Skip to main content
Top
Published in: BMC Cardiovascular Disorders 1/2018

Open Access 01-12-2018 | Research article

Association between periodontitis and peripheral artery disease: a systematic review and meta-analysis

Authors: Shuo Yang, Li Sheng Zhao, Chuan Cai, Quan Shi, Ning Wen, Juan Xu

Published in: BMC Cardiovascular Disorders | Issue 1/2018

Login to get access

Abstract

Background

Inflammation is a common feature of both peripheral arterial disease (PAD) and periodontitis. Some studies have evaluated the association between PAD and periodontitis. However, there is still no specialized meta-analysis that has quantitatively assessed the strength of the association. Thus, we conducted this meta-analysis to critically assess the strength of the association between PAD and periodontitis.

Methods

PubMed, Embase, and the Cochrane Library were searched for observational studies of the association between periodontitis and PAD in February 2018. Risk ratios (RRs) and their 95% confidence intervals (CIs) from included studies were pooled to evaluate the strength of the association between periodontitis and PAD. Weighted mean differences (WMDs) and their 95% CIs were pooled to compare the difference in periodontal-related parameters between PAD and non-PAD patients.

Results

Seven studies including a total of 4307 participants were included in the meta-analysis. The pooled analysis showed that there was a significant difference in the risk of periodontitis between PAD patients and non-PAD participants (RR = 1.70, 95% CI = 1.25–2.29, P = 0.01). There was also a significant difference in number of missing teeth between PAD patients and non-PAD participants (WMD = 3.75, 95% CI = 1.31–6.19, P = 0.003). No significant difference was found in clinical attachment loss between PAD patients and non-PAD participants (WMD = − 0.05, 95% CI = − 0.03–0.19, P = 0.686).

