Mechanisms underlying the association between periodontitis and atherosclerotic disease

Schenkein, Harvey A.; Papapanou, Panos N.; Genco, Robert; Sanz, Mariano

doi:10.1111/prd.12304

Cited by 440Oral microbiology and periodontitis researchAtherosclerosis and Cardiovascular DiseasesInfective Endocarditis Diagnosis and Management

Mechanisms underlying the association between periodontitis and atherosclerotic disease

Schenkein, Harvey A., Papapanou, Panos N., Genco, Robert, Sanz, Mariano·2020·Periodontology 2000

DOI 10.1111/prd.12304

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Abstract

Atherosclerosis is central to the pathology of cardiovascular diseases, a group of diseases in which arteries become occluded with atheromas that may rupture, leading to different cardiovascular events, such as myocardial infarction or ischemic stroke. There is a large body of epidemiologic and animal model evidence associating periodontitis with atherosclerotic disease, and many potential mechanisms linking these diseases have been elucidated. This chapter will update knowledge on these mechanisms, which generally fall into 2 categories: microbial invasion and infection of atheromas; and inflammatory and immunologic. With respect to the invasion and infection of atheromas, it is well established that organisms from the subgingival biofilm can enter the circulation and lodge in most distant tissues. Bacteremias resulting from oral interventions, and even oral hygiene activities, are well documented. More recently, indirect routes of entry of oral organisms (via phagocytes or dendritic cells) have been described for many oral organisms, into many tissues. Such organisms include the periodontal pathogens Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans, Prevotella intermedia, Tannerella forsythia , and Fusobacterium nucleatum . Intracellular survival of these organisms with dissemination to distant sites (The Trojan Horse approach) has been described. Their relative contribution to atheroma formation and progression has been studied mainly in experimental research, with results demonstrating that these organisms can invade endothelial cells and phagocytic cells within the atheroma, leading to pathogenic changes and progression of the atheroma lesion. The second category of mechanisms potentially linking periodontitis to atherosclerosis includes the dumping of inflammatory mediators originating from periodontal lesions into the systemic circulation. These inflammatory mediators, such as C‐reactive protein, matrix metalloproteinases, fibrinogen, and other hemostatic factors, would further accelerate atheroma formation and progression, mainly through oxidative stress and inflammatory dysfunction. Moreover, direct effects on lipid oxidation have also been described. In summary, the evidence supports the concept that periodontitis enhances the levels of systemic mediators of inflammation that are risk factors for atherosclerotic diseases.

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Patients with severe periodontitis have higher blood neutrophil counts and pro-inflammatory mediator levels (IL-1, IL-6, CRP, fibrinogen) compared to healthy controls.
“Patients with severe periodontitis had higher blood neutrophil counts and pro-inflammatory mediator levels (such as IL-1, IL-6, CRP, and fibrinogen) compared to healthy controls [14–17]”
From Effect of non-surgical periodontal therapy on risk markers of cardiovascular disease: a systematic review and meta-analysis (2024) · cites this paper as [17]
Dental plaque harbour pathogens and endotoxins, which in presence of reduced permeability at the gingival level, could result in short-term bacteraemia and affect the entire vasculature and existing atherosclerotic plaque deposits.
“Dental plaque harbour pathogens and endotoxins, which in presence of reduced permeability at the gingival level, could result in short‐term bacteraemia and affect the entire vasculature and existing atherosclerotic plaque deposits (Schenkein et al., 2020).”
From Treatment of periodontitis and <scp>C</scp> ‐reactive protein: A systematic review and meta‐analysis of randomized clinical trials (2023) · cites this paper as Schenkein et al., 2020
Periodontitis patients have a more atherogenic lipid profile, with elevated LDL, TG, small dense LDL, and VLDL, and decreased HDL concentration.
“Furthermore, several studies indicate that periodontitis patients have a more atherogenic lipid profile in the form of elevated LDL, TG, small dense LDL, as well as very low-density lipoprotein cholesterol (VLDL), along with decreased levels of HDL concentration [17, 19].”
From Effect of non-surgical periodontal therapy on risk markers of cardiovascular disease: a systematic review and meta-analysis (2024) · cites this paper as [17]
Experimental preclinical studies have shown that periodontal bacteria and their products and virulence factors may influence the pathogenesis of atherosclerosis.
“As proven in experimental pre-clinical studies, these bacteria and their products and virulence factors may influence the pathogenesis of atherosclerosis [17].”
From Effect of non-surgical periodontal therapy on risk markers of cardiovascular disease: a systematic review and meta-analysis (2024) · cites this paper as [17]

Role of C-Reactive Protein at Sites of Inflammation and Infection
Sproston, N. R., & Ashworth, J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00754 · Cited by 3,053 · see citing works
Treatment of periodontitis and endothelial function
Tonetti, M. S., D'Aiuto, F., Nibali, L., Donald, A., Storry, C., Parkar, M., Suvan, J., Hingorani, A. D., Vallance, P., & Deanfield, J. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa063186 · Cited by 1,326 · see citing works
Human oral, gut, and plaque microbiota in patients with atherosclerosis
Koren, O., Spor, A., Felin, J., Fåk, F., Stombaugh, J., Tremaroli, V., Behre, C. J., Knight, R., Fagerberg, B., Ley, R. E., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011383107 · Cited by 1,196 · see citing works
Elevation of Systemic Markers Related to Cardiovascular Diseases in the Peripheral Blood of Periodontitis Patients
Loos, B. G., Craandijk, J., Hoek, F. J., Dillen, P. M. E. W., & van der Velden, U. (2000) · Journal of Periodontology · doi:10.1902/jop.2000.71.10.1528 · Cited by 810 · see citing works
Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAPWorkshop on Periodontitis and Systemic Diseases
Tonetti, M. S., Dyke, T. E. V., & on behalf of working group 1 of the joint EFP/AAP workshop (2013) · Journal of Periodontology · doi:10.1902/jop.2013.1340019 · Cited by 701 · see citing works
Periodontal Infections Contribute to Elevated Systemic C‐Reactive Protein Level
Noack, B., Genco, R. J., Trevisan, M., Grossi, S. M., Zambon, J. J., & Nardin, E. D. (2001) · Journal of Periodontology · doi:10.1902/jop.2000.72.9.1221 · Cited by 680 · see citing works
Self-citation
Endothelial Dysfunction and Hypertension
Konukoğlu, D., & Uzun, H. (2016) · Advances in experimental medicine and biology · doi:10.1007/5584_2016_90 · Cited by 605 · see citing works
Human Atherosclerotic Plaque Contains Viable Invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis
Kozarov, E. V., Dorn, B. R., Shelburne, C. E., Dunn, W. A., & Progulske‐Fox, A. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000155018.67835.1a · Cited by 476 · see citing works
Acute-phase Inflammatory Response to Periodontal Disease in the US Population
Slade, G. D., Offenbacher, S., Beck, J. D., HEISS, G. M., & Pankow, J. S. (2000) · Journal of Dental Research · doi:10.1177/00220345000790010701 · Cited by 458 · see citing works
Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases
Schenkein, H. A., & Loos, B. G. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12060 · Cited by 456 · see citing works
Self-citation
Porphyromonas gingivalis Infection Accelerates the Progression of Atherosclerosis in a Heterozygous Apolipoprotein E–Deficient Murine Model
Li, L., Messas, E., Júnior, E. L. B., Levine, R. A., & Amar, S. (2002) · Circulation · doi:10.1161/hc0702.104178 · Cited by 424 · see citing works
Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis
Ebersole, J. L., Machen, R. L., Steffen, M. J., & Willmann, D. E. (1997) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1997.270-ce1162.x · Cited by 419 · see citing works
Multiple infections in carotid atherosclerotic plaques
Chiu, B. (1999) · American Heart Journal · doi:10.1016/s0002-8703(99)70294-2 · Cited by 410 · see citing works
Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases
Tonetti, M. S., Van Dyke, T. E., & working group 1 of the joint EFP/AAP workshop (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12089 · Cited by 395 · see citing works
Oral Infection With a Periodontal Pathogen Accelerates Early Atherosclerosis in Apolipoprotein E–Null Mice
Lalla, E., Lamster, I. B., Hofmann, M. A., Bucciarelli, L. G., Jerud, A. P., Tucker, S., Lu, Y., Papapanou, P. N., & Schmidt, A. M. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000082462.26258.fe · Cited by 384 · see citing works
Self-citation
Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation
Amar, S., Gokce, N., Morgan, S., Loukideli, M., Van Dyke, T. E., & Vita, J. A. (2003) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000078603.90302.4a · Cited by 361 · see citing works
Treatment of periodontitis improves the atherosclerotic profile: a systematic review and meta‐analysis
Teeuw, W. J., Slot, D. E., Susanto, H., Gerdes, V. E. A., Abbas, F., D’Aiuto, F., Kastelein, J. J. P., & Loos, B. G. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12171 · Cited by 354 · see citing works
Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial
D'Aiuto, F., Parkar, M., Nibali, L., Suvan, J., Lessem, J., & Tonetti, M. S. (2006) · American Heart Journal · doi:10.1016/j.ahj.2005.06.018 · Cited by 332 · see citing works
Innate Immune Recognition of Invasive Bacteria Accelerates Atherosclerosis in Apolipoprotein E-Deficient Mice
Gibson, F. C., Hong, C. C., Chou, H., Yumoto, H., Chen, J., Lien, E., Wong, J., & Genco, C. A. (2004) · Circulation · doi:10.1161/01.cir.0000129769.17895.f0 · Cited by 329 · see citing works
C-Reactive Protein in Atherothrombosis and Angiogenesis
Badimón, L., Peña, E., Arderiu, G., Padró, T., SLEVIN, M. A., Vilahur, G., & Chiva‐Blanch, G. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00430 · Cited by 323 · see citing works
Relationship Between Periodontal Disease and C-Reactive Protein Among Adults in the Atherosclerosis Risk in Communities Study
Slade, G. D., Ghezzi, E. M., HEISS, G. M., Beck, J. D., Riché, E. L., & Offenbacher, S. (2003) · Archives of Internal Medicine · doi:10.1001/archinte.163.10.1172 · Cited by 318 · see citing works
Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: a shared pathology via oxidative stress and mitochondrial dysfunction?
