SciELO - Scientific Electronic Library Online

 
vol.29 issue3Periodontal medicine (II). Obesity author indexsubject indexarticles search
Home Pagealphabetic serial listing  

My SciELO

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Avances en Periodoncia e Implantología Oral

On-line version ISSN 2340-3209Print version ISSN 1699-6585

Avances en Periodoncia vol.29 n.3 Madrid Dec. 2017

 

Originales

Medicina periodontal (III). Enfermedad cardiovascular y Síndrome Metabólico

Periodontal medicine (III). Cardiovascular disease and Metabolic Syndrom

A Bascones-Martínez*  , J Bascones-Ilundain**  , C Bascones-Ilundain*** 

*Catedrático de Medicina Bucal y Periodoncia. Departamento de Medicina y Cirugía Bucofacial. Facultad de Odontología. U.C.M

**Prof. Ayudante Doctor. Departamento de Odontología Conservadora

***Prof. Asociado. Departamento de Medicina y Cirugía Bucal

Resumen

Las condiciones orales como gingivitis y periodontis crónica están muy extendidas entre las más prevalentes de las enfermedades microbianas y está claro que las infecciones orales pueden representar un factor de riesgo para las enfermedades sistémicas por lo que su control es esencial en el manejo de estas entidades(en especial infección periodontal con enfermedad cardiovascular. Esta es una de las entidades más frecuentes en la mortalidad junto con la arterioesclerosis, siendo multifactorial. Hay importantes referencias a esta relación. La cavidad oral es una fuente de infección por lo que es importante tratar de minimizar esta situación

PALABRAS CLAVE Síndrome metabólico; enfermedad cardiovascular

Summary

Oral conditions such as gingivitis and chronic periodontitis are found worldwide and are among the most prevalent microbial diseases of mankind. It is clear that oral infection may represent a significant risk-factor for systemic diseases, and hence the control of oral disease is essential in the prevention and management of these systemic condition for the interaction of oral disease (more specifically, periodontal infections) with cardiovascular disease. Cardiovascular disease is a major cause of death worldwide, with atherosclerosis as the underlying aetiology in the vast majority of case It is concluded that although atherosclerotic cardiovascular disease is almost certainly a multifactorial disease, there is now strong evidence that infection and inflammation are important risk factors. As the oral cavity is one potential source of infection, it is wise to try to ensure that any oral disease is minimised.

KEY WORDS Metabolic syndrome; cardiovascular desease

ENFERMEDAD CARDIOVASCULAR

DEFINICIÓN: Las enfermedades cardiovasculares (ECV) son un grupo de enfermedades progresivas y crónicas, caracterizadas por la formación de ateroma en el interior de las arterias grandes y medianas, por tanto es sinónimo del término de arteriosclerosis. Esto produce la reducción de la luz de las arterias y predispone a la trombosis, y a eventos obstructivos e isquémicos. Estos eventos pueden presentarse de manera crónica o precipitar un evento oclusivo súbito (presentación aguda).

La evidencia disponible sugiere que el rol del status periodontal en la prevalencia de bacteriemias después de la masticación, cepillado y raspado presenta una alta prevalencia/incidencia y una alta biodiversidad, incluyendo a patógenos periodontales en pacientes con periodontitis, y en contraposición a pacientes sanos o con gingivitis. La asociación entre la prevalencia de bacteriemia y los índices de placa/gingival fue demostrada en el año 2013 por Tomás y cols (Tomás et al., 2012).

Por otro lado, evaluando la presencia de antígenos bacterianos y la señalización molecular en las lesiones ateromatosas, al menos 2 estudios reportan una correlación entre el status periodontal (tanto moderada versus severa periodontitis, como sanos versus pacientes con periodontitis), y la presencia de patógenos periodontales. Al menos 8 estudios describen la correlación entre la microbiota subgingival y los patógenos detectados en las lesiones vasculares (Tonetti et al., 2013).

En los últimos 23 años, un importante número de estudios clínicos, mayoritariamente estudios transversales y casos control, han demostrado la asociación positiva entre la enfermedad periodontal y la enfermedad cardiovascular. En los últimos 8 años, diversas revisiones sistemáticas y narrativas han reunido y sintetizado la evidencia científica sobre esta asociación (Bahekar et al., 2007; Beck & Offenbacher, 2005; Humphrey et al., 2008; Meurman et al., 2004; Mustapha et al., 2007; Dietrich et al., 2013).

Dietrich y cols (Dietrich et al., 2013) realizaron una revisión sistemática donde evaluaron toda la evidencia epidemiológica disponible de la asociación entre la enfermedad periodontal y la enfermedad cardiovascular. En ella se incluyeron 12 estudios, entre los que 6 trataban sobre enfermedades coronarias, 3 sobre accidente cerebrovascular, 2 sobre la mortalidad de las dos enfermedades anteriormente expuestas, y uno sobre la enfermedad arterial periférica. Todos a excepción de uno, mostraron una asociación positiva entre las diferentes medidas de enfermedad periodontal y la incidencia de enfermedad cardiovascular, al menos en subgrupos específicos. La asociación fue mayor en pacientes adultos jóvenes, no existiendo evidencia de la asociación en pacientes mayores de 65 años. Sólo un estudio evaluó la asociación entre la enfermedad periodontal y los eventos cardiovasculares secundarios, lo cual resulta insuficiente evidencia para establecer una asociación fuerte. Sin embargo, este estudio no realizó metaanálisis como dos revisiones que se exponen a continuación.

