Skip to main content
Erschienen in: Clinical Oral Investigations 6/2016

28.09.2015 | Original Article

Long-term evaluation of oral gavage with periodontopathogens or ligature induction of experimental periodontal disease in mice

verfasst von: Rafael Scaf de Molon, Vinicius Ibiapina Mascarenhas, Erica Dorigatti de Avila, Livia Sertori Finoti, Gustavo Boze Toffoli, Denise Madalena Palomari Spolidorio, Raquel Mantuaneli Scarel-Caminaga, Sotirios Tetradis, Joni Augusto Cirelli

Erschienen in: Clinical Oral Investigations | Ausgabe 6/2016

Einloggen, um Zugang zu erhalten

Abstract

Objective

To evaluate in long-term periods the destruction of periodontal tissues and bacterial colonization induced by oral gavage with periodontopathogens or ligature experimental periodontal disease models.

Material and methods

Forty-eight C57BL/6 J mice were divided into four groups: group C: negative control; group L: ligature; group G-Pg: oral gavage with Porphyromonas gingivalis; and group G-PgFn: oral gavage with Porphyromonas gingivalis associated with Fusobacterium nucleatum. Mice were infected by oral gavage five times in 2-day intervals. After 45 and 60 days, animals were sacrificed and the immune-inflammatory response in the periodontal tissue was assessed by stereometric analysis. The alveolar bone loss was evaluated by live microcomputed tomography and histometric analysis. qPCR was used to confirm the bacterial colonization in all the groups. Data were analyzed using the Kruskal-Wallis, Wilcoxon, and ANOVA tests, at 5 % of significance level.

Results

Ligature model induced inflammation and bone resorption characterized by increased number of inflammatory cells and decreased number of fibroblasts, followed by advanced alveolar bone loss at 45 and 60 days (p < 0.05). Bacterial colonization in groups G-Pg and G-PgFn was confirmed by qPCR but inflammation and bone resorption were not observed (p < 0.05).

Conclusions

The ligature model but not the oral gavage models were effective to induce inflammation and bone loss in long-term periods. Pg colonization was observed in all models of experimental periodontal disease induction, independent of tissue alterations. These mice models of periodontitis validates, compliments, and enhances published PD models that utilize ligature or oral gavage and supports the importance of a successful colonization of a susceptible host, a bacterial invasion into vulnerable tissue, and host-bacterial interactions that lead to tissue destruction.