Bullón, P., Newman, H. N., & Battino, M. A. (2013) · Periodontology 2000 · doi:10.1111/j.1600-0757.2012.00455.x · Cited by 304 · see citing works
Plasma lipid and blood glucose levels in patients with destructive periodontal disease
Lösche, W., Karapetow, F., Pohl, A., et al. (2000) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2000.027008537.x · Cited by 298 · see citing works
Periodontal health status and bacteraemia from daily oral activities: systematic review/meta‐analysis
Tomás, I., Diz, P., Tobías, A., Scully, C., & Donos, N. (2012) · Journal of Clinical Periodontology · doi:10.1111/j.1600-051x.2011.01784.x · Cited by 291 · see citing works
Risk factors for cardiovascular disease in patients with periodontitis
Buhlin, K. (2003) · European Heart Journal · doi:10.1016/j.ehj.2003.09.016 · Cited by 287 · see citing works
Severe periodontitis is associated with systemic inflammation and a dysmetabolic status: a case–control study
Nibali, L., D’Aiuto, F., Griffiths, G. S., Patel, K., Suvan, J. E., & Tonetti, M. S. (2007) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2007.01133.x · Cited by 279 · see citing works
Periodontal treatment improves endothelial dysfunction in patients with severe periodontitis
Seinost, G., Wimmer, G., Skerget, M., Thaller, E., Brodmann, M., Gasser, R. N. A., Bratschko, R. O., & Pilger, E. (2005) · American Heart Journal · doi:10.1016/j.ahj.2004.09.059 · Cited by 253 · see citing works
Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients
Higashi, Y., Goto, C., Jitsuiki, D., Umemura, T., Nishioka, K., Hidaka, T., Takemoto, H., Nakamura, S., Soga, J., Chayama, K., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.101535 · Cited by 250 · see citing works
Dental Disease, Fibrinogen and White Cell Count; Links with Myocardial Infarction?
Kweider, M., Lowe, G. D. O., Murray, G. D., Kinane, D. F., & McGowan, D. (1993) · Scottish Medical Journal · doi:10.1177/003693309303800304 · Cited by 246 · see citing works
Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology
Reyes, L., Herrera, D., Kozarov, E., Roldán, S., & Progulske‐Fox, A. (2013) · Journal of Clinical Periodontology · doi:10.1111/jcpe.12079 · Cited by 237 · see citing works
Effect of treatment of chronic periodontitis on levels of serum markers of acute‐phase inflammatory and vascular responses
Ide, M., McPartlin, D., Coward, P. Y., Crook, M. A., Lumb, P. J., & Wilson, R. F. (2003) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2003.00282.x · Cited by 231 · see citing works
Evidence that periodontal treatment improves biomarkers and CVD outcomes
D’Aiuto, F., Orlandi, M., & Gunsolley, J. C. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12061 · Cited by 225 · see citing works
Oral infections and cardiovascular disease
Kholy, K. E., Genco, R. J., & Dyke, T. E. V. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.03.001 · Cited by 201 · see citing works
Self-citation
Periodontal Therapy Reduces Plasma Levels of Interleukin‐6, C‐Reactive Protein, and Fibrinogen in Patients With Severe Periodontitis and Refractory Arterial Hypertension
Vidal, F., Figueredo, C. M., Cordovil, I., & Fischer, R. G. (2009) · Journal of Periodontology · doi:10.1902/jop.2009.080471 · Cited by 200 · see citing works
Resolvin E1 (RvE1) Attenuates Atherosclerotic Plaque Formation in Diet and Inflammation-Induced Atherogenesis
Hasturk, H., Abdallah, R., Kantarci, A., Nguyen, D., Giordano, N., Hamilton, J., & Van Dyke, T. E. (2015) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.115.305324 · Cited by 199 · see citing works
Active Invasion of Oral and Aortic Tissues by Porphyromonas gingivalis in Mice Causally Links Periodontitis and Atherosclerosis
Velsko, I. M., Chukkapalli, S. S., Rivera, M. F., Lee, J. Y., Chen, H., Zheng, D., Bhattacharyya, I., Gangula, P. R., Lucas, A., & Kesavalu, L. N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097811 · Cited by 192 · see citing works
Effect of periodontal treatment on the C‐reactive protein and proinflammatory cytokine levels in Japanese periodontitis patients
Yamazaki, K., Honda, T., Oda, T., Ueki‐Maruyama, K., Nakajima, T. E., Yoshie, H., & Seymour, G. J. (2004) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2004.00772.x · Cited by 188 · see citing works
Serum C-reactive protein in the prediction of cardiovascular diseases: overview of the latest clinical studies and public health practice
Avan, A., Tavakoly Sany, S. B., Ghayour‐Mobarhan, M., Rahimi, H. R., Tajfard, M., & Ferns, G. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26791 · Cited by 182 · see citing works
Systemic Inflammatory Markers, Periodontal Diseases, and Periodontal Infections in an Elderly Population
Bretz, W. A., Weyant, R. J., Corby, P. M. A., Ren, D., Weissfeld, L. A., Kritchevsky, S. B., Harris, T. B., Tamura, M. K., Satterfield, S., Visser, M., et al. (2005) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2005.53468.x · Cited by 181 · see citing works
Porphyromonas gingivalis Bacteremia Induces Coronary and Aortic Atherosclerosis in Normocholesterolemic and Hypercholesterolemic Pigs
Brodala, N., Merricks, E. P., Bellinger, D. A., Damrongsri, D., Offenbacher, S., Beck, J. D., Madianos, P., Sotres, D., Chang, Y., Koch, G. G., et al. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000167525.69400.9c · Cited by 181 · see citing works
Role for Periodontitis in the Progression of Lipid Deposition in an Animal Model
Jain, A. R., Júnior, E. L. B., Serhan, C. N., Stahl, G. L., & Dyke, T. E. V. (2003) · Infection and Immunity · doi:10.1128/iai.71.10.6012-6018.2003 · Cited by 180 · see citing works
Linkages between oral commensal bacteria and atherosclerotic plaques in coronary artery disease patients
Chhibber‐Goel, J., Singhal, V., Bhowmik, D., Vivek, R., Parakh, N., Bhargava, B., & Sharma, A. (2016) · npj Biofilms and Microbiomes · doi:10.1038/s41522-016-0009-7 · Cited by 179 · see citing works
Periodontitis decreases the antiatherogenic potency of high density lipoprotein
Pussinen, P. J., Jauhiainen, M., Vilkuna-Rautiainen, T., Sundvall, J., Vesanen, M., Mattila, K. J., Palosuo, T., Alfthan, G., & Asikainen, S. E. (2004) · Journal of Lipid Research · doi:10.1194/jlr.m300250-jlr200 · Cited by 173 · see citing works
Systemic Inflammation in Cardiovascular and Periodontal Disease: Comparative Study
Glurich, I., Grossi, S. M., Albini, B., Ho, A. W., Shah, R., Zeid, M., Baumann, H., Genco, R. J., & Nardin, E. D. (2002) · Clinical and Vaccine Immunology · doi:10.1128/cdli.9.2.425-432.2002 · Cited by 172 · see citing works
Self-citation
Antimicrobial Periodontal Treatment Decreases Serum C‐Reactive Protein, Tumor Necrosis Factor‐Alpha, But Not Adiponectin Levels in Patients with Chronic Periodontitis
Iwamoto, Y., Nishimura, F., Soga, Y., Takeuchi, K., Kurihara, M., Takashiba, S., & Murayama, Y. (2003) · Journal of Periodontology · doi:10.1902/jop.2003.74.8.1231 · Cited by 171 · see citing works
Microbial Carriage State of Peripheral Blood Dendritic Cells (DCs) in Chronic Periodontitis Influences DC Differentiation, Atherogenic Potential
Carrion, J. A., Scisci, E., Miles, B., Sabino, G. J., Zeituni, A. E., Gu, Y., Bear, A., Genco, C. A., Brown, D. L., & Cutler, C. W. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201053 · Cited by 170 · see citing works
Evidence that periodontal treatment improves biomarkers and CVD outcomes.