No obstante, es importante reconocer las limitaciones de los estudios realizados, que valoran esta asociación. Una de los puntos débiles identificados en la evidencia clínica disponible es la exposición a errores de clasificación que lleva a una subestimación de los verdaderos factores de riesgo asociados con la enfermedad periodontal. Esto limitaría significativamente la evidencia disponible, ya que muy pocos estudios evalúan adecuadamente el grado de exposición (severidad de la enfermedad periodontal), y en la mayoría de ellos el tamaño muestral era pequeño además de que estos investigadores no valoraron adecuadamente el número de drop-out o no actualizaron regularmente el grado de exposición a lo largo del estudio. Otra limitación es el incompleto ajuste de algunos estudios por los factores de riesgo Framingham. A pesar de ello, Humphrey y cols., realizaron un subgrupo de análisis de la calidad de los estudios con el ajuste de estos factores anteriormente mencionados, identificando de esta manera una asociación independiente entre la enfermedad periodontal y CHD. También otra limitación es el ajuste de la asociación a un factor de confusión como es el tabaco (Hujoel et al., 2002).

Durante muchos años esta asociación fue un tema de gran controversia precisándose estudios longitudinales con medidas estandarizadas de enfermedad periodontal y un cuidadoso seguimiento con el ajuste de factores de confusión conocidos con el fin de esclarecer el "link" entre la ECV y la enfermedad periodontal. Sin embargo, en el International Workshop de 2013 (Tonetti et al., 2013), se establece definitivamente la periodontitis como factor de riesgo de la ECV, así como los pasos a seguir para realizar estudios en este ámbito y revisión de su plausibilidad biológica.

SÍNDROME METABÓLICO

DEFINICIÓN: El Síndrome Metabólico (SMet) es un cluster de múltiples entidades diferentes. El estrés oxidativo parece tener el mayor rol en la patogénesis de todos los componentes que forman parte de este síndrome. El síndrome metabólico es una patología largamente extendida en países occidentales. Sus criterios diagnósticos han sido recientemente definidos, aunque continúan siendo ambiguos debido a que estas enfermedades, entre las que están obesidad, hiperglucemia, hiperinsulinemia, y dislipidemia, son consideradas serios factores de riesgo de ECV (Reaven, 1998). Debido a que el SMet está caracterizado por numerosos factores, es bastante difícil establecer un correcto diagnóstico y un tratamiento adecuado.

Inicialmente, el SMet fue definido como el Síndrome X (Reaven, 1998), para después denominarse "cuarteto mortal", debido a la sinergia entre sus componentes como son la hiperinsulinemia, hipertensión, hiperglucemia, y obesidad visceral. Más tarde, se pasó a definir Síndrome de Resistencia a la insulina puesto que algunos autores creían que la resistencia a la insulina era el factor predominante que predisponía a la aparición de los síntomas.

CLÍNICA

Actualmente, el SMet es objeto de clara controversia, debido a las numerosas definiciones que han sido propuestas para definir dicho síndrome, siendo los criterios propuestos por el National Cholesterol Education Program Adult Treatment Panel III los más usados. No obstante, la AHA define el SMet como un síndrome caracterizado por un grupo de factores de riesgo metabólicos en un individuo (Marchetti et al., 2012). Entre estos factores están los siguientes:

  • Obesidad abdominal: Acumulación excesiva de tejido graso alrededor del abdomen.

  • Dislipidemia aterogénica: Triglicéridos altos, HDL bajo, y alto LDL que provoca la formación de placa ateromatosas en la pared de arterias.

  • Elevada presión arterial.

  • Resistencia a la insulina o intolerancia a la glucosa: El cuerpo no es capaz de usar la insulina o la glucosa en sangre.

  • Estado protrombótico: Fibrinógeno alto o inhibidor del activador de plasminógeno-1 en sangre.

  • Estado proinflamatorio: Elevado CRP en sangre.

La AHA y el National Heart, Lung and Blood Istitute (NHLBI) recomienda el diagnóstico de SMet con la presencia de 3 o más de los siguientes componentes (Grundy et al., 2005):

  • Circunferencia en cintura elevada:

  • Hombres: igual o mayor que 102 cm.

  • Mujeres: igual o mayor de 88 cm.

  • Triglicéridos elevados: igual o mayor de 150 mg/dl.

  • HDL reducido ("colesterol bueno"):

  • Hombres menos de 40 mg/dl.

  • Mujeres: menos de 50 mg/dl.

  • Presión arterial elevada: igual o mayor de 130/85 mm Hg.

  • Glucosa en ayunas elevada: igual o mayor de 100 mg/dl.

La resistencia a la insulina es una condición en la que la cantidad normal de insulina es insuficiente para obtener una respuesta adecuada de los tejidos adiposo y muscular aso como de las células hepáticas, dando lugar a una hiperglucemia severa con efecto deletéreo sistémico, como son las bajas defensas intracelulares antioxidantes (Di Filippo et al., 2007; Tilg & Moschen, 2008; Bruce et al., 2003; Koyama et al., 2005).

En este punto, está claro que el denominador común entre el grupo de patologías que componen el SMet es el estrés oxidativo y la consecuente hiperinflamación que prima en la cadena de interacciones y que da lugar a graves complicaciones sistémicas como es la ECV, o complicaciones locales como es la periodontitis. El SMet permite un estado pro-oxidativo en los tejidos periodontales, alterando los mecanismos de defensa antioxidantes. Esto afecta a la repuesta tisular con el ataque bacteriano. Por el contrario, la periodontitis, siendo una gran fuente de marcadores oxidativos, promueve el comienzo de la resistencia a la insulina, y el círculo vicioso característico del SMet (Chapple et al., 2007).

