The Pathobiology of Periodontal Diseases May Affect Systemic Diseases: Inversion of a Paradigm

Page, Roy C.

doi:10.1902/annals.1998.3.1.108

Cited by 420Oral microbiology and periodontitis researchPeriodontal Regeneration and TreatmentsDental Research and COVID-19

The Pathobiology of Periodontal Diseases May Affect Systemic Diseases: Inversion of a Paradigm

Page, Roy C.·1998·Annals of Periodontology

DOI 10.1902/annals.1998.3.1.108

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Abstract

A new paradigm for the pathobiology of periodontitis is presented, and the manner in which periodontitis may relate to susceptibility for certain systemic diseases such as cardiovascular disease and preterm labor is described. Periodontitis is caused by a small group of Gram‐negative bacteria present on the tooth root surfaces as biofilms. Lipopolysaccharide (LPS) and other substances gain access to the gingival tissues, initiate and perpetuate immunoinflammation, resulting in production of high levels of proinflammatory cytokines. These induce production of matrix metalloproteinases which destroy the connective tissues of the gingiva and periodontal ligament, and prostaglandins which mediate alveolar bone destruction. Periodontitis may enhance susceptibility to systemic diseases in several ways. LPS and viable Gram‐negative bacteria from the biofilms and proinflammatory cytokines from the inflamed periodontal tissues may enter the circulation in pathogenic quantities. In addition, periodontitis and certain systemic diseases, such as cardiovascular disease, share risk factors including tobacco smoking, male gender, race/ethnicity, stress, and aging. Ann Periodontol 1998;3:108–120.

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Periodontal disease shares many associative and causative links with systemic disease, and it increases susceptibility to systemic diseases via shared risk factors, such as by harboring pathogenic gram-negative anaerobes in subgingival biofilms, and by fashioning the periodontium as a reservoir for pro-inflammatory mediators.
“Periodontal disease shares many associative and causative links with systemic disease, and it increases susceptibility to systemic diseases via shared risk factors, such as by harboring pathogenic gram‐negative anaerobes in subgingival biofilms, and by fashioning the periodontium as a reservoir for pro‐inflammatory mediators.199”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [199]
Periodontal disease predisposes humans to cardiovascular pathologies, such as atherosclerosis and myocardial infarction, as a result of inducing increased levels of systemic pro-inflammatory cytokines, inflammatory cells and infiltrates, and white blood cell counts.
“Periodontal disease predisposes humans to cardiovascular pathologies, such as atherosclerosis and myocardial infarction, as a result of inducing increased levels of systemic pro‐inflammatory cytokines, inflammatory cells and infiltrates, and white blood cell counts.199”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [199]

