Black Tea Extract and Its Theaflavin Derivatives Inhibit the Growth of Periodontopathogens and Modulate Interleukin-8 and β-Defensin Secretion in Oral Epithelial Cells

Over the years, several studies have brought evidence suggesting that tea polyphenols, mostly from green tea, may have oral health benefits. Since few data are available concerning the beneficial properties of black tea and its theaflavin derivatives against periodontal disease, the objective of this study was to investigate their antibacterial activity as well as their ability to modulate interleukin-8 and human β-defensin (hBD) secretion in oral epithelial cells. Among the periodontopathogenic bacteria tested, Porphyromonas gingivalis was found to be highly susceptible to the black tea extract and theaflavins. Moreover, our data indicated that the black tea extract, theaflavin and theaflavin-3,3’-digallate can potentiate the antibacterial effect of metronidazole and tetracycline against P. gingivalis. Using lipopolysaccharide-stimulated oral epithelial cells, the black tea extract (100 μg/ml), as well as theaflavin and theaflavin-3,3’-digallate (50 μg/ml) reduced interleukin-8 (IL-8) secretion by 85%, 79%, and 86%, respectively, thus suggesting an anti-inflammatory property. The ability of the black tea extract and its theaflavin derivatives to induce the secretion of the antimicrobial peptides hBD-1, hBD-2 and hBD-4 by oral epithelial cells was then evaluated. Our results showed that the black tea extract as well as theaflavin-3,3’-digallate were able to increase the secretion of the three hBDs. In conclusion, the ability of a black tea extract and theaflavins to exert antibacterial activity against major periodontopathogens, to attenuate the secretion of IL-8, and to induce hBD secretion in oral epithelial cells suggest that these components may have a beneficial effect against periodontal disease.

[1]  J. Gamonal,et al.  Characterization of cellular infiltrate, detection of chemokine receptor CCR5 and interleukin-8 and RANTES chemokines in adult periodontitis. , 2001, Journal of periodontal research.

[2]  D. Aizenbud,et al.  Green tea: a promising natural product in oral health. , 2012, Archives of oral biology.

[3]  S. Kashket,et al.  Inhibition of Salivary Amylase by Black and Green Teas and Their Effects on the Intraoral Hydrolysis of Starch , 1998, Caries Research.

[4]  Vasundhara Sharma,et al.  A Thought on the Biological Activities of Black Tea , 2009, Critical reviews in food science and nutrition.

[5]  M. Gamaa,et al.  ound healing activity of the human antimicrobial peptide LL 37 , 2011 .

[6]  H. Azakami,et al.  Effects of the tea catechin epigallocatechin gallate on Porphyromonas gingivalis biofilms , 2014, Journal of applied microbiology.

[7]  Craig S. Miller,et al.  Periodontal disease immunology: 'double indemnity' in protecting the host. , 2013, Periodontology 2000.

[8]  M. Friedman,et al.  Molecular binding of black tea theaflavins to biological membranes: relationship to bioactivities. , 2011, Journal of agricultural and food chemistry.

[9]  T. Kawai,et al.  Susceptibility of periodontopathogenic and cariogenic bacteria to defensins and potential therapeutic use of defensins in oral diseases. , 2007, Current pharmaceutical design.

[10]  K. Takada,et al.  Improvement of periodontal status by green tea catechin using a local delivery system: a clinical pilot study. , 2002, Journal of periodontal research.

[11]  Aditi Jain,et al.  Tea and human health: the dark shadows. , 2013, Toxicology letters.

[12]  M. Pinto Tea: A new perspective on health benefits , 2013 .

[13]  U. Malik,et al.  Tea and Its Consumption: Benefits and Risks , 2015, Critical reviews in food science and nutrition.

[14]  Reyes Artacho,et al.  Beneficial Effects of Green Tea—A Review , 2006, Journal of the American College of Nutrition.

[15]  M. Iriti,et al.  Plant polyphenols and oral health: old phytochemicals for new fields. , 2012, Current medicinal chemistry.

[16]  W. Loesche,et al.  Periodontal Disease as a Specific, albeit Chronic, Infection: Diagnosis and Treatment , 2001, Clinical Microbiology Reviews.

[17]  S. Haswell,et al.  Synergistic antibacterial effects of theaflavin in combination with ampicillin against hospital isolates of Stenotrophomonas Maltophilia , 2012 .

[18]  G. Garlet,et al.  Chemokines in Oral Inflammatory Diseases: Apical Periodontitis and Periodontal Disease , 2007, Journal of dental research.

[19]  Lingxue Kong,et al.  Theaflavins inhibit pathogenic properties of P. gingivalis and MMPs production in P. gingivalis-stimulated human gingival fibroblasts. , 2015, Archives of oral biology.

