La Inflamación Como el Nexo Entre la Enfermedad Periodontal y la Enfermedad Cardiovascular

Autores/as

  • L N Nicolosi Universidad de Buenos Aires. Facultad de Odontología. Cátedra de Medicina Interna. Buenos Aires, Argentina. / Hospital Español de Buenos Aires. Buenos Aires, Argentina.
  • M C Rubio Universidad de Buenos Aires. Facultad de Odontología. Cátedra de Medicina Interna. Buenos Aires, Argentina. / Hospital Español de Buenos Aires. Buenos Aires, Argentina.
  • S M Friedman Universidad de Buenos Aires. Facultad de Odontología. Cátedra de Bioquímica General y Bucal. Buenos Aires, Argentina.

Palabras clave:

periodontitis, hipertensión arterial, infarto agudo de miocardio, demencia, enfermedad cardiovascular

Resumen

La periodontitis es una enfermedad no transmisible, con una alta prevalencia, que oscila entre el 45% y el 50% de la población mundial, ocupando el sexto lugar entre las enfermedades más frecuentes de la humanidad. Existe suficiente evidencia que avala la relación entre la enfermedad periodontal y la enfermedad cardiovascular, responsable de aproximadamente el 45% de las muertes en países desarrollados, comprendiendo en su causalidad al infarto de miocardio, el accidente cerebrovascular, la insuficiencia cardíaca y las arritmias, que causan alrededor del 95 % de las muertes relacionadas con la enfermedad cardiovascular. Ambas patologías presentan factores de riesgo comunes ampliamente reconocidos como la diabetes y el tabaquismo, pero además manifiestan características genéticas y epigenéticas que avalan distintos mecanismos etiopatológicos. Más allá de los factores de riesgo comunes, se han propuesto dos mecanismos para explicar la relación entre la enfermedad periodontal y las cardiovasculares. Uno de ellos, constituye la invasión directa de patógenos periodontales en las células endoteliales. El otro mecanismo sugerido (vía indirecta), ocasionado por la respuesta inflamatoria sistémica que resulta en niveles crónicamente elevados de diferentes citoquinas, también relacionadas con la enfermedad vascular aterosclerótica, como IL-1β, IL-6, IL-8, TNF-α, PCR y la proteína quimioatrayente de monocitos, podría estar mediado por productos bacterianos, como los lipopolisacáridos que alcanzarían la circulación induciendo una potente respuesta inmunitaria. Estos mecanismos pueden actuar inflamando las células endoteliales, modulando el metabolismo de los lípidos y aumentando el estrés oxidativo, favoreciendo la aterosclerosis, conformando la expresión de un fenotipo arterial inflamatorio, generando el nexo entre la enfermedad periodontal y las patologías cardiovasculares.

Citas

Arvanitidis, E., Bizzarro, S., Alvarez Rodriguez, E., Loos, B. G., y Nicu, E. A. (2017). Reduced platelet hyper-reactivity and platelet-leukocyte aggregation after periodontal therapy. Thrombosis Journal, 15(1), 1–10. https://doi.org/10.1186/s12959-016-0125-x

Baniulyte, G., Piela, K., y Culshaw, S. (2021). How strong is the link between periodontitis and stroke? Evidence-Based Dentistry, 22(1), 10–11. https://doi.org/10.1038/s41432-021-0161-7

Bochenek, G., Häsler, R., El Mokhtari, N. E., König, I. R., Loos, B. G., Jepsen, S., Rosenstiel, P., Schreiber, S., y Schaefer, A. S. (2013). The large non-coding RNA ANRIL, which is associated with atherosclerosis, periodontitis and several forms of cancer, regulates ADIPOR1, VAMP3 and C11ORF10. Human Molecular Genetics, 22(22), 4516–4527. https://doi.org/10.1093/hmg/ddt299

Bodanese, L. C., Louzeiro, G. C., Magnus, G. A., Baptista, Â. H., Salum, F. G., y Mattiello, R. (2021). Association between periodontitis and myocardial infarction: systematic review and meta-analysis. International Journal of Cardiovascular Sciences, 34(5 Suppl 1), 121–127. https://doi.org/10.36660/ijcs.20200055

Cardoso, E. M., Reis, C., y Manzanares-Céspedes, M. C. (2018). Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases. Postgraduate Medicine, 130(1), 98–104. https://doi.org/10.1080/00325481.2018.1396876

