Skip to main content
Top
Published in: Odontology 2/2018

01-04-2018 | Original Article

Effects of experimental periodontitis on the metabolic system in rats with diet-induced obesity (DIO): an analysis of serum biochemical parameters

Authors: Ryutaro Kuraji, Miyako Fujita, Hiroshi Ito, Shuichi Hashimoto, Yukihiro Numabe

Published in: Odontology | Issue 2/2018

Login to get access

Abstract

Recent studies have shown that periodontitis accelerates the progression of obesity-associated metabolic diseases. Thus, we examined the influence of periodontitis on serum biochemical parameters of metabolic disease in a diet-induced obesity (DIO) rat. First, we established the DIO model using ten male rats fed with either basal diet (lean group) or high-fat diet (DIO group) for 12 weeks. Second, to examine the interaction between periodontitis and obesity, we divided 24 DIO rats into the following four groups. (1) Porphyromonas gingivalis (Pg) group was applied with Pg around the maxillary first molar (M1). (2) Ligature group was applied with ligature placement around M1. (3) Ligature/Pg group was treated with both ligature placement and Pg. (4) Control was non-treatment group. Serum biochemical parameters and maxillary histopathology were evaluated at 12 weeks. The DIO model demonstrated significant increases in body weight, serum insulin, alanine aminotransaminase (ALT) levels, and insulin resistance (HOMA-IR) compared to the lean group. In the DIO ligature and ligature/Pg groups, alveolar bone resorption and inflammatory cell infiltration were significantly increased compared to the control. Serum levels of fasting glucose, lactate dehydrogenase, and uric acid were also significantly higher, while the liver damage markers ALT and aspartate aminotransferase were only higher in ligature/Pg group. However, we observed no significant differences between the Pg group and Control. The present study suggested a possibility that periodontitis induced by ligature placement changed serum metabolic parameter regarding organs such as the liver in DIO rat.
Literature
1.
2.
go back to reference Reilly MP, Lehrke M, Wolfe ML, Rohatgi A, Lazar MA, Rader DJ. Resistin is an inflammatory marker of atherosclerosis in humans. Circulation. 2005;22:932–9.CrossRef Reilly MP, Lehrke M, Wolfe ML, Rohatgi A, Lazar MA, Rader DJ. Resistin is an inflammatory marker of atherosclerosis in humans. Circulation. 2005;22:932–9.CrossRef
3.
go back to reference Ghanim H, Aljada A, Hofmeyer D, Syed T, Mohanty P, Dandona P. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 2004;21:1564–71.CrossRef Ghanim H, Aljada A, Hofmeyer D, Syed T, Mohanty P, Dandona P. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation. 2004;21:1564–71.CrossRef
4.
go back to reference Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;14:860–7.CrossRef Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;14:860–7.CrossRef
5.
go back to reference Hujoel PP, White BA, García RI, Listgarten MA. The dentogingival epithelial surface area revisited. J Periodontal Res. 2001;36:48–55.CrossRefPubMed Hujoel PP, White BA, García RI, Listgarten MA. The dentogingival epithelial surface area revisited. J Periodontal Res. 2001;36:48–55.CrossRefPubMed
6.
go back to reference Tonetti MS, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani AD, Vallance P, Deanfield J. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;1:911–20.CrossRef Tonetti MS, D’Aiuto F, Nibali L, Donald A, Storry C, Parkar M, Suvan J, Hingorani AD, Vallance P, Deanfield J. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;1:911–20.CrossRef
7.
go back to reference Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol. 1996;67:1085–93.CrossRef Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. J Periodontol. 1996;67:1085–93.CrossRef