Clinical relevance

The ligature model was an effective approach to induce inflammation and bone loss similar to human periodontitis, but the oral gavage models were not efficient in inducing periodontal inflammation and tissue destruction in the conditions studied. Ligature models can provide a basis for future interventional studies that contribute to the understanding of the disease pathogenesis and the complex host response to microbial challenge.
Literatur
1.
Zurück zum Zitat Eke PI, Genco RJ (2007) CDC periodontal disease surveillance project: background, objectives, and progress report. J Periodontol 78:1366–1371CrossRefPubMed Eke PI, Genco RJ (2007) CDC periodontal disease surveillance project: background, objectives, and progress report. J Periodontol 78:1366–1371CrossRefPubMed
2.
Zurück zum Zitat Albandar JM, Rams TE (2002) Global epidemiology of periodontal diseases: an overview. Periodontol 2000(29):7–10CrossRef Albandar JM, Rams TE (2002) Global epidemiology of periodontal diseases: an overview. Periodontol 2000(29):7–10CrossRef
3.
Zurück zum Zitat Kornman KS, Crane A, Wang HY, di Giovine FS, Newman MG, Pirk FW, Wilson TG Jr, Higginbottom FL, Duff GW (1997) The interleukin-1 genotype as a severity factor in adult periodontal disease. J Clin Periodontol 24:72–77CrossRefPubMed Kornman KS, Crane A, Wang HY, di Giovine FS, Newman MG, Pirk FW, Wilson TG Jr, Higginbottom FL, Duff GW (1997) The interleukin-1 genotype as a severity factor in adult periodontal disease. J Clin Periodontol 24:72–77CrossRefPubMed
4.
Zurück zum Zitat Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS (1997) Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000 14:216–248CrossRefPubMed Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS (1997) Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000 14:216–248CrossRefPubMed
5.
Zurück zum Zitat Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732CrossRefPubMedPubMedCentral Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Garlet GP, Cardoso CR, Silva TA, Ferreira BR, Avila-Campos MJ, Cunha FQ, Silva JS (2006) Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol Immunol 21:12–20CrossRefPubMed Garlet GP, Cardoso CR, Silva TA, Ferreira BR, Avila-Campos MJ, Cunha FQ, Silva JS (2006) Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol Immunol 21:12–20CrossRefPubMed
7.
Zurück zum Zitat Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000(38):72–122CrossRef Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000(38):72–122CrossRef
8.
Zurück zum Zitat Kesavalu L, Sathishkumar S, Bakthavatchalu V, Matthews C, Dawson D, Steffen M, Ebersole JL (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75:1704–1712CrossRefPubMedPubMedCentral Kesavalu L, Sathishkumar S, Bakthavatchalu V, Matthews C, Dawson D, Steffen M, Ebersole JL (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75:1704–1712CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Polak D, Wilensky A, Shapira L, Halabi A, Goldstein D, Weiss EI, Houri-Haddad Y (2009) Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: bone loss and host response. J Clin Periodontol 36:406–410CrossRefPubMed Polak D, Wilensky A, Shapira L, Halabi A, Goldstein D, Weiss EI, Houri-Haddad Y (2009) Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: bone loss and host response. J Clin Periodontol 36:406–410CrossRefPubMed
10.
Zurück zum Zitat Holt SC, Ebersole J, Felton J, Brunsvold M, Kornman KS (1988) Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239:55–57CrossRefPubMed Holt SC, Ebersole J, Felton J, Brunsvold M, Kornman KS (1988) Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239:55–57CrossRefPubMed
11.
Zurück zum Zitat Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144CrossRefPubMed Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144CrossRefPubMed
12.
Zurück zum Zitat Craig RG, Yip JK, So MK, Boylan RJ, Socransky SS, Haffajee AD (2003) Relationship of destructive periodontal disease to the acute-phase response. J Periodontol 74:1007–1016CrossRefPubMed Craig RG, Yip JK, So MK, Boylan RJ, Socransky SS, Haffajee AD (2003) Relationship of destructive periodontal disease to the acute-phase response. J Periodontol 74:1007–1016CrossRefPubMed
13.
Zurück zum Zitat Haffajee AD, Socransky SS (2005) Microbiology of periodontal diseases: introduction. Periodontol 2000(38):9–12CrossRef Haffajee AD, Socransky SS (2005) Microbiology of periodontal diseases: introduction. Periodontol 2000(38):9–12CrossRef
14.