Conclusion

In conclusion, the results of this meta-analysis revealed a significant relationship between periodontitis and PAD. Moreover, our study indicated that PAD patients had more missing teeth than control subjects did. Further high-quality and well-designed studies with specific inclusion and exclusion criteria are required to strengthen the conclusions of this study.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lundmark A, Davanian H, Bage T, Johannsen G, Koro C, Lundeberg J, et al. Transcriptome analysis reveals mucin 4 to be highly associated with periodontitis and identifies pleckstrin as a link to systemic diseases. Sci Rep. 2015;5:18475.CrossRefPubMedPubMedCentral Lundmark A, Davanian H, Bage T, Johannsen G, Koro C, Lundeberg J, et al. Transcriptome analysis reveals mucin 4 to be highly associated with periodontitis and identifies pleckstrin as a link to systemic diseases. Sci Rep. 2015;5:18475.CrossRefPubMedPubMedCentral
3.
go back to reference Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet (London, England). 2005;366(9499):1809–20.CrossRef Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet (London, England). 2005;366(9499):1809–20.CrossRef
4.
go back to reference Eke PI, Zhang X, Lu H, Wei L, Thornton-Evans G, Greenlund KJ, et al. Predicting periodontitis at state and local levels in the United States. J Dent Res. 2016;95(5):515–22.CrossRefPubMedPubMedCentral Eke PI, Zhang X, Lu H, Wei L, Thornton-Evans G, Greenlund KJ, et al. Predicting periodontitis at state and local levels in the United States. J Dent Res. 2016;95(5):515–22.CrossRefPubMedPubMedCentral
5.
go back to reference Rutter-Locher Z, Smith TO, Giles I, Sofat N. Association between systemic lupus erythematosus and periodontitis: a systematic review and meta-analysis. Front Immunol. 2017;8:1295.CrossRefPubMedPubMedCentral Rutter-Locher Z, Smith TO, Giles I, Sofat N. Association between systemic lupus erythematosus and periodontitis: a systematic review and meta-analysis. Front Immunol. 2017;8:1295.CrossRefPubMedPubMedCentral
6.
go back to reference Hobbins S, Chapple IL, Sapey E, Stockley RA. Is periodontitis a comorbidity of COPD or can associations be explained by shared risk factors/behaviors? IntJ Chron Obstruct Pulmon Dis. 2017;12:1339–49.CrossRef Hobbins S, Chapple IL, Sapey E, Stockley RA. Is periodontitis a comorbidity of COPD or can associations be explained by shared risk factors/behaviors? IntJ Chron Obstruct Pulmon Dis. 2017;12:1339–49.CrossRef
7.
go back to reference Shi Q, Zhang B, Huo N, Cai C, Liu H, Xu J. Association between myocardial infarction and periodontitis: a meta-analysis of case-control studies. Front Physiol. 2016;7:519.CrossRefPubMedPubMedCentral Shi Q, Zhang B, Huo N, Cai C, Liu H, Xu J. Association between myocardial infarction and periodontitis: a meta-analysis of case-control studies. Front Physiol. 2016;7:519.CrossRefPubMedPubMedCentral
8.
go back to reference Cardoso EM, Reis C, Manzanares-Cespedes MC. Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases. Postgrad Med. 2018;130(1):98–104.CrossRefPubMed Cardoso EM, Reis C, Manzanares-Cespedes MC. Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases. Postgrad Med. 2018;130(1):98–104.CrossRefPubMed
9.
go back to reference Petersen PE, Kwan S. The 7th WHO global conference on health promotion: towards integration of oral health (Nairobi, Kenya, 2009). Community Dent Health. 2010;27(Suppl 1):1–9. Petersen PE, Kwan S. The 7th WHO global conference on health promotion: towards integration of oral health (Nairobi, Kenya, 2009). Community Dent Health. 2010;27(Suppl 1):1–9.
10.
go back to reference Ebersole JL, Machen RL, Steffen MJ, Willmann DE. Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clin Exp Immunol. 1997;107(2):347–52.CrossRefPubMedPubMedCentral Ebersole JL, Machen RL, Steffen MJ, Willmann DE. Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clin Exp Immunol. 1997;107(2):347–52.CrossRefPubMedPubMedCentral
11.
go back to reference Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol. 2003;30(12):1046–52.CrossRefPubMed Gorska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madalinski K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol. 2003;30(12):1046–52.CrossRefPubMed
12.
go back to reference Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol. 2000;71(10):1528–34.CrossRefPubMed Loos BG, Craandijk J, Hoek FJ, Wertheim-van Dillen PM, van der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol. 2000;71(10):1528–34.CrossRefPubMed
13.
go back to reference Ouma GO, Jonas RA, Usman MH, Mohler ER 3rd. Targets and delivery methods for therapeutic angiogenesis in peripheral artery disease. Vasc Med (London, England). 2012;17(3):174–92.CrossRef Ouma GO, Jonas RA, Usman MH, Mohler ER 3rd. Targets and delivery methods for therapeutic angiogenesis in peripheral artery disease. Vasc Med (London, England). 2012;17(3):174–92.CrossRef
14.
