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Actividad antimicrobiana de extractos enológicos y vino sobre los patógenos Porphyronomas gingivalis, Aggregatibacter actinomycentemcomitans y Fusobacterium nucleatum incluidos en un modelo de biopelícula oral in vitro

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2017
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Objetivos Investigaciones anteriores avalan la capacidad antimicrobiana de los polifenoles frente a diversos patógenos, sin embargo, la evidencia disponible sobre la eficacia de su efecto contra los patógenos periodontales es aún escasa. Dado que las bacterias se organizan en biopelículas en la cavidad oral, el objetivo de este estudio es analizar la capacidad antimicrobiana del vino y de diferentes extractos enológicos sobre los patógenos periodontales Porphyromonas gingivalis, Aggregatibacter actinomycentemcomitans y Fusobacterium nucleatum, y en el recuento total de bacterias incluidas en un modelo de biopelícula oral in vitro. Materiales y métodos Se utilizó un modelo in vitro estático de biopelícula, que incluye seis especies bacterianas implicadas en el desarrollo de la biopelícula oral subgingival in vivo, representando colonizadores iniciales (Streptococcus oralis y Actinomyces naeslundii), tempranos (Veillonela parvula), secundarios (F. nucleatum) y colonizadores tardíos (P. gingivalis y A. actinomycetemcomitans). Las biopelículas se formaron sobre discos estériles de hidroxiapatita, en placas de cultivo. Tras 72 h de incubación, se expusieron las biopelículas por inmersión durante 1 y 5 minutos a las soluciones de vino (desalcoholizado o no) y durante 30 segundos y 1 minuto a los extractos enológicos ProvinolsTM y Vitaflavan®. Se usaron como controles, tampón fosfato salino (PBS, por sus siglas en inglés), Dimetilsulfóxido (DMSO) al 4% y Etanol (EtOH) al 12%. El recuento de las bacterias vivas antes y después del tratamiento, expresadas como unidades formadoras de colonias por mililitro (UFC/mL), se evaluaron mediante la técnica cuantitativa de la reacción en cadena de la polimerasa (qPCR) combinada con Propidio de MonoAzida (PMA). Resultados El vino tinto y el vino tinto desalcoholizado, causaron una reducción estadísticamente significativa en el recuento de A. actinomycetemcomitans, P. gingivalis, F. nucleatum y en el recuento total de las bacterias incluidas en una biopelícula multi-especie, generada in vitro después de 5 minutos de exposición. Solamente P. gingivalis sufrió una reducción de la vitalidad después de 1 minuto de tratamiento tanto con el vino tinto como con la solución desalcoholizada. Se encontraron diferencias estadísticamente significativas en A. actinomycetemcomitans, F. nucleatum y en el número total de bacterias de la biopelícula después de la exposición de 30 segundos y 1 minuto ante los extractos ProvinolsTM y Vitaflavan®, con un efecto menor sobre P. gingivalis. Significación Los resultados proporcionan evidencia de que el vino tinto (desalcoholizado o no) y los extractos enológicos utilizados en el estudio (ProvinolsTM y Vitaflavan®) tienen efecto para de reducir la carga total bacteriana, sugiriendo que los patógenos periodontales A. actinomycetemcomitans, P. gingivalis y F. nucleatum son susceptibles a la acción de los mismos.