Zurück zum Zitat Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000(38):135–187CrossRef Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000(38):135–187CrossRef
15.
Zurück zum Zitat Zubery Y, Dunstan CR, Story BM, Kesavalu L, Ebersole JL, Holt SC, Boyce BF (1998) Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66:4158–4162PubMedPubMedCentral Zubery Y, Dunstan CR, Story BM, Kesavalu L, Ebersole JL, Holt SC, Boyce BF (1998) Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66:4158–4162PubMedPubMedCentral
16.
Zurück zum Zitat Baker PJ, Evans RT, Roopenian DC (1994) Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39:1035–1040CrossRefPubMed Baker PJ, Evans RT, Roopenian DC (1994) Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39:1035–1040CrossRefPubMed
17.
Zurück zum Zitat de Molon RS, de Avila ED, Boas Nogueira AV, Chaves de Souza JA, Avila-Campos MJ, de Andrade CR, Cirelli JA (2014) Evaluation of the host response in various models of induced periodontal disease in mice. J Periodontol 85:465–477CrossRefPubMed de Molon RS, de Avila ED, Boas Nogueira AV, Chaves de Souza JA, Avila-Campos MJ, de Andrade CR, Cirelli JA (2014) Evaluation of the host response in various models of induced periodontal disease in mice. J Periodontol 85:465–477CrossRefPubMed
18.
Zurück zum Zitat de Molon RS, de Avila ED, Cirelli JA (2013) Host responses induced by different animal models of periodontal disease: a literature review. J Investig Clin Dent 4:211–218CrossRefPubMed de Molon RS, de Avila ED, Cirelli JA (2013) Host responses induced by different animal models of periodontal disease: a literature review. J Investig Clin Dent 4:211–218CrossRefPubMed
19.
Zurück zum Zitat Graves DT, Fine D, Teng YT, Van Dyke TE, Hajishengallis G (2008) The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 35:89–105CrossRefPubMedPubMedCentral Graves DT, Fine D, Teng YT, Van Dyke TE, Hajishengallis G (2008) The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 35:89–105CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Graves DT, Kang J, Andriankaja O, Wada K, Rossa C Jr (2012) Animal models to study host-bacteria interactions involved in periodontitis. Front Oral Biol 15:117–132CrossRefPubMed Graves DT, Kang J, Andriankaja O, Wada K, Rossa C Jr (2012) Animal models to study host-bacteria interactions involved in periodontitis. Front Oral Biol 15:117–132CrossRefPubMed
21.
Zurück zum Zitat Saadi-Thiers K, Huck O, Simonis P, Tilly P, Fabre JE, Tenenbaum H, Davideau JL (2013) Periodontal and systemic responses in various mice models of experimental periodontitis: respective roles of inflammation duration and porphyromonas gingivalis infection. J Periodontol 84:396–406CrossRefPubMed Saadi-Thiers K, Huck O, Simonis P, Tilly P, Fabre JE, Tenenbaum H, Davideau JL (2013) Periodontal and systemic responses in various mice models of experimental periodontitis: respective roles of inflammation duration and porphyromonas gingivalis infection. J Periodontol 84:396–406CrossRefPubMed
22.
Zurück zum Zitat Klausen B (1991) Microbiological and immunological aspects of experimental periodontal disease in rats: a review article. J Periodontol 62:59–73CrossRefPubMed Klausen B (1991) Microbiological and immunological aspects of experimental periodontal disease in rats: a review article. J Periodontol 62:59–73CrossRefPubMed
23.
Zurück zum Zitat Bezerra MM, Brito GA, Ribeiro RA, Rocha FA (2002) Low-dose doxycycline prevents inflammatory bone resorption in rats. Braz J Med Biol Res 35:613–616CrossRefPubMed Bezerra MM, Brito GA, Ribeiro RA, Rocha FA (2002) Low-dose doxycycline prevents inflammatory bone resorption in rats. Braz J Med Biol Res 35:613–616CrossRefPubMed
24.
Zurück zum Zitat Duarte PM, Tezolin KR, Figueiredo LC, Feres M, Bastos MF (2010) Microbial profile of ligature-induced periodontitis in rats. Arch Oral Biol 55:142–147CrossRefPubMed Duarte PM, Tezolin KR, Figueiredo LC, Feres M, Bastos MF (2010) Microbial profile of ligature-induced periodontitis in rats. Arch Oral Biol 55:142–147CrossRefPubMed
25.
Zurück zum Zitat Rovin S, Costich ER, Gordon HA (1966) The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J Periodontal Res 1:193–204CrossRefPubMed Rovin S, Costich ER, Gordon HA (1966) The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J Periodontal Res 1:193–204CrossRefPubMed
26.
