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Shine BK, Son M, Moon SY, Han SH. Metabolic Dysfunction-Associated Steatotic Liver Disease and the Risk of Chronic Periodontitis: A Nationwide Cohort Study. Nutrients 2024; 17:125. [PMID: 39796559 PMCID: PMC11723414 DOI: 10.3390/nu17010125] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/03/2024] [Revised: 12/18/2024] [Accepted: 12/28/2024] [Indexed: 01/13/2025] Open
Abstract
Background: Chronic periodontitis (CP) and metabolic dysfunction-associated steatotic liver disease (MASLD) have emerged as interconnected conditions with shared mechanisms, such as systemic inflammation and metabolic dysregulation. However, the risk of CP in the newly classified subgroups of steatotic liver disease (SLD), including MASLD and metabolic alcohol-associated liver disease (MetALD), has not been extensively studied. This study investigated the association between SLD subtypes and the incidence of CP in a nationwide cohort. Methods: This retrospective cohort study used data from the Korean National Health Insurance Service database. The study included 115,619 participants aged 40 and older who underwent health screenings between 2009 and 2010. The participants were classified into four groups: normal without risk factors, normal with risk factors, MASLD, and MetALD. The primary outcome was the incidence of CP as defined by ICD-10 codes and dental treatment records. Hazard ratios (HRs) were calculated using the Cox proportional hazards model and adjusted for demographic, clinical, and lifestyle factors. Results: Over a mean follow-up of 7.4 years, individuals with MASLD and MetALD had significantly higher risks of developing CP compared with the normal group without risk factors (MASLD: adjusted HR 1.14, 95% confidence interval (CI): 1.11-1.17; MetALD: adjusted HR 1.21, 95% CI: 1.15-1.27). The risk was more pronounced for severe CP, particularly for those with MetALD (adjusted HR 1.29, 95% CI: 1.22-1.36). Subgroup and sensitivity analyses confirmed these findings across the various definitions of hepatic steatosis and metabolic risk factors. Conclusions: This study reveals that individuals with MASLD and MetALD are at an elevated risk of developing CP, highlighting the need for integrated care strategies that address both periodontal health and metabolic liver conditions. These findings underscore the importance of periodontal health management in reducing the risk of CP among SLD populations.
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Affiliation(s)
- Bo-Kyung Shine
- Department of Family Medicine, College of Medicine, Dong-A University, Busan 49201, Republic of Korea;
| | - Minkook Son
- Department of Physiology, College of Medicine, Dong-A University, Busan 49201, Republic of Korea;
- Interdisciplinary Program, Department of Data Sciences Convergence, Dong-A University, Busan 49201, Republic of Korea
| | - Sang Yi Moon
- Interdisciplinary Program, Department of Data Sciences Convergence, Dong-A University, Busan 49201, Republic of Korea
- Division of Gastroenterology and Hepatology, Department of Internal Medicine, College of Medicine, Dong-A University, Busan 49201, Republic of Korea
| | - Seong-Ho Han
- Department of Family Medicine, College of Medicine, Dong-A University, Busan 49201, Republic of Korea;
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Kuraji R, Shiba T, Dong TS, Numabe Y, Kapila YL. Periodontal treatment and microbiome-targeted therapy in management of periodontitis-related nonalcoholic fatty liver disease with oral and gut dysbiosis. World J Gastroenterol 2023; 29:967-996. [PMID: 36844143 PMCID: PMC9950865 DOI: 10.3748/wjg.v29.i6.967] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/16/2022] [Revised: 11/14/2022] [Accepted: 01/30/2023] [Indexed: 02/10/2023] Open
Abstract
A growing body of evidence from multiple areas proposes that periodontal disease, accompanied by oral inflammation and pathological changes in the microbiome, induces gut dysbiosis and is involved in the pathogenesis of nonalcoholic fatty liver disease (NAFLD). A subgroup of NAFLD patients have a severely progressive form, namely nonalcoholic steatohepatitis (NASH), which is characterized by histological findings that include inflammatory cell infiltration and fibrosis. NASH has a high risk of further progression to cirrhosis and hepatocellular carcinoma. The oral microbiota may serve as an endogenous reservoir for gut microbiota, and transport of oral bacteria through the gastro-intestinal tract can set up a gut microbiome dysbiosis. Gut dysbiosis increases the production of potential hepatotoxins, including lipopolysaccharide, ethanol, and other volatile organic compounds such as acetone, phenol and cyclopentane. Moreover, gut dysbiosis increases intestinal permeability by disrupting tight junctions in the intestinal wall, leading to enhanced translocation of these hepatotoxins and enteric bacteria into the liver through the portal circulation. In particular, many animal studies support that oral administration of Porphyromonas gingivalis, a typical periodontopathic bacterium, induces disturbances in glycolipid metabolism and inflammation in the liver with gut dysbiosis. NAFLD, also known as the hepatic phenotype of metabolic syndrome, is strongly associated with metabolic complications, such as obesity and diabetes. Periodontal disease also has a bidirectional relationship with metabolic syndrome, and both diseases may induce oral and gut microbiome dysbiosis with insulin resistance and systemic chronic inflammation cooperatively. In this review, we will describe the link between periodontal disease and NAFLD with a focus on basic, epidemiological, and clinical studies, and discuss potential mechanisms linking the two diseases and possible therapeutic approaches focused on the microbiome. In conclusion, it is presumed that the pathogenesis of NAFLD involves a complex crosstalk between periodontal disease, gut microbiota, and metabolic syndrome. Thus, the conventional periodontal treatment and novel microbiome-targeted therapies that include probiotics, prebiotics and bacteriocins would hold great promise for preventing the onset and progression of NAFLD and subsequent complications in patients with periodontal disease.