D'Aiuto, F., Orlandi, M., & Gunsolley, J. (2013) · The Journal of Periodontology · doi:10.1902/jop.2013.134007 · Cited by 165 · see citing works
Controversies in hypertension
Kaplan, N. M., & Opie, L. H. (2006) · The Lancet · doi:10.1016/s0140-6736(06)67965-8 · Cited by 164 · see citing works
On the association between hypercholesterolemia, cardiovascular disease and severe periodontal disease
Katz, J., Chaushu, G., & Sharabi, Y. (2001) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2001.028009865.x · Cited by 163 · see citing works
Specialized proresolving mediator targets for RvE1 and RvD1 in peripheral blood and mechanisms of resolution
Fredman, G., & Serhan, C. N. (2011) · Biochemical Journal · doi:10.1042/bj20110327 · Cited by 159 · see citing works
Oral infection-inflammatory pathway, periodontitis, is a risk factor for endothelial dysfunction in patients with coronary artery disease
Higashi, Y., Goto, C., Hidaka, T., Soga, J., Nakamura, S., Fujii, Y., Hata, T., Idei, N., Fujimura, N., Chayama, K., et al. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.03.037 · Cited by 157 · see citing works
Periodontitis-associated up-regulation of systemic inflammatory mediator level may increase the risk of coronary heart disease
Nakajima, T. E., Honda, T., Domon, H., et al. (2009) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2009.01209.x · Cited by 155 · see citing works
Impaired Phagocytosis in Localized Aggressive Periodontitis: Rescue by Resolvin E1
Fredman, G., Oh, S. F., Ayilavarapu, S., Hastürk, H., Serhan, C. N., & Dyke, T. E. V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024422 · Cited by 154 · see citing works
Periodontitis and atherogenesis: causal association or simple coincidence?
D’Aiuto, F., Parkar, M., Andreou, G., Brett, P., Ready, D. R., & Tonetti, M. S. (2004) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2004.00580.x · Cited by 152 · see citing works
Relationships Among Clinical Measures of Periodontal Disease and Their Associations With Systemic Markers
Beck, J. D., & Offenbacher, S. (2002) · Annals of Periodontology · doi:10.1902/annals.2002.7.1.79 · Cited by 139 · see citing works
Cardiovascular Disease Parameters in Periodontitis
Monteiro, A. M., Jardini, M. A. N., Alves, S. I. P. M. D. N., Giampaoli, V., Aubin, E. D. C. Q., Neto, A. M. F., & Gidlund, M. (2009) · Journal of Periodontology · doi:10.1902/jop.2009.080431 · Cited by 137 · see citing works
Bacteria and bacterial DNA in atherosclerotic plaque and aneurysmal wall biopsies from patients with and without periodontitis
Armingohar, Z., Jorgensen, J. J., Kristoffersen, A. K., Abesha-Belay, E., & Olsen, I. (2014) · Journal of Oral Microbiology · doi:10.3402/jom.v6.23408 · Cited by 135 · see citing works
Chronic Periodontitis and C‐Reactive Protein Levels
Gomes‐Filho, I. S., Coelho, J. M. F., da Cruz, S. S., Passos‐Soares, J. D. S., de Freitas, C. O. T., Farias, N. S. A., da Silva, R. A., Pereira, M. V. S., Lima, T. L., & Barreto, M. L. (2010) · Journal of Periodontology · doi:10.1902/jop.2010.100511 · Cited by 135 · see citing works
Full-mouth Tooth Extraction Lowers Systemic Inflammatory and Thrombotic Markers of Cardiovascular Risk
Taylor, B. A., Tofler, G. H., Carey, H. M. R., Morel‐Kopp, M., Philcox, S., Carter, T. R., Elliott, M., Kull, A., Wård, C., & Schenck, K. (2006) · Journal of Dental Research · doi:10.1177/154405910608500113 · Cited by 132 · see citing works
Dissemination of Periodontal Pathogens in the Bloodstream after Periodontal Procedures: A Systematic Review
Horliana, A. C. R. T., Chambrone, L., Foz, A. M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098271 · Cited by 131 · see citing works
Periodontal health improves systemic inflammatory and haemostatic status in subjects with coronary heart disease
Montebugnoli, L., Servidio, D., MIATON, R. A., Prati, C., Tricoci, P., Melloni, C., & Melandri, G. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00641.x · Cited by 129 · see citing works
Bacteria Present in Carotid Arterial Plaques Are Found as Biofilm Deposits Which May Contribute to Enhanced Risk of Plaque Rupture
Lanter, B. B., Sauer, K., & Davies, D. G. (2014) · mBio · doi:10.1128/mbio.01206-14 · Cited by 129 · see citing works
Risk factors for atherosclerosis in cases with severe periodontitis
Buhlin, K., Hultin, M., Norderyd, O. M., Persson, L., Pockley, A. G., Rabe, P., Klinge, B., & Gustafsson, A. K. (2009) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2009.01430.x · Cited by 124 · see citing works
Periodontal bacterial invasion and infection: contribution to atherosclerotic pathology
Reyes, L., Herrera, D., Kozarov, E. V., Roldá, S., & Progulske‐Fox, A. (2013) · Journal of Periodontology · doi:10.1902/jop.2013.1340012 · Cited by 124 · see citing works
Poor oral health is associated with coronary heart disease and elevated systemic inflammatory and haemostatic factors
Montebugnoli, L., Servidio, D., MIATON, R. A., et al. (2003) · Journal Of Clinical Periodontology · doi:10.1111/j.0303-6979.2004.00432.x · Cited by 123 · see citing works
Periodontitis is associated with platelet activation
Papapanagiotou, D., Nicu, E. A., Bizzarro, S., et al. (2008) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2008.05.035 · Cited by 122 · see citing works
Heterogeneity of systemic inflammatory responses to periodontal therapy
Behle, J. H., Sedaghatfar, M. H., Demmer, R. T., et al. (2009) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2009.01382.x · Cited by 122 · see citing works
Is There an Association between Periodontitis and Hypertension?
