, Vohra F (2016) Cytokine profile in chronic periodontitis patients with and without obesity: a systematic review and meta-analysis. Dis Markers 2016:4801418CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Almeida JM, Theodoro LH, Bosco AF, Nagata MJ, Oshiiwa M, Garcia VG (2007) Influence of photodynamic therapy on the development of ligature-induced periodontitis in rats. J Periodontol 78:566–575CrossRefPubMedGoogle Scholar
  27. 27.
    Deschner J, Eick S, Damanaki A, Nokhbehsaim M (2014) The role of adipokines in periodontal infection and healing. Mol Oral Microbiol 29:258–269CrossRefPubMedGoogle Scholar
  28. 28.
    Khosla S (2001) Minireview: the OPG/ RANKL/RANK system. Endocrinol 142:5050–5055CrossRefGoogle Scholar
  29. 29.
    Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ (2009) Bone-marrow adipocytes as negative regulators of the haemotopoietic microenvironment. Nature 460:259–263CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wilkins LM, Kaye EK, Wang HY, Rogus J, Doucette-Stamm L, Komman K, Garcia RI (2017) Influence of obesity on periodontitis progression is conditional on interleukin-1 inflammatory genetic variation. J Periodontol 88:59–68CrossRefPubMedGoogle Scholar
  31. 31.
    Stanton MC, Chen SC, Jackson JV et al (2011) Inflammatory signals shift from adipose to liver during high fat feeding and influence the development of steatohepatitis in mice. J Inflamm 8:8CrossRefGoogle Scholar
  32. 32.
    Xu H, Barnes GT, Yang Q et al (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821–1830CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Buckman LB, Hasty AH, Flaherty DK et al (2014) Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav Immun 35:33–42CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Elizangela Partata Zuza
    • 1
    • 2
  • Valdir Gouveia Garcia
    • 3
  • Letícia Helena Theodoro
    • 3
  • Edilson Ervolino
    • 4
  • Luiz Fernando Veloso Favero
    • 5
  • Mariéllen Longo
    • 3
  • Fernando Salimon Ribeiro
    • 5
  • Alex Tadeu Martins
    • 5
  • Luís Carlos Spolidorio
    • 6
  • José Antônio Sampaio Zuanon
    • 6
  • Benedicto Egbert Corrêa de Toledo
    • 7
  • Juliana Rico Pires
    • 5
  1. 1.Department of Periodontology, School of DentistryFluminense Federal University (UFF)Rio de JaneiroBrazil
  2. 2.Elizangela Partata ZuzaInstituto de Saúde de Nova Friburgo (ISNF)—UFFRio de JaneiroBrazil
  3. 3.Department of Surgery and Integrated Clinic, School of DentistrySão Paulo State University (Unesp)AraçatubaBrazil
  4. 4.Department of Basic Science, School of DentistrySão Paulo State University (Unesp)AraçatubaBrazil
  5. 5.Department of Dentistry, School of DentistryEducational Foundation of Barretos (Unifeb)BarretosBrazil
  6. 6.Department of Physiology and Pathology, School of DentistrySão Paulo State University (Unesp)AraraquaraBrazil
  7. 7.Department of Diagnosis and Surgery, School of DentistrySão Paulo State University (Unesp)AraraquaraBrazil

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