Periodontal microbiota and microorganisms isolated from heart valves in patients undergoing valve replacement surgery in a clinic in Cali, Colombia
Abstract
Introduction: Periodontitis is an infectious disease that affects the support tissue of the teeth and it is associated with different systemic diseases, including cardiovascular disease. Microbiological studies facilitate the detection of microorganisms from subgingival and cardiovascular samples.
Objective: To describe the cultivable periodontal microbiota and the presence of microorganisms in heart valves from patients undergoing valve replacement surgery in a clinic in Cali.
Materials and methods: We analyzed 30 subgingival and valvular tissue samples by means of two-phase culture medium, supplemented blood agar and trypticase soy agar with antibiotics. Conventional PCR was performed on samples of valve tissue.
Results: The periodontal pathogens isolated from periodontal pockets were: Fusobacterium nucleatum (50%), Prevotella intermedia/ nigrescens (40%), Campylobacter rectus (40%), Eikenella corrodens (36.7%), Gram negative enteric bacilli (36.7%), Porphyromonas gingivalis (33.3%), and Eubacterium spp. (33.3%). The pathogens isolated from the aortic valve were Propionibacterium acnes (12%), Gram negative enteric bacilli (8%), Bacteroides merdae (4%), and Clostridium bifermentans (4%), and from the mitral valve we isolated P. acnes and Clostridium beijerinckii. Conventional PCR did not return positive results for oral pathogens and bacterial DNA was detected only in two samples.
Conclusions: Periodontal microbiota of patients undergoing surgery for heart valve replacement consisted of species of Gram-negative bacteria that have been associated with infections in extraoral tissues. However, there is no evidence of the presence of periodontal pathogens in valve tissue, because even though there were valve and subgingival samples positive for Gram-negative enteric bacilli, it is not possible to maintain they corresponded to the same phylogenetic origin.
Downloads
References
Darveau R. Periodontitis: A polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010;8:481-90. https://doi.org/10.1038/nrmicro2337
Zijnge V, van Leeuwen B, Degener J, Abbas F, Thurnheer T, Gmur R, et al. Oral biofilm architecture on natural teeth. Plos One. 2012;5:9321. https://doi.org/10.1371/journal.pone. 0009321
Socransky SS, Hafajee AD. Dental biofilms: Difficult thera-peutic targets. Periodontol 2000. 2002;28:12-55. https://doi.org/10.1034/j.1600-0757.2002.280102.x
Desvarieux M, Demmer R, Rundek T, Boden-Albala B, Jacobs D, Papapanou S, et al. Periodontal microbiota and carotid intima-media thickness. Circulation. 2005;111:576-82. https://doi.org/10.1161/01.CIR.0000154582.37101.15
Demmer R, Desvarieux M. Periodontal infections and cardiovascular disease: The heart of the matter. J Am Dent Assoc. 2006;137:S14-20. https://doi.org/10.14219/jada.archive.2006.0402
Parkar SM, Modi GN, Jani J. Periodontitis as risk factor for acute myocardial infarction: A case control study. Heart Views. 2013;14:5-11. https://doi.org/10.4103/1995-705X.107113
Nonnenmacher C, Stelzel M, Susin C, Jacovi L. Periodontal microbiota in patients with coronary artery disease measured by real-time polymerase chain reaction: A case-control study. J Periodontol. 2012;78:1724-30. https://doi.org/10.1902/jop.2007.060345
Gaetti-Jardim E, Marcelino S, Feitosa A, Romito G, Ávila-Campos M. Quantitative detection of periodontopathic bacteria in atherosclerotic plaques from coronary arteries. J Med Microbiol. 2009;58:1568-75. https://doi.org/10.1099/jmm.0.013383-0
Kozarov E. Bacterial invasion of vascular cell types: Vascular infectology and atherogenesis. Future Cardiol. 2012;8:123-38.https://doi.org/10.2217/fca.11.75
Belstrom D, Holmstrup P, Damgaard C, Borch T, Skjodt M, Bendtzen K, et al. The atherogenic bacterium Porphyromonas gingivalis evades circulating phagocytes by adhering to erythrocytes. Infect Immun. 2011;79:1559-65. https://doi.org/10.1128/IAI.01036-10
Rafferty B, Jönsson D, Kalachikov S, Demmer RT, Nowygrod R, Elkind MS, et al. Impact of monocytic cells on recovery of uncultivable bacteria from atherosclerotic lesions. J Intern Med. 2011;270:273-80. https://doi.org/10. 1111/j.1365-2796.2011.02373.x
Costalonga M, Herzberg M. The oral microbiome and the immunobiology of periodontal disease and caries. Immunol Lett. 2014;162:22-38. https://doi.org/10.1016/j.imlet.2014. 08.017
Hajishengallis G. Periodontitis: From microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15:30-44. https://doi.org/10.1038/nri3785
Loos B. Systemic markers of inflammation in periodontitis. J Periodontol. 2005;76:2106-15. https://doi.org/10.1902/jop. 2005.76.11-S.2106
Premoli G, Villareal J, González A. Proteína C reactiva y su relación con la enfermedad periodontal y aterosclerosis. Acta Odontológica Venezolana. 2008;46:1-12.