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Affiliation(s)
- Ryutaro Kuraji
- Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo 102-0071, Japan
- Department of Orofacial Sciences, University of California San Francisco, San Francisco, CA 94143, United States
| | - Takahiko Shiba
- Department of Oral Medicine, Infection, and Immunity, Harvard School of Dental Medicine, Boston, MA 02115, United States
- Department of Periodontology, Tokyo Medical and Dental University, Tokyo 113-8549, Japan
| | - Tien S Dong
- The Vatche and Tamar Manoukian Division of Digestive Diseases, University of California Los Angeles, Department of Medicine, University of California David Geffen School of Medicine, Los Angeles, CA 90095, United States
| | - Yukihiro Numabe
- Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo 102-8159, Japan
| | - Yvonne L Kapila
- Department of Orofacial Sciences, University of California San Francisco, San Francisco, CA 94143, United States
- Sections of Biosystems and Function and Periodontics, Professor and Associate Dean of Research, Felix and Mildred Yip Endowed Chair in Dentistry, University of California Los Angeles, Los Angeles, CA 90095, United States
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Gheorghe DN, Bennardo F, Popescu DM, Nicolae FM, Ionele CM, Boldeanu MV, Camen A, Rogoveanu I, Surlin P. Oral and Periodontal Implications of Hepatitis Type B and D. Current State of Knowledge and Future Perspectives. J Pers Med 2022; 12:1580. [PMID: 36294719 PMCID: PMC9604856 DOI: 10.3390/jpm12101580] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2022] [Revised: 09/19/2022] [Accepted: 09/20/2022] [Indexed: 08/30/2023] Open
Abstract
Periodontitis is characterized by low-grade inflammation of the periodontal tissues, the structures that support and connect the teeth to the maxilla and mandible. This inflammation is caused by the accumulation of subgingival bacterial biofilm and gradually leads to the extensive damage of these tissues and the consequent loss of teeth. Hepatitis B is a major global health concern; infection with the hepatitis B virus causes significant inflammation of the liver and the possibility of its gradual evolution to cirrhosis. Hepatitis D, caused by infection with the delta hepatitis virus, is manifest only in patients already infected with the type B virus in a simultaneous (co-infected) or superimposed (superinfected) manner. The dental and periodontal status of patients with hepatitis B/D could exhibit significant changes, increasing the risk of periodontitis onset. Moreover, the progression of liver changes in these patients could be linked to periodontitis; therefore, motivating good oral and periodontal health could result in the prevention and limitation of pathological effects. Given that both types of diseases have a significant inflammatory component, common pro-inflammatory mediators could drive and augment the local inflammation at both a periodontal and hepatic level. This suggests that integrated management of these patients should be proposed, as therapeutical means could deliver an improvement to both periodontal and hepatic statuses. The aim of this review is to gather existing information on the proposed subject and to organize significant data in order to improve scientific accuracy and comprehension on this topic while generating future perspectives for research.