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Background
Crystal structure of gingipain R: an Arg‐specific bacterial cysteine proteinase with a caspase‐like fold
Eichinger, A., Beisel, H., Jacob, U., Huber, R., Medrano, F. J., Banbula, A., Potempa, J., Travis, J., & Bode, W. (1999) · The EMBO Journal · doi:10.1093/emboj/18.20.5453 · Cited by 185 · see citing works
“In addition, severe periodontitis may predispose to more serious systemic conditions such as cardiovascular diseases and the delivery of preterm infants (Page, 1998).”
Background
Inflammatory mechanisms linking periodontal diseases to cardiovascular diseases
Schenkein, H. A., & Loos, B. G. (2013) · Journal of Periodontology · doi:10.1902/jop.2013.134006 · Cited by 175 · see citing works
“Page, R. C. (1998) The pathobiology of periodontal diseases may affect systemic diseases: inver-”
Periodontitis and Alzheimer’s Disease: A Possible Comorbidity between Oral Chronic Inflammatory Condition and Neuroinflammation
Teixeira, F. B., Saito, M. T., MATHEUS, F. C., Prediger, R. D., Yamada, E. S., Maia, C. D. S. F., & Lima, R. R. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00327 · Cited by 175 · see citing works
“…(Hanes and Krishna, 2010; Otomo-Corgel et al., 2012; Preshaw et al., 2012), cancer (Martelli et al., 2017), autoimmunity and cardiovascular disease (Page, 1998; Friedewald et al., 2009; Pejcic et al., 2011; Otomo-Corgel et al., 2012; Martelli et al., 2017), dementia (Pazos et al., 2016) and…”
Background
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
Relationship of Serum Advanced Glycation End Products With Deterioration of Periodontitis in Type 2 Diabetes Patients
TAKEDA, M., Ojima, M., Yoshioka, H., Inaba, H., Kogo, M., Shizukuishi, S., Nomura, M., & Amano, A. (2006) · Journal of Periodontology · doi:10.1902/jop.2006.77.1.15 · Cited by 152 · see citing works
Bacterial proteinases as targets for the development of second-generation antibiotics
Travis, J. W., & Potempa, J. (2000) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/s0167-4838(99)00278-2 · Cited by 152 · see citing works
Clinical and biochemical effects of diode laser as an adjunct to nonsurgical treatment of chronic periodontitis: a randomized, controlled clinical trial
Sağlam, M., Kantarcı, A., Dündar, N., & Hakki, S. S. (2012) · Lasers in Medical Science · doi:10.1007/s10103-012-1230-0 · Cited by 140 · see citing works
Periodontal disease–related nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: An emerging concept of oral‐liver axis
Kuraji, R., Sekino, S., Kapila, Y. L., & Numabe, Y. (2021) · Periodontology 2000 · doi:10.1111/prd.12387 · Cited by 137 · see citing works
Relationship between markers of metabolic control and inflammation on severity of periodontal disease in patients with diabetes mellitus
Lim, L. P., Tay, F. B., Sum, C. F., & Thai, A. C. (2006) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2006.01032.x · Cited by 136 · see citing works
“Local and systemic factors have been implicated in the modulation of the host’s inflammatory response (Page 1998).”
Background
The Short‐Term Effects of Treatment of Chronic Periodontitis on Circulating Levels of Endotoxin, C‐Reactive Protein, Tumor Necrosis Factor‐α, and Interleukin‐6
Ide, M., Jagdev, D., Coward, P. Y., Crook, M. A., Barclay, G. R., & Wilson, R. F. (2004) · Journal of Periodontology · doi:10.1902/jop.2004.75.3.420 · Cited by 131 · see citing works
Association of periodontal disease to anxiety and depression symptoms, and psychosocial stress factors
Solis, A. C. D. O., Lotufo, R. F. M., Pannuti, C. M., Brunheiro, E. C., Marques, A. H., & Lotufo‐Neto, F. (2004) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2004.00538.x · Cited by 121 · see citing works
Prevalence of Periodontopathic Bacteria in Aggressive Periodontitis Patients in a Chilean Population
Gajardo, M., Silva, N., Gómez, L., León, R., Parra, B., Contreras, A., & Gamonal, J. A. (2005) · Journal of Periodontology · doi:10.1902/jop.2005.76.2.289 · Cited by 118 · see citing works
Periodontal Disease and Mortality From All Causes in the VA Dental Longitudinal Study
García, R. I., Krall, E. A., & Vokonas, P. (1998) · Annals of Periodontology · doi:10.1902/annals.1998.3.1.339 · Cited by 116 · see citing works
Molecular and Imaging Techniques for Bacterial Biofilms in Joint Arthroplasty Infections
Stoodley, P., Kathju, S., Hu, F. Z., Erdös, G., Levenson, J. E., Mehta, N. S., Dice, B., Johnson, S. A., Hall‐Stoodley, L., Nistico, L., et al. (2005) · Clinical Orthopaedics and Related Research · doi:10.1097/01.blo.0000175129.83084.d5 · Cited by 113 · see citing works