Zurück zum Zitat Amar S, Wu SC, Madan M (2009) Is Porphyromonas gingivalis cell invasion required for atherogenesis? Pharmacotherapeutic implications. J Immunol 182:1584–1592CrossRefPubMed Amar S, Wu SC, Madan M (2009) Is Porphyromonas gingivalis cell invasion required for atherogenesis? Pharmacotherapeutic implications. J Immunol 182:1584–1592CrossRefPubMed
27.
Zurück zum Zitat Barros SP, Arce RM, Galloway P, Lawter R, Offenbacher S (2011) Therapeutic effect of a topical CCR2 antagonist on induced alveolar bone loss in mice. J Periodontal Res 46:246–251CrossRefPubMed Barros SP, Arce RM, Galloway P, Lawter R, Offenbacher S (2011) Therapeutic effect of a topical CCR2 antagonist on induced alveolar bone loss in mice. J Periodontal Res 46:246–251CrossRefPubMed
28.
Zurück zum Zitat Cantley MD, Bartold PM, Marino V, Reid RC, Fairlie DP, Wyszynski RN, Zilm PS, Haynes DR (2009) The use of live-animal micro-computed tomography to determine the effect of a novel phospholipase A2 inhibitor on alveolar bone loss in an in vivo mouse model of periodontitis. J Periodontal Res 44:317–322CrossRefPubMed Cantley MD, Bartold PM, Marino V, Reid RC, Fairlie DP, Wyszynski RN, Zilm PS, Haynes DR (2009) The use of live-animal micro-computed tomography to determine the effect of a novel phospholipase A2 inhibitor on alveolar bone loss in an in vivo mouse model of periodontitis. J Periodontal Res 44:317–322CrossRefPubMed
29.
Zurück zum Zitat Glowacki AJ, Yoshizawa S, Jhunjhunwala S, Vieira AE, Garlet GP, Sfeir C, Little SR (2013) Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci U S A 110:18525–18530CrossRefPubMedPubMedCentral Glowacki AJ, Yoshizawa S, Jhunjhunwala S, Vieira AE, Garlet GP, Sfeir C, Little SR (2013) Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci U S A 110:18525–18530CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Feuille F, Ebersole JL, Kesavalu L, Stepfen MJ, Holt SC (1996) Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun 64:2094–2100PubMedPubMedCentral Feuille F, Ebersole JL, Kesavalu L, Stepfen MJ, Holt SC (1996) Mixed infection with Porphyromonas gingivalis and Fusobacterium nucleatum in a murine lesion model: potential synergistic effects on virulence. Infect Immun 64:2094–2100PubMedPubMedCentral
31.
Zurück zum Zitat Nahid MA, Rivera M, Lucas A, Chan EK, Kesavalu L (2011) Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease. Infect Immun 79:1597–1605CrossRefPubMedPubMedCentral Nahid MA, Rivera M, Lucas A, Chan EK, Kesavalu L (2011) Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease. Infect Immun 79:1597–1605CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Li CH, Amar S (2007) Morphometric, histomorphometric, and microcomputed tomographic analysis of periodontal inflammatory lesions in a murine model. J Periodontol 78:1120–1128CrossRefPubMed Li CH, Amar S (2007) Morphometric, histomorphometric, and microcomputed tomographic analysis of periodontal inflammatory lesions in a murine model. J Periodontol 78:1120–1128CrossRefPubMed
33.
Zurück zum Zitat Meulman T, Peruzzo DC, Stipp RN, Goncalves PF, Sallum EA, Casati MZ, Goncalves RB, Nociti FH Jr (2011) Impact of Porphyromonas gingivalis inoculation on ligature-induced alveolar bone loss. A pilot study in rats. J Periodontal Res 46:629–636PubMed Meulman T, Peruzzo DC, Stipp RN, Goncalves PF, Sallum EA, Casati MZ, Goncalves RB, Nociti FH Jr (2011) Impact of Porphyromonas gingivalis inoculation on ligature-induced alveolar bone loss. A pilot study in rats. J Periodontal Res 46:629–636PubMed
34.
Zurück zum Zitat Wilensky A, Gabet Y, Yumoto H, Houri-Haddad Y, Shapira L (2005) Three-dimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J Periodontol 76:1282–1286CrossRefPubMed Wilensky A, Gabet Y, Yumoto H, Houri-Haddad Y, Shapira L (2005) Three-dimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J Periodontol 76:1282–1286CrossRefPubMed
35.
Zurück zum Zitat Wilensky A, Polak D, Awawdi S, Halabi A, Shapira L, Houri-Haddad Y (2009) Strain-dependent activation of the mouse immune response is correlated with Porphyromonas gingivalis-induced experimental periodontitis. J Clin Periodontol 36:915–921CrossRefPubMed Wilensky A, Polak D, Awawdi S, Halabi A, Shapira L, Houri-Haddad Y (2009) Strain-dependent activation of the mouse immune response is correlated with Porphyromonas gingivalis-induced experimental periodontitis. J Clin Periodontol 36:915–921CrossRefPubMed
36.
Zurück zum Zitat Kilkenny C, Browne WJ, Cuthi I, Emerson M, Altman DG (2012) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Vet Clin Pathol 41:27–31CrossRefPubMed Kilkenny C, Browne WJ, Cuthi I, Emerson M, Altman DG (2012) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Vet Clin Pathol 41:27–31CrossRefPubMed