Solamente se ha realizado un estudio longitudinal prospectivo que evalúe la asociación entre SMet y enfermedad periodontal. Morita y cols. (T. Morita et al., 2010) realizan un estudio de cohortes, en una muestra de 1.023 pacientes con un seguimiento a 4 años. El OR fue de 1,6 con un IC al 95% (1,1-2,2). Con ello determinan que la presencia de bolsas periodontales está asociado con la conversión positiva de los componentes de SMet, considerando finalmente que la prevención de la enfermedad periodontal podría prevenir el SMet.

Sin embargo, todas estas investigaciones presentan una serie de limitaciones debido a la falta de consenso tanto en la definición de periodontitis (Page & Eke, 2007; Tonetti et al., 2005) como en la definición de síndrome metabólico (Grundy et al., 2005), la cual parece estar aun en controversia. Ello da lugar a muestras heterogéneas, dispersas y no representativas de la población, alterando de esta manera los resultados y dificultando la investigación en este campo de la medicina periodontal. Además, según un estudio realizado por Futura y cols. (Furuta et al., 2013), existe unas diferencias entre sexos, que hay que tener en cuenta a la hora de analizar y estratificar los datos, puesto que las mujeres presentan una mayor prevalencia que los hombres.

BIBLIOGRAFÍA

1. Águeda A, Ramón JM, Manau C, Guerrero A, Echeverria JJ. Periodontal disease as a risk factor for adverse pregnancy outcomes: a prospective cohort study. Journal of clinical periodontology;35:16, 2008. [ Links ]

2. Al-Zahrani MS, Bissada NF. Obesity and periodontal disease in young, middle-aged, and older adults. Journal of Periodontol;74:610, 2003. [ Links ]

3. Alikhani M, et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone;40 (2):345, 2007. [ Links ]

4. Almeida RF, Alba AL. Efectos de las enfermedades periodontales sobre la diabetes. Periodoncia y Osteointegración;23 (3):181, 2013. [ Links ]

5. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes care;35 Suppl 1:S64, 2012. [ Links ]

6. Aquilante CL, et al. Relationship between plasma resistin concentrations, inflammatory chemokines, and components of the metabolic syndrome in adults. Metabolism: clinical and experimental;57 (4):494, 2008. [ Links ]

7. Armutcu F, et al. Oxidative stress markers, C-reactive protein and heat shock protein 70 levels in subjects with metabolic syndrome. Clinical chemistry and laboratory medicine: CCLM / FESCC, 46 (6):785, 2008. [ Links ]

8. Bahekar AA, et al. The prevalence and incidence of coronary heart disease is significantly increased in periodontitis: A meta-analysis. American heart journal;154 (5):830, 2007. [ Links ]

9. Bawadi HA, et al. The association between periodontal disease, physical activity and healthy diet among adults in Jordan. Journal of periodontal research;46 (1):74, 2011. [ Links ]

10. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG: an international journal of obstetrics and gynaecology;109, 527, 2002. [ Links ]

11. Beck JD, Offenbacher S. Systemic effects of periodontitis: epidemiology of periodontal disease and cardiovascular disease. Journal of Periodontology;76 (11 Suppl):2089, 2005. [ Links ]

12. Beck JD, et al. The Periodontitis and Vascular Events (PAVE) pilot study: adverse events. Journal of Periodontology;79 (1):90, 2008. [ Links ]

13. Benguigui C, et al. Metabolic syndrome, insulin resistance, and periodontitis: a cross-sectional study in a middle-aged French population. Journal of clinical periodontology;37 (7):.601, 2010. [ Links ]

14. Bensley L, VanEenwyk J, Ossiander EM. Associations of self-reported periodontal disease with metabolic syndrome and number of self-reported chronic conditions. Preventing chronic disease;8 (3):A50, 2011. [ Links ]

15. Bibby E, Stewart A. The epidemiology of preterm birth. Neuro endocrinology letters;25 Suppl 1:43, 2004. [ Links ]

16. Boggess KA, Beck JD, Murtha AP, Moss K, Offenbacher, S. Maternal periodontal disease in early pregnancy and risk for a small-for-gestational-age infant. American journal of obstetrics and gynecology;194:1316, 2006. [ Links ]

17. Boggess KA, Lieff S, Murtha AP, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstetrics and gynecology;101:227, 2003. [ Links ]

18. Borges, I. et al. Proinflammatory and oxidative stress markers in patients with periodontal disease. Mediators of inflammation; p.45794, 2007a. [ Links ]

19. Borges PK, de O, et al. Prevalence and characteristics associated with metabolic syndrome in Japanese-Brazilians with and without periodontal disease. Cadernos de saúde pública;23 (3):657, 2007b. [ Links ]

20. Borgnakke WS, et al. Effect of periodontal disease on diabetes:systematic review of epidemiologic observational evidence. Journal of clinical periodontology;40 Suppl 14:S135, 2013. [ Links ]

21. Brock GR, et al. Local and systemic total antioxidant capacity in periodontitis and health. Journal of clinical periodontology;31 (7):515, 2004. [ Links ]

22. Bruce CR, et al. Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes;52 (9):2338, 2003. [ Links ]

23. Bullon P, et al. Metabolic syndrome and periodontitis: is oxidative stress a common link?. Journal of Dental Research;88 (6):503, 2009. [ Links ]

24. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease?The common soil hypothesis revisited. Arteriosclerosis, thrombosis, and vascular biology;24 (5):816, 2004. [ Links ]

25. Chaffee BW, Weston SJ. Association between chronic periodontal disease and obesity:a systematic review and meta-analysis. Journal of Periodontology;81 (12):1708, 2010. [ Links ]

26. Chambrone L, Guglielmetti MR, Pannuti CM, Chambrone LA. Evidence grade associating periodontitis to preterm birth and/or low birth weight: I. A systematic review of prospective cohort studies. Journal of clinical periodontology;38:795, 2011a. [ Links ]