Carrion, J., Scisci, E., Miles, B., Sabino, G. J., Zeituni, A. E., Gu, Y., Bear, A., Genco, C. A., Brown, D. L., y Cutler, C. W. (2012). Microbial carriage state of peripheral blood dendritic cells (DCs) in chronic periodontitis influences DC differentiation, atherogenic potential. The Journal of Immunology, 189(6), 3178–3187. https://doi.org/10.4049/jimmunol.1201053

Chapple, I. L., Genco, R., y Working group 2 of joint EFP/AAP workshop (2013). Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. Journal of Clinical Periodontology, 40(Suppl 14), S106–S112. https://doi.org/10.1111/jcpe.12077

Chavakis, T., Mitroulis, I., y Hajishengallis, G. (2019). Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation. Nature Immunology, 20 (7), 802–811. https://doi.org/10.1038/s41590-019-0402-5

de Oliveira, C., Watt, R., y Hamer, M. (2010). Toothbrushing, inflammation, and risk of cardiovascular disease: results from Scottish Health Survey. BMJ, 340(may27 1), 1–6. https://doi.org/10.1136/bmj.c2451

Demmer, R. T., Trinquart, L., Zuk, A., Fu, B. C., Blomkvist, J., Michalowicz, B. S., Ravaud, P., y Desvarieux, M. (2013). The influence of anti-infective periodontal treatment on C-reactive protein: a systematic review and meta-analysis of randomized controlled trials. PloS One, 8(10), 1–9. https://doi.org/10.1371/journal.pone.0077441

Desvarieux, M., Demmer, R. T., Jacobs, D. R., Rundek, T., Boden-Albala, B., Sacco, R. L., y Papapanou, P. N. (2010). Periodontal bacteria and hypertension: The oral infections and vascular disease epidemiology study (INVEST). Journal of Hypertension, 28(7), 1413–1421. https://doi.org/10.1097/HJH.0b013e328338cd36

Fagundes, N. C. F., Almeida, A. P. C. P. S. C., Vilhena, K. F. B., Magno, M. B., Maia, L. C., y Lima, R. R. (2019). Periodontitis as a risk factor for stroke: a systematic review and meta-analysis. Vascular Health and Risk Management, 15, 519–532. https://doi.org/10.2147/VHRM.S204097

Farrugia, C., Stafford, G. P., Potempa, J., Wilkinson, R. N., Chen, Y., Murdoch, C., y Widziolek, M. (2021). Mechanisms of vascular damage by systemic dissemination of the oral pathogen Porphyromonas gingivalis. FEBS Journal, 288(5), 1479–1495. https://doi.org/10.1111/febs.15486

Ford, P. J., Gemmell, E., Chan, A., Carter, C. L., Walker, P. J., Bird, P. S., West, M. J., Cullinan, M. P., y Seymour, G. J. (2006). Inflammation, heat shock proteins and periodontal pathogens in atherosclerosis: An immunohistologic study. Oral Microbiology and Immunology, 21(4), 206–211. https://doi.org/10.1111/j.1399-302X.2006.00276.x

Fröhlich, H., Herrmann, K., Franke, J., Karimi, A., Täger, T., Cebola, R., Katus, H. A., Zugck, C., y Frankenstein, L. (2016). Periodontitis in chronic heart failure. Texas Heart Institute Journal, 43(4), 297–304. https://doi.org/10.14503/THIJ-15-5200

Hamza, S. A., Asif, S., Khurshid, Z., Zafar, M. S., y Bokhari, S. A. H. (2021). Emerging role of epigenetics in explaining relationship of periodontitis and cardiovascular diseases. Diseases, 9(3), 1–9. https://doi.org/10.3390/diseases9030048

Holmlund, A., Lampa, E., y Lind, L. (2017). Poor response to periodontal treatment may predict future cardiovascular disease. Journal of Dental Research, 96(7), 768–773. https://doi.org/10.1177/0022034517701901

Ilhan, F., y Kalkanli, S. T. (2015). Atherosclerosis and the role of immune cells. World Journal of Clinical Cases, 3(4), 345–352. https://doi.org/10.12998/wjcc.v3.i4.345

Ishai, A., Osborne, M. T., El Kholy, K., Takx, R. A. P., Ali, A., Yuan, N., Hsue, P., Van Dyke, T. E., y Tawakol, A. (2019). Periodontal disease associates with arterial inflammation via potentiation of a hematopoietic-arterial axis. JACC. Cardiovascular Imaging, 12(11 Pt 1), 2271–2273. https://doi.org/10.1016/j.jcmg.2019.05.015