8.
go back to reference Lafaurie GI, Mayorga-Fayad I, Torres MF, Castillo DM, Aya MR, Barón A, Hurtado PA. Periodontopathic microorganisms in peripheric blood after scaling and root planing. J Clin Periodontol. 2007;34:873–9.CrossRefPubMed Lafaurie GI, Mayorga-Fayad I, Torres MF, Castillo DM, Aya MR, Barón A, Hurtado PA. Periodontopathic microorganisms in peripheric blood after scaling and root planing. J Clin Periodontol. 2007;34:873–9.CrossRefPubMed
9.
go back to reference Lafaurie GI, Mayorga-Fayad I, Torres MF, Castillo DM, Aya MR, Barón A, Hurtado PA. Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J Periodontol. 2011;82:1469–77.CrossRef Lafaurie GI, Mayorga-Fayad I, Torres MF, Castillo DM, Aya MR, Barón A, Hurtado PA. Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J Periodontol. 2011;82:1469–77.CrossRef
10.
go back to reference Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic americans with type 2 diabetes. J Periodontol. 2008;79:637–46.CrossRefPubMed Ebersole JL, Holt SC, Hansard R, Novak MJ. Microbiologic and immunologic characteristics of periodontal disease in Hispanic americans with type 2 diabetes. J Periodontol. 2008;79:637–46.CrossRefPubMed
11.
go back to reference Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, Markland J, Robinson D, Elias B, Newkirk M, Toes RM, Huizinga TW, El-Gabalawy HS. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol. 2010;37:1105–12.CrossRefPubMed Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, Markland J, Robinson D, Elias B, Newkirk M, Toes RM, Huizinga TW, El-Gabalawy HS. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol. 2010;37:1105–12.CrossRefPubMed
12.
go back to reference Yoneda M, Naka S, Nakano K, Wada K, Endo H, Mawatari H, Imajo K, Nomura R, Hokamura K, Ono M, Murata S, Tohnai I, Sumida Y, Shima T, Kuboniwa M, Umemura K, Kamisaki Y, Amano A, Okanoue T, Ooshima T, Nakajima A. Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease. BMC Gastroenterol. 2012;12:16.CrossRefPubMedPubMedCentral Yoneda M, Naka S, Nakano K, Wada K, Endo H, Mawatari H, Imajo K, Nomura R, Hokamura K, Ono M, Murata S, Tohnai I, Sumida Y, Shima T, Kuboniwa M, Umemura K, Kamisaki Y, Amano A, Okanoue T, Ooshima T, Nakajima A. Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease. BMC Gastroenterol. 2012;12:16.CrossRefPubMedPubMedCentral
13.
go back to reference Han DH, Lim S, Paek D, Kim HD. Periodontitis could be related factors on metabolic syndrome among Koreans: a case-control study. J Clin Periodontol. 2012;39:30–7.CrossRefPubMed Han DH, Lim S, Paek D, Kim HD. Periodontitis could be related factors on metabolic syndrome among Koreans: a case-control study. J Clin Periodontol. 2012;39:30–7.CrossRefPubMed
14.
go back to reference Nibali L, D’Aiuto F, Griffiths G, Patel K, Suvan J, Tonetti MS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol. 2007;34:931–7.CrossRefPubMed Nibali L, D’Aiuto F, Griffiths G, Patel K, Suvan J, Tonetti MS. Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case-control study. J Clin Periodontol. 2007;34:931–7.CrossRefPubMed
15.
go back to reference Saito T, Shimazaki Y. Metabolic disorders related to obesity and periodontal disease. Periodontol. 2000;2007(43):254–66. Saito T, Shimazaki Y. Metabolic disorders related to obesity and periodontal disease. Periodontol. 2000;2007(43):254–66.
16.
go back to reference Ahmad A, Furuta M, Shinagawa T, Takeuchi K, Takeshita T, Shimazaki Y, Yamashita Y. Association of periodontal status with liver abnormalities and metabolic syndrome. J Oral Sci. 2015;57:335–43.CrossRefPubMed Ahmad A, Furuta M, Shinagawa T, Takeuchi K, Takeshita T, Shimazaki Y, Yamashita Y. Association of periodontal status with liver abnormalities and metabolic syndrome. J Oral Sci. 2015;57:335–43.CrossRefPubMed
17.
