Skip to main content
Erschienen in: Odontology 2/2018

14.12.2017 | Original Article

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

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

Erschienen in: Odontology | Ausgabe 2/2018

Einloggen, um Zugang zu erhalten

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.
Literatur
1.
2.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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
30.
31.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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
Metadaten
Titel
Effects of experimental periodontitis on the metabolic system in rats with diet-induced obesity (DIO): an analysis of serum biochemical parameters
verfasst von
Ryutaro Kuraji
Miyako Fujita
Hiroshi Ito
Shuichi Hashimoto
Yukihiro Numabe
Publikationsdatum
14.12.2017
Verlag
Springer Japan
Erschienen in
Odontology / Ausgabe 2/2018
Print ISSN: 1618-1247
Elektronische ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-017-0322-5

Weitere Artikel der Ausgabe 2/2018

Odontology 2/2018 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.