Periodontitis As A Risk Factor For Stroke: A Systematic Review And Meta-Analysis

Nathalia Carolina Fernandes Fagundes, Anna Paula Costa Ponte Sousa Carvalho Almeida, Kelly Fernanda Barbosa Vilhena, Marcela Baraúna Magno, Lucianne Cople Maia, Rafael Rodrigues Lima, Nathalia Carolina Fernandes Fagundes, Anna Paula Costa Ponte Sousa Carvalho Almeida, Kelly Fernanda Barbosa Vilhena, Marcela Baraúna Magno, Lucianne Cople Maia, Rafael Rodrigues Lima

Abstract

This systematic review and meta-analysis investigate the association between periodontitis and stroke. This review followed the methods established by the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines. Searches were conducted in five databases and two sources of grey literature. After the selection of the articles, a risk of bias evaluation was performed. Three meta-analyzes were performed: Assessing the overall association between stroke and periodontitis in case-control studies; Ischemic stroke and periodontitis in case-control studies; The association between stroke and periodontitis in cohort studies. Heterogeneity was assessed using the I2 index and the odds ratio was also calculated (p < 0.05). The Grading of Recommendations Assessment, Development and Evaluation (GRADE) was applied to evaluate the level of evidence. 2193 potentially relevant studies were identified, with 10 studies included in qualitative and quantitative analysis. All the articles were considered with low risk of bias and a low level of certainty. The results demonstrated a positive association between both disorders and increased risk for stroke among cohort studies (RR 1.88 [1.55, 2.29], p<0.00001, I2=0%) and for ischemic stroke events in case-control studies (RR 2.72 [2.00, 3.71], p<0.00001, I2= 4%). Periodontitis may represent a risk factor for stroke, especially in ischemic events. However, new studies with a robust design are necessary for a reliable conclusion.

Keywords: central nervous system; cerebrovascular disorders; periodontal attachment loss; periodontitis; stroke.

Conflict of interest statement

The authors report no conflicts of interest in this work.

© 2019 Fagundes et al.

Figures

Figure 1
Figure 1
Flow diagram of literature searches and selection, according to the PRISMA statement.
Figure 2
Figure 2
Forest plot to CVA in case–control studies.
Figure 3
Figure 3
Forest plot to Ischemic stroke in case–control studies.
Figure 4
Figure 4
Forest plot to CVA in cohort studies.

