Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease

Masato Yoneda, Shuhei Naka, Kazuhiko Nakano, Koichiro Wada, Hiroki Endo, Hironori Mawatari, Kento Imajo, Ryota Nomura, Kazuya Hokamura, Masafumi Ono, Shogo Murata, Iwai Tohnai, Yoshio Sumida, Toshihide Shima, Masae Kuboniwa, Kazuo Umemura, Yoshinori Kamisaki, Atsuo Amano, Takeshi Okanoue, Takashi OoshimaAtsushi Nakajima

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

Background: Non-alcoholic fatty liver disease (NAFLD) is a hepatic manifestation of metabolic syndrome that is closely associated with multiple factors such as obesity, hyperlipidemia and type 2 diabetes mellitus. However, other risk factors for the development of NAFLD are unclear. With the association between periodontal disease and the development of systemic diseases receiving increasing attention recently, we conducted this study to investigate the relationship between NAFLD and infection with Porphyromonas gingivalis (P. gingivalis), a major causative agent of periodontitis.Methods: The detection frequencies of periodontal bacteria in oral samples collected from 150 biopsy-proven NAFLD patients (102 with non-alcoholic steatohepatitis (NASH) and 48 with non-alcoholic fatty liver (NAFL) patients) and 60 non-NAFLD control subjects were determined. Detection of P. gingivalis and other periodontopathic bacteria were detected by PCR assay. In addition, effect of P. gingivalis-infection on mouse NAFLD model was investigated. To clarify the exact contribution of P. gingivalis-induced periodontitis, non-surgical periodontal treatments were also undertaken for 3 months in 10 NAFLD patients with periodontitis.Results: The detection frequency of P. gingivalis in NAFLD patients was significantly higher than that in the non-NAFLD control subjects (46.7% vs. 21.7%, odds ratio: 3.16). In addition, the detection frequency of P. gingivalis in NASH patients was markedly higher than that in the non-NAFLD subjects (52.0%, odds ratio: 3.91). Most of the P. gingivalis fimbria detected in the NAFLD patients was of invasive genotypes, especially type II (50.0%). Infection of type II P. gingivalis on NAFLD model of mice accelerated the NAFLD progression. The non-surgical periodontal treatments on NAFLD patients carried out for 3 months ameliorated the liver function parameters, such as the serum levels of AST and ALT.Conclusions: Infection with high-virulence P. gingivalis might be an additional risk factor for the development/progression of NAFLD/NASH.

Original languageEnglish
Article number16
JournalBMC Gastroenterology
Volume12
DOIs
Publication statusPublished - Feb 16 2012
Externally publishedYes

Fingerprint

Porphyromonas gingivalis
Fatty Liver
Periodontitis
Liver Diseases
Infection
Non-alcoholic Fatty Liver Disease
Odds Ratio
Bacteria
Liver
Periodontal Diseases
Hyperlipidemias
Type 2 Diabetes Mellitus
Virulence
Disease Progression
Obesity

Keywords

  • Insulin resistance
  • Non-alcoholic fatty liver disease (NAFLD)
  • Non-alcoholic steatohepatitis (NASH)
  • Oral bacteria
  • P. gingivalis

ASJC Scopus subject areas

  • Gastroenterology

Cite this

Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease. / Yoneda, Masato; Naka, Shuhei; Nakano, Kazuhiko; Wada, Koichiro; Endo, Hiroki; Mawatari, Hironori; Imajo, Kento; Nomura, Ryota; Hokamura, Kazuya; Ono, Masafumi; Murata, Shogo; Tohnai, Iwai; Sumida, Yoshio; Shima, Toshihide; Kuboniwa, Masae; Umemura, Kazuo; Kamisaki, Yoshinori; Amano, Atsuo; Okanoue, Takeshi; Ooshima, Takashi; Nakajima, Atsushi.

In: BMC Gastroenterology, Vol. 12, 16, 16.02.2012.