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Affiliation(s)
- Dorin Nicolae Gheorghe
- Department of Periodontology, Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Francesco Bennardo
- School of Dentistry, Department of Health Sciences, Magna Graecia University of Catanzaro, Viale Europa, 88100 Catanzaro, Italy
| | - Dora Maria Popescu
- Department of Periodontology, Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Flavia Mirela Nicolae
- Department of Periodontology, Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Claudiu Marinel Ionele
- Department of Gastroenterology, Faculty of Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Mihail Virgil Boldeanu
- Department of Immunology, Faculty of Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Adrian Camen
- Department of Oral Surgery, Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Ion Rogoveanu
- Department of Gastroenterology, Faculty of Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
| | - Petra Surlin
- Department of Periodontology, Faculty of Dental Medicine, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
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Oliveira CDS, Galdino TM, Limeira FIR, Moreira AN, de Magalhães CS, Abreu LG. Is dental caries associated with liver transplantation? A systematic review and meta-analysis. Oral Dis 2021; 27:1346-1355. [PMID: 32469441 DOI: 10.1111/odi.13439] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/17/2020] [Revised: 05/06/2020] [Accepted: 05/14/2020] [Indexed: 11/28/2022]
Abstract
OBJECTIVE The aim of this systematic review and meta-analysis was to evaluate the experience of dental caries in individuals pre- or postliver transplant. MATERIALS AND METHODS Searches in PubMed, Scopus, Web of Science, Ovid, and Lilacs from databases' inception date up to April 2020 were undertaken. Gray literature and manual searches were also conducted. Observational studies were eligible. The retrieved references were evaluated by two independent reviewers. Meta-analysis and risk of bias assessment using the University of Adelaide tool were conducted. The strength of the evidence was assessed with GRADE. RESULTS The search retrieved 1990 references. Twenty-four cross-sectional studies were included. One subgroup analysis demonstrated no significant difference in the number of teeth with dental caries between pre-liver transplant and healthy individuals (mean difference = 1.65, confidence interval = -0.87 to 4.17). The prevalence of dental caries among pre-liver transplant individuals was 73.82% and in the post-transplant individuals was 72.83%. In the included studies, the main concern regarding risk of bias was the absence of control for confounding variables. The strength of the evidence was very low. CONCLUSIONS Dental caries may be a relevant issue in pre- and postliver transplant individuals. Oral health counseling should be included in the care of pre- and/or postliver transplant individuals.
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Affiliation(s)
- Carla de Souza Oliveira
- Post-Graduate Program in Dentistry, University Federal de Minas Gerais, Belo Horizonte, Brazil
| | - Tuélita Marques Galdino
- Post-Graduate Program in Dentistry, University Federal de Minas Gerais, Belo Horizonte, Brazil
| | | | - Allyson Nogueira Moreira
- Department of Restorative Dentistry, Faculty of Dentistry, University Federal de Minas Gerais, Belo Horizonte, Brazil
| | - Cláudia Silami de Magalhães
- Department of Restorative Dentistry, Faculty of Dentistry, University Federal de Minas Gerais, Belo Horizonte, Brazil
| | - Lucas Guimarães Abreu
- Department of Child and Adolescent Oral Health, Faculty of Dentistry, University Federal de Minas Gerais, Belo Horizonte, Brazil
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Kuraji R, Sekino S, Kapila Y, Numabe Y. Periodontal disease-related nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: An emerging concept of oral-liver axis. Periodontol 2000 2021; 87:204-240. [PMID: 34463983 PMCID: PMC8456799 DOI: 10.1111/prd.12387] [Citation(s) in RCA: 62] [Impact Index Per Article: 15.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
Periodontal disease, a chronic inflammatory disease of the periodontal tissues, is not only a major cause of tooth loss, but it is also known to exacerbate/be associated with various metabolic disorders, such as obesity, diabetes, dyslipidemia, and cardiovascular disease. Recently, growing evidence has suggested that periodontal disease has adverse effects on the pathophysiology of liver disease. In particular, nonalcoholic fatty liver disease, a hepatic manifestation of metabolic syndrome, has been associated with periodontal disease. Nonalcoholic fatty liver disease is characterized by hepatic fat deposition in the absence of a habitual drinking history, viral infections, or autoimmune diseases. A subset of nonalcoholic fatty liver diseases can develop into more severe and progressive forms, namely nonalcoholic steatohepatitis. The latter can lead to cirrhosis and hepatocellular carcinoma, which are end‐stage liver diseases. Extensive research has provided plausible mechanisms to explain how periodontal disease can negatively affect nonalcoholic fatty liver disease and nonalcoholic steatohepatitis, namely via hematogenous or enteral routes. During periodontitis, the liver is under constant exposure to various pathogenic factors that diffuse systemically from the oral cavity, such as bacteria and their by‐products, inflammatory cytokines, and reactive oxygen species, and these can be involved in disease promotion of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Also, gut microbiome dysbiosis induced by enteral translocation of periodontopathic bacteria may impair gut wall barrier function and promote the transfer of hepatotoxins and enterobacteria to the liver through the enterohepatic circulation. Moreover, in a population with metabolic syndrome, the interaction between periodontitis and systemic conditions related to insulin resistance further strengthens the association with nonalcoholic fatty liver disease. However, most of the pathologic links between periodontitis and nonalcoholic fatty liver disease in humans are provided by epidemiologic observational studies, with the causal relationship not yet being established. Several systematic and meta‐analysis studies also show conflicting results. In addition, the effect of periodontal treatment on nonalcoholic fatty liver disease has hardly been studied. Despite these limitations, the global burden of periodontal disease combined with the recent nonalcoholic fatty liver disease epidemic has important clinical and public health implications. Emerging evidence suggests an association between periodontal disease and liver diseases, and thus we propose the term periodontal disease–related nonalcoholic fatty liver disease or periodontal disease–related nonalcoholic steatohepatitis. Continued efforts in this area will pave the way for new diagnostic and therapeutic approaches based on a periodontologic viewpoint to address this life‐threatening liver disease.
