Información del artículo
Resumen
Las enfermedades periodontales son patologías crónicas de alta prevalencia en la población afectando principalmente a los adultos mayores de 40 años, sin embargo si tenemos en cuenta las gingivitis, la prevalencia de ambas patologías asciende al 80%. Múltiples estudios sugieren un incremento en el riesgo de presentar enfermedades cardiovasculares (ECV) en sujetos con periodontitis. Recientes hallazgos permiten proponer que las periodontitis no tratada y quizá las gingivitis crónicas, puedan generar efectos sistémicos y de esta forma promover la aterogénesis por dos vías principales :
- 1.
Vía directa: a través de un efecto directo, representado por bacterias periodontopaticas que invaden las células endoteliales y estimulan la producción de mediadores pro-inflamatorios que favorecen el desarrollo de aterosclerosis.
- 2.
La segunda vía plausible o vía indirecta se genera por el aumento de citoquinas proinflamatorias que estimulan la expresión de moléculas de adhesión en el endotelio (e-selectina, ICAM-1 y VCAM) favoreciendo la migración de leucocitos a las lesiones ateromatosas.
Existe plausibilidad biológica de que por alguna de las vías o su combinación, se asocie la periodontitis con las enfermedades cardiovasculares. El tratamiento periodontal exitoso reduce los niveles plasmáticos de citoquinas proinflamatorias y reactantes de fase aguda. Adicionalmente, se ha descrito una mejoría de la función endotelial posterior al tratamiento periodontal en sujetos con periodontitis severa.
La enfermedad periodontal por su alta prevalencia ha recibido una creciente atención por ser un posible factor de riesgo modificable en la prevención primaria y secundaria de eventos cardiovasculares. Sin embargo, se requieren más estudios de observación que confirmen el vinculo entre periodontitis y aterosclerosis, así como ensayos clínicos controlados que permitan establecer si, el tratamiento periodontal reduce el riesgo cardiovascular.
Palabras clave:
Periodontitis
enfermedad cardiovascular
riesgo
evidencia epidemiológica
plausibilidad biológica
Abstract
Periodontitis is mostly a chronic pathology that affects adults over 40 years old in all populations. However, if gingivitis is added to periodontitis then the prevalence may be increased to affect almost 80% of the people. Several studies suggest a posible link between periodontitis and cardiovascular disease (CVD). Recent epidemiological and experimental evidence lead to think that untreated periodontitis and gingivitis produce some effects on the General Health and promote the atherogenesis by at least two ways :
- 1.
Direct damage : thourough a direct effect caused by invasión of periodontal pathogens of endotelial cells that are stimulated to produce pro-inflammatory cytokines that favour atherogenesis.
- 2.
Secondary damage : It is generated by the increase of pro-inflammatory cytokines that increase the expresión of adhesión molecules on endotelial cells like e-selectine, ICAM -1 and VCAM, and favours the migration of leukocytes into the atheroma lesions.
Its posible that periodontitis may be linked to CVD by diverse mechanisms. Succesfull periodontal treatment could reduce plasmatic levels of proimflammatoty cytokines and acute phase proteins. In addition, there is evidence that Periodontal tretatment could improve endotelial function among people affected by severe periodontitis.
Periodontitis is a prevalent disease that has claimed recent Public Health interest because It is a modifiable factor to prevent/reduce cardiovascular disease. However, more and better epidemiological evidence needs to be produced to confirm the posible link between periodontitis and cardiovascular disease. Clinical controlled trials are neccesary to determine the positive effect of periodontal intervention by lowering the risk of Cardiovascular disease.
Key words:
Periodontitis
cardiovascular disease
epidemiological studies
biological plausibility
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Referencias Bibliográficas
[1.]
A. Lazzini, S. Lazzini.
Cardiovascular disease: an economical perspective.
Curr Pharm Des, 15 (2009), pp. 1142-1156
[2.]
F. Levi, L. Chatenoud, P. Bertuccio, F. Lucchini, E. Negri, C.L. Vecchia.
Mortality from cardiovascular and cerebrovascular diseases in Europe and other areas of the world: an update.
Eur J Cardiovasc Prev Rehabil, (2009),
[3.]
D. Wood.
Established and emerging cardiovascular risk factors.
Am Heart J, 141 (2001), pp. S49-S57
[4.]
K.J. Mukamal, R.A. Kronmal, R.P. Tracy, M. Cushman, D.S. Siscovick.