go back to reference Howell MA, Colgan MP, Seeger RW, Ramsey DE, Sumner DS. Relationship of severity of lower limb peripheral vascular disease to mortality and morbidity: a six-year follow-up study. J Vasc Surg. 1989;9(5):691–6. discussion 696-697CrossRefPubMed Howell MA, Colgan MP, Seeger RW, Ramsey DE, Sumner DS. Relationship of severity of lower limb peripheral vascular disease to mortality and morbidity: a six-year follow-up study. J Vasc Surg. 1989;9(5):691–6. discussion 696-697CrossRefPubMed
15.
go back to reference McKenna M, Wolfson S, Kuller L. The ratio of ankle and arm arterial pressure as an independent predictor of mortality. Atherosclerosis. 1991;87(2–3):119–28.CrossRefPubMed McKenna M, Wolfson S, Kuller L. The ratio of ankle and arm arterial pressure as an independent predictor of mortality. Atherosclerosis. 1991;87(2–3):119–28.CrossRefPubMed
16.
go back to reference Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, et al. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA. 2001;286(11):1317–24.CrossRefPubMed Hirsch AT, Criqui MH, Treat-Jacobson D, Regensteiner JG, Creager MA, Olin JW, et al. Peripheral arterial disease detection, awareness, and treatment in primary care. JAMA. 2001;286(11):1317–24.CrossRefPubMed
17.
go back to reference Blaizot A, Vergnes JN, Nuwwareh S, Amar J, Sixou M. Periodontal diseases and cardiovascular events: meta-analysis of observational studies. Int Dent J. 2009;59(4):197–209.PubMed Blaizot A, Vergnes JN, Nuwwareh S, Amar J, Sixou M. Periodontal diseases and cardiovascular events: meta-analysis of observational studies. Int Dent J. 2009;59(4):197–209.PubMed
18.
go back to reference Sfyroeras GS, Roussas N, Saleptsis VG, Argyriou C, Giannoukas AD. Association between periodontal disease and stroke. J Vasc Surg. 2012;55(4):1178–84.CrossRefPubMed Sfyroeras GS, Roussas N, Saleptsis VG, Argyriou C, Giannoukas AD. Association between periodontal disease and stroke. J Vasc Surg. 2012;55(4):1178–84.CrossRefPubMed
19.
go back to reference Botti C, Maione C, Dogliotti G, Russo P, Signoriello G, Molinari AM, et al. Circulating cytokines present in the serum of peripheral arterial disease patients induce endothelial dysfunction. J Biol Regul Homeost Agents. 2012;26(1):67–79.PubMed Botti C, Maione C, Dogliotti G, Russo P, Signoriello G, Molinari AM, et al. Circulating cytokines present in the serum of peripheral arterial disease patients induce endothelial dysfunction. J Biol Regul Homeost Agents. 2012;26(1):67–79.PubMed
20.
go back to reference Moreno VP, Subira D, Meseguer E, Llamas P. IL-6 as a biomarker of ischemic cerebrovascular disease. Biomark Med. 2008;2(2):125–36.CrossRefPubMed Moreno VP, Subira D, Meseguer E, Llamas P. IL-6 as a biomarker of ischemic cerebrovascular disease. Biomark Med. 2008;2(2):125–36.CrossRefPubMed
21.
go back to reference Kofler S, Nickel T, Weis M. Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. Clini Sci (London). 2005;108(3):205–13.CrossRef Kofler S, Nickel T, Weis M. Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. Clini Sci (London). 2005;108(3):205–13.CrossRef
22.
go back to reference Aoyama N, Suzuki JI, Kobayashi N, Hanatani T, Ashigaki N, Yoshida A, et al. Associations among tooth loss, systemic inflammation and antibody titers to periodontal pathogens in Japanese patients with cardiovascular disease. J Periodontal Res. 2018;53(1):117-22. Aoyama N, Suzuki JI, Kobayashi N, Hanatani T, Ashigaki N, Yoshida A, et al. Associations among tooth loss, systemic inflammation and antibody titers to periodontal pathogens in Japanese patients with cardiovascular disease. J Periodontal Res. 2018;53(1):117-22.
23.
go back to reference Li C, Lv Z, Shi Z, Zhu Y, Wu Y, Li L, et al. Periodontal therapy for the management of cardiovascular disease in patients with chronic periodontitis. Cochrane Database Syst Rev. 2017;11:Cd009197.PubMed Li C, Lv Z, Shi Z, Zhu Y, Wu Y, Li L, et al. Periodontal therapy for the management of cardiovascular disease in patients with chronic periodontitis. Cochrane Database Syst Rev. 2017;11:Cd009197.PubMed
25.
go back to reference Mendez MV, Scott T, LaMorte W, Vokonas P, Menzoian JO, Garcia R. An association between periodontal disease and peripheral vascular disease. Am J Surg. 1998;176(2):153–7.CrossRefPubMed Mendez MV, Scott T, LaMorte W, Vokonas P, Menzoian JO, Garcia R. An association between periodontal disease and peripheral vascular disease. Am J Surg. 1998;176(2):153–7.CrossRefPubMed
26.
go back to reference Soto-Barreras U, Olvera-Rubio JO, Loyola-Rodriguez JP, Reyes-Macias JF, Martinez-Martinez RE, Patino-Marin N, et al. Peripheral arterial disease associated with caries and periodontal disease. J Periodontol. 2013;84(4):486–94.CrossRefPubMed Soto-Barreras U, Olvera-Rubio JO, Loyola-Rodriguez JP, Reyes-Macias JF, Martinez-Martinez RE, Patino-Marin N, et al. Peripheral arterial disease associated with caries and periodontal disease. J Periodontol. 2013;84(4):486–94.CrossRefPubMed
27.