Jacobi, N., Walther, C., Borof, K., Heydecke, G., Seedorf, U., Lamprecht, R., Beikler, T., Debus, S. E., Waldeyer, C., Blankenberg, S., Schnabel, R. B., Aarabi, G., y Behrendt, C. A. (2021). The association of periodontitis and peripheral arterial occlusive disease in a prospective population-based cross-sectional cohort study. Journal of Clinical Medicine, 10(10), 1–8. https://doi.org/10.3390/jcm10102048

Jurdziński, K. T., Potempa, J., y Grabiec, A. M. (2020). Epigenetic regulation of inflammation in periodontitis: cellular mechanisms and therapeutic potential. Clinical Epigenetics, 12(1), 1–18. https://doi.org/10.1186/s13148-020-00982-7

Kampits, C., Montenegro, M. M., Ribeiro, I. W. J., Furtado, M. V., Polanczyk, C. A., Rösing, C. K., y Haas, A. N. (2016). Periodontal disease and inflammatory blood cytokines in patients with stable coronary artery disease. Journal of Applied Oral Science, 24(4), 352–358. https://doi.org/10.1590/1678-775720160082

Kaschwich, M., Behrendt, C.-A., Heydecke, G., Bayer, A., Debus, E. S., Seedorf, U., y Aarabi, G. (2019). The association of periodontitis and peripheral arterial occlusive disease-a systematic review. International Journal of Molecular Sciences, 20(12), 1–12. https://doi.org/10.3390/ijms20122936

Kassebaum, N. J., Bernabé, E., Dahiya, M., Bhandari, B., Murray, C. J. L., y Marcenes, W. (2014). Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression. Journal of Dental Research, 93(11), 1045–1053. https://doi.org/10.1177/0022034514552491

King, K. Y., y Goodell, M. A. (2011). Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nature Reviews Immunology, 11(10), 685–692. https://doi.org/10.1038/nri3062

Koppolu, P., Durvasula, S., Palaparthy, R., Rao, M., Sagar, V., Reddy, S. K., y Lingam, S. (2013). Estimate of CRP and TNF-alpha level before and after periodontal therapy in cardiovascular disease patients. The Pan African Medical Journal, 15, 1–10. https://doi.org/10.11604/pamj.2013.15.92.2326

Kozarov, E. V., Dorn, B. R., Shelburne, C. E., Dunn, W. A., y Progulske-Fox, A. (2005). Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arteriosclerosis, Thrombosis, and Vascular Biology, 25(3), e17–e18. https://doi.org/10.1161/01.atv.0000155018.67835.1a

Mai, J., Virtue, A., Shen, J., Wang, H., y Yang, X. F. (2013). An evolving new paradigm: Endothelial cells - Conditional innate immune cells. Journal of Hematology and Oncology, 6(1), 1–13. https://doi.org/10.1186/1756-8722-6-61

Mendez, M. V., Scott, T., LaMorte, W., Vokonas, P., Menzoian, J. O., y Garcia, R. (1998). An association between periodontal disease and peripheral vascular disease. American Journal of Surgery, 176(2), 153–157. https://doi.org/10.1016/S0002-9610(98)00158-5

Mitroulis, I., Kalafati, L., Hajishengallis, G., y Chavakis, T. (2018). Myelopoiesis in the context of innate immunity. Journal of Innate Immunity, 10(5-6), 365–372. https://doi.org/10.1159/000489406

Miyajima, S. I., Naruse, K., Kobayashi, Y., Nakamura, N., Nishikawa, T., Adachi, K., Suzuki, Y., Kikuchi, T., Mitani, A., Mizutani, M., Ohno, N., Noguchi, T., y Matsubara, T. (2014). Periodontitis-activated monocytes/macrophages cause aortic inflammation. Scientific Reports, 4, 1–9. https://doi.org/10.1038/srep05171

Munz, M., Richter, G. M., Loos, B. G., Jepsen, S., Divaris, K., Offenbacher, S., Teumer, A., Holtfreter, B., Kocher, T., Bruckmann, C., Jockel-Schneider, Y., Graetz, C., Munoz, L., Bhandari, A., Tennstedt, S., Staufenbiel, I., van der Velde, N., Uitterlinden, A. G., de Groot, L. C. P. G. M., … Schaefer, A. S. (2018). Genome-wide association meta-analysis of coronary artery disease and periodontitis reveals a novel shared risk locus. Scientific Reports, 8(1), 1–10. https://doi.org/10.1038/s41598-018-31980-8

Muñoz Aguilera, E., Suvan, J., Buti, J., Czesnikiewicz-Guzik, M., Barbosa Ribeiro, A., Orlandi, M., Guzik, T. J., Hingorani, A. D., Nart, J., y D’Aiuto, F. (2020). Periodontitis is associated with hypertension: A systematic review and meta-analysis. Cardiovascular Research, 116(1), 28–39. https://doi.org/10.1093/cvr/cvz201