Traditional and novel risk factors in older adults: cardiovascular risk assessment late in life.
Am J Geriatr Cardiol, 13 (2004), pp. 69-80
[5.]
G.K. Hansson.
Inflammation, atherosclerosis, and coronary artery disease.
N Engl J Med, 352 (2005), pp. 1685-1695
[6.]
L.G. Best, Y. Zhang, E.T. Lee, J.L. Yeh, L. Cowan, V. Palmieri, et al.
C-reactive protein as a predictor of cardiovascular risk in a population with a high prevalence of diabetes: the Strong Heart Study.
Circulation, 112 (2005), pp. 1289-1295
[7.]
J.M. Sinning, C. Bickel, C.M. Messow, R. Schnabel, E. Lubos, H.J. Rupprecht, et al.
Impact of C-reactive protein and fibrinogen on cardiovascular prognosis in patients with stable angina pectoris: the AtheroGene study.
Eur Heart J, 27 (2006), pp. 2962-2968
[8.]
D. Tanne, M. Benderly, U. Goldbourt, M. Haim, A. Tenenbaum, E.Z. Fisman, et al.
C-reactive protein as a predictor of incident ischemic stroke among patients with preexisting cardiovascular disease.
Stroke, 37 (2006), pp. 1720-1724
[9.]
E. Reszka, B. Jegier, W. Wasowicz, M. Lelonek, M. Banach, R. Jaszewski.
Detection of infectious agents by polymerase chain reaction in human aortic wall.
Cardiovasc Pathol, 17 (2008), pp. 297-302
[10.]
E. Kozarov, D. Sweier, C. Shelburne, A. Progulske-Fox, D. Lopatin.
Detection of bacterial DNA in atheromatous plaques by quantitative PCR.
Microbes Infect, 8 (2006), pp. 687-693
[11.]
E.V. Kozarov, B.R. Dorn, C.E. Shelburne, W.A. Dunn Jr., A. Progulske-Fox.
Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis.
Arterioscler Thromb Vasc Biol, 25 (2005), pp. e17-e18
[12.]
J.E. Botero, A. Contreras, B. Parra.
Profiling of inflammatory cytokines produced by gingival fibroblasts after human cytomegalovirus infection.
Oral Microbiol Immunol, 23 (2008), pp. 291-298
[13.]
J.E. Botero, B. Parra, A. Jaramillo, A. Contreras.
Subgingival human cytomegalovirus correlates with increased clinical periodontal parameters and bacterial coinfection in periodontitis.
J Periodontol, 78 (2007), pp. 2303-2310
[14.]
A. Contreras, H. Nowzari, J. Slots.
Herpesviruses in periodontal pocket and gingival tissue specimens.
Oral Microbiol Immunol, 15 (2000), pp. 15-18
[15.]
C. Lunardi, M. Dolcino, D. Peterlana, C. Bason, R. Navone, N. Tamassia, et al.
Endothelial cells’ activation and apoptosis induced by a subset of antibodies against human cytomegalovirus: relevance to the pathogenesis of atherosclerosis.
PLoS One, 2 (2007), pp. e473
[16.]
E. Lalla, I.B. Lamster, M.A. Hofmann, L. Bucciarelli, A.P. Jerud, S. Tucker, et al.
Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice.
Arterioscler Thromb Vasc Biol, 23 (2003), pp. 1405-1411
[17.]
R.G. Deshpande, M.B. Khan, C.A. Genco.
Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis.
Infect Immun, 66 (1998), pp. 5337-5343
[18.]
B.R. Dorn, W.A. Dunn Jr., A. Progulske-Fox.
Invasion of human coronary artery cells by periodontal pathogens.
Infect Immun, 67 (1999), pp. 5792-5798
[19.]
K.J. Mattila, P.J. Pussinen, S. Paju.
Dental infections and cardiovascular diseases: a review.
J Periodontol, 76 (2005), pp. 2085-2088
[20.]
G.J. Seymour, P.J. Ford, M.P. Cullinan, S. Leishman, K. Yamazaki.
Relationship between periodontal infections and systemic disease.
Clin Microbiol Infect, 13 (2007), pp. 3-10
[21.]
K.J. Mattila, M.S. Nieminen, V.V. Valtonen, V.P. Rasi, Y.A. Kesaniemi, S.L. Syrjala, et al.
Association between dental health and acute myocardial infarction.
BMJ, 298 (1989), pp. 779-781
[22.]