Paizan, M. L. M., & Vilela-Martin, J. F. (2014) · Current Cardiology Reviews · doi:10.2174/1573403x10666140416094901 · Cited by 120 · see citing works
C‐Reactive Protein Levels in Patients With Aggressive Periodontitis
Salzberg, T. N., Overstreet, B. T., Rogers, J. D., Califano, J. V., Best, A. M., & Schenkein, H. A. (2006) · Journal of Periodontology · doi:10.1902/jop.2006.050165 · Cited by 119 · see citing works
Self-citation
Non‐surgical periodontal treatment reduces cardiovascular risk in refractory hypertensive patients: a pilot study
Vidal, F., Cordovil, I., Figueredo, C. M. S., & Fischer, R. G. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12110 · Cited by 118 · see citing works
Antibodies to apolipoprotein A‐I, high‐density lipoprotein, and C‐reactive protein are associated with disease activity in patients with systemic lupus erythematosus
O'Neill, S. G., Giles, I., Lambrianides, A., Manson, J. J., D’Cruz, D. P., Schrieber, L., MARCH, L. M., Latchman, D. S., Isenberg, D. A., & Rahman, A. (2010) · Arthritis & Rheumatism · doi:10.1002/art.27286 · Cited by 114 · see citing works
Impact of monocytic cells on recovery of uncultivable bacteria from atherosclerotic lesions: Live bacteria in atheromas
Rafferty, B., Jönsson, D., Kalachikov, S., Demmer, R. T., Nowygrod, R., Elkind, M. S. V., Bush, H., & Kozarov, E. (2011) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2011.02373.x · Cited by 106 · see citing works
Severity of periodontal disease correlates to inflammatory systemic status and independently predicts the presence and angiographic extent of stable coronary artery disease
Amabile, N., Susini, G., Pettenati-Soubayroux, I., Bonello, L., Gil, J. ‐., Arquès, S., Bonfil, J. J., & Paganelli, F. F. (2008) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2007.01916.x · Cited by 106 · see citing works
Systemic effects of periodontitis: lessons learned from research on atherosclerotic vascular disease and adverse pregnancy outcomes
Papapanou, P. N. (2015) · International Dental Journal · doi:10.1111/idj.12185 · Cited by 105 · see citing works
Self-citation
Self-heat shock protein 60 induces tumour necrosis factor-αin monocyte-derived macrophage: possible role in chronic inflammatory periodontal disease
Ueki, K., Tabeta, K., Yoshie, H., & Yamazaki, K. (2002) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2002.01723.x · Cited by 94 · see citing works
Polymicrobial Oral Infection with Four Periodontal Bacteria Orchestrates a Distinct Inflammatory Response and Atherosclerosis in ApoEnull Mice
Chukkapalli, S. S., Velsko, I. M., Rivera‐Kweh, M. F., Zheng, D., Lucas, A., & Kesavalu, L. N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143291 · Cited by 93 · see citing works
Detection of specific periodontal microorganisms from bacteraemia samples after periodontal therapy using molecular-based diagnostics
Castillo, D. M., Sánchez, M. C., Castellanos, J. E., Sanz‐Sánchez, I., Mayorga‐Fayad, I., Sanz, M., & Lafaurie, G. I. (2011) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2011.01717.x · Cited by 92 · see citing works
Self-citation
The association between periodontitis and dyslipidemia based on the fourth Korea National Health and Nutrition Examination Survey
Lee, J., Yi, H., & Bae, K. (2013) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12095 · Cited by 91 · see citing works
Periodontitis in Humans and Non‐Human Primates: Oral‐Systemic Linkage Inducing Acute Phase Proteins
Ebersole, J. L., Cappelli, D. P., Mathys, E. C., Steffen, M. J., Singer, R. E., Montgomery, M., Mott, G. E., & Novak, M. J. (2002) · Annals of Periodontology · doi:10.1902/annals.2002.7.1.102 · Cited by 86 · see citing works
Lipoprotein‐associated phospholipase A2 and plasma lipids in patients with destructive periodontal disease
Lösche, W., Marshal, G. J., Krause, S., Kocher, T., & Kinane, D. F. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00725.x · Cited by 84 · see citing works
Porphyromonas gingivalisinduces its uptake by human macrophages and promotes foam cell formation in vitro
Giacona, M. B., Papapanou, P. N., Lamster, I. B., Rong, L., D’Agati, V. D., Schmidt, A., & Lalla, E. (2004) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2004.10.009 · Cited by 84 · see citing works
Self-citation
Elevated platelet and leukocyte response to oral bacteria in periodontitis
Nicu, E. A., van der Velden, U., Nieuwland, R., Everts, V. E., & Loos, B. G. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.03219.x · Cited by 83 · see citing works
The effect of periodontal therapy on cardiovascular risk markers: a 6‐month randomized clinical trial
Caúla, A. L., Lira‐Junior, R., Tinoco, E. M. B., & Fischer, R. G. (2014) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12290 · Cited by 81 · see citing works
Microbial Diversity Similarities in Periodontal Pockets and Atheromatous Plaques of Cardiovascular Disease Patients
Filho, W. L. S. E. S., Casarin, R. C. V., Nicolela, E., Passos, H. M., Sallum, A. W., & Gonçalves, R. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109761 · Cited by 80 · see citing works
C-reactive protein as a systemic marker of inflammation in periodontitis
Pejčić, A., Kesić, L. G., & Milašin, J. (2010) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-010-1101-1 · Cited by 80 · see citing works
Invasion of Oral and Aortic Tissues by Oral Spirochete Treponema denticola in ApoE −/− Mice Causally Links Periodontal Disease and Atherosclerosis
Chukkapalli, S. S., Rivera, M. F., Velsko, I. M., Lee, J. Y., Chen, H., Zheng, D., Bhattacharyya, I., Gangula, P. R., Lucas, A., & Kesavalu, L. N. (2014) · Infection and Immunity · doi:10.1128/iai.01511-14 · Cited by 79 · see citing works
Beneficial Effects of Periodontal Treatment on Metabolic Control of Hypercholesterolemia
Oz, S. G., Fentoğlu, Ö., Kılıçarslan, A., Guven, G. S., Tanrtover, M. D., Aykaç, Y., & Sözen, T. (2007) · Southern Medical Journal · doi:10.1097/smj.0b013e31802fa327 · Cited by 79 · see citing works
Periodontal bacteria in human carotid atherothrombosis as a potential trigger for neutrophil activation
Rangé, H., Labreuche, J., Louedec, L., Rondeau, P., Planesse, C., Sebbag, U., Bourdon, E., Michel, J., Bouchard, P., & Meilhac, O. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.07.034 · Cited by 78 · see citing works
Heat shock protein 60 (GroEL) fromPorphyromonas gingivalis: Molecular cloning and sequence analysis of its gene and purification of the recombinant protein
Maeda, H. A., Miyamoto, M., Hongyo, H., et al. (1994) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1994.tb06879.x · Cited by 76 · see citing works
Periodontitis is characterized by elevated PAI‐1 activity
Bizzarro, S., van der Velden, U., ten Heggeler, J. M., Leivadaros, E., Hoek, F. J., Gerdes, V. E. A., Bakker, S. J. L., Gans, R. O. B., Cate, H. T., & Loos, B. G. (2007) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2007.01095.x · Cited by 75 · see citing works
Quantification of Periodontal Pathogens in Vascular, Blood, and Subgingival Samples From Patients With Peripheral Arterial Disease or Abdominal Aortic Aneurysms
Figuero, E., Lindahl, C., Marín, M. J., Renvert, S., Herrera, D., Ohlsson, O., Wetterling, T., & Sanz, M. (2014) · Journal of Periodontology · doi:10.1902/jop.2014.130604 · Cited by 74 · see citing works
Self-citation
Lipopolysaccharide associates with pro-atherogenic lipoproteins in periodontitis patients
Kallio, K., Buhlin, K., Jauhiainen, M., Keva, R., Tuomainen, A. M., Klinge, B., Gustafsson, A. K., & Pussinen, P. J. (2008) · Innate Immunity · doi:10.1177/1753425908095130 · Cited by 72 · see citing works
Nasal Immunization with Porphyromonas gingivalis Outer Membrane Protein Decreases P. gingivalis -Induced Atherosclerosis and Inflammation in Spontaneously Hyperlipidemic Mice
Koizumi, Y., Kurita‐Ochiai, T., Oguchi, S., & Yamamoto, M. (2008) · Infection and Immunity · doi:10.1128/iai.01572-07 · Cited by 70 · see citing works
Evidence for the Involvement of Matrix-Degrading Metalloproteinases (MMPs) in Atherosclerosis
Brown, B. A., Williams, H. J., & George, S. J. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.01.004 · Cited by 70 · see citing works
Fusobacterium nucleatum GroEL induces risk factors of atherosclerosis in human microvascular endothelial cells and ApoE−/− mice
Lee, H., Jun, H., Kim, H., Lee, S. H., & Choi, B. (2011) · Molecular Oral Microbiology · doi:10.1111/j.2041-1014.2011.00636.x · Cited by 69 · see citing works
Evaluation of C-Reactive Protein and Fibrinogen in Patients with Chronic and Aggressive Periodontitis: A Clinico-Biochemical Study
Chandy, S. (2017) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2017/23100.9552 · Cited by 69 · see citing works
Anti-cardiolipin Antibodies in Sera from Patients with Periodontitis
Schenkein, H. A., Berry, C. R., Burmeister, J. A., Brooks, C. N., Barbour, S. E., Best, A. M., & Tew, J. G. (2003) · Journal of Dental Research · doi:10.1177/154405910308201114 · Cited by 67 · see citing works
Self-citation
Non‐Surgical Periodontal Therapy Lowers Serum Inflammatory Markers: A Pilot Study
Bokhari, S. A. H., Khan, A. A., Tatakis, D. N., Azhar, M., Hanif, M., & Izhar, M. (2009) · Journal of Periodontology · doi:10.1902/jop.2009.090001 · Cited by 67 · see citing works
Periodontal Pathogens Invade Gingiva and Aortic Adventitia and Elicit Inflammasome Activation in αvβ6 Integrin-Deficient Mice
Velsko, I. M., Chukkapalli, S. S., Rivera‐Kweh, M. F., Zheng, D., Aukhil, I., Lucas, A., Larjava, H., & Kesavalu, L. N. (2015) · Infection and Immunity · doi:10.1128/iai.01077-15 · Cited by 66 · see citing works
Periodontal infections and atherosclerosis: mere associations?