[20]  W. K. Leung,et al.  Relationship of changes in interleukin-8 levels and granulocyte elastase activity in gingival crevicular fluid to subgingival periodontopathogens following non-surgical periodontal therapy in subjects with chronic periodontitis. , 2002, Journal of clinical periodontology.

[21]  T. Theoharides,et al.  Use of polyphenols in periodontal inflammation. , 2013, European journal of pharmacology.

[22]  D. Grenier,et al.  Green tea extract and its major constituent, epigallocatechin-3-gallate, induce epithelial beta-defensin secretion and prevent beta-defensin degradation by Porphyromonas gingivalis. , 2014, Journal of periodontal research.

[23]  S. Socransky,et al.  Microbial complexes in subgingival plaque. , 1998, Journal of clinical periodontology.

[24]  A. Kantarcı,et al.  Inflammatory and immune pathways in the pathogenesis of periodontal disease. , 2014, Periodontology 2000.

[25]  S. Kuriyama,et al.  Association between green tea consumption and tooth loss: cross-sectional results from the Ohsaki Cohort 2006 Study. , 2010, Preventive medicine.

[26]  R. F. Middleton,et al.  The fractional inhibitory concentration (FIC) index as a measure of synergy. , 1983, The Journal of antimicrobial chemotherapy.

[27]  Y. Shimazaki,et al.  Relationship Between Intake of Green Tea and Periodontal Disease , 2009 .

[28]  Y. Shimazaki,et al.  Relationship between intake of green tea and periodontal disease. , 2009, Journal of periodontology.

[29]  U. Lerner,et al.  Cytokine responses against periodontal infection: protective and destructive roles. , 2010, Periodontology 2000.

[30]  M. Kagnoff,et al.  Epithelial cells as sensors for microbial infection. , 1997, The Journal of clinical investigation.

[31]  Xuedong Zhou,et al.  The Tea Catechin Epigallocatechin Gallate Suppresses Cariogenic Virulence Factors of Streptococcus mutans , 2010, Antimicrobial Agents and Chemotherapy.

[32]  B. Dale Periodontal epithelium: a newly recognized role in health and disease. , 2002, Periodontology 2000.

[33]  L. Domingues,et al.  Wound healing activity of the human antimicrobial peptide LL37 , 2011, Peptides.

[34]  H. Wong,et al.  Theaflavin, a black tea extract, is a novel anti-inflammatory compound , 2004, Critical care medicine.

[35]  C. Ruxton,et al.  Black tea – helpful or harmful? A review of the evidence , 2007, European Journal of Clinical Nutrition.

[36]  Mark A Reynolds,et al.  State of the science: chronic periodontitis and systemic health. , 2012, The journal of evidence-based dental practice.

[37]  D. Grenier,et al.  Green tea extract and its major constituent epigallocatechin-3-gallate inhibit growth and halitosis-related properties of Solobacterium moorei , 2015, BMC Complementary and Alternative Medicine.

[38]  H. Dommisch,et al.  Expression of defensins in gingiva and their role in periodontal health and disease. , 2007, Current pharmaceutical design.

[39]  Q. Vuong Epidemiological Evidence Linking Tea Consumption to Human Health: A Review , 2014, Critical reviews in food science and nutrition.

[40]  T. Matsuo,et al.  Tea polyphenols inhibit IL-6 production in tumor necrosis factor superfamily 14-stimulated human gingival fibroblasts. , 2010, Molecular nutrition & food research.

[41]  M. Rouabhia,et al.  Porphyromonas gingivalis-Epithelial Cell Interactions in Periodontitis , 2006, Journal of dental research.

[42]  I. Chapple,et al.  Differential activation of NF‐κB and gene expression in oral epithelial cells by periodontal pathogens , 2007, Clinical and experimental immunology.

[43]  I. Khouly,et al.  Effectiveness of systemic antimicrobial therapy in combination with scaling and root planing in the treatment of periodontitis: a systematic review. , 2015, Journal of the American Dental Association.

[44]  R. Darveau,et al.  Microbial shift and periodontitis. , 2011, Periodontology 2000.

[45]  J. Slots,et al.  Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in human periodontal disease: occurrence and treatment. , 1999, Periodontology 2000.

[46]  S. Brand,et al.  Human beta defensin 2 promotes intestinal wound healing in vitro , 2008, Journal of cellular biochemistry.

[47]  Hang Xiao,et al.  Black Tea Polyphenols: A Mechanistic Treatise , 2014, Critical reviews in food science and nutrition.

[48]  E. Könönen,et al.  Understanding the roles of gingival beta-defensins , 2012, Journal of oral microbiology.