Research output: Contribution to journalArticle

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 2012, 'Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease', BMC Gastroenterology, vol. 12, 16. https://doi.org/10.1186/1471-230X-12-16
Yoneda, Masato ; Naka, Shuhei ; Nakano, Kazuhiko ; Wada, Koichiro ; Endo, Hiroki ; Mawatari, Hironori ; Imajo, Kento ; Nomura, Ryota ; Hokamura, Kazuya ; Ono, Masafumi ; Murata, Shogo ; Tohnai, Iwai ; Sumida, Yoshio ; Shima, Toshihide ; Kuboniwa, Masae ; Umemura, Kazuo ; Kamisaki, Yoshinori ; Amano, Atsuo ; Okanoue, Takeshi ; Ooshima, Takashi ; Nakajima, Atsushi. / Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease. In: BMC Gastroenterology. 2012 ; Vol. 12.
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abstract = "Background: Non-alcoholic fatty liver disease (NAFLD) is a hepatic manifestation of metabolic syndrome that is closely associated with multiple factors such as obesity, hyperlipidemia and type 2 diabetes mellitus. However, other risk factors for the development of NAFLD are unclear. With the association between periodontal disease and the development of systemic diseases receiving increasing attention recently, we conducted this study to investigate the relationship between NAFLD and infection with Porphyromonas gingivalis (P. gingivalis), a major causative agent of periodontitis.Methods: The detection frequencies of periodontal bacteria in oral samples collected from 150 biopsy-proven NAFLD patients (102 with non-alcoholic steatohepatitis (NASH) and 48 with non-alcoholic fatty liver (NAFL) patients) and 60 non-NAFLD control subjects were determined. Detection of P. gingivalis and other periodontopathic bacteria were detected by PCR assay. In addition, effect of P. gingivalis-infection on mouse NAFLD model was investigated. To clarify the exact contribution of P. gingivalis-induced periodontitis, non-surgical periodontal treatments were also undertaken for 3 months in 10 NAFLD patients with periodontitis.Results: The detection frequency of P. gingivalis in NAFLD patients was significantly higher than that in the non-NAFLD control subjects (46.7{\%} vs. 21.7{\%}, odds ratio: 3.16). In addition, the detection frequency of P. gingivalis in NASH patients was markedly higher than that in the non-NAFLD subjects (52.0{\%}, odds ratio: 3.91). Most of the P. gingivalis fimbria detected in the NAFLD patients was of invasive genotypes, especially type II (50.0{\%}). Infection of type II P. gingivalis on NAFLD model of mice accelerated the NAFLD progression. The non-surgical periodontal treatments on NAFLD patients carried out for 3 months ameliorated the liver function parameters, such as the serum levels of AST and ALT.Conclusions: Infection with high-virulence P. gingivalis might be an additional risk factor for the development/progression of NAFLD/NASH.",
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T1 - Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease

AU - Yoneda, Masato

AU - Naka, Shuhei

AU - Nakano, Kazuhiko

AU - Wada, Koichiro

AU - Endo, Hiroki

AU - Mawatari, Hironori

AU - Imajo, Kento

AU - Nomura, Ryota

AU - Hokamura, Kazuya

AU - Ono, Masafumi

AU - Murata, Shogo

AU - Tohnai, Iwai

AU - Sumida, Yoshio

AU - Shima, Toshihide

AU - Kuboniwa, Masae

AU - Umemura, Kazuo

AU - Kamisaki, Yoshinori

AU - Amano, Atsuo

AU - Okanoue, Takeshi

AU - Ooshima, Takashi

AU - Nakajima, Atsushi

PY - 2012/2/16

Y1 - 2012/2/16

N2 - Background: Non-alcoholic fatty liver disease (NAFLD) is a hepatic manifestation of metabolic syndrome that is closely associated with multiple factors such as obesity, hyperlipidemia and type 2 diabetes mellitus. However, other risk factors for the development of NAFLD are unclear. With the association between periodontal disease and the development of systemic diseases receiving increasing attention recently, we conducted this study to investigate the relationship between NAFLD and infection with Porphyromonas gingivalis (P. gingivalis), a major causative agent of periodontitis.Methods: The detection frequencies of periodontal bacteria in oral samples collected from 150 biopsy-proven NAFLD patients (102 with non-alcoholic steatohepatitis (NASH) and 48 with non-alcoholic fatty liver (NAFL) patients) and 60 non-NAFLD control subjects were determined. Detection of P. gingivalis and other periodontopathic bacteria were detected by PCR assay. In addition, effect of P. gingivalis-infection on mouse NAFLD model was investigated. To clarify the exact contribution of P. gingivalis-induced periodontitis, non-surgical periodontal treatments were also undertaken for 3 months in 10 NAFLD patients with periodontitis.Results: The detection frequency of P. gingivalis in NAFLD patients was significantly higher than that in the non-NAFLD control subjects (46.7% vs. 21.7%, odds ratio: 3.16). In addition, the detection frequency of P. gingivalis in NASH patients was markedly higher than that in the non-NAFLD subjects (52.0%, odds ratio: 3.91). Most of the P. gingivalis fimbria detected in the NAFLD patients was of invasive genotypes, especially type II (50.0%). Infection of type II P. gingivalis on NAFLD model of mice accelerated the NAFLD progression. The non-surgical periodontal treatments on NAFLD patients carried out for 3 months ameliorated the liver function parameters, such as the serum levels of AST and ALT.Conclusions: Infection with high-virulence P. gingivalis might be an additional risk factor for the development/progression of NAFLD/NASH.

AB - Background: Non-alcoholic fatty liver disease (NAFLD) is a hepatic manifestation of metabolic syndrome that is closely associated with multiple factors such as obesity, hyperlipidemia and type 2 diabetes mellitus. However, other risk factors for the development of NAFLD are unclear. With the association between periodontal disease and the development of systemic diseases receiving increasing attention recently, we conducted this study to investigate the relationship between NAFLD and infection with Porphyromonas gingivalis (P. gingivalis), a major causative agent of periodontitis.Methods: The detection frequencies of periodontal bacteria in oral samples collected from 150 biopsy-proven NAFLD patients (102 with non-alcoholic steatohepatitis (NASH) and 48 with non-alcoholic fatty liver (NAFL) patients) and 60 non-NAFLD control subjects were determined. Detection of P. gingivalis and other periodontopathic bacteria were detected by PCR assay. In addition, effect of P. gingivalis-infection on mouse NAFLD model was investigated. To clarify the exact contribution of P. gingivalis-induced periodontitis, non-surgical periodontal treatments were also undertaken for 3 months in 10 NAFLD patients with periodontitis.Results: The detection frequency of P. gingivalis in NAFLD patients was significantly higher than that in the non-NAFLD control subjects (46.7% vs. 21.7%, odds ratio: 3.16). In addition, the detection frequency of P. gingivalis in NASH patients was markedly higher than that in the non-NAFLD subjects (52.0%, odds ratio: 3.91). Most of the P. gingivalis fimbria detected in the NAFLD patients was of invasive genotypes, especially type II (50.0%). Infection of type II P. gingivalis on NAFLD model of mice accelerated the NAFLD progression. The non-surgical periodontal treatments on NAFLD patients carried out for 3 months ameliorated the liver function parameters, such as the serum levels of AST and ALT.Conclusions: Infection with high-virulence P. gingivalis might be an additional risk factor for the development/progression of NAFLD/NASH.

KW - Insulin resistance

KW - Non-alcoholic fatty liver disease (NAFLD)

KW - Non-alcoholic steatohepatitis (NASH)

KW - Oral bacteria

KW - P. gingivalis

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