Pussinen, P. J., & Mattila, K. J. (2004) · Current Opinion in Lipidology · doi:10.1097/00041433-200410000-00013 · Cited by 64 · see citing works
Interaction of Porphyromonas gingivalis with low‐density lipoproteins: implications for a role for periodontitis in atherosclerosis
Miyakawa, H., Honma, K., Qi, M., & Kuramitsu, H. K. (2003) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2004.00697.x · Cited by 64 · see citing works
Heat-shock protein 60 kDa and atherogenic dyslipidemia in patients with untreated mild periodontitis: a pilot study
Rizzo, M., Cappello, F., Marfil‐Álvarez, R., Nibali, L., Marino, A., Rappa, F., Bonaventura, G., Galindo‐Moreno, P., O’Valle, F., Zummo, G., et al. (2012) · Cell Stress and Chaperones · doi:10.1007/s12192-011-0315-1 · Cited by 63 · see citing works
Lipoprotein modifications by gingipains of Porphyromonas gingivalis
Lönn, J., Ljunggren, S., Klarström-Engström, K., Demirel, I., Bengtsson, T., & Karlsson, H. (2018) · Journal of Periodontal Research · doi:10.1111/jre.12527 · Cited by 63 · see citing works
Periodontitis‐induced lipid peroxidation in rat descending aorta is involved in the initiation of atherosclerosis
Ekuni, D., Tomofuji, T., Sanbe, T., Irie, K., AZUMA, T., Maruyama, T., Tamaki, N., Murakami, J., Kokeguchi, S., & Yamamoto, T. (2009) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2008.01122.x · Cited by 62 · see citing works
Characterization of Heat Shock Protein-Specific T Cells in Atherosclerosis
Ford, P. J., Gemmell, E., Walker, P., et al. (2005) · Clinical and Vaccine Immunology · doi:10.1128/cdli.12.2.259-267.2005 · Cited by 61 · see citing works
High‐sensitivity serum C‐reactive protein levels in subjects with or without myocardial infarction or periodontitis
Persson, G. R., Pettersson, T., Ohlsson, O., & Renvert, S. (2005) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2005.00648.x · Cited by 60 · see citing works
Recognition of Porphyromonas gingivalis Gingipain Epitopes by Natural IgM Binding to Malondialdehyde Modified Low-Density Lipoprotein
Turunen, S. P., Kummu, O., Harila, K., Veneskoski, M., Soliymani, R., Baumann, M., Pussinen, P. J., & Hörkkö, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034910 · Cited by 59 · see citing works
Elevation of C‐reactive protein and interleukin‐6 in plasma of patients with aggressive periodontitis
Sun, X., Meng, H., Shi, D., Xu, L., Zhang, L., Chen, Z. B., Feng, X., Lu, R., & Ren, X. Y. (2008) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2008.01131.x · Cited by 58 · see citing works
Periodontal disease, but not edentulism, is independently associated with increased plasma fibrinogen levels
Schwahn, C., Völzke, H., Robinson, D., Luedemann, J., Bernhardt, O., Gesch, D., John, U., & Kocher, T. (2004) · Thrombosis and Haemostasis · doi:10.1160/th04-02-0092 · Cited by 58 · see citing works
Interactions of Porphyromonas gingivalis with Host Cells: Implications for Cardiovascular Diseases
Kuramitsu, H. K., Kang, I., & Qi, M. (2003) · Journal of Periodontology · doi:10.1902/jop.2003.74.1.85 · Cited by 58 · see citing works
Cross‐reactivity of specific antibodies directed to heat shock proteins from periodontopathogenic bacteria of human origin
Hinode, D., Nakamura, R., Grenier, D., & Mayrand, D. (1998) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1998.tb00752.x · Cited by 56 · see citing works
Matrix metalloproteinase‐9 and tissue inhibitor of matrix metalloproteinase‐1 in blood as markers for early atherosclerosis in subjects with chronic periodontitis
Söder, P., Meurman, J. H., Jogestrand, T., Nowak, J., & Söder, B. (2009) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2008.01145.x · Cited by 56 · see citing works
Association of Increased Levels of Fibrinogen and the –455G/A Fibrinogen Gene Polymorphism with Chronic Periodontitis
Sahingur, S. E., Sharma, A., Genco, R. J., & Nardin, E. D. (2003) · Journal of Periodontology · doi:10.1902/jop.2003.74.3.329 · Cited by 55 · see citing works
Self-citation
Salivary Matrix Metalloproteinase-8 and -9 and Myeloperoxidase in Relation to Coronary Heart and Periodontal Diseases: A Subgroup Report from the PAROKRANK Study (Periodontitis and Its Relation to Coronary Artery Disease)
Rathnayake, N., Gustafsson, A. K., Norhammar, A., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126370 · Cited by 54 · see citing works
Doxycycline affects diet- and bacteria-associated atherosclerosis in an ApoE heterozygote murine model: Cytokine profiling implications
Madan, M., Bishayi, B., Hoge, M., Messas, E., & Amar, S. (2006) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2006.02.026 · Cited by 54 · see citing works
Periodontitis and Endothelial Dysfunction: Periodontal Clinical Parameters and Levels of Salivary Markers Interleukin‐1β, Tumor Necrosis Factor‐α, Matrix Metalloproteinase‐2, Tissue Inhibitor of Metalloproteinases‐2 Complex, and Nitric Oxide
Moura, M. F., Navarro, T. P., Silva, T. A., Cota, L. O. M., Oliveira, A. M. S. D., & Costa, F. O. (2017) · Journal of Periodontology · doi:10.1902/jop.2017.170023 · Cited by 54 · see citing works
Association between periodontitis and blood lipid levels in a Korean population
Lee, S., Im, A.-J., Burm, E., et al. (2017) · Journal of Periodontology · doi:10.1902/jop.2017.170111 · Cited by 53 · see citing works
Antiphosphorylcholine Antibody Levels Are Elevated in Humans with Periodontal Diseases
Schenkein, H. A., Gunsolley, J. C., Best, A. M., et al. (1999) · Infection and Immunity · doi:10.1128/iai.67.9.4814-4818.1999 · Cited by 52 · see citing works
Self-citation
Association between serum and oral matrix metalloproteinase‐8 levels and periodontal health status
Noack, B., Kipping, T., Tervahartiala, T. I., Sorsa, T. A., Hoffmann, T. K., & Lorenz, K. (2017) · Journal of Periodontal Research · doi:10.1111/jre.12450 · Cited by 52 · see citing works
Vitamin C intake attenuates the degree of experimental atherosclerosis induced by periodontitis in the rat by decreasing oxidative stress