References

    1. Lima RR, Santana LN, Fernandes RM, et al. Neurodegeneration and glial response after acute striatal stroke: histological basis for neuroprotective studies. Oxid Med Cell Longev. 2016;2016:3173564. doi:10.1155/2016/3173564
    1. Colaianni V, Mazzei R, Cavallaro S. Copy number variations and stroke. Neurol Sci. 2016;37(12):1895–1904. doi:10.1007/s10072-016-2658-y
    1. Amarenco P, Bogousslavsky J, Caplan LR, Donnan GA, Hennerici MG. Classification of stroke subtypes. Cerebrovasc Dis. 2009;27(5):493–501. doi:10.1159/000210432
    1. Dziedzic T. Systemic inflammation as a therapeutic target in acute ischemic stroke. Expert Rev Neurother. 2015;15(5):523–531. doi:10.1586/14737175.2015.1035712
    1. Dye BA. Global periodontal disease epidemiology. Periodontol 2000. 2012;58(1):10–25. doi:10.1111/j.1600-0757.2011.00413.x
    1. Eke PI, Dye BA, Wei L, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol. 2015;86(5):611–622. doi:10.1902/jop.2015.140520
    1. Oppermann RV, Haas AN, Rosing CK, Susin C. Epidemiology of periodontal diseases in adults from Latin America. Periodontol 2000. 2015;67(1):13–33. doi:10.1111/prd.12061
    1. Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89 Suppl 1:S173–S182. doi:10.1002/JPER.17-0721
    1. Kamer AR, Craig RG, Dasanayake AP, Brys M, Glodzik-Sobanska L, de Leon MJ. Inflammation and Alzheimer’s disease: possible role of periodontal diseases. Alzheimers Dement. 2008;4(4):242–250. doi:10.1016/j.jalz.2007.08.004
    1. Teixeira FB, Saito MT, Matheus FC, et al. Periodontitis and alzheimer’s disease: a possible comorbidity between oral chronic inflammatory condition and neuroinflammation. Front Aging Neurosci. 2017;9(OCT). doi:10.3389/fnagi.2017.00077.
    1. Passoja A, Puijola I, Knuuttila M, et al. Serum levels of interleukin-10 and tumour necrosis factor-alpha in chronic periodontitis. J Clin Periodontol. 2010;37(10):881–887. doi:10.1111/j.1600-051X.2010.01602.x
    1. Gani DK, Mallineni SK, Ambalavanan, Ramakrishnan, Deepalakshmi EP. Estimation of the levels of C-reactive protein, interleukin-6, total leukocyte count, and differential count in peripheral blood smear of patients with chronic periodontitis in a South Indian population. West Indian Med J. 2012;61(8):826–831.
    1. Kaur S, Bright R, Proudman SM, Bartold PM. Does periodontal treatment influence clinical and biochemical measures for rheumatoid arthritis? A systematic review and meta-analysis. Semin Arthritis Rheum. 2014;44(2):113–122. doi:10.1016/j.semarthrit.2014.04.009
    1. Zeng XT, Leng WD, Lam YY, et al. Periodontal disease and carotid atherosclerosis: a meta-analysis of 17,330 participants. Int J Cardiol. 2016;203:1044–1051. doi:10.1016/j.ijcard.2015.11.092
    1. Lee YT, Lee HC, Hu CJ, et al. Periodontitis as a modifiable risk factor for dementia: a nationwide population-based cohort study. J Am Geriatr Soc. 2017;65(2):301–305. doi:10.1111/jgs.14449
    1. Ide M, Harris M, Stevens A, et al. Periodontitis and cognitive decline in Alzheimer’s disease. PLoS One. 2016;11(3):e0151081. doi:10.1371/journal.pone.0151081
    1. Janket SJ, Baird AE, Chuang SK, Jones JA. Meta-analysis of periodontal disease and risk of coronary heart disease and stroke. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003;95(5):559–569. doi:10.1067/moe.2003.107
    1. Lafon A, Tala S, Ahossi V, Perrin D, Giroud M, Béjot Y. Association between periodontal disease and non-fatal ischemic stroke: a case-control study. Acta Odontol Scand. 2014;72(8):687–693. doi:10.3109/00016357.2014.898089
    1. Leira Y, Seoane J, Blanco M, et al. Association between periodontitis and ischemic stroke: a systematic review and meta-analysis. Eur J Epidemiol. 2017;32(1):43–53. doi:10.1007/s10654-016-0170-6
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097
    1. Fowkes FG, Fulton PM. Critical appraisal of published research: introductory guidelines. BMJ. 1991;302(6785):1136–1140. doi:10.1136/bmj.302.6785.1136