go back to reference Altay U, Gürgan CA, Ağbaht K. Changes in inflammatory and metabolic parameters after periodontal treatment in patients with and without obesity. J Periodontol. 2013;84:13–23.CrossRefPubMed Altay U, Gürgan CA, Ağbaht K. Changes in inflammatory and metabolic parameters after periodontal treatment in patients with and without obesity. J Periodontol. 2013;84:13–23.CrossRefPubMed
18.
go back to reference D’Aiuto F, Nibali L, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res. 2005;84:269–73.CrossRefPubMed D’Aiuto F, Nibali L, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res. 2005;84:269–73.CrossRefPubMed
19.
go back to reference Graziani F, Cei S, La Ferla F, Vano M, Gabriele M, Tonetti M. Effects of non-surgical periodontal therapy on the glomerular filtration rate of the kidney: an exploratory trial. J Clin Periodontol. 2010;37:638–43.CrossRefPubMed Graziani F, Cei S, La Ferla F, Vano M, Gabriele M, Tonetti M. Effects of non-surgical periodontal therapy on the glomerular filtration rate of the kidney: an exploratory trial. J Clin Periodontol. 2010;37:638–43.CrossRefPubMed
20.
go back to reference Kuraji R, Ito H, Fujita M, Ishiguro H, Hashimoto S, Numabe Y. Porphyromonas gingivalis induced periodontitis exacerbates progression of non-alcoholic steatohepatitis (NASH) in rats. Clinical and Experimental Dental Research. 2016;2:216–25.CrossRef Kuraji R, Ito H, Fujita M, Ishiguro H, Hashimoto S, Numabe Y. Porphyromonas gingivalis induced periodontitis exacerbates progression of non-alcoholic steatohepatitis (NASH) in rats. Clinical and Experimental Dental Research. 2016;2:216–25.CrossRef
21.
go back to reference Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring). 2011;19:1109–17.CrossRefPubMedPubMedCentral Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring). 2011;19:1109–17.CrossRefPubMedPubMedCentral
22.
go back to reference Atici K, Yamalik N, Eratalay K, Etikan I. Analysis of gingival crevicular fluid intracytoplasmic enzyme activity in patients with adult periodontitis and rapidly progressive periodontitis. A longitudinal study model with periodontal treatment. J Periodontol. 1998;69:1155–63.CrossRefPubMed Atici K, Yamalik N, Eratalay K, Etikan I. Analysis of gingival crevicular fluid intracytoplasmic enzyme activity in patients with adult periodontitis and rapidly progressive periodontitis. A longitudinal study model with periodontal treatment. J Periodontol. 1998;69:1155–63.CrossRefPubMed
23.
go back to reference Loo WY, Yue Y, Fan CB, Bai LJ, Dou YD, Wang M, Liang H, Cheung MN, Chow LW, Li JL, Tian Y, Qing L. Comparing serum levels of cardiac biomarkers in cancer patients receiving chemotherapy and subjects with chronic periodontitis. J Transl Med. 2012;19:S5.CrossRef Loo WY, Yue Y, Fan CB, Bai LJ, Dou YD, Wang M, Liang H, Cheung MN, Chow LW, Li JL, Tian Y, Qing L. Comparing serum levels of cardiac biomarkers in cancer patients receiving chemotherapy and subjects with chronic periodontitis. J Transl Med. 2012;19:S5.CrossRef
24.
go back to reference Caúla AL, Lira-Junior R, Tinoco EM, Fischer RG. Serum creatinine and alkaline phosphatase levels are associated with severe chronic periodontitis. J Periodontal Res. 2015;50:793–7.CrossRefPubMed Caúla AL, Lira-Junior R, Tinoco EM, Fischer RG. Serum creatinine and alkaline phosphatase levels are associated with severe chronic periodontitis. J Periodontal Res. 2015;50:793–7.CrossRefPubMed
25.
go back to reference Atici K, Yamalik N, Eratalay K, Etikan I. Analysis of gingival crevicular fluid intracytoplasmic enzyme activity in patients with adult periodontitis and rapidly progressive periodontitis. A longitudinal study model with periodontal treatment. J Periodontol. 1998;69:1155–63.CrossRefPubMed Atici K, Yamalik N, Eratalay K, Etikan I. Analysis of gingival crevicular fluid intracytoplasmic enzyme activity in patients with adult periodontitis and rapidly progressive periodontitis. A longitudinal study model with periodontal treatment. J Periodontol. 1998;69:1155–63.CrossRefPubMed