Ekuni, D., Tomofuji, T., Sanbe, T., Irie, K., Azuma, T., Maruyama, T., Tamaki, N., Murakami, J., Kokeguchi, S., & Yamamoto, T. (2009) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2009.02.006 · Cited by 51 · see citing works
The Contribution of Autoantibodies to Inflammatory Cardiovascular Pathology
Meier, L. A., & Binstadt, B. A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00911 · Cited by 51 · see citing works
The role of Porphyromonas gingivalis gingipains in platelet activation and innate immune modulation
Engström, K. K., Khalaf, H., Kälvegren, H., et al. (2014) · Molecular Oral Microbiology · doi:10.1111/omi.12067 · Cited by 49 · see citing works
Detection of stress proteins inPorphyromonas gingivalisand other oral bacteria by Western immunoblotting analysis
Vayssier, C., Mayrand, D., & Grenier, D. (1994) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1994.tb07117.x · Cited by 49 · see citing works
Pathogen-Accelerated Atherosclerosis Occurs Early after Exposure and Can Be Prevented via Immunization
Miyamoto, T., Yumoto, H., Takahashi, Y., Davey, M., Gibson, F. C., & Genco, C. A. (2006) · Infection and Immunity · doi:10.1128/iai.74.2.1376-1380.2006 · Cited by 49 · see citing works
Aggregatibacter actinomycetemcomitans induces MMP-9 expression and proatherogenic lipoprotein profile in apoE-deficient mice
Tuomainen, A. M., Jauhiainen, M., Kovanen, P. T., Metso, J., Paju, S., & Pussinen, P. J. (2007) · Microbial Pathogenesis · doi:10.1016/j.micpath.2007.08.011 · Cited by 48 · see citing works
Estimate of CRP and TNF-alpha level before and after periodontal therapy in cardiovascular disease patients
Koppolu, P., Durvasula, S., Palaparthy, R., Rao, M., Sagar, V., Reddy, S. K., & Swapna, L. A. (2013) · Pan African Medical Journal · doi:10.11604/pamj.2013.15.92.2326 · Cited by 48 · see citing works
Cardiovascular Risk Factors in the Antiphospholipid Syndrome
da Silva, F. F., Levy, R. A., & de Carvalho, J. F. (2014) · Journal of Immunology Research · doi:10.1155/2014/621270 · Cited by 47 · see citing works
Structural and functional changes in HDL with low grade and chronic inflammation
O'Neill, F., Riwanto, M., Charakida, M., Colin, S., Manz, J., McLoughlin, E., Khan, T. A., Klein, N. J., Kay, C. W. M., Patel, K., et al. (2015) · International Journal of Cardiology · doi:10.1016/j.ijcard.2015.03.058 · Cited by 47 · see citing works
Molecular analysis of aortic intimal hyperplasia caused byPorphyromonas gingivalisinfection in mice with endothelial damage
Hokamura, K., Inaba, H., Nakano, K., et al. (2009) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2009.01242.x · Cited by 46 · see citing works
Elevation of white blood cells and platelet counts in patients having chronic periodontitis
Al‐Rasheed, A. (2011) · The Saudi Dental Journal · doi:10.1016/j.sdentj.2011.10.006 · Cited by 46 · see citing works
Assessment of high‐sensitivity C‐reactive protein and lipid levels in healthy adults and patients with coronary artery disease, with and without periodontitis – a cross‐sectional study
Kumar, K. R. V., Ranganath, V., Naik, R., Banu, S., & Nichani, A. (2014) · Journal of Periodontal Research · doi:10.1111/jre.12172 · Cited by 45 · see citing works
Phosphorylcholine-Dependent Cross-Reactivity between Dental Plaque Bacteria and Oxidized Low-Density Lipoproteins
Schenkein, H. A., Berry, C. R., Purkall, D. B., Burmeister, J. A., Brooks, C. N., & Tew, J. G. (2001) · Infection and Immunity · doi:10.1128/iai.69.11.6612-6617.2001 · Cited by 45 · see citing works
Self-citation
Periodontal microbiota and phospholipases: The Oral Infections and Vascular Disease Epidemiology Study (INVEST)
Boillot, A., Demmer, R. T., Mallat, Z., Sacco, R. L., Jacobs, D. R., Bénessiano, J., Tedgui, A., Rundek, T., Papapanou, P. N., & Desvarieux, M. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.07.039 · Cited by 44 · see citing works
Self-citation
The detection of platelet-activating factor in inflamed human gingival tissue
Noguchi, K., Morita, I., & Murota, S. (1989) · Archives of Oral Biology · doi:10.1016/0003-9969(89)90044-7 · Cited by 43 · see citing works
Stress response of Porphyromonas gingivalis
Lu, B., & McBride, B. C. (1994) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.1994.tb00054.x · Cited by 43 · see citing works
Anti‐Cardiolipin and Increased Serum Adhesion Molecule Levels in Patients With Aggressive Periodontitis
Schenkein, H. A., Best, A. M., Brooks, C. N., et al. (2007) · Journal of Periodontology · doi:10.1902/jop.2007.060305 · Cited by 41 · see citing works
Self-citation
Atherogenic lipoprotein parameters in patients with aggressive periodontitis
Rufail, M. L., Schenkein, H. A., Koertge, T. E., Best, A. M., Barbour, S. E., Tew, J. G., & van Antwerpen, R. (2007) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2007.00973.x · Cited by 40 · see citing works
Self-citation
Abdominal obesity modifies long-term associations between periodontitis and markers of systemic inflammation
Gocke, C., Holtfreter, B., Meisel, P., Grotevendt, A., Jablonowski, L., Nauck, M. A., Markus, M. R. P., & Kocher, T. (2014) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2014.05.926 · Cited by 39 · see citing works
C‐Reactive Protein in Peripheral Blood of Patients with Chronic and Aggressive Periodontitis, Gingivitis, and Gingival Recessions
Podzimek, Š., Myšák, J., Janatova, T., & Duskova, J. (2015) · Mediators of Inflammation · doi:10.1155/2015/564858 · Cited by 38 · see citing works
Tannerella forsythia BspA increases the risk factors for atherosclerosis in ApoE −/− mice
Lee, H., Jun, H., & Choi, B. (2013) · Oral Diseases · doi:10.1111/odi.12214 · Cited by 36 · see citing works
Porphyromonas gingivalisaccelerates atherosclerosis through oxidation of high-density lipoprotein
Kim, H., Cha, G. S., Kim, H. J., Kwon, E.-Y., Lee, J. Y., Choi, J., & Joo, J. (2018) · Journal of Periodontal & Implant Science · doi:10.5051/jpis.2018.48.1.60 · Cited by 36 · see citing works
The GroEL protein of Porphyromonas gingivalis regulates atherogenic phenomena in endothelial cells mediated by upregulating toll-like receptor 4 expression.