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• Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I. & Dewhirst, F. E. (2005) Defining the normal bacterial flora of the oral cavity. Journal of Clinical Microbiology 43, 5721-5732. • Arts, I. C. W. & Hollman, P. C. H. (2005) Polyphenols and disease risk in epidemiologic studies. The American Journal of Clinical Nutrition 81, 317S-325S. • Badet, C. & Quero, F. (2011) The in vitro effect of manuka honeys on growth and adherence of oral bacteria. Anaerobe 17, 19-22. • Bakri, I. M. & Douglas, C. W. I. (2005) Inhibitory effect of garlic extract on oral bacteria. Archives of Oral Biology 50, 645-651. • Beecher, G. R. (2003) Overview of dietary flavonoids: nomenclature, occurrence and intake. The Journal of Nutrition 133, 3248S-3254S. • Beikler, T., Abdeen, G., Schnitzer, S., Sälzer, S., Ehmke, B., Heinecke, A. & Flemmig, T. F. (2004) Microbiological shifts in intra-and extraoral habitats following mechanical periodontal therapy. Journal of Clinical Periodontology 31, 777-783. • Boutaga, K., van Winkelhoff, A. J., Vandenbroucke-Grauls, C. M. J. E. & Savelkoul, P. H. M. (2003) Comparison of real-time PCR and culture for detection of Porphyromonas gingivalis in subgingival plaque samples. Journal of Clinical Microbiology 41, 4950-4954. • Boutaga, K., van Winkelhoff, A. J., Vandenbroucke-Grauls, C. M. J. E. & Savelkoul, P. H. M. (2005) Periodontal pathogens: a quantitative comparison of anaerobic culture and real-time PCR. FEMS immunology and medical microbiology 45, 191-199. • • Choi, J.-S., Ha, Y.-M., Joo, C.-U., Cho, K. K., Kim, S.-J. & Choi, I. S. (2012) Inhibition of oral pathogens and collagenase activity by seaweed extracts. Journal of Environmental Biology 33, 115-121 • Christersson, L. A., Slots, J., Rosling, B. G. & Genco, R. J. (1985) Microbiological and clinical effects of surgical treatment of localized juvenile periodontitis. Journal of Clinical Periodontology 12, 465-476 • Cobb, C. M. (2002) Clinical significance of non-surgical periodontal therapy: an evidence-based perspective of scaling and root planing. Journal of Clinical Periodontology 29 Suppl 2, 6-16. • • Cueva, C., Mingo, S., Muñoz-González, I., Bustos, I., Requena, T., del Campo, R., Martín-Álvarez, • P. J., Bartolomé, B. & Moreno-Arribas, M. V. (2012) Antibacterial activity of wine phenolic compounds and oenological extracts against potential respiratory pathogens. Letters in Applied Microbiology 54, 557-563. • Daglia, M., Papetti, A., Grisoli, P., Aceti, C., Dacarro, C. & Gazzani, G. (2007) Antibacterial activity of red and white wine against oral streptococci. Journal of Agricultural and Food Chemistry 55, 5038-5042. • Daroch, F., Hoeneisen, M., González, C. L., Kawaguchi, F., Salgado, F., Solar, H. & García, A. (2001) In vitro antibacterial activity of Chilean red wines against Helicobacter pylori. Microbios 104, 79-85 • Davey, M. E. & Costerton, J. W. (2006) Molecular genetics analyses of biofilm formation in oral isolates. Periodontology 2000 42, 13-26 • Dolara, P., Arrigucci, S., Cassetta, M. I., Fallani, S. & Novelli, A. (2005) Inhibitory activity of diluted wine on bacterial growth: the secret of water purification in antiquity. International Journal of Antimicrobial Agents 26, 338-340. • Furiga, A., Lonvaud-Funel, A., Dorignac, G. & Badet, C. (2008) In vitro anti-bacterial and anti¬adherence effects of natural polyphenolic compounds on oral bacteria. Journal of Applied Microbiology 105, 1470-1476. • Furiga, A., Roques, C. & Badet, C. (2014) Preventive effects of an original combination of grape seed polyphenols with amine fluoride on dental biofilm formation and oxidative damage by oral bacteria. Journal of Applied Microbiology 116, 761-771. • Geoghegan, F., Wong, R. W. K. & Rabie, A. B. M. (2010) Inhibitory effect of quercetin on periodontal pathogens in vitro. Phytotherapy Research: PTR 24, 817-820. • Graf, B. A., Milbury, P. E. & Blumberg, J. B. (2005) Flavonols, flavones, flavanones, and human health: epidemiological evidence. Journal of Medicinal Food 8, 281-290. • Haffajee, A. D. & Socransky, S. S. (1994) Microbial etiological agents of destructive periodontal diseases. Periodontology 2000 5, 