S.J. Arbes Jr., G.D. Slade, J.D. Beck.
Association between extent of periodontal attachment loss and self-reported history of heart attack: an analysis of NHANES III data.
J Dent Res, 78 (1999), pp. 1777-1782
[23.]
F. DeStefano, R.F. Anda, H.S. Kahn, D.F. Williamson, C.M. Russell.
Dental disease and risk of coronary heart disease and mortality.
BMJ, 306 (1993), pp. 688-691
[24.]
J. Beck, R. Garcia, G. Heiss, P.S. Vokonas, S. Offenbacher.
Periodontal disease and cardiovascular disease.
J Periodontol, 67 (1996), pp. 1123-1137
[25.]
J.D. Beck, J.R. Elter, G. Heiss, D. Couper, S.M. Mauriello, S. Offenbacher.
Relationship of periodontal disease to carotid artery intima-media wall thickness: the atherosclerosis risk in communities (ARIC) study.
Arterioscler Thromb Vasc Biol, 21 (2001), pp. 1816-1822
[26.]
J.D. Beck, P. Eke, D. Lin, P. Madianos, D. Couper, K. Moss, et al.
Associations between IgG antibody to oral organisms and carotid intima-medial thickness in community-dwelling adults.
Atherosclerosis, 183 (2005), pp. 342-348
[27.]
H.C. Hung, K.J. Joshipura, G. Colditz, J.E. Manson, E.B. Rimm, F.E. Speizer, et al.
The association between tooth loss and coronary heart disease in men and women.
J Public Health Dent, 64 (2004), pp. 209-215
[28.]
K.J. Joshipura, H.C. Wand, A.T. Merchant, E.B. Rimm.
Periodontal disease and biomarkers related to cardiovascular disease.
J Dent Res, 83 (2004), pp. 151-155
[29.]
S.P. Engebretson, I.B. Lamster, M.S. Elkind, T. Rundek, N.J. Serman, R.T. Demmer, et al.
Radiographic measures of chronic periodontitis and carotid artery plaque.
Stroke, 36 (2005), pp. 561-566
[30.]
M. Desvarieux, R.T. Demmer, T. Rundek, B. Boden-Albala, D.R. Jacobs Jr., R.L. Sacco, et al.
Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST).
Circulation, 111 (2005), pp. 576-582
[31.]
P.O. Soder, B. Soder, J. Nowak, T. Jogestrand.
Early carotid atherosclerosis in subjects with periodontal diseases.
Stroke, 36 (2005), pp. 1195-1200
[32.]
P.J. Pussinen, G. Alfthan, H. Rissanen, A. Reunanen, S. Asikainen, P. Knekt.
Antibodies to periodontal pathogens and stroke risk.
Stroke, 35 (2004), pp. 2020-2023
[33.]
P.J. Pussinen, K. Nyyssonen, G. Alfthan, R. Salonen, J.A. Laukkanen, J.T. Salonen.
Serum antibody levels to Actinobacillus actinomycetemcomitans predict the risk for coronary heart disease.
Arterioscler Thromb Vasc Biol, 25 (2005), pp. 833-838
[34.]
C.C. Abnet, Y.L. Qiao, S.M. Dawsey, Z.W. Dong, P.R. Taylor, S.D. Mark.
Tooth loss is associated with increased risk of total death and death from upper gastrointestinal cancer, heart disease, and stroke in a Chinese populationbased cohort.
Int J Epidemiol, 34 (2005), pp. 467-474
[35.]
A. Agueda, J.M. Ramon, C. Manau, A. Guerrero, J.J. Echeverria.
Periodontal disease as a risk factor for adverse pregnancy outcomes: a prospective cohort study.
J Clin Periodontol, 35 (2008), pp. 16-22
[36.]
C. Manau, A. Echeverria, A. Agueda, A. Guerrero, J.J. Echeverria.
Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes.
J Clin Periodontol, 35 (2008), pp. 385-397
[37.]
A. Fardi, D. Papadimitriou.
Periodontal and atherosclerosis-induced diseases.
Int Angiol, 26 (2007), pp. 197-205
[38.]
I.Z. Mustapha, S. Debrey, M. Oladubu, R. Ugarte.
Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: a systematic review and meta-analysis.
J Periodontol, 78 (2007), pp. 2289-2302
[39.]
F.A. Scannapieco, R.B. Bush, S. Paju.
Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review.
Ann Periodontol, 8 (2003), pp. 38-53
[40.]