    1. Penoni DC, Fidalgo TK, Torres SR, et al. Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res. 2017;96(3):261–269. doi:10.1177/0022034516682017
    1. Borenstein M, Hedges L, Higgins JPT, Rothstein H. An Introduction to Meta-Analysis. Vol. 19; 2009.
    1. Higgins J, Green S. Cochrane handbook for systematic reviews of interventions. Versão 5.1.0. A Colaboração cochrane; 2011. Available from: Accessed October8, 2019.
    1. Balshem H, Helfand M, Schunemann HJ, et al. GRADE guidelines: 3. Rating the quality of evidence. J Clin Epidemiol. 2011;64(4):401–406. doi:10.1016/j.jclinepi.2010.07.015
    1. Elter JR, Offenbacher S, Toole JF, Beck JD. Relationship of periodontal disease and edentulism to stroke/TIA. J Dent Res. 2003;82(12):998–1001. doi:10.1177/154405910308201212
    1. Joshipura KJ, Hung HC, Rimm EB, Willett WC, Ascherio A. Periodontal disease, tooth loss, and incidence of ischemic stroke. Stroke. 2003;34(1):47–52. doi:10.1161/01.str.0000052974.79428.0c
    1. Grau AJ, Becher H, Ziegler CM, et al. Periodontal disease as a risk factor for ischemic stroke. Stroke. 2004;35(2):496–501. doi:10.1161/01.STR.0000110789.20526.9D
    1. Lee HJ, Garcia RI, Janket SJ, et al. The association between cumulative periodontal disease and stroke history in older adults. J Periodontol. 2006;77(10):1744–1754. doi:10.1902/jop.2006.050339
    1. Sim SJ, Kim HD, Moon JY, et al. Periodontitis and the risk for non-fatal stroke in Korean adults. J Periodontol. 2008;79(9):1652–1658. doi:10.1902/jop.2008.080015
    1. Jimenez M, Krall EA, Garcia RI, Vokonas PS, Dietrich T. Periodontitis and incidence of cerebrovascular disease in men. Ann Neurol. 2009;66(4):505–512. doi:10.1002/ana.21742
    1. Kim HD, Sim SJ, Moon JY, Hong YC, Han DH. Association between periodontitis and hemorrhagic stroke among Koreans: a case-control study. J Periodontol. 2010;81(5):658–665. doi:10.1902/jop.2010.090614
    1. Hashemipour MA, Afshar AJ, Borna R, Seddighi B, Motamedi A. Gingivitis and periodontitis as a risk factor for stroke: a case-control study in the Iranian population. Dent Res J (Isfahan). 2013;10(5):613–619.
    1. Holmlund A, Lampa E, Lind L. Oral health and cardiovascular disease risk in a cohort of periodontitis patients. Atherosclerosis. 2017;262:101–106. doi:10.1016/j.atherosclerosis.2017.05.009
    1. Beck JD, Moss KL, Morelli T, Offenbacher S. Periodontal profile class is associated with prevalent diabetes, coronary heart disease, stroke, and systemic markers of C-reactive protein and interleukin-6. J Periodontol. 2018;89(2):157–165. doi:10.1002/JPER.17-0426
    1. Wu TJ, Trevisan M, Genco RJ, Dorn JP, Falkner KL, Sempos CT. Periodontal disease and risk of cerebrovascular disease - The first national health and nutrition examination survey and its follow-up study. Arch Intern Med. 2000;160(18):2749–2755. doi:10.1001/archinte.160.18.2749
    1. Holmlund A, Holm G, Lind L. Number of teeth as a predictor of cardiovascular mortality in a cohort of 7,674 subjects followed for 12 years. J Periodontol. 2010;81(6):870–876. doi:10.1902/jop.2010.090680
    1. Sen S, Giamberardino LD, Moss K, et al. periodontal disease, regular dental care use, and incident ischemic stroke. Stroke. 2018;49(2):355–362. doi:10.1161/STROKEAHA.117.018990
    1. Dörfer CE, Becher H, Ziegler CM, et al. The association of gingivitis and periodontitis with ischemic stroke. J Clin Periodontol. 2004;31(5):396–401. doi:10.1111/j.1600-051x.2004.00579.x
    1. Pradeep AR, Hadge P, Raju PA, Shetty SR, Shareef K, Guruprasad CN. Periodontitis as a risk factor for cerebrovascular accident: a case-control study in the Indian population. J Periodontal Res. 2010;45(2):223–228. doi:10.1111/j.1600-0765.2009.01220.x
    1. Abolfazli N, Ghoreishizadeh A, Ayramlu H, Ghavimi M, Ghoreishizadeh M, Salehsaber F. Periodontal disease and risk of cerebral ischemic stroke. J Neurol Sci. 2011;28(3):307–316.