37.
Zurück zum Zitat Nogueira AV, de Souza JA, de Molon RS, Pereira Eda S, de Aquino SG, Giannobile WV, Cirelli JA (2014) HMGB1 localization during experimental periodontitis. Mediat Inflamm 2014, 816320 Nogueira AV, de Souza JA, de Molon RS, Pereira Eda S, de Aquino SG, Giannobile WV, Cirelli JA (2014) HMGB1 localization during experimental periodontitis. Mediat Inflamm 2014, 816320
38.
Zurück zum Zitat Liu R, Bal HS, Desta T, Krothapalli N, Alyassi M, Luan Q, Graves DT (2006) Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res 85:510–514CrossRefPubMedPubMedCentral Liu R, Bal HS, Desta T, Krothapalli N, Alyassi M, Luan Q, Graves DT (2006) Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res 85:510–514CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Odze RD, Marcial MA, Antonioli D (1996) Gastric fundic gland polyps: a morphological study including mucin histochemistry, stereometry, and MIB-1 immunohistochemistry. Hum Pathol 27:896–903CrossRefPubMed Odze RD, Marcial MA, Antonioli D (1996) Gastric fundic gland polyps: a morphological study including mucin histochemistry, stereometry, and MIB-1 immunohistochemistry. Hum Pathol 27:896–903CrossRefPubMed
40.
Zurück zum Zitat Duarte PM, Goncalves P, Casati MZ, de Toledo S, Sallum EA, Nociti FH Jr (2006) Estrogen and alendronate therapies may prevent the influence of estrogen deficiency on the tooth-supporting alveolar bone: a histometric study in rats. J Periodontal Res 41:541–546CrossRefPubMed Duarte PM, Goncalves P, Casati MZ, de Toledo S, Sallum EA, Nociti FH Jr (2006) Estrogen and alendronate therapies may prevent the influence of estrogen deficiency on the tooth-supporting alveolar bone: a histometric study in rats. J Periodontal Res 41:541–546CrossRefPubMed
41.
Zurück zum Zitat de Molon RS, Cheong S, Bezouglaia O, Dry SM, Pirih F, Cirelli JA, Aghaloo TL, Tetradis S (2014) Spontaneous osteonecrosis of the jaws in the maxilla of mice on antiresorptive treatment: a novel ONJ mouse model. Bone 68:11–19CrossRefPubMedPubMedCentral de Molon RS, Cheong S, Bezouglaia O, Dry SM, Pirih F, Cirelli JA, Aghaloo TL, Tetradis S (2014) Spontaneous osteonecrosis of the jaws in the maxilla of mice on antiresorptive treatment: a novel ONJ mouse model. Bone 68:11–19CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat de Molon RS, Shimamoto H, Bezouglaia O, Pirih FQ, Dry SM, Kostenuik P, Boyce RW, Dwyer D, Aghaloo TL, Tetradis S (2015) OPG-Fc but not zoledronic acid discontinuation reverses Osteonecrosis of the Jaws (ONJ) in Mice. J Bone Miner Res 30(9):1627–1640. doi:10.1002/jbmr.2490 de Molon RS, Shimamoto H, Bezouglaia O, Pirih FQ, Dry SM, Kostenuik P, Boyce RW, Dwyer D, Aghaloo TL, Tetradis S (2015) OPG-Fc but not zoledronic acid discontinuation reverses Osteonecrosis of the Jaws (ONJ) in Mice. J Bone Miner Res 30(9):1627–1640. doi:10.​1002/​jbmr.​2490
43.
Zurück zum Zitat Teixeira SR, Mattarazo F, Feres M, Figueiredo LC, de Faveri M, Simionato MR, Mayer MP (2009) Quantification of porphyromonas gingivalis and fimA genotypes in smoker chronic periodontitis. J Clin Periodontol 36:482–487CrossRefPubMed Teixeira SR, Mattarazo F, Feres M, Figueiredo LC, de Faveri M, Simionato MR, Mayer MP (2009) Quantification of porphyromonas gingivalis and fimA genotypes in smoker chronic periodontitis. J Clin Periodontol 36:482–487CrossRefPubMed
44.
Zurück zum Zitat Amano A, Nakagawa I, Kataoka K, Morisaki I, Hamada S (1999) Distribution of Porphyromonas gingivalis strains with fimA genotypes in periodontitis patients. J Clin Microbiol 37:1426–1430PubMedPubMedCentral Amano A, Nakagawa I, Kataoka K, Morisaki I, Hamada S (1999) Distribution of Porphyromonas gingivalis strains with fimA genotypes in periodontitis patients. J Clin Microbiol 37:1426–1430PubMedPubMedCentral
45.
Zurück zum Zitat Liu YF, Wu LA, Wang J, Wen LY, Wang XJ (2010) Micro-computerized tomography analysis of alveolar bone loss in ligature- and nicotine-induced experimental periodontitis in rats. J Periodontal Res 45:714–719CrossRefPubMed Liu YF, Wu LA, Wang J, Wen LY, Wang XJ (2010) Micro-computerized tomography analysis of alveolar bone loss in ligature- and nicotine-induced experimental periodontitis in rats. J Periodontal Res 45:714–719CrossRefPubMed
46.