Huang, C., Shih, C. M., Tsao, N.-W., et al. (2016) · PubMed · Cited by 35 · see citing works
Temporal Association of Elevated C‐Reactive Protein and Periodontal Disease in Men
Yoshii, S., Tsuboi, S., Morita, I., Takami, Y., Adachi, K., Inukai, J., Inagaki, K., Mizuno, K., & Nakagaki, H. (2009) · Journal of Periodontology · doi:10.1902/jop.2009.080537 · Cited by 34 · see citing works
Platelet-activating factor levels of serum and gingival crevicular fluid in nonsmoking patients with periodontitis and/or coronary heart disease
Chen, H., Zheng, P., Zhu, H., et al. (2009) · Clinical Oral Investigations · doi:10.1007/s00784-009-0346-5 · Cited by 34 · see citing works
Comparison of the detection of periodontal pathogens in bacteraemia after tooth brushing by culture and molecular techniques
Marín, M. J., Figuero, E., Gonzalez, I., Connor, A., Dios, P. D., Álvarez-Fernández, M., Herrera, D., & Sanz, M. (2016) · Medicina oral, patología oral y cirugía bucal · doi:10.4317/medoral.20842 · Cited by 33 · see citing works
Self-citation
Oral infection with Porphyromonas gingivalis and systemic cytokine profile in C57BL/6.KOR‐ApoEshl mice
Miyauchi, S., Maekawa, T., Yudai, A. O. K. I., Miyazawa, H., Tabeta, K., Nakajima, T. E., & Yamazaki, K. (2011) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2011.01441.x · Cited by 32 · see citing works
Molecular mimicry of Aggregatibacter actinomycetemcomitans with β2 glycoprotein I
Wang, D., Nagasawa, T., Chen, Y., 牛田, 由., Kobayashi, H., Takeuchi, Y., Umeda, M., & Izumi, Y. (2008) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.2008.00442.x · Cited by 32 · see citing works
Evaluation of Serum Anti‐Cardiolipin and Oxidized Low‐Density Lipoprotein Levels in Chronic Periodontitis Patients With Essential Hypertension
Türkoğlu, O., Barış, N., Kütükçüler, N., Şenarslan, Ö., Güneri, S., & Atilla, G. (2008) · Journal of Periodontology · doi:10.1902/jop.2008.070321 · Cited by 30 · see citing works
Effect of Phase I Periodontal Therapy on Anti‐Cardiolipin Antibodies in Patients With Acute Myocardial Infarction Associated With Chronic Periodontitis
Gunupati, S., Chava, V. K., & Krishna, B. P. (2011) · Journal of Periodontology · doi:10.1902/jop.2011.110002 · Cited by 29 · see citing works
Locally Produced Anti‐Phosphorylcholine and Anti‐Oxidized Low‐Density Lipoprotein Antibodies in Gingival Crevicular Fluid from Aggressive Periodontitis Patients
Schenkein, H. A., Berry, C. R., Burmeister, J. A., et al. (2004) · Journal of Periodontology · doi:10.1902/jop.2004.75.1.146 · Cited by 29 · see citing works
Self-citation
Reduced platelet hyper-reactivity and platelet-leukocyte aggregation after periodontal therapy
Arvanitidis, E., Bizzarro, S., Rodriguez, E. A., Loos, B. G., & Nicu, E. A. (2017) · Thrombosis Journal · doi:10.1186/s12959-016-0125-x · Cited by 29 · see citing works
Oxidative Stress and IgG Antibody Modify Periodontitis-CRP Association
Singer, R. E., MOSS, K. L., Kim, S. J., Beck, J. D., & Offenbacher, S. (2015) · Journal of Dental Research · doi:10.1177/0022034515602693 · Cited by 28 · see citing works
Anti‐apolipoprotein A ‐1 autoantibodies as biomarker for atherosclerosis burden in patients with periodontitis
Wick, P., Mombelli, A., Pagano, S., Moren, X., Giannopoulou, C., Mach, F., Roux-Lombard, P., & Vuilleumier, N. (2012) · Journal of Periodontal Research · doi:10.1111/jre.12014 · Cited by 28 · see citing works
Dendritic Cells, Antibodies Reactive with oxLDL, and Inflammation
Tew, J. G., Shikh, M. E. E., Sayed, R. M. E., et al. (2011) · Journal of Dental Research · doi:10.1177/0022034511407338 · Cited by 28 · see citing works
Evaluation of serum levels of C-reactive protein and lipid profiles in patients with chronic periodontitis and/or coronary heart disease in an ethnic Han population.
Liu, J., Wu, Y., Ding, Y., et al. (2010) · PubMed · Cited by 28 · see citing works
Immunization with malondialdehyde-modified low-density lipoprotein (LDL) reduces atherosclerosis in LDL receptor-deficient mice challenged with Porphyromonas gingivalis
Turunen, S. P., Kummu, O., Wang, C., et al. (2014) · Innate Immunity · doi:10.1177/1753425914542444 · Cited by 27 · see citing works
Heat Shock Proteins: Mediators of Atherosclerotic Development
Deniset, J., & Pierce, G. N. (2015) · Current Drug Targets · doi:10.2174/1389450116666150416115423 · Cited by 26 · see citing works
Oral P. gingivalis infection alters the vascular reactivity in healthy and spontaneously atherosclerotic mice
Pereira, R. B., Vasquez, E. C., Stefanon, I., & Meyrelles, S. S. (2011) · Lipids in Health and Disease · doi:10.1186/1476-511x-10-80 · Cited by 26 · see citing works
Prevelance of periodontopathogenic bacteria in subgingival biofilm and atherosclerotic plaques of patients undergoing coronary revascularization surgery
Mahendra, J., Mahendra, L., Felix, J., & Romanos, G. E. (2013) · Journal of Indian Society of Periodontology · doi:10.4103/0972-124x.124476 · Cited by 24 · see citing works
Lp-PLA2 Inhibitors for the Reduction of Cardiovascular Events
Steen, D. L., & O’Donoghue, M. L. (2013) · Cardiology and Therapy · doi:10.1007/s40119-013-0022-3 · Cited by 22 · see citing works
Very low density lipoproteins derived from periodontitis patients facilitate macrophage activation via lipopolysaccharide function
Kallio, K. A. E., Hyvärinen, K., Kovanen, P. T., et al. (2012) · Metabolism · doi:10.1016/j.metabol.2012.09.015 · Cited by 21 · see citing works
The Association Between Dental Status and Systemic Lipid Profile and Inflammatory Mediators in Patients After Myocardial Infarction
Górski, B., Nargiełło, E., Opolski, G., Ganowicz, E., & Górska, R. (2016) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/62937 · Cited by 19 · see citing works
The Association between Periodontal Status, Serum Lipid Levels, Lipoprotein Associated Phosholipase A2 (Lp-PLA2) in Chronic Periodontitis Subjects and Healthy Controls
Koshy, B. S. (2017) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2017/27628.10565 · Cited by 19 · see citing works
Periodontal parameters and platelet‐activating factor levels in serum and gingival crevicular fluid in a Chinese population
Zheng, P., Chen, H., Shi, S., et al. (2006) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2006.00987.x · Cited by 18 · see citing works
Human β-defensin-3 alleviates the progression of atherosclerosis accelerated by Porphyromonas gingivalis lipopolysaccharide
Li, L., Bian, T., Lyu, J., et al. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.06.003 · Cited by 18 · see citing works
Cross‐reactive saliva IgA antibodies to oxidized LDL and periodontal pathogens in humans
Akhi, R., Wang, C., Kyrklund, M., et al. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12748 · Cited by 18 · see citing works
Role of Inflammatory Diseases in Hypertension
Bartoloni, E., Alunno, A., Valentini, V., et al. (2017) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-017-0214-3 · Cited by 18 · see citing works
C-reactive protein in relation to early atherosclerosis and periodontitis
Yakob, M., Meurman, J. H., Jogestrand, T., Nowak, J., Söder, P., & Söder, B. (2010) · Clinical Oral Investigations · doi:10.1007/s00784-010-0487-6 · Cited by 17 · see citing works
Levels of C-Reactive Protein and Protein C in Periodontitis Patients with and without Cardiovascular Disease
Malali, E., Başar, I., Emekli‐Alturfan, E., Elemek, E., Oktay, Ş., Ayan, F., Emekli, N., & Noyan, Ü. (2010) · Pathophysiology of Haemostasis and Thrombosis · doi:10.1159/000318189 · Cited by 16 · see citing works
Evaluation of various hematological parameters in patients with periodontitis after nonsurgical therapy at different intervals
Nagdeve, S., Siddeshappa, S., Yeltiwar, R. K., et al. (2016) · Journal of Indian Society of Periodontology · doi:10.4103/0972-124x.175172 · Cited by 16 · see citing works
[Effect of periodontal initial therapy on the serum level of lipid in the patients with both periodontitis and hyperlipidemia].