78-111. • Haffajee, A. D., Teles, R. P. & Socransky, S. S. (2006) The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontology 2000 42, 219-258. • Hannig, C., Sorg, J., Spitzmüller, B., Hannig, M. & Al-Ahmad, A. (2009) Polyphenolic beverages reduce initial bacterial adherence to enamel in situ. Journal of Dentistry 37, 560-566. • Heitz-Mayfield, L. J. A., Trombelli, L., Heitz, F., Needleman, I. & Moles, D. (2002) A systematic review of the effect of surgical debridement vs non-surgical debridement for the treatment of chronic periodontitis. Journal of Clinical Periodontology 29 Suppl 3, 92-102-discussion 160¬102 • Helm, L. & Macdonald, I. A. (2015) Impact of beverage intake on metabolic and cardiovascular health. Nutrition Reviews 73 Suppl 2, 120-129. • • Herrera, D., Matesanz, P., Bascones-Martínez, A. & Sanz, M. (2012) Local and systemic antimicrobial therapy in periodontics. The journal of Evidence-Based Dental Practice 12, 50¬60. • Hersh, E. V. & Moore, P. A. (2008) Adverse drug interactions in dentistry. Periodontology 2000 46, 109-142 • Hill, D. A., Hoffmann, C., Abt, M. C., Du, Y., Kobuley, D., Kirn, T. J., Bushman, F. D. & Artis, D. (2010) Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunology 3, 148-158 • Hirasawa, M., Takada, K., Makimura, M. & Otake, S. (2002) Improvement of periodontal status by green tea catechin using a local delivery system: a clinical pilot study. Journal of Periodontal Research 37, 433-438. • Kang, M.-S., Oh, J.-S., Kang, I.-C., Hong, S.-J. & Choi, C.-H. (2008) Inhibitory effect of methyl gallate and gallic acid on oral bacteria. Journal of Microbiology (Seoul, Korea) 46, 744-750. • Kornman, K. S. & Robertson, P. B. (1985) Clinical and microbiological evaluation of therapy for juvenile periodontitis. Journal of Periodontology 56, 443-446. • La, V. D., Howell, A. B. & Grenier, D. (2010) Anti-Porphyromonas gingivalis and anti¬inflammatory activities of A-type cranberry proanthocyanidins. Antimicrobial Agents and Chemotherapy 54, 1778-1784. • Li, M. & Xu, Z. (2008) Quercetin in a lotus leaves extract may be responsible for antibacterial activity. Archives of Pharmacal Research 31, 640-644. • Listgarten, M. A. (1988) Bacterial invasion of periodontal tissues. Journal of Periodontology 59, 412-413. • Mah, T. F. & O'Toole, G. A. (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends in Microbiology 9, 34-39. • Mahady, G. B., Pendland, S. L. & Chadwick, L. R. (2003) Resveratrol and red wine extracts inhibit the growth of CagA+ strains of Helicobacter pylori in vitro. The American Journal of Gastroenterology 98, 1440-1441. • Marsh, P. & Martin, M. (1992) Oral Microbiology. Boston, MA: Springer US. • Marsh, P. D. (1994) Microbial ecology of dental plaque and its significance in health and disease. Advances in Dental Research 8, 263-271. • Marsh, P. D. (2005) Dental plaque: biological significance of a biofilm and community life-style. Journal of Clinical Periodontology 32 Suppl 6, 7-15. • Marsh, P. D., Moter, A. & Devine, D. A. (2011) Dental plaque biofilms: communities, conflict and control. Periodontology 2000 55, 16-35. • • Matesanz-Pérez, P., García-Gargallo, M., Figuero, E., Bascones-Martínez, A., Sanz, M. & Herrera, • D. (2013) A systematic review on the effects of local antimicrobials as adjuncts to subgingival debridement, compared with subgingival debridement alone, in the treatment of chronic periodontitis. Journal of Clinical Periodontology 40, 227-241. • Middleton, E., Kandaswami, C. & Theoharides, T. C. (2000) The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacological Reviews 52, 673-751. • Mitjavila, M. T. & Moreno, J. J. (2012) The effects of polyphenols on oxidative stress and the arachidonic acid cascade. Implications for the prevention/treatment of high prevalence diseases. Biochemical Pharmacology 84, 1113-1122. • Mombelli, A., Gmür, R., Gobbi, C. & Lang, N. P. (1994) Actinobacillus actinomycetemcomitans in adult periodontitis. II. Characterization of isolated strains and effect of mechanical periodontal treatment. Journal of Periodontology 65, 827-834. • Mombelli, A., Gmür, R., Gobbi, C. & Lang, N. P. (1994) Actinobacillus actinomycetemcomitans in adult periodontitis. I. Topographic