26.
go back to reference Shi D, Meng H, Xu L, Zhang L, Chen Z, Feng X, Lu R, Sun X, Ren X. Systemic inflammation markers in patients with aggressive periodontitis: a pilot study. J Periodontol. 2008;79:2340–6.CrossRefPubMed Shi D, Meng H, Xu L, Zhang L, Chen Z, Feng X, Lu R, Sun X, Ren X. Systemic inflammation markers in patients with aggressive periodontitis: a pilot study. J Periodontol. 2008;79:2340–6.CrossRefPubMed
27.
go back to reference Gaddale R, Mudda JA, Karthikeyan I, Desai SR, Shinde H, Deshpande P. Changes in cellular and molecular components of peripheral blood in patients with generalized aggressive periodontitis. J Investig Clin Dent. 2016;7:59–64.CrossRefPubMed Gaddale R, Mudda JA, Karthikeyan I, Desai SR, Shinde H, Deshpande P. Changes in cellular and molecular components of peripheral blood in patients with generalized aggressive periodontitis. J Investig Clin Dent. 2016;7:59–64.CrossRefPubMed
28.
go back to reference Saito T, Shimazaki Y, Koga T, Tsuzuki M, Ohshima A. Relationship between periodontitis and hepatic condition in Japanese women. J Int Acad Periodontol. 2006;8:89–95.PubMed Saito T, Shimazaki Y, Koga T, Tsuzuki M, Ohshima A. Relationship between periodontitis and hepatic condition in Japanese women. J Int Acad Periodontol. 2006;8:89–95.PubMed
29.
go back to reference Takahashi M, Ikemoto S, Ezaki O. Effect of the fat/carbohydrate ratio in the diet on obesity and oral glucose tolerance in C57BL/6 J mice. J Nutr Sci Vitaminol (Tokyo). 1999;45:583–93.CrossRefPubMed Takahashi M, Ikemoto S, Ezaki O. Effect of the fat/carbohydrate ratio in the diet on obesity and oral glucose tolerance in C57BL/6 J mice. J Nutr Sci Vitaminol (Tokyo). 1999;45:583–93.CrossRefPubMed
31.
go back to reference Watanabe K, Petro BJ, Shlimon AE, Unterman TG. Effect of periodontitis on insulin resistance and the onset of type 2 diabetes mellitus in Zucker diabetic fatty rats. J Periodontol. 2008;79:1208–16.CrossRefPubMed Watanabe K, Petro BJ, Shlimon AE, Unterman TG. Effect of periodontitis on insulin resistance and the onset of type 2 diabetes mellitus in Zucker diabetic fatty rats. J Periodontol. 2008;79:1208–16.CrossRefPubMed
32.
go back to reference Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontal. 2006;33:401–7.CrossRef Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontal. 2006;33:401–7.CrossRef
33.
go back to reference Lockhart PB, Brennan MT, Sasser HC, Fox PC, Paster BJ, Bahrani-Mougeot FK. Bacteremia associated with toothbrushing and dental extraction. Circulation. 2008;117:3118–25.CrossRefPubMedPubMedCentral Lockhart PB, Brennan MT, Sasser HC, Fox PC, Paster BJ, Bahrani-Mougeot FK. Bacteremia associated with toothbrushing and dental extraction. Circulation. 2008;117:3118–25.CrossRefPubMedPubMedCentral
34.
go back to reference Müller-Glauser W, Schroeder HE. The pocket epithelium: a light- and electronmicro- scopic study. J Periodontol. 1982;53:133–44.CrossRefPubMed Müller-Glauser W, Schroeder HE. The pocket epithelium: a light- and electronmicro- scopic study. J Periodontol. 1982;53:133–44.CrossRefPubMed
35.
go back to reference Hujoel PP, White BA. Garc.a RI, Listgarten MA. The dentogingival epithelial surface area revisited. J Periodontal Res. 2001;36:48–55.CrossRefPubMed Hujoel PP, White BA. Garc.a RI, Listgarten MA. The dentogingival epithelial surface area revisited. J Periodontal Res. 2001;36:48–55.CrossRefPubMed
36.
go back to reference Oz HS, Puleo DA. Animal models for periodontal disease. J Biomed Biotechnol. 2011;2011:1–8.CrossRef Oz HS, Puleo DA. Animal models for periodontal disease. J Biomed Biotechnol. 2011;2011:1–8.CrossRef