Nahrendorf, M. (2018). Myeloid cell contributions to cardiovascular health and disease. Nature Medicine, 24(6), 711–720. https://doi.org/10.1038/s41591-018-0064-0

Nakano, K., Nemoto, H., Nomura, R., Inaba, H., Yoshioka, H., Taniguchi, K., Amano, A., y Ooshima, T. (2009). Detection of oral bacteria in cardiovascular specimens. Oral Microbiology and Immunology, 24(1), 64–68. https://doi.org/10.1111/j.1399-302X.2008.00479.x

Neele, A. E., Van Den Bossche, J., Hoeksema, M. A., y De Winther, M. P. J. (2015). Epigenetic pathways in macrophages emerge as novel targets in atherosclerosis. European Journal of Pharmacology, 763(Pt A), 79–89. https://doi.org/10.1016/j.ejphar.2015.03.101

Nicolosi, L. N., Lewin, P. G., Rudzinski, J. J., Pompeo, M., Guanca, F., Rodríguez, P., Gelpi, R. J., y Rubio, M. C. (2017). Relation between periodontal disease and arterial stiffness. Journal of Periodontal Research, 52(1), 122–126. https://doi.org/10.1111/jre.12376

Park, S. Y., Kim, S. H., Kang, S. H., Yoon, C. H., Lee, H. J., Yun, P. Y., Youn, T. J., y Chae, I. H. (2019). Improved oral hygiene care attenuates the cardiovascular risk of oral health disease: a population-based study from Korea. European Heart Journal, 40(14), 1138–1145. https://doi.org/10.1093/eurheartj/ehy836

Paul, O., Arora, P., Mayer, M., y Chatterjee, S. (2021). Inflammation in periodontal disease: possible link to vascular disease. Frontiers in Physiology, 11, 1–11. https://doi.org/10.3389/fphys.2020.609614

Pazos, P., Leira, Y., Domínguez, C., Pías-Peleteiro, J. M., Blanco, J., y Aldrey, J. M. (2018). Association between periodontal disease and dementia: a literature review. Neurologia, 33(9), 602–613. https://doi.org/10.1016/j.nrl.2016.07.013

Pucar, A., Milasin, J., Lekovic, V., Vukadinovic, M., Ristic, M., Putnik, S., y Kenney, E. B. (2007). Correlation between atherosclerosis and periodontal putative pathogenic bacterial infections in coronary and internal mammary arteries. Journal of Periodontology, 78(4), 677–682. https://doi.org/10.1902/jop.2007.060062

Qin, X., Zhao, Y., y Guo, Y. (2021). Periodontal disease and myocardial infarction risk: a meta-analysis of cohort studies. American Journal of Emergency Medicine, 48, 103–109. https://doi.org/10.1016/j.ajem.2021.03.071

Roth, G. A., Forouzanfar, M. H., Moran, A. E., Barber, R., Nguyen, G., Feigin, V. L., Naghavi, M., Mensah, G. A., y Murray, C. J. L. (2015). Demographic and epidemiologic drivers of global cardiovascular mortality. New England Journal of Medicine, 372(14), 1333–1341. https://doi.org/10.1056/nejmoa1406656

Rubio, M. del, Rudzinski, J., Ramos, C., Lifshitz, F., Friedman, S., y Nicolosi, L. (2020). Cognitive impairment related to arterial stiffness in cardiovascular disease patients with severe periodontitis. Acta Odontológica Latinoamericana, 33(3), 200–208. https://doi.org/10.54589/aol.33/3/200

Sanz, M., Marco Del Castillo, A., Jepsen, S., Gonzalez-Juanatey, J. R., D'Aiuto, F., Bouchard, P., Chapple, I., Dietrich, T., Gotsman, I., Graziani, F., Herrera, D., Loos, B., Madianos, P., Michel, J. B., Perel, P., Pieske, B., Shapira, L., Shechter, M., Tonetti, M., Vlachopoulos, C., … Wimmer, G. (2020). Periodontitis and cardiovascular diseases: consensus report. Journal of Clinical Periodontology, 47(3), 268–288. https://doi.org/10.1111/jcpe.13189

Schaefer, A. S., Bochenek, G., Jochens, A., Ellinghaus, D., Dommisch, H., Güzeldemir-Akçakanat, E., Graetz, C., Harks, I., Jockel-Schneider, Y., Weinspach, K., Meyle, J., Eickholz, P., Linden, G. J., Cine, N., Nohutcu, R., Weiss, E., Houri-Haddad, Y., Iraqi, F., Folwaczny, M., Noack, B., … Schreiber, S. (2015). Genetic evidence for PLASMINOGEN as a shared genetic risk factor of coronary artery disease and periodontitis. Circulation. Cardiovascular Genetics, 8(1), 159–167. https://doi.org/10.1161/CIRCGENETICS.114.000554