distribution before and after treatment. Journal of Periodontology 65, 820-826. • • Mombelli, A., Schmid, B., Rutar, A. & Lang, N. P. (2000) Persistence patterns of Porphyromonas • gingivalis, Prevotella intermedia/nigrescens, and Actinobacillus actinomyetemcomitans after mechanical therapy of periodontal disease. Journal of Periodontology 71, 14-21. • Monagas, M., Gómez-Cordovés, C., Bartolomé, B., Laureano, O. & Ricardo da Silva, J. M. (2003) Monomeric, oligomeric, and polymeric flavan-3-ol composition of wines and grapes from Vitis vinifera L. Cv. Graciano, Tempranillo, and Cabernet Sauvignon. Journal of Agricultural and Food Chemistry 51, 6475-6481. • • Muñoz-González, I., Jiménez-Girón, A., Martín-Álvarez, P. J., Bartolomé, B. & Moreno-Arribas, • M. V. (2013) Profiling of microbial-derived phenolic metabolites in human feces after moderate red wine intake. Journal of Agricultural and Food Chemistry 61, 9470-9479. • Muñoz-González, I., Thurnheer, T., Bartolomé, B. & Moreno-Arribas, M. V. (2014) Red wine and oenological extracts display antimicrobial effects in an oral bacteria biofilm model. Journal of Agricultural and Food Chemistry 62, 4731-4737. • Nadkarni, M. A., Martin, F. E., Jacques, N. A. & Hunter, N. (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology (Reading, England) 148, 257-266. • • Navarro, L., Zarazaga, M., Sáenz, J., Ruiz-Larrea, F. & Torres, C. (2000) Bacteriocin production by lactic acid bacteria isolated from Rioja red wines. Journal of Applied Microbiology 88, 44¬51. • Page, R. C. & Kornman, K. S. (1997) The pathogenesis of human periodontitis: an introduction. Periodontology 2000 14, 9-11. • Palaska, I., Papathanasiou, E. & Theoharides, T. C. (2013) Use of polyphenols in periodontal inflammation. European Journal of Pharmacology 720, 77-83. • Pandey, K. B. & Rizvi, S. I. (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Medicine and Cellular Longevity 2, 270-278. • Papapanou, P. N. (2002) Population studies of microbial ecology in periodontal health and disease. Annals of Periodontology 7, 54-61. • Papapanou, P. N., Neiderud, A. M., Papadimitriou, A., Sandros, J. & Dahlen, G. (2000) "Checkerboard" assessments of periodontal microbiota and serum antibody responses: a case-control study. Journal of Periodontology 71, 885-897. • Percival, R. S., Devine, D. A., Duggal, M. S., Chartron, S. & Marsh, P. D. (2006) The effect of cocoa polyphenols on the growth, metabolism, and biofilm formation by Streptococcus mutans and Streptococcus sanguinis. European Journal of Oral Sciences 114, 343-348. • Quirynen, M. & Van Assche, N. (2011) Microbial changes after full-mouth tooth extraction, followed by 2-stage implant placement. Journal of Clinical Periodontology 38, 581-589. • Rams, T. E., Degener, J. E. & van Winkelhoff, A. J. (2014) Antibiotic resistance in human peri-implantitis microbiota. Clinical Oral Implants Research 25, 82-90. • Rams, T. E. & Slots, J. (1996) Local delivery of antimicrobial agents in the periodontal pocket. Periodontology 2000 10, 139-159. • Sachdeo, A., Haffajee, A. D. & Socransky, S. S. (2008) Biofilms in the edentulous oral cavity. Journal of Prosthodontics : Official Journal of the American College of Prosthodontists 17, 348-356. • Sakanaka, S., Aizawa, M., Kim, M. & Yamamoto, T. (1996) Inhibitory effects of green tea polyphenols on growth and cellular adherence of an oral bacterium, Porphyromonas gingivalis. Bioscience, Biotechnology, and Biochemistry 60, 745-749. • • Sampaio, F. C., Pereira, M. d. S. V., Dias, C. S., Costa, V. C. O., Conde, N. C. O. & Buzalaf, M. A. • R. (2009) In vitro antimicrobial activity of Caesalpinia ferrea Martius fruits against oral pathogens. Journal of Ethnopharmacology 124, 289-294. • • Sánchez, M. C., Llama-Palacios, A., Blanc, V., León, R., Herrera, D. & Sanz, M. (2011) Structure, • viability and bacterial kinetics of an in vitro biofilm model using six bacteria from the subgingival microbiota. Journal of Periodontal Research 46, 252-260. • Sánchez, M. C., Marín, M. J., Figuero, E., Llama-Palacios, A., León, R., Blanc, V., Herrera, D. & Sanz, M. (2014) Quantitative real-time PCR combined with propidium monoazide for the selective