37.
go back to reference Evans RT, Klausen B, Ramamurthy NS, Golub LM, Sfintescu C, Genco RJ. Periodontopathic potential of two strains of Porphyromonas gingivalis in gnotobiotic rats. Arch Oral Biol. 1992;37:813–9.CrossRefPubMed Evans RT, Klausen B, Ramamurthy NS, Golub LM, Sfintescu C, Genco RJ. Periodontopathic potential of two strains of Porphyromonas gingivalis in gnotobiotic rats. Arch Oral Biol. 1992;37:813–9.CrossRefPubMed
38.
go back to reference Roeterink CH, van Steenbergen TJ, de Jong WF, de Graaff J. Histopathological effects in the palate of the rat induced by injection with different black-pigmented Bacteroides strains. J Periodontal Res. 1984;19:292–302.CrossRefPubMed Roeterink CH, van Steenbergen TJ, de Jong WF, de Graaff J. Histopathological effects in the palate of the rat induced by injection with different black-pigmented Bacteroides strains. J Periodontal Res. 1984;19:292–302.CrossRefPubMed
39.
go back to reference Furusho H, Miyauchi M, Hyogo H, Inubushi T, Ao M, Ouhara K, Hisatune J, Kurihara H, Sugai M, Hayes CN, Nakahara T, Aikata H, Takahashi S, Chayama K, Takata T. Dental infection of Porphyromonas gingivalis exacerbates high fat diet-induced steatohepatitis in mice. J Gastroenterol. 2013;48:1259–70.CrossRefPubMed Furusho H, Miyauchi M, Hyogo H, Inubushi T, Ao M, Ouhara K, Hisatune J, Kurihara H, Sugai M, Hayes CN, Nakahara T, Aikata H, Takahashi S, Chayama K, Takata T. Dental infection of Porphyromonas gingivalis exacerbates high fat diet-induced steatohepatitis in mice. J Gastroenterol. 2013;48:1259–70.CrossRefPubMed
40.
go back to reference Banu S, Jabir NR, Mohan R, Manjunath NC, Kamal MA, Kumar KR, Zaidi SK, Khan MS, Tabrez S. Correlation of Toll-like receptor 4, interleukin-18, transaminases, and uric acid in patients with chronic periodontitis and healthy adults. J Periodontol. 2015;86:431–9.CrossRefPubMed Banu S, Jabir NR, Mohan R, Manjunath NC, Kamal MA, Kumar KR, Zaidi SK, Khan MS, Tabrez S. Correlation of Toll-like receptor 4, interleukin-18, transaminases, and uric acid in patients with chronic periodontitis and healthy adults. J Periodontol. 2015;86:431–9.CrossRefPubMed
41.
go back to reference Ter Maaten JC, Voorburg A, Heine RJ, Ter Wee PM, Donker AJ, Gans RO. Renal handling of urate and sodium during acute physiological hyperinsulinaemia in healthy subjects. Clin Sci (Lond). 1997;92:51–8.CrossRefPubMed Ter Maaten JC, Voorburg A, Heine RJ, Ter Wee PM, Donker AJ, Gans RO. Renal handling of urate and sodium during acute physiological hyperinsulinaemia in healthy subjects. Clin Sci (Lond). 1997;92:51–8.CrossRefPubMed
42.
go back to reference Matsuura F, Yamashita S, Nakamura T, Nishida M, Nozaki S, Funahashi T, Matsuzawa Y. Effect of visceral fat accumulation on uric acid metabolism in male obese subjects: visceral fat obesity is linked more closely to overproduction of uric acid than subcutaneous fat obesity. Metabolism. 1998;47:929–33.CrossRefPubMed Matsuura F, Yamashita S, Nakamura T, Nishida M, Nozaki S, Funahashi T, Matsuzawa Y. Effect of visceral fat accumulation on uric acid metabolism in male obese subjects: visceral fat obesity is linked more closely to overproduction of uric acid than subcutaneous fat obesity. Metabolism. 1998;47:929–33.CrossRefPubMed
Metadata
Title
Effects of experimental periodontitis on the metabolic system in rats with diet-induced obesity (DIO): an analysis of serum biochemical parameters
Authors
Ryutaro Kuraji
Miyako Fujita
Hiroshi Ito
Shuichi Hashimoto
Yukihiro Numabe
Publication date
01-04-2018
Publisher
Springer Japan
Published in
Odontology / Issue 2/2018
Print ISSN: 1618-1247
Electronic ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-017-0322-5

Other articles of this Issue 2/2018

Odontology 2/2018 Go to the issue