S. Ajwani, K.J. Mattila, R.S. Tilvis, A. Ainamo.
Periodontal disease and mortality in an aged population.
Spec Care Dentist, 23 (2003), pp. 125-130
[41.]
J.H. Meurman, M. Sanz, S.J. Janket.
Oral health, atherosclerosis, and cardiovascular disease.
Crit Rev Oral Biol Med, 15 (2004), pp. 403-413
[42.]
M.V. Vettore.
Periodontal disease cardiovascular disease.
Evid Based Dent, 5 (2004), pp. 69
[43.]
Y.S. Khader, Z.S. Albashaireh, M.A. Alomari.
Periodontal diseases and the risk of coronary heart and cerebrovascular diseases: a meta-analysis.
J Periodontol, 75 (2004), pp. 1046-1053
[44.]
S.A. Harding, J. Sarma, D.H. Josephs, N.L. Cruden, J.N. Din, P.J. Twomey, et al.
Upregulation of the CD40/CD40 ligand dyad and platelet-monocyte aggregation in cigarette smokers.
Circulation, 109 (2004), pp. 1926-1929
[45.]
C.R. Conti, J.L. Mehta.
Acute myocardial ischemia: role of atherosclerosis, thrombosis, platelet activation, coronary vasospasm, and altered arachidonic acid metabolism.
Circulation, 75 (1987), pp. V84-V95
[46.]
A. Lourbakos, Y.P. Yuan, A.L. Jenkins, J. Travis, P. Andrade-Gordon, R. Santulli, et al.
Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity.
Blood, 97 (2001), pp. 3790-3797
[47.]
X. Li, T. Iwai, H. Nakamura, Y. Inoue, Y. Chen, M. Umeda, et al.
An ultrastructural study of Porphyromonas gingivalis-induced platelet aggregation.
Thromb Res, 122 (2008), pp. 810-819
[48.]
M. Nylander, T.L. Lindahl, T. Bengtsson, M. Grenegard.
The periodontal pathogen Porphyromonas gingivalis sensitises human blood platelets to epinephrine.
Platelets, 19 (2008), pp. 352-358
[49.]
M.C. Herzberg, M.W. Weyer.
Dental plaque, platelets, and cardiovascular diseases.
Ann Periodontol, 3 (1998), pp. 151-160
[50.]
M.W. Meyer, K. Gong, M.C. Herzberg.
Streptococcus sanguis-induced platelet clotting in rabbits and hemodynamic and cardiopulmonary consequences.
Infect Immun, 66 (1998), pp. 5906-5914
[51.]
D. Papapanagiotou, E.A. Nicu, S. Bizzarro, V.E. Gerdes, J.C. Meijers, R. Nieuwland, et al.
Periodontitis is associated with platelet activation.
Atherosclerosis, 202 (2009), pp. 605-611
[52.]
R. Rajaiah, K.D. Moudgil.
Heat-shock proteins can promote as well as regulate autoimmunity.
Autoimmun Rev, 8 (2009), pp. 388-393
[53.]
K. Yamazaki, Y. Ohsawa, H. Itoh, K. Ueki, K. Tabeta, T. Oda, et al.
T-cell clonality to Porphyromonas gingivalis and human heat shock protein 60s in patients with atherosclerosis and periodontitis.
Oral Microbiol Immunol, 19 (2004), pp. 160-167
[54.]
P. Ford, E. Gemmell, P. Walker, M. West, M. Cullinan, G. Seymour.
Characterization of heat shock protein-specific T cells in atherosclerosis.
Clin Diagn Lab Immunol, 12 (2005), pp. 259-267
[55.]
J.G. Argueta, S. Shiota, N. Yamaguchi, Y. Masuhiro, S. Hanazawa.
Induction of Porphyromonas gingivalis GroEL signaling via binding to Toll-like receptors 2 and 4.
Oral Microbiol Immunol, 21 (2006), pp. 245-251
[56.]
B. Chiu.
Multiple infections in carotid atherosclerotic plaques.
Am Heart J, 138 (1999), pp. S534-S536
[57.]
M. Khlgatian, H. Nassar, H.H. Chou, F.C. Gibson 3rd, C.A. Genco.
Fimbriadependent activation of cell adhesion molecule expression in Porphyromonas gingivalis-infected endothelial cells.
Infect Immun, 70 (2002), pp. 257-267
[58.]