Zurück zum Zitat Genco CA, Van Dyke T, Amar S (1998) Animal models for porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 6:444–449CrossRefPubMed Genco CA, Van Dyke T, Amar S (1998) Animal models for porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 6:444–449CrossRefPubMed
47.
Zurück zum Zitat Garcia de Aquino S, Manzolli Leite FR, Stach-Machado DR, Francisco da Silva JA, Spolidorio LC, Rossa C Jr (2009) Signaling pathways associated with the expression of inflammatory mediators activated during the course of two models of experimental periodontitis. Life Sci 84:745–754CrossRefPubMed Garcia de Aquino S, Manzolli Leite FR, Stach-Machado DR, Francisco da Silva JA, Spolidorio LC, Rossa C Jr (2009) Signaling pathways associated with the expression of inflammatory mediators activated during the course of two models of experimental periodontitis. Life Sci 84:745–754CrossRefPubMed
48.
Zurück zum Zitat Yuan H, Gupte R, Zelkha S, Amar S (2011) Receptor activator of nuclear factor kappa B ligand antagonists inhibit tissue inflammation and bone loss in experimental periodontitis. J Clin Periodontol 38:1029–1036CrossRefPubMed Yuan H, Gupte R, Zelkha S, Amar S (2011) Receptor activator of nuclear factor kappa B ligand antagonists inhibit tissue inflammation and bone loss in experimental periodontitis. J Clin Periodontol 38:1029–1036CrossRefPubMed
49.
Zurück zum Zitat Karimbux NY, Ramamurthy NS, Golub LM, Nishimura I (1998) The expression of collagen I and XII mRNAs in porphyromonas gingivalis-induced periodontitis in rats: the effect of doxycycline and chemically modified tetracycline. J Periodontol 69:34–40CrossRefPubMed Karimbux NY, Ramamurthy NS, Golub LM, Nishimura I (1998) The expression of collagen I and XII mRNAs in porphyromonas gingivalis-induced periodontitis in rats: the effect of doxycycline and chemically modified tetracycline. J Periodontol 69:34–40CrossRefPubMed
50.
Zurück zum Zitat de Aquino SG, Guimaraes MR, Stach-Machado DR, da Silva JA, Spolidorio LC, Rossa C Jr (2009) Differential regulation of MMP-13 expression in two models of experimentally induced periodontal disease in rats. Arch Oral Biol 54:609–617CrossRefPubMed de Aquino SG, Guimaraes MR, Stach-Machado DR, da Silva JA, Spolidorio LC, Rossa C Jr (2009) Differential regulation of MMP-13 expression in two models of experimentally induced periodontal disease in rats. Arch Oral Biol 54:609–617CrossRefPubMed
51.
Zurück zum Zitat Kimura S, Nagai A, Onitsuka T, Koga T, Fujiwara T, Kaya H, Hamada S (2000) Induction of experimental periodontitis in mice with porphyromonas gingivalis-adhered ligatures. J Periodontol 71:1167–1173CrossRefPubMed Kimura S, Nagai A, Onitsuka T, Koga T, Fujiwara T, Kaya H, Hamada S (2000) Induction of experimental periodontitis in mice with porphyromonas gingivalis-adhered ligatures. J Periodontol 71:1167–1173CrossRefPubMed
52.
Zurück zum Zitat Baker PJ, Dixon M, Roopenian DC (2000) Genetic control of susceptibility to porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 68:5864–5868CrossRefPubMedPubMedCentral Baker PJ, Dixon M, Roopenian DC (2000) Genetic control of susceptibility to porphyromonas gingivalis-induced alveolar bone loss in mice. Infect Immun 68:5864–5868CrossRefPubMedPubMedCentral
53.
Zurück zum Zitat de Aquino SG, Abdollahi-Roodsaz S, Koenders MI, van de Loo FA, Pruijn GJ, Marijnissen RJ, Walgreen B, Helsen MM, van den Bersselaar LA, de Molon RS, Avila Campos MJ, Cunha FQ, Cirelli JA, van den Berg WB (2014) Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-driven Th17 response. J Immunol 192:4103–4111CrossRefPubMed de Aquino SG, Abdollahi-Roodsaz S, Koenders MI, van de Loo FA, Pruijn GJ, Marijnissen RJ, Walgreen B, Helsen MM, van den Bersselaar LA, de Molon RS, Avila Campos MJ, Cunha FQ, Cirelli JA, van den Berg WB (2014) Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1-driven Th17 response. J Immunol 192:4103–4111CrossRefPubMed
54.
Zurück zum Zitat Polak D, Naddaf R, Shapira L, Weiss EI, Houri-Haddad Y (2013) Protective potential of non-dialyzable material fraction of cranberry juice on the virulence of P. gingivalis and F. nucleatum mixed infection. J Periodontol 84:1019–1025CrossRefPubMed Polak D, Naddaf R, Shapira L, Weiss EI, Houri-Haddad Y (2013) Protective potential of non-dialyzable material fraction of cranberry juice on the virulence of P. gingivalis and F. nucleatum mixed infection. J Periodontol 84:1019–1025CrossRefPubMed
55.