Effect of oral hygiene maintenance on HbA1c levels and peri‐implant parameters around immediately‐loaded dental implants placed in type‐2 diabetic patients: 2 years follow‐up
Amri, M. D. A., Kellesarian, S. V., Kheraif, A. A. A., Malmström, H., Javed, F., & Romanos, G. E. (2016) · Clinical Oral Implants Research · doi:10.1111/clr.12758 · Cited by 110 · see citing works
“Studies (Beck et al. 1996; Page 1998; Grossi 2001; Javed et al. 2014, 2015a,b,c) have reported that bacteria and their products (such as lipopolysaccharides) enter systemic circulation from infected periodontal pockets that may in turn worsen insulin resistance by potentially increasing low-grade…”
Background
An investigation into the association among preterm birth, cytokine gene polymorphisms and periodontal disease
Moore, S., Ide, M., Randhawa, M., Walker, J. J., Reid, J., & Simpson, N. (2004) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.00024.x-i1 · Cited by 108 · see citing works
“The pathogenesis of the disease is thought to be host mediated, with an inflammatory and immune response to the mixed bacterial populations modulated by inflammatory mediators, such as cytokines.(4,5) Risk factors for periodontal disease include smoking, age, Black ethnicity, and low socio-economic status.”
Background
Structure and Mechanism of Cysteine Peptidase Gingipain K (Kgp), a Major Virulence Factor of Porphyromonas gingivalis in Periodontitis
de Diego, I., Veillard, F., Sztukowska, M. N., Guevara, T., Potempa, B. A., Pomowski, A., Huntington, J. A., Potempa, J., & Gomis‐Rüth, F. X. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.602052 · Cited by 107 · see citing works
“In addition, bacteria and their products can enter the circulation, contributing to development and severity of systemic diseases at distal sites, such as cardiovascular diseases (6), rheumatoid arthritis (7), diabetes (8), and preterm delivery (9).”
Background
Relationship between periodontitis and rheumatoid arthritis and the effect of non-surgical periodontal treatment
Pinho, M. D. N., Oliveira, R. D. R., Novaes, A. B., & Voltarelli, J. C. (2009) · Brazilian Dental Journal · doi:10.1590/s0103-64402009000500001 · Cited by 104 · see citing works
Periodontal disease and preterm delivery of low-birth-weight infants.
McGaw, T. (2002) · PubMed · Cited by 101 · see citing works
Effect of Vitamin D and Calcium on Periodontitis
Hildebolt, C. F. (2005) · Journal of Periodontology · doi:10.1902/jop.2005.76.9.1576 · Cited by 99 · see citing works
Tetracyclines in Biology, Chemistry and Medicine
Nelson, M. J., Greenwald, R. A., & Hillen, W. (2001) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-8306-1 · Cited by 97 · see citing works
Evaluation of the Incidence of Periodontitis‐Associated Bacteria in the Atherosclerotic Plaque of Coronary Blood Vessels
Zaremba, M., Górska, R., Suwalski, P., & Kowalski, J. (2007) · Journal of Periodontology · doi:10.1902/jop.2006.060081 · Cited by 94 · see citing works
Oral Mucosal Immunology: An Overview
Walker, D. M. (2004) · Annals of the Academy of Medicine Singapore · doi:10.47102/annals-acadmedsg.v33n4p27s · Cited by 91 · see citing works
Milestones in periodontal research and the remaining critical issues
Page, R. C. (1999) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.1999.tb02262.x · Cited by 90 · see citing works
Self-citation
Effect of Porphyromonas gingivalis‐induced inflammation on the development of rheumatoid arthritis
Bartold, P. M., Marino, V., Cantley, M. D., & Haynes, D. R. (2010) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2010.01552.x · Cited by 90 · see citing works
Effects of etanercept, a tumour necrosis factor‐α antagonist, in an experimental model of periodontitis in rats
Paola, R. D., Mazzon, E., Muià, C., Crisafulli, C., Terrana, D., Greco, S., Britti, D., Santori, D., Oteri, G., Cordasco, G., et al. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706979 · Cited by 89 · see citing works
“…Journal of Pharmacology (2007) 150, 286–297 & 2007 Nature Publishing Group All rights reserved 0007–1188/07 $30.00 www.brjpharmacol.org possibly the release of anti-inflammatory cytokines including transforming growth factor-a, interleukin-4 (IL-4), interleukin-10 (IL-10) and IL- 12 (Page, 1998).”
BackgroundInfluential
Nonhuman Primates: A Critical Role in Current Disease Research
Sibal, L. R., & Samson, K. (2001) · ILAR Journal · doi:10.1093/ilar.42.2.74 · Cited by 88 · see citing works
Association Between Respiratory Disease in Hospitalized Patients and Periodontal Disease: A Cross‐Sectional Study