Thakare K, Deo V, Bhongade M. Evaluation of the C-reactive protein serum levels in periodontitis patients with or without atherosclerosis. Indian J Dent Res. 2010;21:326-9. https://doi.org/10.4103/0970-9290.70787
Persson GR, Persson RE. Cardiovascular disease and periodontitis: An update on the associations and risk. J Clin Periodontol. 2008;35:362-79. https://doi.org/10.1111/j.1600-051X.2008.01281.x
Ramírez J. ¿Es la enfermedad periodontal un factor de riesgo cardiovascular? Revisión de la evidencia experimental y clínica. Rev Estomatol. 2005;2:18-26.
Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontol 2000. 2004;34:9-21. https://doi.org/10.1046/j.0906-6713.2002.003421.x
Jaramillo A, Betancourth M, Mayorga-Fayad I, Castillo D, Aya M, Lafaurie G, et al. Perfiles antimicrobianos de bacterias subgingivales en pacientes con periodontitis en Colombia. Rev Clin Periodoncia Implantol Rehabil Oral. 2008;1:61-5. https://doi.org/10.1016/S0718-5391(08)70010-7
Ashimoto A, Chen C, Bakker I, Slots J. Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol. 1996;11:266-73. https://doi.org/10.1111/j.1399-302X.1996.tb00180.x
Contreras A, Moreno S, Jaramillo A, Peláez M, Duque A, Botero JE, et al. Periodontal microbiology in Latin America. Periodontology. 2000. 2015;67:58-86. https://doi.org/10.1111/prd.12074
Lafaurie G, Contreras A, Barón A, Botero J, Mayorga I, Jaramillo A, et al. Demographic, clinical, and microbial aspects of chronic and aggressive periodontitis in Colombia: A multicenter study. J Periodontol. 2007;78:629-39. https://doi.org/10.1902/jop.2007.060187
Mayorga-Fayad I, Lafaurie GI, Contreras A, Castillo DM, Barón A, Aya M del R. Microflora subgingival en periodontitis crónica y agresiva en Bogotá, Colombia: un acercamiento epidemiológico. Biomédica. 2007;27:21-33. https://doi.org/10.7705/biomedica.v27i1.230
Botero JE, Contreras A, Lafaurie G, Jaramillo A, Betancourt M, Arce RM. Occurrence of periodontopathic and superinfecting bacteria in chronic and aggressive perio-dontitis subjects in a Colombian population. J Periodontol. 2007;78:696-704. https://doi.org/10.1902/jop. 2007.060129
Chapple ILC, Genco R. Diabetes and periodontal diseases: Consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol. 2013;40:106-12. https://doi.org/10.1111/jcpe.12077
Borgnakke WS, Ylostalo PV, Taylor GW, Genco RJ. Effect of periodontal disease on diabetes: Systematic review of epidemiologic observational evidence. J Clin Periodontol. 2013;40:135-52. https://doi.org/10.1111/jcpe.12080
Angeli F, Verdecchia P, Pellegrino C, Pellegrino RG, Pellegrino G, Prosciutti L, et al. Association between periodontal disease and left ventricle mass in essential hypertension. Hypertension. 2003;41:488-92. https://doi.org/10.1161/01.HYP.0000056525.17476.D7