    1. Ghizoni JS, Taveira L, Garlet GP, et al. Increased levels of Porphyromonas gingivalis are associated with ischemic and hemorrhagic cerebrovascular disease in humans: an in vivo study. J Appl Oral Sci. 2012;20(1):104–112. doi:10.1590/s1678-77572012000100019
    1. Palm F, Lahdentausta L, Sorsa T, et al. Biomarkers of periodontitis and inflammation in ischemic stroke: a case-control study. Innate Immun. 2014;20(5):511–518. doi:10.1177/1753425913501214
    1. Diouf M, Basse A, Ndiaye M, Cisse D, Lo CM, Faye D. Stroke and periodontal disease in Senegal: case-control study. Public Health. 2015;129(12):1669–1673. doi:10.1016/j.puhe.2015.02.033
    1. Leira Y, Lopez-Dequidt I, Arias S, et al. Chronic periodontitis is associated with lacunar infarct: a case-control study. Eur J Neurol. 2016;23(10):1572–1579. doi:10.1111/ene.13080
    1. Abd El-Aleem SA, Morales-Aza BM, Donaldson LF. Sensory neuropeptide mRNa up-regulation is bilateral in periodontitis in the rat: a possible neurogenic component to symmetrical periodontal disease. Eur J Neurosci. 2004;19(3):650–658. doi:10.1111/j.1460-9568.2004.03179.x
    1. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700. doi:10.1136/bmj.b2651
    1. Fleming PS, Lynch CD, Pandis N. Randomized controlled trials in dentistry: common pitfalls and how to avoid them. J Dent. 2014;42(8):908–914. doi:10.1016/j.jdent.2014.06.004
    1. Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol. 2015;15(1):30–44. doi:10.1038/nri3785
    1. Esenwa CC, Elkind MS. Inflammatory risk factors, biomarkers and associated therapy in ischaemic stroke. Nat Rev Neurol. 2016;12(10):594–604. doi:10.1038/nrneurol.2016.125
    1. Pejcic A, Kesic LJ, Milasin J. C-reactive protein as a systemic marker of inflammation in periodontitis. Eur J Clin Microbiol Infect Dis. 2011;30(3):407–414. doi:10.1007/s10096-010-1101-1
    1. Vidale S, Consoli A, Arnaboldi M, Consoli D. postischemic inflammation in acute stroke. J Clin Neurol. 2017;13(1):1–9. doi:10.3988/jcn.2017.13.1.1
    1. Hoffmann A, Zhu G, Wintermark M. Advanced neuroimaging in stroke patients: prediction of tissue fate and hemorrhagic transformation. Expert Rev Cardiovasc Ther. 2012;10(4):515–524. doi:10.1586/erc.12.30
    1. Perry VH, Teeling J. Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration. Semin Immunopathol. 2013;35(5):601–612. doi:10.1007/s00281-013-0382-8
    1. Alhadidi Q, Shah ZA. Cofilin mediates LPS-induced microglial cell activation and associated neurotoxicity through activation of NF-kappaB and JAK-STAT pathway. Mol Neurobiol. 2018;55(2):1676–1691. doi:10.1007/s12035-017-0432-7
    1. Winning L, Linden GJ. Periodontitis and systemic disease: association or causality? Current Oral Health Rep. 2017;4(1):1–7. doi:10.1007/s40496-017-0121-7
    1. Li C, Lv Z, Shi Z, et al. Periodontal therapy for the management of cardiovascular disease in patients with chronic periodontitis. Cochrane Database Syst Rev. 2017;2017:11.
    1. Mituuti CT, Bianco VC, Bentim CG, de Andrade EC, Rubo JH, Berretin-Felix G. Influence of oral health condition on swallowing and oral intake level for patients affected by chronic stroke. Clin Interv Aging. 2015;10:29–35. doi:10.2147/CIA.S62314
    1. Darby IB, Mooney J, Kinane DF. Changes in subgingival microflora and humoral immune response following periodontal therapy. J Clin Periodontol. 2001;28(8):796–805. doi:10.1034/j.1600-051x.2001.280812.x
    1. Ajwani S, Jayanti S, Burkolter N, et al. Integrated oral health care for stroke patients - a scoping review. J Clin Nurs. 2017;26(7–8):891–901. doi:10.1111/jocn.13520
    1. Terezakis E, Needleman I, Kumar N, Moles D, Agudo E. The impact of hospitalization on oral health: a systematic review. J Clin Periodontol. 2011;38(7):628–636. doi:10.1111/j.1600-051X.2011.01727.x
    1. Grau AJ, Buggle F, Ziegler C, et al. Association between acute cerebrovascular ischemia and chronic and recurrent infection. Stroke. 1997;28(9):1724–1729. doi:10.1161/01.str.28.9.1724

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