Sharma, N., & Shamsuddin, H. (2011) · Journal of Periodontology · doi:10.1902/jop.2011.100582 · Cited by 85 · see citing works
Relationship Between Periodontitis and Diabetes: Lessons From Rodent Studies
Pontes, C. D. N., Flyvbjerg, A., Buschard, K., & Holmstrup, P. (2007) · Journal of Periodontology · doi:10.1902/jop.2007.060491 · Cited by 81 · see citing works
Periodontal Status and Metabolic Syndrome in Middle‐Aged Japanese
Fukui, N., Shimazaki, Y., Shinagawa, T., & Yamashita, Y. (2012) · Journal of Periodontology · doi:10.1902/jop.2012.110605 · Cited by 81 · see citing works
Porphyrin-Mediated Binding to Hemoglobin by the HA2 Domain of Cysteine Proteinases (Gingipains) and Hemagglutinins from the Periodontal PathogenPorphyromonas gingivalis
DeCarlo, A. A., Paramaesvaran, M., Yun, P. L. W., Collyer, C. A., & Hunter, N. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.12.3784-3791.1999 · Cited by 79 · see citing works
“Periodontal disease affects the majority of adults to some degree and may be associated with significant systemic morbidity (2, 46), including dental infection and loss of teeth (36).”
Background
Severe COVID-19 Lung Infection in Older People and Periodontitis
Aquino-Martínez, R., & Vigueras, S. H. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10020279 · Cited by 76 · see citing works
“Periodontal Gram-negative bacteria continuously challenge the host immune defense, but they are also a sustained source of Lipopolysaccharide (LPS) and toxins that can reach systemic circulation [99].”
Background
Influence of implant microstructure on the dynamics of bone healing around immediate implants placed into periodontally infected sites
Papalexiou, V., Novaes, A. B., Grisi, M. F. M., Souza, S. S. L. S., Taba, M., & Kajiwara, J. K. (2004) · Clinical Oral Implants Research · doi:10.1111/j.1600-0501.2004.00995.x · Cited by 75 · see citing works
Stress and periodontal disease: The link and logic!!
Goyal, S., Gupta, G., Thomas, B., Bhat, K., & Bhat, G. (2013) · Industrial Psychiatry Journal · doi:10.4103/0972-6748.123585 · Cited by 74 · see citing works
The impact of oral health status on COVID-19 severity, recovery period and C-reactive protein values
Kamel, A. H. M., Basuoni, A., Salem, Z. A., & AbuBakr, N. (2021) · BDJ · doi:10.1038/s41415-021-2656-1 · Cited by 73 · see citing works
An assessment of periodontal health in patients with schizophrenia and taking antipsychotic medication
Eltas, A., Kartalcı, Ş., Eltas, Ş., Dündar, S., & Uslu, M. (2012) · International Journal of Dental Hygiene · doi:10.1111/j.1601-5037.2012.00558.x · Cited by 70 · see citing works
Activation of Human Prothrombin by Arginine-specific Cysteine Proteinases (Gingipains R) from Porphyromonas gingivalis *
Imamura, T., Banbula, A., Pereira, P. J. B., Travis, J. W., & Potempa, J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006760200 · Cited by 70 · see citing works
The association of periodontal disease parameters with systemic medical conditions and tobacco use
Molloy, J., Wolff, L. F., Lopez‐Guzman, A., & Hodges, J. S. (2004) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2004.00539.x · Cited by 69 · see citing works
Periodontal disease and diabetes mellitus
Pucher, J. J., & Stewart, J. E. (2004) · Current Diabetes Reports · doi:10.1007/s11892-004-0011-y · Cited by 69 · see citing works
Informational Paper: Modulation of the Host Response in Periodontal Therapy
Research, S. (2002) · Journal of Periodontology · doi:10.1902/jop.2002.73.4.460 · Cited by 68 · see citing works
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
Herpesviruses in HIV-periodontitis
Contreras, A., Mardirossian, A., & Slots, J. (2001) · Journal Of Clinical Periodontology · doi:10.1034/j.1600-051x.2001.280115.x · Cited by 67 · see citing works
Full‐mouth profile of active MMP‐8 in periodontitis patients
Kraft‐Neumärker, M., Lorenz, K., Koch, R., Hoffmann, T. K., Mäntylä, P., Sorsa, T. A., & Netuschil, L. (2011) · Journal of Periodontal Research · doi:10.1111/j.1600-0765.2011.01416.x · Cited by 66 · see citing works
Effects of Tumor Necrosis Factor‐α Inhibitors Pentoxifylline and Thalidomide on Alveolar Bone Loss in Short‐Term Experimental Periodontal Disease in Rats
Lima, V., Vidal, F. D. P., Rocha, F. A. C., Brito, G. A. D. C., & Ribeiro, R. A. (2004) · Journal of Periodontology · doi:10.1902/jop.2004.75.1.162 · Cited by 64 · see citing works
A Role for Non-Antimicrobial Actions of Tetracyclines in Combating Oxidative Stress in Periodontal and Metabolic Diseases: A Literature Review
Soory, M. (2008) · The Open Dentistry Journal · doi:10.2174/1874210600802010005 · Cited by 63 · see citing works