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Affiliation(s)
- Ryutaro Kuraji
- Department of Life Science Dentistry, The Nippon Dental University, Tokyo, Japan.,Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo, Japan.,Department of Orofacial Sciences, University of California San Francisco School of Dentistry, San Francisco, California, USA
| | - Satoshi Sekino
- Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo, Japan
| | - Yvonne Kapila
- Department of Orofacial Sciences, University of California San Francisco School of Dentistry, San Francisco, California, USA
| | - Yukihiro Numabe
- Department of Periodontology, The Nippon Dental University School of Life Dentistry at Tokyo, Tokyo, Japan
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6
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Sah AK, Dewangan M, Suresh PK. Potential of chitosan-based carrier for periodontal drug delivery. Colloids Surf B Biointerfaces 2019; 178:185-198. [PMID: 30856588 DOI: 10.1016/j.colsurfb.2019.02.044] [Citation(s) in RCA: 54] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2018] [Revised: 02/18/2019] [Accepted: 02/21/2019] [Indexed: 10/27/2022]
Abstract
Periodontal diseases are chronic infectious diseases and are a major oral health burden. With the progress in the understanding of etiology, epidemiology and pathogenesis of periodontal diseases coupled with the understanding of the polymicrobial synergy in the dysbiotic oral microbial flora, several new therapeutic targets have been identified. The strategies to curb bacterial growth and production of factors that gradually destroy the tissue surrounding and supporting the teeth have been the cornerstone for inhibiting periodontitis. Systemic administration of antibiotics for the treatment of periodontitis have shown several drawbacks including: inadequate antibiotic concentration at the site of the periodontal pocket, a rapid decline of the plasma antibiotic concentration to sub-therapeutic levels, the development of microbial resistance due to sub-therapeutic drug levels and peak-plasma antibiotic concentrations which may be associated with various side effects. These obvious disadvantages have evoked an interest in the development of localized drug delivery systems that can provide an effective concentration of antibiotic at the periodontal site for the duration of the treatment with minimal side effects. A targeted sustained release device which could be inserted in the periodontal pocket and prolong the therapeutic levels at the site of action at a much lower dose is the need of the hour. Chitosan, a deacetylated derivative of chitin has attracted considerable attention owing to its special properties including antimicrobial efficacy, biodegradability, biocompatibility and non-toxicity. It also has the propensity to act as hydrating agent and display tissue healing and osteoinducting effect. The aim of this review is to shine a spotlight on the chitosan based devices developed for drug delivery application in the effective treatment of various periodontal disorders. The chitosan based carriers like fibers, films, sponge, microparticles, nanoparticles, gels that have been designed for sustained release of drug into the periodontal pocket are highlighted.
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Affiliation(s)
- Abhishek K Sah
- Department of Pharmacy, Shri G. S. Institute of Technology & Science, 23-Park Road, Indore, 452003, MP, India
| | - Mahendra Dewangan
- Department of Pharmaceutics, University Institute of Pharmacy, Faculty of Technology, Pt. Ravishankar Shukla University, Raipur, 492010, CG, India
| | - Preeti K Suresh
- Department of Pharmaceutics, University Institute of Pharmacy, Faculty of Technology, Pt. Ravishankar Shukla University, Raipur, 492010, CG, India.