quantification of viable periodontal pathogens in an in vitro subgingival biofilm model. Journal of Periodontal Research 49, 20-28. • Serrano, J., Escribano, M., Roldán, S., Martín, C. & Herrera, D. (2015) Efficacy of adjunctive anti-plaque chemical agents in managing gingivitis: a systematic review and meta-analysis. Journal of Clinical Periodontology 42 Suppl 16, S106-138. • Shahzad, M., Millhouse, E., Culshaw, S., Edwards, C. A., Ramage, G. & Combet, E. (2015) Selected dietary (poly)phenols inhibit periodontal pathogen growth and biofilm formation. Food & Function 6, 719-729. • • Slots, J. & Rosling, B. G. (1983) Suppression of the periodontopathic microflora in localized juvenile periodontitis by systemic tetracycline. Journal of Clinical Periodontology 10, 465¬486. • Socransky, S. S. & Haffajee, A. D. (2002) Dental biofilms: difficult therapeutic targets. Periodontology 2000 28, 12-55. • Socransky, S. S. & Haffajee, A. D. (2005) Periodontal microbial ecology. Periodontology 2000 38, 135-187. • Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C. & Kent, R. L. (1998) Microbial complexes in subgingival plaque. Journal of Clinical Periodontology 25, 134-144. • Sugita-Konishi, Y., Hara-Kudo, Y., Iwamoto, T. & Kondo, K. (2001) Wine has activity against entero-pathogenic bacteria in vitro but not in vivo. Bioscience, Biotechnology, and Biochemistry 65, 954-957. • Teles, R., Teles, F., Frias-Lopez, J., Paster, B. & Haffajee, A. (2013) Lessons learned and unlearned in periodontal microbiology. Periodontology 2000 62, 95-162. • Thimothe, J., Bonsi, I. A., Padilla-Zakour, O. I. & Koo, H. (2007) Chemical characterization of red wine grape (Vitis vinifera and Vitis interspecific hybrids) and pomace phenolic extracts and their biological activity against Streptococcus mutans. Journal of Agricultural and Food Chemistry 55, 10200-10207. • Tonetti, M. S., Chapple, I. L. C. & Working Group 3 of Seventh European Workshop on, P. Biological approaches to the development of novel periodontal therapies--consensus of the Seventh European Workshop on Periodontology. In: Journal of Clinical Periodontology, Suppl. 1 edition, pp. 114-118. Blackwell Publishing Ltd. • • Toukairin, T., Uchino, K., Iwamoto, M., Murakami, S., Tatebayashi, T., Ogawara, H. & Tonosaki, • Y. (1991) New polyphenolic 5'-nucleotidase inhibitors isolated from the wine grape "Koshu" and their biological effects. Chemical & Pharmaceutical Bulletin 39, 1480-1483. • Tsui, V. W. K., Wong, R. W. K. & Rabie, A. B. M. (2008) The inhibitory effects of naringin on the growth of periodontal pathogens in vitro. Phytotherapy Research : PTR 22, 401-406. • Van der Weijden, G. A. & Timmerman, M. F. (2002) A systematic review on the clinical efficacy of subgingival debridement in the treatment of chronic periodontitis. Journal of Clinical Periodontology 29 Suppl 3, 55-71-discussion 90-51. • Van Strydonck, D. A. C., Slot, D. E., Van der Velden, U. & Van der Weijden, F. (2012) Effect of a chlorhexidine mouthrinse on plaque, gingival inflammation and staining in gingivitis patients: a systematic review. Journal of Clinical Periodontology 39, 1042-1055. • van Winkelhoff, A. J. (2012) Antibiotics in the treatment of peri-implantitis. European Journal of Oral Implantology 5 Suppl, S43-50. • • White, D. A., Tsakos, G., Pitts, N. B., Fuller, E., Douglas, G. V. A., Murray, J. J. & Steele, J. G. (2012) Adult Dental Health Survey 2009: common oral health conditions and their impact • on the population. British Dental Journal 213, 567-572. • Wu, C. D. (2009) Grape products and oral health. The Journal of Nutrition 139, 1818S-1823S. • Xie, Q., Li, J. & Zhou, X. (2008) Anticaries effect of compounds extracted from Galla chinensis in a multispecies biofilm model. Oral Microbiology and Immunology 23, 459-465. • Yamamoto, H. & Ogawa, T. (2002) Antimicrobial activity of perilla seed polyphenols against oral pathogenic bacteria. Bioscience, Biotechnology, and Biochemistry 66, 921-924. • Yamanaka, A., Kouchi, T., Kasai, K., Kato, T., Ishihara, K. & Okuda, K. (2007) Inhibitory effect of cranberry polyphenol on biofilm formation and cysteine proteases of Porphyromonas gingivalis. Journal of Periodontal Research 42, 589-592.