27. Chambrone L, Pannuti CM, Guglielmetti MR, Chambrone LA. Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: a systematic review of randomized trials evaluating the effects of periodontal treatment. Journal of clinical periodontology;38, 902:2011b. [ Links ]

28. Chapple ILC, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontology 2000;43:160, 2007. [ Links ]

29. Chapple ILC, et al. Compromised GCF total antioxidant capacity in periodontitis: cause or effect?. Journal of clinical Periodontology;34 (2):103, 2007. [ Links ]

30. Chapple ILC, Genco R. Working group 2 of the joint EFP/AAP workshop, 2013. Diabetes and periodontal diseases: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. Journal of Periodontology;84 (4 Suppl):S106–12. [ Links ]

31. Collins JG, Windley HW, 3RD, Arnold RR, Offenbacher S. Effects of a Porphyromonas gingivalis infection on inflammatory mediator response and pregnancy outcome in hamsters. Infection and immunity;62:4356, 1994. [ Links ]

32. Couper DJ, et al. The Periodontitis and Vascular Events (PAVE) pilot study: recruitment, retention, and community care controls. Journal of Periodontology;79 (1):80, 2008. [ Links ]

33. D'Aiuto F, Tonetti MS. Contribution of periodontal therapy on individual cardiovascular risk assessment. Archives of internal medicine;165 (16):1920, 2005. [ Links ]

34. D'Aiuto, F, et al. Association of the metabolic syndrome with severe periodontitis in a large U.S. population-based survey. The Journal of clinical endocrinology and metabolism;93 (10):3989, 2008. [ Links ]

35. D'Aiuto F, et al. Oxidative stress, systemic inflammation, and severe periodontitis. Journal of Dental Research;89 (11):1241, 2010. [ Links ]

36. D'Aiuto F, et al. Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial. American heart journal;151 (5):977, 2006. [ Links ]

37. D'Aiuto F, et al. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. Journal of Dental Research;84 (3):269, 2005. [ Links ]

38. D'Aiuto F, Orlandi M, Gunsolley JC. Evidence that periodontal treatment improves biomarkers and CVD outcomes. Journal of Periodontology;84 (4 Suppl):S85, 2013. [ Links ]

39. Dahiya P, Kamal R, Gupta R. Obesity, periodontal and general health:Relationship and management. Indian journal of endocrinology and metabolism;16 (1),:88, 2012. [ Links ]

40. Dalla Vecchia CF, et al. Overweight and Obesity as Risk Indicators for Periodontitis in Adults. Journal of Periodontology;76 (10):1721, 2005. [ Links ]

41. Di Filippo C, et al. Insulin resistance and postprandial hyperglycemia the bad companions in natural history of diabetes:effects on health of vascular tree. Current diabetes reviews;3 (4):268, 2007. [ Links ]

42. Dietrich T, et al. The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. Journal of Periodontology;84 (4 Suppl):S70, 2013. [ Links ]

43. Ekuni D, et al. Relationship between body mass index and periodontitis in young Japanese adults. Journal of periodontal research;43 (4):417, 2008. [ Links ]

44. El-Haschimi K, et al. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. The Journal of clinical investigation;105 (12):1827, 2000. [ Links ]

45. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. Journal of Periodontology;62 (2):123, 1991. [ Links ]

46. Engebretson S, Kocher T. Evidence that periodontal treatment improves diabetes outcomes:a systematic review and meta-analysis. Journal of clinical periodontology;40 Suppl 14:S153, 2013. [ Links ]

47. Faria-Almeida R, Navarro A, Bascones A. Clinical and Metabolic Changes After Conventional Treatment of Type 2 Diabetic Patients With Chronic Periodontitis. Journal of Periodontology;77 (4):591, 2006. [ Links ]

48. Fogacci MF, Vettore MV, Leao AT. The effect of periodontal therapy on preterm low birth weight: a meta-analysis. Obstetrics and gynecology;117, 153:2011. [ Links ]

49. Furuta M, et al. Gender differences in the association between metabolic syndrome and periodontal disease: the Hisayama Study. Journal of clinical periodontology;40 (8):743, 2013. [ Links ]

50. George A, Shamim S, Johnson M, Ajwani S, Bhole S, Blinkhorn A, Ellis S, Andrews K. Periodontal treatment during pregnancy and birth outcomes: a meta-analysis of randomised trials. International journal of evidence-based healthcare;9:122 2011. [ Links ]

51. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. The New England journal of medicine;342:1500, 2000. [ Links ]

52. Gorman A, et al. Overweight and obesity predict time to periodontal disease progression in men. Journal of clinical periodontology;39 (2):107, 2012. [ Links ]

53. Grossi SG, et al. Treatment of periodontal disease in diabetics reduces glycated hemoglobin. Journal of Periodontology;68 (8):713, 1997. [ Links ]

54. Grundy SM, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association / National Heart, Lung, and Blood Institute Scientific Statement. Circulation; 112 (17):2735, 2005. [ Links ]

55. Han D-H, et al. The association of metabolic syndrome with periodontal disease is confounded by age and smoking in a Korean population: the Shiwha-Banwol Environmental Health Study. Journal of clinical periodontology;37 (7):609, 2010. [ Links ]

56. Hansen LL, et al. Insulin signaling is inhibited by micromolar concentrations of H (2)O (2). Evidence for a role of H (2)O (2) in tumor necrosis factor alpha-mediated insulin resistance. The Journal of biological chemistry;274 (35):25078, 1999. [ Links ]

57. Hotamisligil GS, et al. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. The Journal of clinical investigation;95 (5):2409, 1995. [ Links ]

58. Hujoel PP, et al. Pre-existing cardiovascular disease and periodontitis:a follow-up study. Journal of Dental Research;81 (3):186, 2002. [ Links ]