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Ramaglia AHF, Salzedas-Netto AA, Monteiro MM, Pimentel-Mota CFMG, Abranches DC, Rangel EB, Gonzalez AM. Necessidade de tratamento odontológico em pacientes candidatos a transplante simultâneo de pâncreas-rim e fígado num centro único. Rev Col Bras Cir 2019; 46:e20192224. [DOI: 10.1590/0100-6991e-20192224] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2019] [Accepted: 07/02/2019] [Indexed: 12/13/2022] Open
Abstract
RESUMO Objetivo: avaliar as condições bucais e os principais fatores predisponentes para tratamento odontológico de pacientes em lista de espera para transplante simultâneo de pâncreas-rim e para transplante hepático, em um centro único. Métodos: foram avaliados 100 pacientes na fila de espera, 50 candidatos a transplante hepático e 50 a transplante simultâneo de pâncreas-rim, no período de agosto de 2015 a fevereiro de 2018. Exames extra e intrabucais foram correlacionados com variáveis demográficas pré-transplante. Resultados: a principal alteração bucal nos candidatos a transplante de pâncreas-rim e de transplante hepático foram dentes cariados, perdidos e obturados, presentes em 83% e 100% dos candidatos, respectivamente (P=0,03). A necessidade de tratamento odontológico foi igual nos dois grupos: 71% e 70%. Nos candidatos a transplante hepático, os fatores predisponentes para tratamento odontológico foram idade, cor e diagnóstico etiológico da cirrose hepática. Não identificamos fatores predisponentes para tratamento odontológico nos candidatos a transplante simultâneo pâncreas-rim. Conclusão: pacientes candidatos a transplante simultâneo de pâncreas-rim e transplante hepático apresentaram higiene bucal precária com presença de cárie, raízes residuais, gengivite e periodontite, revelando que a avaliação odontológica deve fazer parte do protocolo de atendimento dos pacientes em fila de espera para transplantes.
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Braga Diniz JM, Espaladori MC, Souza E Silva ME, Brito LCN, Vieira LQ, Ribeiro Sobrinho AP. Immunological profile of teeth with inflammatory periapical disease from chronic liver disease patients. Int Endod J 2018; 52:149-157. [PMID: 30091243 DOI: 10.1111/iej.12992] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2017] [Accepted: 08/05/2018] [Indexed: 12/15/2022]
Abstract
AIM To evaluate the mRNA expression levels of the cytokines interferon-γ, tumour necrosis factor-α, interleukin (IL)-1β, IL-10, IL-6, VEGF, and AGT and the chemokine CCL2/MCP-1 in periapical interstitial fluid associated with root canal infections before and after the reduction of the bacterial load using a cleaning procedure. METHODOLOGY The case group included 11 patients with chronic liver disease, and the control group included 11 healthy patients. Clinical samples were taken from teeth with pulp necrosis. After cleaning and drying the canal, three paper points were introduced into the root canal and passed through the root apex (2 mm) into the periapical tissues for 1 min. The samples were collected immediately after root canal cleaning and 7 days later to characterize those gene expression levels using real-time PCR. The data were subjected to the Shapiro-Wilk and the Wilcoxon tests. RESULTS In the control group, significantly increased expression of the pro-inflammatory cytokines IFN-γ and TNF-α was observed in teeth with restrained bacterial loads (day 7) (P < 0.05). Similarly, increased TNF-α expression was found on day 7 in the liver group (P < 0.05). No differences were observed in the expression levels of the IL-1β, IL-10 and, IL-6, MCP-1/CCL-2 and VEGF between the first collection (day 0) and second collection (day 7), over time in either group. CONCLUSION Chronic liver disease patients exhibited sufficient immunologic ability showing relatively similar expression levels of cytokines, chemokines and angiogenic factors in periapical samples compared with the responses from no-chronic liver disease patients. The outcomes of this study suggest that liver impairment did not compromise the periapical immune response.
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Affiliation(s)
- J M Braga Diniz
- Department of Operative Dentistry, School of Dentistry, Federal University of Minas Gerais, Belo Horizonte, Brazil
| | - M C Espaladori
- Department of Operative Dentistry, School of Dentistry, Federal University of Minas Gerais, Belo Horizonte, Brazil
| | - M E Souza E Silva
- Department of Operative Dentistry, School of Dentistry, Federal University of Minas Gerais, Belo Horizonte, Brazil
| | - L C N Brito
- Faculty of Dentistry, University of Itaúna, Itaúna, Brazil
| | - L Q Vieira
- Department of Biochemistry and Immunology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, MG, Brazil
| | - A P Ribeiro Sobrinho
- Department of Operative Dentistry, School of Dentistry, Federal University of Minas Gerais, Belo Horizonte, Brazil
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