Schenkein, H. A., Papapanou, P. N., Genco, R., y Sanz, M. (2020). Mechanisms underlying the association between periodontitis and atherosclerotic disease. Periodontology 2000, 83(1), 90–106. https://doi.org/10.1111/prd.12304

Sen, S., Giamberardino, L. D., Moss, K., Morelli, T., Rosamond, W. D., Gottesman, R. F., Beck, J., y Offenbacher, S. (2018). Periodontal disease, regular dental care use, and incident ischemic stroke. Stroke, 49(2), 355–362. https://doi.org/10.1161/STROKEAHA.117.018990

Seoane, T., Bullon, B., Fernandez-Riejos, P., Garcia-Rubira, J. C., Garcia-Gonzalez, N., Villar-Calle, P., Quiles, J. L., Battino, M., y Bullon, P. (2022). Periodontitis and other risk factors related to myocardial infarction and its follow-up. Journal of Clinical Medicine, 11(9), 1–16. https://doi.org/10.3390/jcm11092618

Shin, H. S., Shin, M. S., Ahn, Y. B., Choi, B. Y., Nam, J. H., y Kim, H. D. (2016). Periodontitis is associated with cognitive impairment in elderly Koreans: results from the Yangpyeong cohort study. Journal of the American Geriatrics Society, 64(1), 162–167. https://doi.org/10.1111/jgs.13781

Sorokin, V., Vickneson, K., Kofidis, T., Woo, C. C., Lin, X. Y., Foo, R., y Shanahan, C. M. (2020). Role of vascular smooth muscle cell plasticity and interactions in vessel wall inflammation. Frontiers in Immunology, 11, 1–16. https://doi.org/10.3389/fimmu.2020.599415

Takizawa, H., Regoes, R. R., Boddupalli, C. S., Bonhoeffer, S., y Manz, M. G. (2011). Dynamic variation in cycling of hematopoietic stem cells in steady state and inflammation. Journal of Experimental Medicine, 208(2), 273–284. https://doi.org/10.1084/jem.20101643

Tsakos, G., Sabbah, W., Hingorani, A. D., Netuveli, G., Donos, N., Watt, R. G., y D’Aiuto, F. (2010). Is periodontal inflammation associated with raised blood pressure? Evidence from a National US survey. Journal of Hypertension, 28(12), 2386–2393. https://doi.org/10.1097/HJH.0b013e32833e0fe1

Wang, G., Jacquet, L., Karamariti, E., y Xu, Q. (2015). Origin and differentiation of vascular smooth muscle cells. Journal of Physiology, 593(14), 3013–3030. https://doi.org/10.1113/JP270033

Wojtkowska, A., Zapolski, T., Wysokińska-Miszczuk, J., y Wysokiński, A. P. (2021). The inflammation link between periodontal disease and coronary atherosclerosis in patients with acute coronary syndromes: case-control study. BMC Oral Health, 21(1), 1–17. https://doi.org/10.1186/s12903-020-01356-4

Zardawi, F., Gul, S., Abdulkareem, A., Sha, A., y Yates, J. (2021). Association between periodontal disease and atherosclerotic cardiovascular diseases: revisited. Frontiers in Cardiovascular Medicine, 7, 1–17. https://doi.org/10.3389/fcvm.2020.625579

Zeki Al Hazzouri, A., y Yaffe, K. (2014). Arterial stiffness and cognitive function in the elderly. Journal of Alzheimer’s Disease, 42(Suppl 4), S503–S514. https://doi.org/10.3233/JAD-141563

Zhao, J. L., Ma, C., O’Connell, R. M., Mehta, A., Diloreto, R., Heath, J. R., y Baltimore, D. (2014). Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stress-induced hematopoiesis. Cell Stem Cell, 14(4), 445–459. https://doi.org/10.1016/j.stem.2014.01.007

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2023-05-24

Cómo citar

Nicolosi, L. N., Rubio, M. C., & Friedman, S. M. (2023). La Inflamación Como el Nexo Entre la Enfermedad Periodontal y la Enfermedad Cardiovascular. Revista De La Facultad De Odontologia De La Universidad De Buenos Aires, 37(87), 67–78. Recuperado a partir de https://revista.odontologia.uba.ar/index.php/rfouba/article/view/139