Reyes L, Herrera D, Kozarov E, Roldán S, Progulske-Fox A. Periodontal bacterial invasion and infection: Contribution to atherosclerotic pathology. J Clin Periodontol. 2013;40:30-50. https://doi.org/10.1902/jop.2013.1340012
Nakano K, Nemoto H, Nomura R, Inaba H, Yoshioka H, Taniguchi K, et al. Detection of oral bacteria in cardio-vascular specimens. Oral Microbiol Immunol. 2009:24:64-8. https://doi.org/10.1111/j.1399-302X.2008.00479.x
Kozarov E, Sweier D, Shelburne CH, Progulske-Fox A, Lopatin D. Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect. 2006;8:687-93. https://doi.org/10.1016/j.micinf.2005.09.004
Rafferty B, Dolgilevich S, Kalachikov S, Morozova I, Ju J, Whittier S, et al. Cultivation of Enterobacter hormaechei from human atherosclerotic tissue. J Atheroscler Thromb. 2011;18:72-81. https://doi.org/10.5551/jat.5207
Nakano K, Inaba H, Nomura R, Nemoto H, Tamura K, Miyamoto E, et al. Detection and serotype distribution of Actinobacillus actinomycetemcomitans in cardiovascular specimens from Japanese patients. Oral Microbiol Immunol. 2007:22:136-9. https://doi.org/10.1111/j.1399-302X.2007. 00332.x
Nakano K, Inaba H, Nomura R, Nemoto H, Takeda M, Yoshioka H, et al. Detection of cariogenic Streptococcus mutans in extirpated heart valve and atheromatous plaque specimens. J Clin Microbiol. 2006;44:3313-7. https://doi.org/10.1128/JCM.00377-06
Perry AL, Lambert PA. Propionibacterium acnes. Lett Appl Microbiol. 2006;42:185-8. https://doi.org/10.1111/j.1472-765X.2006.01866.x
Caballero J, Arana R, Calle G, Caballero FJ, Sancho M, Piñero C, et al. Endocarditis aguda sobre válvula aórtica nativa por Propionibacterium acnes. Rev Esp Cardiol. 1997;50:906-8.
Hinestrosa F, Djurkovic S, Bourbeau P, Foltzer M. Propionibacterium acnes as a cause of prosthetic valve aortic root abscess. J Clin Microbiol. 2007;45:259-61. https://doi.org/10.1128/JCM.01598-06
Delahaye F, Fol S, Célard M, Vandenesch F, Beaune J, Bozio A, et al. Propionibacterium acnes infective endocarditis. Study of 11 cases and review of literature. Arch Mal Coeur Vaiss. 2005;98:1212-8.
Kurz M, Kaufmann B, Baddour L, Widmer A. Propionibacterium acnes prosthetic valve endocarditis with abscess formation: A case report. BMC Infect Dis. 2014;14:105. https://doi.org/10.1186/1471-2334-14-105
Scanlan D, Smith M, Isenberg H, Engrassia S, Hilton E. Clostridium bifermentans bacteremia with metastatic osteomyelitis. J Clin Microbiol. 1994;32:2867-8.
Ardila-Medina CM, Alzate-Vega J, Guzmán-Zuluaga IC. Correlación de bacilos entéricos Gram-negativos con pará-metros clínicos y demográficos de pacientes con periodontitis crónica. Av Periodon Implantol. 2014;2677-82.