59. Humphrey LL, et al. Periodontal Disease and Coronary Heart Disease Incidence: A Systematic Review and Meta-analysis. Journal of General Internal Medicine;23 (12):2079, 2008. [ Links ]

60. Jain A, et al. Role for periodontitis in the progression of lipid deposition in an animal model. Infection and Immunity, 71 (10):6012, 2003. [ Links ]

61. Janket S-J, et al. Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics;95 (5):559, 2003. [ Links ]

62. Jeffcoat M, Parry S, Sammel M, Clothier B, Catlin A, Macones G. Periodontal infection and preterm birth: successful periodontal therapy reduces the risk of preterm birth. BJOG: an international journal of obstetrics and gynaecology;118:250, 2011. [ Links ]

63. Jeffcoat MK, Geurs NC, Reddy MS, Cliver SP, Goldenberg RL, Hauth JC. Periodontal infection and preterm birth: results of a prospective study. Journal of the American Dental Association;132:875, 2001. [ Links ]

64. Jeffcoat MK, Hauth JC, Geurs NC, Reddy MS, Cliver SP, Hodgkins PM, Goldenberg RL. Periodontal disease and preterm birth: results of a pilot intervention study. Journal of Periodontology;74:1214, 2003. [ Links ]

65. Jiménez M, et al. Prospective associations between measures of adiposity and periodontal disease. Obesity (Silver Spring, Md.);20 (8):1718, 2012. [ Links ]

66. Kahn R. Metabolic syndrome-what is the clinical usefulness?. Lancet;371 (9628):1892, 2008. [ Links ]

67. Khader YS, et al. The association between periodontal disease and obesity among adults in Jordan. Journal of clinical periodontology;36 (1):18, 2009. [ Links ]

68. Khader YS, Ta'ani Q. Periodontal diseases and the risk of preterm birth and low birth weight: a meta-analysis. Journal of Periodontology;76:161, 2005. [ Links ]

69. Kim AJ, Lo AJ, Pullin DA, Thornton-Johnson DS, Karimbux NY. Scaling and root planing treatment for periodontitis to reduce preterm birth and low birth weight: a systematic review and meta-analysis of randomized controlled trials. Journal of Periodontology;83:1508, 2012. [ Links ]

70. Kim E-J, Jin B-H, Bae K-H. Periodontitis and obesity:a study of the Fourth Korean National Health and Nutrition Examination Survey. Journal of Periodontology;82 (4):533, 2011. [ Links ]

71. Kiran M, et al. The effect of improved periodontal health on metabolic control in type 2 diabetes mellitus. Journal of clinical periodontology;32 (3):266, 2005. [ Links ]

72. Kowalski M, et al. Estimation of oxidation-reduction balance in subjects with metabolic syndrome together with or without periodontal diseases. Polski merkuriusz lekarski: organ Polskiego Towarzystwa Lekarskiego;26 (156):626, 2009. [ Links ]

73. Koyama H, et al. Plasma level of endogenous secretory RAGE is associated with components of the metabolic syndrome and atherosclerosis. Arteriosclerosis, thrombosis, and vascular biology;25 (12):2587, 2005. [ Links ]

74. Kushiyama M, Shimazaki Y, Yamashita Y. Relationship between metabolic syndrome and periodontal disease in Japanese adults. Journal of Periodontology;80 (10):1610, 2009. [ Links ]

75. Kwon Y-E, et al The relationship between periodontitis and metabolic syndrome among a Korean nationally representative sample of adults. Journal of clinical periodontology;38 (9):781, 2011. [ Links ]

76. Li P, et al. [Detection of the parameters for early atherosclerosis in patients with metabolic syndrome and periodontitis]. Beijing da xue xue bao. Yi xue ban =Journal of Peking University. Health sciences;43 (1):34, 2011. [ Links ]

77. Li P, et al. Relationship of metabolic syndrome to chronic periodontitis. Journal of Periodontology;80 (4):541, 2009. [ Links ]

78. Lieff S, Boggess KA, Murtha AP, Jared H, Madianos PN, Moss K, Beck J, Offenbacher S. The oral conditions and pregnancy study: periodontal status of a cohort of pregnant women. Journal of Periodontology;75:116, 2004. [ Links ]

79. Linden GJ, Lyons A, Scannapieco FA. Periodontal systemic associations: review of the evidence. Journal of Periodontology;84 (4 Suppl):S8, 2013. [ Links ]

80. López NJ, et al. Effects of periodontal therapy on systemic markers of inflammation in patients with metabolic syndrome: a controlled clinical trial. Journal of Periodontology;83 (3):267, 2012. [ Links ]

81. López NJ, Da Silva I., Ipinza J, Gutiérrez J. Periodontal therapy reduces the rate of preterm low birth weight in women with pregnancy-associated gingivitis. Journal of Periodontology;76:2144, 2005. [ Links ]

82. López NJ, Smith PC, Gutiérrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: a randomized controlled trial. Journal of Periodontology;73:911, 2002. [ Links ]

83. MacDorman MF, Martin JA, Mathews TJ, Hoyert DL, Ventura SJ. Explaining the 2001-02 infant mortality increase: data from the linked birth/infant death data set. National vital statistics reports: from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System;53:1, 2005. [ Links ]

84. Macones GA, Parry S, Nelson DB, Strauss JF, Ludmir J, Cohen AW, Stamilio DM, Appleby D, Clothier B, Sammel MD, Jeffcoat M. Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: results from the Periodontal Infections and Prematurity Study (PIPS). American journal of obstetrics and gynecology;202, 147:e1, 2010. [ Links ]