Zurück zum Zitat Polak D, Shapira L, Weiss EI, Houri-Haddad Y (2012) The role of coaggregation between porphyromonas gingivalis and fusobacterium nucleatum on the host response to mixed infection. J Clin Periodontol 39:617–625CrossRefPubMed Polak D, Shapira L, Weiss EI, Houri-Haddad Y (2012) The role of coaggregation between porphyromonas gingivalis and fusobacterium nucleatum on the host response to mixed infection. J Clin Periodontol 39:617–625CrossRefPubMed
56.
Zurück zum Zitat McIntosh ML, Hajishengallis G (2012) Inhibition of porphyromonas gingivalis-induced periodontal bone loss by CXCR4 antagonist treatment. Mol Oral Microbiol 27:449–457CrossRefPubMedPubMedCentral McIntosh ML, Hajishengallis G (2012) Inhibition of porphyromonas gingivalis-induced periodontal bone loss by CXCR4 antagonist treatment. Mol Oral Microbiol 27:449–457CrossRefPubMedPubMedCentral
57.
Zurück zum Zitat Polak D, Shapira L, Weiss EI, Houri-Haddad Y (2013) Virulence mechanism of bacteria in mixed infection: attenuation of cytokine levels and evasion of polymorphonuclear leukocyte phagocytosis. J Periodontol 84:1463–1468CrossRefPubMed Polak D, Shapira L, Weiss EI, Houri-Haddad Y (2013) Virulence mechanism of bacteria in mixed infection: attenuation of cytokine levels and evasion of polymorphonuclear leukocyte phagocytosis. J Periodontol 84:1463–1468CrossRefPubMed
58.
Zurück zum Zitat Polak D, Wilensky A, Shapira L, Weiss EI, Houri-Haddad Y (2010) Vaccination of mice with porphyromonas gingivalis or fusobacterium nucleatum modulates the inflammatory response, but fails to prevent experimental periodontitis. J Clin Periodontol 37:812–817CrossRefPubMed Polak D, Wilensky A, Shapira L, Weiss EI, Houri-Haddad Y (2010) Vaccination of mice with porphyromonas gingivalis or fusobacterium nucleatum modulates the inflammatory response, but fails to prevent experimental periodontitis. J Clin Periodontol 37:812–817CrossRefPubMed
59.
Zurück zum Zitat Li H, Yang H, Ding Y, Aprecio R, Zhang W, Wang Q, Li Y (2013) Experimental periodontitis induced by porphyromonas gingivalis does not alter the onset or severity of diabetes in mice. J Periodontal Res 48:582–590CrossRefPubMed Li H, Yang H, Ding Y, Aprecio R, Zhang W, Wang Q, Li Y (2013) Experimental periodontitis induced by porphyromonas gingivalis does not alter the onset or severity of diabetes in mice. J Periodontal Res 48:582–590CrossRefPubMed
60.
Zurück zum Zitat Nakano K, Kuboniwa M, Nakagawa I, Yamamura T, Nomura R, Okahashi N, Ooshima T, Amano A (2004) Comparison of inflammatory changes caused by porphyromonas gingivalis with distinct fimA genotypes in a mouse abscess model. Oral Microbiol Immunol 19:205–209CrossRefPubMed Nakano K, Kuboniwa M, Nakagawa I, Yamamura T, Nomura R, Okahashi N, Ooshima T, Amano A (2004) Comparison of inflammatory changes caused by porphyromonas gingivalis with distinct fimA genotypes in a mouse abscess model. Oral Microbiol Immunol 19:205–209CrossRefPubMed
61.
Zurück zum Zitat Kesavalu L, Vasudevan B, Raghu B, Browning E, Dawson D, Novak JM, Correll MC, Steffen MJ, Bhattacharya A, Fernandes G, Ebersole JL (2006) Omega-3 fatty acid effect on alveolar bone loss in rats. J Dent Res 85:648–652CrossRefPubMedPubMedCentral Kesavalu L, Vasudevan B, Raghu B, Browning E, Dawson D, Novak JM, Correll MC, Steffen MJ, Bhattacharya A, Fernandes G, Ebersole JL (2006) Omega-3 fatty acid effect on alveolar bone loss in rats. J Dent Res 85:648–652CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat Yoshida-Minami I, Suzuki A, Kawabata K, Okamoto A, Nishihara Y, Minami T, Nagashima S, Morisaki I, Ooshima T (1997) Alveolar bone loss in rats infected with a strain of prevotella intermedia and fusobacterium nucleatum isolated from a child with prepubertal periodontitis. J Periodontol 68:12–17CrossRefPubMed Yoshida-Minami I, Suzuki A, Kawabata K, Okamoto A, Nishihara Y, Minami T, Nagashima S, Morisaki I, Ooshima T (1997) Alveolar bone loss in rats infected with a strain of prevotella intermedia and fusobacterium nucleatum isolated from a child with prepubertal periodontitis. J Periodontol 68:12–17CrossRefPubMed
Metadaten
Titel
Long-term evaluation of oral gavage with periodontopathogens or ligature induction of experimental periodontal disease in mice
verfasst von
Rafael Scaf de Molon
Vinicius Ibiapina Mascarenhas
Erica Dorigatti de Avila
Livia Sertori Finoti
Gustavo Boze Toffoli
Denise Madalena Palomari Spolidorio
Raquel Mantuaneli Scarel-Caminaga
Sotirios Tetradis
Joni Augusto Cirelli
Publikationsdatum
28.09.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 6/2016
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-015-1607-0