“Specific periodontal pathogens and their products associated with host virulence can contribute to a significant systemic inflammatory burden [6-8].”
Background
Analysis of host responses and risk for disease progression
Sahingur, S. E., & Cohen, R. E. (2004) · Periodontology 2000 · doi:10.1046/j.0906-6713.2002.003425.x · Cited by 62 · see citing works
Essentials of periodontal medicine in preventive medicine.
Gulati, M., Anand, V., Jain, N. K., Anand, B., Bahuguna, R., Govila, V., & Rastogi, P. K. (2013) · Europe PMC (PubMed Central) · Cited by 61 · see citing works
Periodontal, metabolic, and cardiovascular disease: Exploring the role of inflammation and mental health
Makkar, H., Reynolds, M. A., Wadhawan, A., Dagdag, A., Merchant, A. T., & Postolache, T. T. (2018) · Pteridines · doi:10.1515/pteridines-2018-0013 · Cited by 64 · see citing works
Stress and periodontal disease
Reners, M., & Brecx, M. C. (2007) · International Journal of Dental Hygiene · doi:10.1111/j.1601-5037.2007.00267.x · Cited by 60 · see citing works
Periodontitis: a potential risk factor for Alzheimer's disease
Cerajewska, T., Davies, M., & West, N. (2015) · BDJ · doi:10.1038/sj.bdj.2014.1137 · Cited by 71 · see citing works
Using 8-Hydroxy-2′-Deoxiguanosine (8-OHdG) as a Reliable Biomarker for Assessing Periodontal Disease Associated with Diabetes
Goriuc, A., Cojocaru, K.-A., Luchian, I. A., Ursu, R. G., Butnaru, O., & Foia, L. G. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031425 · Cited by 59 · see citing works
“The well-vascularized nature of the inflamed periodontium in individuals with periodontal disease results in a sustained release of various substances, including cytokines, potentially modifying diverse physiological states and pathological processes [16].”
Background
Resistin: A Potential Biomarker for Periodontitis Influenced Diabetes Mellitus and Diabetes Induced Periodontitis
Devanoorkar, A., Kathariya, R., Guttiganur, N., Gopalakrishnan, D., & Bagchi, P. (2014) · Disease Markers · doi:10.1155/2014/930206 · Cited by 59 · see citing works
“These cells and the cytokines produced such as TNF-α, CRP, interleukins, prostaglandins, and resistin not only result in the local tissue destruction characterized by periodontal attachment loss and alveolar bone loss but also exert certain distant systemic effects such as increased risk for atherosclerosis, PTLBW, an…”
Background
Capnocytophaga spp. in Periodontitis Patients Manifesting Diabetes Mellitus
Ciantar, M., Gilthorpe, M. S., Hurel, S. J., Newman, H. N., Wilson, M., & Spratt, D. A. (2005) · Journal of Periodontology · doi:10.1902/jop.2005.76.2.194 · Cited by 59 · see citing works
The effects of periodontal therapy on gingival crevicular fluid matrix metalloproteinase‐8, interleukin‐6 and prostaglandin E2 levels in patients with rheumatoid arthritis
Kurgan, Ş., Fentoğlu, Ö., Önder, C., Serdar, M. A., Eser, F., Tatakis, D. N., & Günhan, M. (2015) · Journal of Periodontal Research · doi:10.1111/jre.12337 · Cited by 57 · see citing works
A Chemically Modified Curcumin (CMC 2.24) Inhibits Nuclear Factor κB Activation and Inflammatory Bone Loss in Murine Models of LPS-Induced Experimental Periodontitis and Diabetes-Associated Natural Periodontitis
Elburki, M. S., Rossa, C., Guimarães, M. R., Lee, H., Curylofo‐Zotti, F. A., Johnson, F., & Golub, L. M. (2017) · Inflammation · doi:10.1007/s10753-017-0587-4 · Cited by 56 · see citing works
“IL-1β and TNF-α also activate other mediators of inflammation such as cycloxygenase-2 and 5lipoxygenase, leading to the production of lipid mediators of inflammation, such as prostaglandins and leukotrienes [73].”
Background
Periodontitis Is an Important and Occult Source of Inflammation in Hemodialysis Patients
Kadiroğlu, A. K., Kadiroğlu, E. T., Şit, D., Dağ, A., & Yılmaz, M. E. (2006) · Blood Purification · doi:10.1159/000093683 · Cited by 56 · see citing works
Pathogenic Mechanisms Linking Periodontal Diseases With Adverse Pregnancy Outcomes
Cetin, I., Pileri, P., Villa, A., Calabrese, S., Ottolenghi, L., & Abati, S. (2012) · Reproductive Sciences · doi:10.1177/1933719111432871 · Cited by 53 · see citing works
“39 Furthermore, these mediators can cross fetal membranes; so, it is possible that high levels of these cytokines synthesized at the level of periodontal infection could interfere with fetoplacental functions and contribute to the onset of preterm labor.(40,41) Increased levels of intraamniotic cytokines have indeed b…”
Background
Periodontal infections and community-acquired pneumonia: a case–control study