Sakamoto M, Benno Y. Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov. Int J Syst Evol Microbiol. 2006;56:1599-605. https://doi.org/10.1099/ijs.0.64192-0
Johnson J, Moore W, Moore L. Bacteroides caccae sp. nov., Bacteroides merdae sp. nov., and Bacteroides stercoris sp. nov. isolated from human feces. Int J Syst Bacteriol. 1986; 36:499-501. https://doi.org/10.1099/00207713-36-4-499
Ezeji T, Qureshi N, Blaschek HP. Production of acetone, butanol and ethanol by Clostridium beijerinckii BA101 and in situ recovery by gas stripping. World J Microbiol Biotechnol. 2003;19:595-603. https://doi.org/10.1023/A: 1025103011923
Cairo F, Gaeta C, Dorigo W, Oggioni MR, Pratesi C, Pini Prato GP, et al. Periodontal pathogens in atheromatous plaques. A controlled clinical and laboratory trial. J Periodontal Res. 2004;39:442-6. https://doi.org/10.1111/j.1600-0765.2004.00761.x
Radwan M, Jaworski A, Duś I, Plonek T, Szulc M, Kustrzycki W. Porphyromonas gingivalis in periodontal pockets and heart valves. Virulence. 2014;5:575-80. https://doi.org/10.4161/viru.28657
Some similar items:
- Martine Bonnaure-Mallet, Paula Juliana Pérez-Chaparro, Patrice Gracieux, Vincent Meuric, Zohreh Tamanai-Shacoori, Jaime Eduardo Castellanos, Distribution of Porphyromonas gingivalis fimA genotypes in isolates from subgingival plaque and blood sample during bacteremia , Biomedica: Vol. 29 No. 2 (2009)
- Jessika Consuegra, Sonia Jakeline Gutiérrez, Adriana Jaramillo, Ignacio Sanz, Gilberto Olave, Jorge Enrique Soto, Carlos Valencia, Adolfo Contreras, Enteric Gram negative rods and unfermented of glucose bacteria in patients with peri-implant disease , Biomedica: Vol. 31 No. 1 (2011)
- Sandra Paola Ochoa, Carlos Andrés Ospina, Kelly Johana Colorado, Yenny Paola Montoya, Andrés Fernando Saldarriaga, Marisol Miranda, Natalia Muñoz, María Eugenia Gómez, Fanny Lucía Yepes, Javier Enrique Botero, Periodontal condition and tooth loss in diabetic patients , Biomedica: Vol. 32 No. 1 (2012)
- Anna Carolina Ratto-Tespestini, Paula Juliana Pérez-Chaparro, Giuseppe Alexandre Romito, Luciene Cristina Figueiredo, Marcelo Faveri, Hilana Paula Carillo, Priscila Larcher, Magda Feres, Comparison of independent and dependent culture methods for the detection of transient bacteremia in diabetic subjects with chronic periodontitis , Biomedica: Vol. 36 No. 1 (2016)
- Juana P. Sánchez-Villamil, Carolina Pino-Vélez, Juanita Trejos-Suárez, Néstor Cardona , Dra. Ana, Pedro A. Alfonso, Salivary markers of oxidative stress and periodontal pathogens in patients with periodontitis from Santander, Colombia , Biomedica: Vol. 40 No. Supl. 1 (2020): Mayo, Infecciones en el trópico
- Martha Graciela Fuentes-Lerma, Ana Lourdes Zamora-Pérez, Cecilia Robles-Gómez, Celia Guerrero-Velázquez, Jorge Peregrina-Sandoval, Melva Gutiérrez-Angulo, Rocío Patricia Mariaud-Schmidt, Serum nitric oxide concentration in generalized chronic and aggressive periodontitis in the Mexican population is not related to the severity of the disease. , Biomedica: Vol. 43 No. 1 (2023)
- Mónica Gabriela Huertas , Miguel Rodríguez, Patricia Castro, Sergio Danilo Cruz, Erika Alejandra Cifuentes, Andrés Felipe Yepes, María Mercedes Zambrano , Ana Margarita Baldión, Description of the colonizing mycobiota of endotracheal tubes from patients admitted to two intensive care units in Bogotá, Colombia , Biomedica: Vol. 43 No. Sp. 1 (2023): Agosto, Micología médica
- Martha Puello, Gregorio Young, Paola Suárez, Phospholipase and proteinase activities of isolates of colonizing Candida spp. causing vulvovaginitis in pregnant women , Biomedica: Vol. 43 No. Sp. 1 (2023): Agosto, Micología médica

Article metrics | |
---|---|
Abstract views | |
Galley vies | |
PDF Views | |
HTML views | |
Other views |