Duan, J., Ouyang, X., & Zhou, Y. (2009) · PubMed · Cited by 16 · see citing works
Immunization with gingipain A hemagglutinin domain of Porphyromonas gingivalis induces IgM antibodies binding to malondialdehyde-acetaldehyde modified low-density lipoprotein
Kyrklund, M., Kummu, O., Kankaanpää, J., Akhi, R., Nissinen, A. E. T., Turunen, S. P., Pussinen, P. J., Wang, C., & Hörkkö, S. (2018) · PLoS ONE · doi:10.1371/journal.pone.0191216 · Cited by 15 · see citing works
Detection and quantification of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis and Streptococcus oralis in blood samples with different microbiological identification methods: An in vitro study
Marín, M. J., Ambrosio, N., Virto, L., Dios, P. D., Álvarez-Fernández, M., Herrera, D., Sanz, M., & Figuero, E. (2016) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2016.11.007 · Cited by 12 · see citing works
Self-citation
Are lipid profiles true surrogate biomarkers of coronary heart disease in periodontitis patients? A case-control study in a south Indian population
Gita, B., Sajja, C., & Padmanabhan, P. (2012) · Journal of Indian Society of Periodontology · doi:10.4103/0972-124x.94601 · Cited by 11 · see citing works
Effect of phase I periodontal therapy on pro-coagulant state in chronic periodontitis patients--a clinical and haematological study.
Banthia, R., Jain, P., Banthia, P., et al. (2013) · PubMed · Cited by 10 · see citing works
Natural Monoclonal Antibody to Oxidized Low-Density Lipoprotein and Aggregatibacter actinomycetemcomitans
Wang, C., & Hörkkö, S. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7180-0_12 · Cited by 10 · see citing works
Comparison of independent and dependent culture methods for the detection of transient bacteremia in diabetic subjects with chronic periodontitis
Ratto-Tespestini, A. C., Pérez‐Chaparro, P. J., Alexandre Romito, G., Figueiredo, L. C., Faveri, M., Carillo, H. P., Larcher, P., & Feres, M. (2016) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 9 · see citing works
Clinical immunology Periodontal disease in relation to selected parameters of the cardiovascular system in a group of patients with stable angina pectoris
Włosowicz, M., Wożakowska−Kapłon, B., & Górska, R. (2014) · Central European Journal of Immunology · doi:10.5114/ceji.2014.43720 · Cited by 7 · see citing works
Anti-apolipoprotein A-1 autoantibodies as biomarker for atherosclerosis burden in patients with periodontitis
Wick, P. A., Mombelli, A., Pagano, S., et al. (2013) · Archive ouverte UNIGE (University of Geneva) · Cited by 4 · see citing works
Stress response of porphyromonas gingivalis
Lu, B. (2008) · cIRcle (University of British Columbia) · doi:10.14288/1.0086128 · Cited by 1 · see citing works

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Periodontitis and cardiovascular diseases: Consensus report
Sanz, M., Marco del Castillo, A., Jepsen, S., Gonzalez‐Juanatey, J. R., D’Aiuto, F., Bouchard, P., Chapple, I., Dietrich, T., Gotsman, I., Graziani, F., et al. (2020) · Journal of Clinical Periodontology · doi:10.1111/jcpe.13189 · Cited by 1,482 · see citing works
Self-citation
Association between periodontitis and severity of COVID‐19 infection: A case–control study
Marouf, N., Cai, W., Said, K. N., Daas, H., Diab, H., Chinta, V. R., Hssain, A. A., Nicolau, B., Sanz, M., & Tamimi, F. (2021) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13435 · Cited by 380 · see citing works
Treatment of periodontitis and <scp>C</scp> ‐reactive protein: A systematic review and meta‐analysis of randomized clinical trials
Luthra, S., Orlandi, M., Hussain, S. B., Leira, Y., Botelho, J., Machado, V., Mendes, J. J., Marletta, D., Harden, S., & D'Aiuto, F. (2023) · Journal of Clinical Periodontology · doi:10.1111/jcpe.13709 · Cited by 74 · see citing works
“Dental plaque harbour pathogens and endotoxins, which in presence of reduced permeability at the gingival level, could result in short-term bacteraemia and affect the entire vasculature and existing atherosclerotic plaque deposits (Schenkein et al., 2020).”
Effect of non-surgical periodontal therapy on risk markers of cardiovascular disease: a systematic review and meta-analysis
Meng, R., Xu, J., Fan, C., Liao, H., Wu, Z., & Zeng, Q. (2024) · BMC Oral Health · doi:10.1186/s12903-024-04433-0 · Cited by 26 · see citing works
“Furthermore, several studies indicate that periodontitis patients have a more atherogenic lipid profile in the form of elevated LDL, TG, small dense LDL, as well as very low-density lipoprotein cholesterol (VLDL), along with decreased levels of HDL concentration [17, 19].”
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RT ‐ PCR quantification of periodontal pathogens in crack users and non‐users
Casarin, M., Antoniazzi, R. P., Vaucher, R. D. A., Feldens, C. A., & Zanatta, F. B. (2016) · Oral Diseases · doi:10.1111/odi.12609 · Cited by 7 · see citing works
Determination of antibacterial activity of green coffee bean extract on periodontogenic bacteria like Porphyromonas gingivalis, Prevotella intermedia, Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans: An in vitrostudy
Bharath, N., Sowmya, N., & Mehta, D. S. (2015) · Contemporary Clinical Dentistry · doi:10.4103/0976-237x.156036 · Cited by 47 · see citing works
Bacterial profile of aggressive periodontitis in Morocco: a cross-sectional study
Chahboun, H., Arnau, M. M., Herrera, D., Sanz, M., & Ennibi, O. K. (2015) · BMC Oral Health · doi:10.1186/s12903-015-0006-x · Cited by 34 · see citing works
Self-citation
Comparative Evaluation of Antimicrobial Efficacy of Coffee Extract and 0.2% Chlorhexidine Mouthwash on the Periodontal Pathogens Porphyromonas Gingivalis, Prevotella Intermedia, Fusobacterium Nucleatum and Aggregatibacter Actinomycetemcomitans: An In Vitro Study
Yi, T., Shah, M. A., Raulji, D., & Dave, D. (2016) · Advances in Human Biology · doi:10.4103/2321-8568.190316 · Cited by 21 · see citing works
Detection of subgingival periodonto-pathogens and inflammaory cytokines in Malaysian adults with chronic periodontitis / Nursolehah Shahruddin
Nursolehah, S. (2019) · University of Malaya Students Repository

Authors: Schenkein, H. A., Papapanou, P. N., Genco, R., & Sanz, M.
Affiliations: Virginia Commonwealth University (US)
Columbia University (US)
University at Buffalo, State University of New York (US)
Universidad Complutense de Madrid (ES)
Corresponding author: Sanz, Mariano
ORCID: Schenkein, Harvey A.
Papapanou, Panos N.
Genco, Robert
Sanz, Mariano
Venue: Periodontology 2000
Publisher: Wiley
Published: 2020-05-08
Volume: 83
Issue: 1
Pages: 90-106
ISSN: 0906-6713 (ISSN-L)
1600-0757
DOI: 10.1111/prd.12304
OpenAlex: W3022540031
Cited by: 440
References: 180
Citations by year: 2026: 69 · 2025: 75 · 2024: 77 · 2023: 88 · 2022: 75 · 2021: 45 · 2020: 11
FWCI: 8.90
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Periodontology 2000 (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Health Sciences › Medicine › Epidemiology › Infective Endocarditis Diagnosis and Management
Keywords: periodontitis, atherosclerosis, cardiovascular disease, subgingival plaque, oral bacteria, bacteremia, Trojan horse mechanism, intracellular survival, Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans, Prevotella intermedia, Tannerella forsythia, Fusobacterium nucleatum, systemic inflammation, C-reactive protein, matrix metalloproteinases, fibrinogen, oxidative stress, lipid oxidation, atheroma progression
MeSH terms: Humans, Periodontitis, Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans, Prevotella intermedia, Endothelial Cells, Atherosclerosis

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Mechanisms underlying the association between periodontitis and atherosclerotic disease

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