H.H. Chou, H. Yumoto, M. Davey, Y. Takahashi, T. Miyamoto, F.C. Gibson 3rd, et al.
Porphyromonas gingivalis fimbria-dependent activation of inflammatory genes in human aortic endothelial cells.
Infect Immun, 73 (2005), pp. 5367-5378
[59.]
H. Yumoto, H.H. Chou, Y. Takahashi, M. Davey, F.C. Gibson 3rd, C.A. Genco.
Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion.
Infect Immun, 73 (2005), pp. 8050-8059
[60.]
M.B. Giacona, P.N. Papapanou, I.B. Lamster, L.L. Rong, V.D. D’Agati, A.M. Schmidt, et al.
Porphyromonas gingivalis induces its uptake by human macrophages and promotes foam cell formation in vitro.
FEMS Microbiol Lett, 241 (2004), pp. 95-101
[61.]
M. Qi, H. Miyakawa, H.K. Kuramitsu.
Porphyromonas gingivalis induces murine macrophage foam cell formation.
Microb Pathog, 35 (2003), pp. 259-267
[62.]
A. Jain, E.L. Batista Jr., C. Serhan, G.L. Stahl, T.E. Van Dyke.
Role for periodontitis in the progression of lipid deposition in an animal model.
Infect Immun, 71 (2003), pp. 6012-6018
[63.]
L. Li, E. Messas, E.L. Batista Jr., R.A. Levine, S. Amar.
Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model.
Circulation, 105 (2002), pp. 861-867
[64.]
G. Yan, B. You, S.P. Chen, J.K. Liao, J. Sun.
Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1.
Circ Res, 103 (2008), pp. 591-597
[65.]
R.Z. Zhao, X. Chen, Q. Yao, C. Chen.
TNF-alpha induces interleukin-8 and endothelin-1 expression in human endothelial cells with different redox pathways.
Biochem Biophys Res Commun, 327 (2005), pp. 985-992
[66.]
C.W. Wyble, K.L. Hynes, J. Kuchibhotla, B.C. Marcus, D. Hallahan, B.L. Gewertz.
TNF-alpha and IL-1 upregulate membrane-bound and soluble E-selectin through a common pathway.
J Surg Res, 73 (1997), pp. 107-112
[67.]
A. Rahman, J. Kefer, M. Bando, W.D. Niles, A.B. Malik.
E-selectin expression in human endothelial cells by TNF-alpha-induced oxidant generation and NFkappaB activation.
Am J Physiol, 275 (1998), pp. L533-L544
[68.]
D.S. Celermajer, K.E. Sorensen, V.M. Gooch, D.J. Spiegelhalter, O.I. Miller, I.D. Sullivan, et al.
Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis.
Lancet, 340 (1992), pp. 1111-1115
[69.]
S. Amar, N. Gokce, S. Morgan, M. Loukideli, T.E. Van Dyke, J.A. Vita.
Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation.
Arterioscler Thromb Vasc Biol, 23 (2003), pp. 1245-1249
[70.]
F. D’Aiuto, D. Ready, M.S. Tonetti.
Periodontal disease and C-reactive proteinassociated cardiovascular risk.
J Periodontal Res, 39 (2004), pp. 236-241
[71.]
J.R. Elter, A.L. Hinderliter, S. Offenbacher, J.D. Beck, M. Caughey, N. Brodala, et al.
The effects of periodontal therapy on vascular endothelial function: a pilot trial.
Am Heart J, 151 (2006), pp. 47
[72.]
G. Seinost, G. Wimmer, M. Skerget, E. Thaller, M. Brodmann, R. Gasser, et al.
Periodontal treatment improves endothelial dysfunction in patients with severe periodontitis.
Am Heart J, 149 (2005), pp. 1050-1054
[73.]
M.S. Tonetti, F. D’Aiuto, L. Nibali, A. Donald, C. Storry, M. Parkar, et al.
Treatment of periodontitis and endothelial function.
N Engl J Med, 356 (2007), pp. 911-920
[74.]
Y. Higashi, C. Goto, D. Jitsuiki, T. Umemura, K. Nishioka, T. Hidaka, et al.
Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients.
Hypertension, 51 (2008), pp. 446-453
[75.]
Y. Higashi, C. Goto, T. Hidaka, J. Soga, S. Nakamura, Y. Fujii, et al.
Oral infection-inflammatory pathway, periodontitis, is a risk factor for endothelial dysfunction in patients with coronary artery disease.
Atherosclerosis, (2009),
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