Effect of probiotic therapy on periodontal tissues and intestinal mucosa of rats with ligature-induced periodontitis
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Abstract
Introduction: As periodontitis is caused by dysbiotic biofilm, it is believed that therapy with probiotics can act to control the mechanisms of adhesion and colonization, competing with invading microorganisms. Objective: Evaluate probiotic therapy effect on periodontal tissues and intestinal mucosa of rats with ligature-induced periodontitis. Methods: 32 Wistar rats were divided into four groups (n=8): Control Group (CG); Periodontal disease (PD); Probiotic (PROB); PD + probiotic (PDPRO). PD and PDPRO received a ligature over the first lower molars and PROB and PDPRO the probiotic Lactobacillus acidophilus based were given orally for 44 days. The animals were euthanized and the blood was collected for evaluation of triglyceride and cholesterol concentrations. The hemimandibles were collected for histomorphometric and radiographic analysis. The duodenum was removed for morphological evaluation and gingival tissue around the molars was collected for analysis of IL-17. Results: The ANOVA one-way test was used followed by Tukey Test. PDPRO had a significantly lower bone loss than the PD (p<0.05) and a smaller number of osteoclasts on PDPRO when compared to the PD. As for IL-17, there was a decrease in the PDPRO when compared to the PD. The histomorphometry of the duodenum showed that there was a significant increase in the width of the villi in PROB only. Conclusion: The therapy with probiotics was effective to avoid the development of periodontitis by reducing alveolar bone loss and inflammation modulation and increasing the width of the duodenum villi, which may help to restabilize the balance of the gastrointestinal tract.
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Van Dyke TE, Bartold PM, Reynolds EC. The nexus between periodontal inflammation and dysbiosis. Front Immunol. 2020;11:511. https://doi.org/10.3389/fimmu.2020.00511
Emecen-Huja P, Li HF, Ebersole JL, Lambert J, Bush H. Epidemiologic evaluation of Nhanes for environmental factors and periodontal disease. Sci Rep. 2019;9(1):8227. https://doi.org/10.1038/s41598-019-44445-3
Ebersole JL, Kirakodo S, Novak MJ, Stromberg AJ, Shen S, Orraca L, et al. Cytokine gene expression profiles during initiation, progression and resolution of periodontitis. J Clin Periodontol. 2014;41(9):853-61. https://doi.org/10.1111/jcpe.12286
Raff A, Hunt LC. Probiotics for periodontal health: A review of the literature. J Dent Hyg. 2012;86(2):71-81.
Foureaux RC, Messora MR, Oliveira LFF, Napimoga MH, Pereira AN, Ferreira MS, et al. Effects of probiotic therapy on metabolic and inflammatory parameters of rats with ligature-induced periodontitis associated with restraint stress. J Periodontol. 2014;85(7):975-83. https://doi.org/10.1902/jop.2013.130356
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506-14. https://doi.org/10.1038/nrgastro.2014.66
Teughels W, Essche MV, Sliepen I, Quirynen M. Probiotics and oral healthcare. Periodontol 2000. 2008;48:111-47. https://doi.org/10.1111/j.1600-0757.2008.00254.x
Bastos EM, Brito F, Silva RM, Fischer RG, Figueredo CMS. Probióticos na terapia periodontal. Rev Bras Odontol. 2012;69(2):224-7.
Marchi L, Palezi SC, Pietta GM. Caracterização e avaliação sensorial do Kefir tradicional e derivados. Unoesc Cienc. 2015;(esp):15-22.
Ince G, Gursoy H, Ipçi SD, Cakar G, Emekli-Alturfan E, Yılmaz S. Clinical and biochemical evaluation of Lactobacillus Reuteri containing lozenges as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol. 2015;86(6):746-54. https://doi.org/10.1902/jop.2015.140612
Uyeda M, Buonom HC, Gonzaga MF, Carvalho FLO. Probióticos e prebióticos: benefícios acerca da literatura. Rev Saude UniAGES. 2016;1(1):33-57.
Markowiak P, Śliżewska K. Effects of Probiotics, Prebiotics, and Synbiotics on Human Health. Nutrients. 2017;9(9):1021. https://doi.org/10.3390/nu9091021
Albuquerque-Souza E, Balzarini D, Ando-Suguimoto ES, Ishikawa KH, Simionato MRL, Holzhausen M, et al. Probiotics alter the immune response of gingival epitelial cells challenged by Porphyromonas gingivalis. J Periodontal Res . 2019;54(2):115-27. https://doi.org/10.1111/jre.12608
Stamatova I, Meurman JH. Probiotics: health benefits in the mouth. Am J Dent. 2009;22(6):329-38.