85. Maddux BA, et al. Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by mircomolar concentrations of alpha-lipoic acid. Diabetes;50 (2):404, 2001. [ Links ]

86. Madianos PN, Lieff S, Murtha AP, Boggess KA, Auten RL, Jr, Beck JD, Offenbacher S. Maternal periodontitis and prematurity. Part II:Maternal infection and fetal exposure. Annals of periodontology / the American Academy of Periodontology;6:175, 2001. [ Links ]

87. Manau C, et al. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. Journal of clinical periodontology;35 (5):385, 2008.. [ Links ]

88. Marchetti E, et al. Periodontal disease:the influence of metabolic syndrome. Nutrition &metabolism;9 (1):88, 2012. [ Links ]

89. Marín C, Segura-Egea JJ, Martínez-Sahuquillo A, Bullón P. Correlation between infant birth weight and mother's periodontal status. Journal of clinical periodontology;32:299, 2005. [ Links ]

90. Mealey BL, Oates TW. Diabetes Mellitus and Periodontal Diseases. Journal of Periodontology;77 (8):1289, 2006. [ Links ]

91. Meurman J-H, Sanz M, Janket S-J. Oral health, atherosclerosis, and cardiovascular disease. Critical reviews in oral biology and medicine: an official publication of the American Association of Oral Biologists;15 (6):403, 2004. [ Links ]

92. Michalowicz BS, Hodges JS, Diangelis AJ, Lupo VR, Novak MJ, Ferguson JE, Buchanan W, Bofill J, Papapanou PN, Mitchell DA, Matseoane S, Tschida PA. Treatment of periodontal disease and the risk of preterm birth. The New England journal of medicine;355:1885, 2006. [ Links ]

93. Modéer T, et al. Association between obesity and periodontal risk indicators in adolescents. International journal of pediatric obesity: IJPO: an official journal of the International Association for the Study of Obesity;6 (2-2):e264, 2011. [ Links ]

94. Montebugnoli L, et al. Poor oral health is associated with coronary heart disease and elevated systemic inflammatory and haemostatic factors. Journal of clinical periodontology;31 (1):25, 2004. [ Links ]

95. Moore S, Ide M, Coward PY, Randhawa M, Borkowska E, Baylis R, Wilson RF. A prospective study to investigate the relationship between periodontal disease and adverse pregnancy outcome. British dental journal;197:251;discussion 247, 2004. [ Links ]

96. Moreu G, Téllez L, González-Jaranay M. Relationship between maternal periodontal disease and low-birth-weight pre-term infants. Journal of clinical periodontology;32, 622, 2005. [ Links ]

97. Morita I, et al. Five-year incidence of periodontal disease is related to body mass index. Journal of Dental Research;90 (2):199, 2011. [ Links ]

98. Morita T, et al. A cohort study on the association between periodontal disease and the development of metabolic syndrome. Journal of Periodontology;81 (4):512, 2010. [ Links ]

99. Mustapha IZ, et al. Markers of Systemic Bacterial Exposure in Periodontal Disease and Cardiovascular Disease Risk: A Systematic Review and Meta-Analysis. Journal of Periodontology;78 (12):2289, 2007. [ Links ]

100. Nelson RG, et al. Periodontal disease and NIDDM in Pima Indians. Diabetes care;13 (8):836, 1990. [ Links ]

101. Nesbitt MJ, et al. Association of periodontitis and metabolic syndrome in the Baltimore Longitudinal Study of Aging. Aging clinical and experimental research;22 (3):238, 2010. [ Links ]

102. Newnham JP, Newnham IA, Ball CM, Wright M, Pennell CE, Swain J, Doherty DA. Treatment of periodontal disease during pregnancy: a randomized controlled trial. Obstetrics and gynecology;114:1239, 2009. [ Links ]

103. Nibali L, Donos N. Periodontitis and redox status: a review. Current pharmaceutical design;19 (15):2687, 2013. [ Links ]

104. Nibali L, et al. Clinical review: Association between metabolic syndrome and periodontitis: a systematic review and meta-analysis. The Journal of clinical endocrinology and metabolism;98 (3):913, 2013. [ Links ]

105. Nishimura F, Murayama Y. Periodontal inflammation and insulin resistance-lessons from obesity. Journal of Dental Research;80 (8):1690, 2001. [ Links ]

106. Offenbacher S. Periodontal Diseases: Pathogenesis. Annals of periodontology /the American Academy of Periodontology;1 (1):821, 1996. Available at: http://www.google.es/#q=Frequency+of+the+WHO+metabolic+syndrome+in+European+cohorts%2C+and+an+alternative+definition+of+an+insulin+resistance+syndrome. [ Links ]

107. Offenbacher S, et al. Periodontitis-atherosclerosis syndrome: an expanded model of pathogenesis. Journal of periodontal research;34 (7):346, 1999. [ Links ]

108. Offenbacher S, Beck JD, Jared HL, Mauriello SM, Mendoza LC, Couper DJ, Stewart DD, Murtha, AP, Cochran DL, Dudley DJ, Reddy MS, Geurs NC, Hauth JC. Effects of periodontal therapy on rate of preterm delivery: a randomized controlled trial. Obstetrics and gynecology,;114:551, 2009. [ Links ]

109. Offenbacher S, Boggess KA, Murtha AP, Jared HL, Lieff S, Mckaig RG, Mauriello SM, Moss KL, Beck JD. Progressive periodontal disease and risk of very preterm delivery. Obstetrics and gynecology;107:29, 2006a. [ Links ]

110. Offenbacher S, Jared HL, O'reilly PG, Wells SR, Salvi GE., Lawrence HP, Socransky SS, Beck JD. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Annals of periodontology / the American Academy of Periodontology;3:233, 1998. [ Links ]

111. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, Mckaig R, Beck J. Periodontal infection as a possible risk factor for preterm low birth weight. Journal of Periodontology;67:1103, 1996. [ Links ]

112. Offenbacher S, Lieff S, Boggess KA, Murtha AP, Madianos PN, Champagne CM, Mckaig RG, Jared HL, Mauriello SM, Auten RL, Jr, Herbert WN, Beck JD. Maternal periodontitis and prematurity. Part I: Obstetric outcome of prematurity and growth restriction. Annals of periodontology/the American Academy of Periodontology;6:164, 2001. [ Links ]

113. Offenbacher S, Lin D, Strauss R, Mckaig R, Irving J, Barros SP, Moss K, Barrow DA, Hefti A, Beck JD. Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: a pilot study. Journal of Periodontology;77:2011, 2006b. [ Links ]

114. Offenbacher S, Riche EL, Barros SP, Bobetsis YA, Lin D, Beck JD. Effects of maternal Campylobacter rectus infection on murine placenta, fetal and neonatal survival, and brain development. Journal of Periodontology;76, 2133, 2005. [ Links ]

115. Oliveira AM, De Oliveira PA, Cota LO, Magalhaes CS, Moreira AN, Costa FO.. Periodontal therapy and risk for adverse pregnancy outcomes. Clinical oral investigations;15:609, 2011. [ Links ]

116. Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. Journal of Periodontology;78 (7 Suppl):1387, 2007. [ Links ]

117. Perlstein MI, Bissada NF. Influence of obesity and hypertension on the severity of periodontitis in rats. Oral surgery, oral medicine, and oral pathology;43 (5):707, 1977. [ Links ]

118. Perticone F, et al. Obesity and body fat distribution induce endothelial dysfunction by oxidative stress: protective effect of vitamin C. Diabetes;50 (1):159, 2001. [ Links ]

119. Piconi S, et al. Treatment of periodontal disease results in improvements in endothelial dysfunction and reduction of the carotid intima-media thickness. FASEB journal: official publication of the Federation of American Societies for Experimental Biology, 23 (4):1196, 2009. [ Links ]

120. Pischon T, et al. Leisure-time physical activity and reduced plasma levels of obesity-related inflammatory markers. Obesity research;11 (9):1055, 2003. [ Links ]

121. Pitiphat W, Joshipura KJ, Gillman MW, Williams PL, Douglass CW, Rich-Edwards JW. Maternal periodontitis and adverse pregnancy outcomes. Community dentistry and oral epidemiology;36:3, 2008. [ Links ]

122. Polyzos NP, Polyzos IP, Zavos A, Valachis A, Mauri D, Papanikolaou EG, Tzioras S, Weber D, Messinis IE. Obstetric outcomes after treatment of periodontal disease during pregnancy: systematic review and meta-analysis. BMJ;341:c7017, 2010. [ Links ]

123. Pombo JH, Arno AG. Efectos de la diabetes sobre las enfermedades periodontales. Periodoncia y Osteointegración;23 (3):167, 2013. [ Links ]

124. Preshaw PM, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia, 55 (1):21, 2012. [ Links ]

125. Radnai M, Pal A, Novak T, Urban E, Eller J, Gorzo I. Benefits of periodontal therapy when preterm birth threatens. Journal of dental research;88:280, 2009. [ Links ]

126. Rajapakse PS, Nagarathne M, Chandrasekra KB, Dasanayake AP. Periodontal disease and prematurity among non-smoking Sri Lankan women. Journal of dental research;84:274, 2005. [ Links ]

127. Rakoto-Alson S, Tenenbaum H, Davideau JL. Periodontal diseases, preterm births, and low birth weight: findings from a homogeneous cohort of women in Madagascar. Journal of Periodontology;81:205, 2010. [ Links ]

128. Ramos JG, Martins-Costa S, Edelweiss MI, Costa CA. Placental bed lesions and infant birth weight in hypertensive pregnant women. Brazilian journal of medical and biological research =Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica. [et al.];28:447, 1995. [ Links ]

129. Reaven GM. Insulin resistance and human disease: a short history. Journal of basic and clinical physiology and pharmacology;9 (2-4):387, 1998. [ Links ]

130. Reaven GM. The metabolic syndrome: is this diagnosis necessary?. The American journal of clinical nutrition;83 (6):1237, 2006. [ Links ]

131. Reeves AF, et al. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Archives of pediatrics &adolescent medicine;160 (9):894, 2006. [ Links ]

132. Reyes L, et al. Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology. Journal of clinical periodontology;40 Suppl 14:S30, 2013. [ Links ]

133. Rotter V, Nagaev I, Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-alpha, overexpressed in human fat cells from insulin-resistant subjects. The Journal of biological chemistry;278 (46):45777, 2003. [ Links ]

134. Sadatmansouri S, Sedighpoor N, Aghaloo M. Effects of periodontal treatment phase I on birth term and birth weight. Journal of the Indian Society of Pedodontics and Preventive Dentistry, 24, 23, 2006. [ Links ]

135. Saddki N, Bachok N, Hussain NH, Zainudin SL, Sosroseno W. The association between maternal periodontitis and low birth weight infants among Malay women. Community dentistry and oral epidemiology;36:296, 2008. [ Links ]

136. Sharma R, Maimanuku LR, Morse Z, Pack AR. Preterm low birth weights associated with periodontal disease in the Fiji Islands. International dental journal;57:257, 2007. [ Links ]

137. Scannapieco FA, Bush RB, Paju S. Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Annals of periodontology/the American Academy of Periodontology;8:70, 2003. [ Links ]

138. Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. The New England journal of medicine;339 (7):482, 1998. [ Links ]