Weitere Artikel der Ausgabe 6/2016

Clinical Oral Investigations 6/2016 Zur Ausgabe

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Ein Drittel der jungen Ärztinnen und Ärzte erwägt abzuwandern

07.05.2024 Klinik aktuell Nachrichten

Extreme Arbeitsverdichtung und kaum Supervision: Dr. Andrea Martini, Sprecherin des Bündnisses Junge Ärztinnen und Ärzte (BJÄ) über den Frust des ärztlichen Nachwuchses und die Vorteile des Rucksack-Modells.

Endlich: Zi zeigt, mit welchen PVS Praxen zufrieden sind

IT für Ärzte Nachrichten

Darauf haben viele Praxen gewartet: Das Zi hat eine Liste von Praxisverwaltungssystemen veröffentlicht, die von Nutzern positiv bewertet werden. Eine gute Grundlage für wechselwillige Ärztinnen und Psychotherapeuten.

Parodontalbehandlung verbessert Prognose bei Katheterablation

19.04.2024 Vorhofflimmern Nachrichten

Werden Personen mit Vorhofflimmern in der Blanking-Periode nach einer Katheterablation gegen eine bestehende Parodontitis behandelt, verbessert dies die Erfolgsaussichten. Dafür sprechen die Resultate einer prospektiven Untersuchung.

Newsletter

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