Neto, J. P. M., Melo, M. S. A. E., Pereira, S. A. D. S., Martinez, E. F., Okajima, L. S., & Saba‐Chujfi, E. (2012) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-012-1710-y · Cited by 54 · see citing works
Apical periodontitis and related factors in an adult Lithuanian population
Aleksejūnienė, J., ERIKSEN, H. M., Sidaravičius, B., & Haapasalo, M. (2000) · Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology · doi:10.1067/moe.2000.107059 · Cited by 54 · see citing works
Relationship between NAFLD and Periodontal Disease from the View of Clinical and Basic Research, and Immunological Response
Hatasa, M., Yoshida, S., Takahashi, H., Tanaka, K., Kubotsu, Y., Ohsugi, Y., Katagiri, T., Iwata, T., & Katagiri, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073728 · Cited by 57 · see citing works
“Secondly, in patients with periodontitis, bacteremia may originate from periodontal pockets, as patients with generalized chronic periodontitis showed ulcers in inflamed periodontal pockets, and the total area of the ulcers was estimated to be as large as the size of the palm [15].”
Background
Porphyromonas gingivalis impairs glucose uptake in skeletal muscle associated with altering gut microbiota
Watanabe, K., Katagiri, S., Takahashi, H., Sasaki, N., Maekawa, S., Komazaki, R., Hatasa, M., Kitajima, Y., Maruyama, Y., Shiba, T., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202001158r · Cited by 52 · see citing works
Periodontal treatment and microbiome-targeted therapy in management of periodontitis-related nonalcoholic fatty liver disease with oral and gut dysbiosis
Kuraji, R., Shiba, T., Dong, T. S., Numabe, Y., & Kapila, Y. L. (2023) · World Journal of Gastroenterology · doi:10.3748/wjg.v29.i6.967 · Cited by 51 · see citing works
Effect of nonsurgical periodontal therapy (with or without oral doxycycline delivery) on glycemic status and clinical periodontal parameters in patients with prediabetes: a short-term longitudinal randomized case–control study
Javed, F., Ahmed, H., Mehmood, A., Bain, C., & Romanos, G. (2014) · Clinical Oral Investigations · doi:10.1007/s00784-014-1185-6 · Cited by 46 · see citing works
“Studies [34-36] have anticipated that bacteria and their products (such as lipopolysaccharides) enter systemic circulation from infected periodontal pockets, which may worsen insulin resistance by potentially increasing low-grade inflammation.”
Background
Melatonin as a Topical/Systemic Formulation for the Management of Periodontitis: A Systematic Review
Balaji, T. M., Varadarajan, S., Jagannathan, R., Mahendra, J., Fageeh, H. I., Fageeh, H. N., Mushtaq, S., Baeshen, H. A., Bhandi, S., Gupta, A. A., et al. (2021) · Materials · doi:10.3390/ma14092417 · Cited by 49 · see citing works
“of pro-inflammatory cytokines and mediators such as prostaglandins, leukotrienes, and acute phase reactants such as C-reactive protein [45].”
Background
Treatment of Periodontal Diseases Reduces Chronic Systemic Inflammation in Maintenance Hemodialysis Patients
Siribamrungwong, M., & Puangpanngam, K. (2012) · Renal Failure · doi:10.3109/0886022x.2011.643351 · Cited by 49 · see citing works
Periodontal Disease: A Covert Source of Inflammation in Chronic Kidney Disease Patients
Ismail, G., Dumitriu, H. T., Dumitriu, A. S., & Ismail, F. B. (2013) · International Journal of Nephrology · doi:10.1155/2013/515796 · Cited by 47 · see citing works
DOES THE MOUTH PUT THE HEART AT RISK?
SLAVKIN, H. C. (1999) · The Journal of the American Dental Association · doi:10.14219/jada.archive.1999.0038 · Cited by 46 · see citing works
Prevalência e características associadas à síndrome metabólica em nipo-brasileiros com e sem doença periodontal
Borges, P. K. D. O., Gimeno, S. G. A., Tomita, N. E., & Ferreira, S. R. G. (2007) · Cadernos de Saúde Pública · doi:10.1590/s0102-311x2007000300024 · Cited by 46 · see citing works
Is Periodontitis Associated with Age-Related Cognitive Impairment? The Systematic Review, Confounders Assessment and Meta-Analysis of Clinical Studies
Dziedzic, A. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315320 · Cited by 45 · see citing works
Accuracy of Self‐Reported Periodontal Disease in the Women's Health Initiative Observational Study
LaMonte, M. J., Hovey, K. M. O., Millen, A. E., Genco, R. J., & Wactawski‐Wende, J. (2013) · Journal of Periodontology · doi:10.1902/jop.2013.130488 · Cited by 45 · see citing works
“…study group; 2) the several objective periodontal measures with demonstrated reliability obtained from standardized oral examinations; and 3) the relative consistency of findings according to cohort subgroups in which opportunity for, or recall of, periodontal disease diagnosis could…”