139. Santa Cruz I, Herrera D, Martín C, Herrero A, Sanz M. Association between periodontal status and pre-term and/or low-birth weight in Spain: clinical and microbiological parameters. Journal of periodontal research;48:443, 2013. [ Links ]

140. Saremi, A, et al. 2005. Periodontal disease and mortality in type 2 diabetes. Diabetes care, 28 (1):27–32. [ Links ]

141. Srinivas SK, Sammel MD, Stamilio DM, Clothier B, Jeffcoat MK, Parry S, Macones GA, Elovitz MA, Metlay J. Periodontal disease and adverse pregnancy outcomes: is there an association?. American journal of obstetrics and gynecology;200:497 e1, 2009. [ Links ]

142. Saxlin T, et al. Association between periodontal infection and obesity: results of the Health 2000 Survey. Journal of clinical periodontology, 38 (3):236, 2011. [ Links ]

143. Saxlin T, et al. Overweight and obesity weakly predict the development of periodontal infection. Journal of clinical periodontology;37 (12):1059, 2010. [ Links ]

144. Schenkein HA, Loos BG. Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases. Journal of clinical periodontology;40 Suppl 14:S51, 2013. [ Links ]

145. Sgolastra F, et al. Efficacy of Er: YAG laser in the treatment of chronic periodontitis: systematic review and meta-analysis. Lasers in medical science;27 (3):661, 2012. [ Links ]

146. Shimazaki Y, et al. Relationship of metabolic syndrome to periodontal disease in Japanese women: the Hisayama Study. Journal of Dental Research;86 (3):271, 2007. [ Links ]

147. Shlossman M, Knowler WC, Pettitt DJ, Genco RJ. Type 2 diabetes mellitus and periodontal disease. J Am Dent Assoc;Oct, 121 (4):532, 1990. [ Links ]

148. Tarannum F, Faizuddin M. Effect of periodontal therapy on pregnancy outcome in women affected by periodontitis. Journal of Periodontology;78:2095, 2007. [ Links ]

149. Taylor GW, Becker MP. Increased efficiency of analyses:cumulative logistic regression vs ordinary logistic regression. Community dentistry and oral epidemiology;26 (1):1, 1998. [ Links ]

150. Taylor GW, et al. Glycemic Control and Alveolar Bone Loss Progression in Type 2 Diabetes. Annals of periodontology / the American Academy of Periodontology;3 (1):30, 1998. [ Links ]

151. Taylor, G.W, et al. 1996. Severe periodontitis and risk for poor glycemic control in patients with non-insulin-dependent diabetes mellitus. Journal of Periodontology;67 (10 Suppl):1085–1093. [ Links ]

152. Taylor JJ, Preshaw PM, Lalla E. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. Journal of Periodontology;84 (4 Suppl):S113, 2013. [ Links ]

153. Tilg H, Moschen AR. Inflammatory mechanisms in the regulation of insulin resistance. Molecular medicine (Cambridge, Mass.);14 (3-4):222, 2008. [ Links ]

154. Tomás I, et al. Periodontal health status and bacteraemia from daily oral activities: systematic review/meta-analysis. Journal of clinical periodontology;39 (3):213, 2012. [ Links ]

155. Tonetti MS, et al. Treatment of periodontitis and endothelial function. The New England journal of medicine;356 (9):911, 2007. [ Links ]

156. Tonetti MS, Claffey N. On behalf of the European Workshop in Periodontology group C*. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C Consensus report of the 5th European workshop in periodontology. Journal of clinical periodontology;32 (s6):210, 2005. [ Links ]

157. Tonetti MS, Van Dyke TE. Working group 1 of the joint EFP/AAP workshop. Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. Journal of clinical periodontology;40 Suppl 14:S24, 2013. [ Links ]

158. Uppal A, Uppal S, Pinto A, Dutta M, Shrivatsa S, Dandolu V, Mupparapu M. The effectiveness of periodontal disease treatment during pregnancy in reducing the risk of experiencing preterm birth and low birth weight:a meta-analysis. Journal of the American Dental Association;141:1423, 2010. [ Links ]

159. Uysal KT, et al. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature;389 (6651):610, 1997. [ Links ]

160. Vergnes JN, Sixou M. Preterm low birth weight and maternal periodontal status: a meta-analysis. American journal of obstetrics and gynecology;196:135 e1, 2007. [ Links ]

161. Wimmer G, Pihlstrom BL. A critical assessment of adverse pregnancy outcome and periodontal disease. Journal of clinical periodontology;35:380, 2008. [ Links ]

162. Wood N, Johnson RB, Streckfus CF. Comparison of body composition and periodontal disease using nutritional assessment techniques:Third National Health and Nutrition Examination Survey (NHANES III). Journal of clinical periodontology;30 (4):321, 2003. [ Links ]

163. Xiong X, Buekens P, Fraser WD, Beck J, Offenbacher S. Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG: an international journal of obstetrics and gynaecology;113:135, 2006. [ Links ]

164. Xiong X, Buekens P, Vastardis S, Yu SM. Periodontal disease and pregnancy outcomes: state-of-the-science. Obstetrical &gynecological survey;62:605, 2007. [ Links ]

165. Yeo A, Smith MA, Lin D, Riche EL, Moore A, Elter J, Offenbacher S. Campylobacter rectus mediates growth restriction in pregnant mice. Journal of Periodontology;76:551, 2005. [ Links ]

166. Zimmermann GS, et al. Local and circulating levels of adipocytokines in obese and normal weight individuals with chronic periodontitis. Journal of Periodontology;84 (5):624, 2013. [ Links ]

Received: May 10, 2017; Accepted: May 20, 2017

Creative Commons License Este es un articulo publicado en acceso abierto bajo una licencia Creative Commons