Nassar PO, Nassar CA, Guimarães MR, Aquino SG, Andia DC, Muscara MN, et al. Simvastatin therapy in cyclosporine A-induced alveolar bone loss in rats. J Periodontal Res. 2009;44(4):479-88. https://doi.org/10.1111/j.1600-0765.2008.01143.x
Nassar CA, Nassar PO, Inagaki NS, Girelli Junior C. Efeito de antiinflamatório no desenvolvimento da doença periodontal induzida. Avaliação radiográfica em ratos. Rev Odonto Unesp. 2003;32(2):125-30.
Junqueira LC, Carneiro J, Abrahamsohn P. Histologia básica: texto e atlas. 13 ed. Rio de Janeiro: Guanabara Koogan, 2017.
Ribeiro CAO, Grotzner SR, Reis Filho HS. Técnicas e Métodos para utilização prática em microscopia. São Paulo: Santos, 2012.
Messora MR, Oliveira LFF, Foureaux RC, Taba Jr M, Zangerônimo MG, Furlaneto FA, et al. Probiotic therapy reduces periodontal tissue destruction and improves the intestinal morphology in rats with ligature-induced periodontitis. J Periodontol. 2013;84(12):1818-26. https://doi.org/10.1902/jop.2013.120644
Riccia DND, Bizzini F, Perilli MG, Polimeni A, Trinchieri V, Amicosante G, et al. Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis. 2007;13(4):376-85. https://doi.org/10.1111/j.1601-0825.2006.01291.x
Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksen-Blicks C. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand. 2009;67(1):19-24. https://doi.org/10.1080/00016350802516170
Gatej SM., Marino V, Bright R, Fitzsimmons TR, Gully N, Zilm P, et al. Probiotic Lactobacillus rhamnosus GG prevents alveolar bone loss in a mouse model of experimental periodontitis. J Clinical Periodontol. 2018;45(2):204-12. https://doi.org/10.1111/jcpe.12838
Zhao JJ, Feng XP, Zhang XL, Le KY. Effect of Porphyromonas gingivalis and Lactobacillus acidophilus on secretion of IL1B, IL6, and IL8 by gingival epithelial cells. Inflammation. 2012;35(4):1330-7. https://doi.org/10.1007/s10753-012-9446-5
Reddy MS, Babu MN. How beneficial is bacterial prophylaxis to periodontal health? J Investig Clin Dent. 2011;2(2):95-101. https://doi.org/10.1111/j.2041-1626.2010.00034.x
Park SY, Kim YH, Kim EK, Ryu EY, Lee SJ. Heme oxygenase-1 signals are involved in preferential inhibition of pro-inflammatory cytokine release by surfactin in cells activated with Porphyromonas gingivalis lipopolysaccharide. Chem Biol Interact. 2010;188(3):437-45. https://doi.org/10.1016/j.cbi.2010.09.007
Meurman JH, Stamatova I. Probiotics: contributions to oral health. Oral Dis. 2007;13:443-51. https://doi.org/10.1111/j.1601-0825.2007.01386.x
Maekawa T, Hajishengallis G. Topical treatment with probiotic Lactobacillus brevisCD2 inhibits experimental periodontal inflammation and bone loss. J Periodontal Res. 2014;49(6):785-91. https://doi.org/10.1111/jre.12164
Huang Y, Wang J, Cheng Y, Zheng Y. The hypocholesterolaemic effects of Lactobacillus acidophilus American Type Culture Collection 4356 in rats are mediated by the down-regulation of Niemann- Pick C1-Like 1. Br J Nutr. 2010;104(6):807-12. https://doi.org/10.1017/S0007114510001285
Jeun J, Kim S, Cho SY, Jun HJ, Park HJ, Seo JG, et al. Hypocholesterolemic effects of Lactobacillus plantarum KCTC3928 by increased bile acid excretion in C57BL/6 mice. Nutrition. 2010;26(3):321-30. https://doi.org/10.1016/j.nut.2009.04.011
Wang J, Zhang H, Chen X, Chen Y, Menghebilige, Bao Q. Selection of potential probiotic lactobacilli for cholesterol-lowering properties and their effect on cholesterol metabolism in rats fed a high-lipid diet. J Dairy Sci. 2012;95(4):1645-54. https://doi.org/10.3168/jds.2011-4768
Awaisheh SS, Khalifeh MS, Al-Ruwaili MA, Khalil OM, Al-Ameri OH, Al-Noivo R. Effect of supplementation of probiotics and phytosterols aloneor in combination on serum and hepatic lipid profiles and thyroid hormones of hypercholesterolemic rats. J Dairy Sci. 2013;96(1):9-15. https://doi.org/10.3168/jds.2012-5442
Modanêsi PVG, Mercer NS, Bernardi JFB. Efeitos do uso de probióticos na hipercolesterolemia. Rev Pesq Saude. 2016;17(1):47-50.
Galeano JAC, Herrera A, Suescun JP. The probiotic Enterococcus faecium modifies the intestinal morphometric parameters in weaning piglets. Rev Fac Nac Agron. 2016;69(1):7803-11. https://doi.org/10.15446/rfna.v69n1.54748