go back to reference Ahn YB, Shin MS, Han DH, Sukhbaatar M, Kim MS, Shin HS, et al. Periodontitis is associated with the risk of subclinical atherosclerosis and peripheral arterial disease in Korean adults. Atherosclerosis. 2016;251:311–8.CrossRefPubMed Ahn YB, Shin MS, Han DH, Sukhbaatar M, Kim MS, Shin HS, et al. Periodontitis is associated with the risk of subclinical atherosclerosis and peripheral arterial disease in Korean adults. Atherosclerosis. 2016;251:311–8.CrossRefPubMed
28.
go back to reference Aoyama N, Suzuki JI, Kobayashi N, Hanatani T, Ashigaki N, Yoshida A, et al. Periodontitis deteriorates peripheral arterial disease in Japanese population via enhanced systemic inflammation. Heart Vessel. 2017;32(11):1314–9.CrossRef Aoyama N, Suzuki JI, Kobayashi N, Hanatani T, Ashigaki N, Yoshida A, et al. Periodontitis deteriorates peripheral arterial disease in Japanese population via enhanced systemic inflammation. Heart Vessel. 2017;32(11):1314–9.CrossRef
29.
go back to reference Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ (Clinical research ed). 2009;339:b2700.CrossRef Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ (Clinical research ed). 2009;339:b2700.CrossRef
30.
go back to reference Chen YW, Umeda M, Nagasawa T, Takeuchi Y, Huang Y, Inoue Y, et al. Periodontitis may increase the risk of peripheral arterial disease. Eur J Vasc Endovasc Surg. 2008;35(2):153–8.CrossRefPubMed Chen YW, Umeda M, Nagasawa T, Takeuchi Y, Huang Y, Inoue Y, et al. Periodontitis may increase the risk of peripheral arterial disease. Eur J Vasc Endovasc Surg. 2008;35(2):153–8.CrossRefPubMed
31.
go back to reference Armitage GC. Development of a classification system for periodontal diseases and conditions. Northwest Dent. 2000;79(6):31–5.PubMed Armitage GC. Development of a classification system for periodontal diseases and conditions. Northwest Dent. 2000;79(6):31–5.PubMed
33.
go back to reference Bloemenkamp DG, van den Bosch MA, Mali WP, Tanis BC, Rosendaal FR, Kemmeren JM, et al. Novel risk factors for peripheral arterial disease in young women. Am J Med. 2002;113(6):462–7.CrossRefPubMed Bloemenkamp DG, van den Bosch MA, Mali WP, Tanis BC, Rosendaal FR, Kemmeren JM, et al. Novel risk factors for peripheral arterial disease in young women. Am J Med. 2002;113(6):462–7.CrossRefPubMed
34.
go back to reference Calapkorur MU, Alkan BA, Tasdemir Z, Akcali Y, Saatci E. Association of peripheral arterial disease with periodontal disease: analysis of inflammatory cytokines and an acute phase protein in gingival crevicular fluid and serum. J Periodontal Res. 2017;52(3):532–9.CrossRefPubMed Calapkorur MU, Alkan BA, Tasdemir Z, Akcali Y, Saatci E. Association of peripheral arterial disease with periodontal disease: analysis of inflammatory cytokines and an acute phase protein in gingival crevicular fluid and serum. J Periodontal Res. 2017;52(3):532–9.CrossRefPubMed
35.
go back to reference Savage A, Eaton KA, Moles DR, Needleman I. A systematic review of definitions of periodontitis and methods that have been used to identify this disease. J Clin Periodontol. 2009;36(6):458–67.CrossRefPubMed Savage A, Eaton KA, Moles DR, Needleman I. A systematic review of definitions of periodontitis and methods that have been used to identify this disease. J Clin Periodontol. 2009;36(6):458–67.CrossRefPubMed
36.
go back to reference Hyde S, Dupuis V, Mariri BP, Dartevelle S. Prevention of tooth loss and dental pain for reducing the global burden of oral diseases. Int Dent J. 2017;67(Suppl 2):19–25.CrossRefPubMed Hyde S, Dupuis V, Mariri BP, Dartevelle S. Prevention of tooth loss and dental pain for reducing the global burden of oral diseases. Int Dent J. 2017;67(Suppl 2):19–25.CrossRefPubMed
37.
go back to reference Dye BA, Choudhary K, Shea S, Papapanou PN. Serum antibodies to periodontal pathogens and markers of systemic inflammation. J Clin Periodontol. 2005;32(12):1189–99.CrossRefPubMed Dye BA, Choudhary K, Shea S, Papapanou PN. Serum antibodies to periodontal pathogens and markers of systemic inflammation. J Clin Periodontol. 2005;32(12):1189–99.CrossRefPubMed
38.
go back to reference Jimenez M, Krall EA, Garcia RI, Vokonas PS, Dietrich T. Periodontitis and incidence of cerebrovascular disease in men. Ann Neurol. 2009;66(4):505–12.CrossRefPubMedPubMedCentral Jimenez M, Krall EA, Garcia RI, Vokonas PS, Dietrich T. Periodontitis and incidence of cerebrovascular disease in men. Ann Neurol. 2009;66(4):505–12.CrossRefPubMedPubMedCentral
39.
go back to reference Blum A, Kryuger K, Mashiach Eizenberg M, Tatour S, Vigder F, Laster Z, et al. Periodontal care may improve endothelial function. Eur J Intern Med. 2007;18(4):295–8.CrossRefPubMed Blum A, Kryuger K, Mashiach Eizenberg M, Tatour S, Vigder F, Laster Z, et al. Periodontal care may improve endothelial function. Eur J Intern Med. 2007;18(4):295–8.CrossRefPubMed
Metadata
Title
Association between periodontitis and peripheral artery disease: a systematic review and meta-analysis
Authors
Shuo Yang
Li Sheng Zhao
Chuan Cai
Quan Shi
Ning Wen
Juan Xu
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2018
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-018-0879-0

Other articles of this Issue 1/2018

BMC Cardiovascular Disorders 1/2018 Go to the issue