The Emerging Concepts on the Impact of Periodontitis on Systemic Health
Anil, S., Subash, B. V., Preethanath, R. S., Pradeep, P. S., & Aldosari, A. A. F. (2012) · InTech eBooks · doi:10.5772/26457 · Cited by 9 · see citing works
BIOLOGICAL ASPECTS OF ASSOCIATION BETWEEN CARDIOVASCULAR DISEASES AND PERIODONTITIS
Ostrovskа, S. S., & Герасимчук, П. Г. (2018) · Bulletin of Problems Biology and Medicine · doi:10.29254/2077-4214-2018-4-2-147-58-61 · Cited by 1 · see citing works
Cytokines in Stress
Giannantonio, M. D., Frydas, S., Kempuraj, D., Karagouni, E., Hatzistilianou, M. N., Conti, C. M., Boucher, W. S., Papadopoulou, N., Donelan, J., Cao, J., et al. (2005) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200501800101 · Cited by 82 · see citing works
Periodontal and systemic interrelationship
Kashyap, V., Sikka, N., & Verma, R. (2016)
Are periodontal diseases risk factors for certain systemic disorders--what matters to medical practitioners?
Jin, L., Chiu, G., & Corbet, E. (2003) · PubMed · Cited by 43 · see citing works

Authors: Page, R. C.
Affiliations: University of Washington (US)
Corresponding author: Page, Roy C.
Venue: Annals of Periodontology
Publisher: Wiley
Published: 1998-07
Volume: 3
Issue: 1
Pages: 108-120
ISSN: 1553-0841 (ISSN-L)
2162-5131
DOI: 10.1902/annals.1998.3.1.108
OpenAlex: W1967814211
Cited by: 420
References: 45
Citations by year: 2026: 4 · 2025: 8 · 2024: 16 · 2023: 8 · 2022: 17 · 2021: 20 · 2020: 14 · 2019: 16 · 2018: 12 · 2017: 18 · 2016: 12 · 2015: 18 · 2014: 18 · 2013: 26 · 2012: 34
FWCI: 19.34
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Annals of Periodontology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p01de008555-10)
National Institute of Dental and Craniofacial Research (T32 DE 07063, P30 DE09743, P01DE08555, T32DE007063, P30DE009743)
Topics: Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
Health Sciences › Dentistry › General Dentistry › Dental Research and COVID-19
Keywords: periodontitis, cardiovascular disease, preterm labor, Gram-negative bacteria, biofilm, lipopolysaccharide, immune inflammation, inflammatory cytokines, matrix metalloproteinases, prostaglandins, alveolar bone loss, periodontal ligament, risk factors, smoking
MeSH terms: Animals, Cardiovascular Diseases, Disease Susceptibility, Focal Infection, Dental, Gram-Negative Anaerobic Bacteria, Health Status, Humans, Periodontitis, Risk Factors, Cytokines, Biofilms, Inflammation Mediators

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The Pathobiology of Periodontal Diseases May Affect Systemic Diseases: Inversion of a Paradigm

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