Periodontitis: from microbial immune subversion to systemic inflammation

Hajishengallis, George

doi:10.1038/nri3785

Cited by 3,046Oral microbiology and periodontitis researchGut microbiota and healthDental Research and COVID-19

Periodontitis: from microbial immune subversion to systemic inflammation

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Hajishengallis, George·2015·Nature Reviews Immunology

DOI 10.1038/nri3785PMC PMC4276050

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Abstract

Periodontitis is a dysbiotic inflammatory disease with an adverse impact on systemic health. Recent studies have provided insights into the emergence and persistence of dysbiotic oral microbial communities that can mediate inflammatory pathology at local as well as distant sites. This Review discusses the mechanisms of microbial immune subversion that tip the balance from homeostasis to disease in oral or extra-oral sites.

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Recent studies have highlighted that the mineralized structure of calculus may promote a dysbiotic shift in the microbial community, contributing to persistent inflammation and disease progression.
“Recent studies have also highlighted that the mineralized structure of calculus may promote a dysbiotic shift in the microbial community, contributing to persistent inflammation and disease progression [4].”
From In vitro biomimetic development of artificial dental calculus: a proof of concept study (2025) · cites this paper as [4]
Periodontal disease is caused by dysbiosis of subgingival microbial communities that adversely affects the host immune system such that it creates and maintains unmitigated inflammation in gingival and periodontal tissues, thus preventing immune subversion and tissue recovery.
“Periodontal disease is caused by dysbiosis of subgingival microbial communities that adversely affects the host immune system such that it creates and maintains unmitigated inflammation in gingival and periodontal tissues, thus preventing immune subversion and tissue recovery.10”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [10]
Aspiration pneumonia is closely related to oral microorganisms due to the aspiration of oropharyngeal secretions.
“It is speculated that aspiration pneumonia is also closely related to oral microorganisms due to the aspiration of oropharyngeal secretions (Hajishengallis, 2015).”
From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Hajishengallis, 2015

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Belstrøm, D., Holmstrup, P., Damgaard, C., Borch, T. S., Skjoedt, M., Bendtzen, K., & Nielsen, C. H. (2011) · Infection and Immunity · doi:10.1128/iai.01036-10 · Cited by 48 · see citing works
Porphyromonas gingivalis modulates Pseudomonas aeruginosa-induced apoptosis of respiratory epithelial cells through the STAT3 signaling pathway
Li, Q., Pan, C., Teng, D., Lin, L., Kou, Y., Haase, E. M., Scannapieco, F. A., & Pan, Y. (2013) · Microbes and Infection · doi:10.1016/j.micinf.2013.10.006 · Cited by 47 · see citing works
Pathogen-Mediated Proteolysis of the Cell Death Regulator RIPK1 and the Host Defense Modulator RIPK2 in Human Aortic Endothelial Cells
Madrigal, A. G., Barth, K., Papadopoulos, G., & Genco, C. A. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002723 · Cited by 45 · see citing works
Genetic Characteristics and Pathogenic Mechanisms of Periodontal Pathogens
Amano, A., Chen, C., Honma, K., Li, C., Settem, R. P., & Sharma, A. (2014) · Advances in Dental Research · doi:10.1177/0022034514526237 · Cited by 44 · see citing works
Porphyromonas gingivalis -impaired innate immune response via NLRP3 proteolysis in endothelial cells
Huck, O., Elkaïm, R., Davideau, J., & Tenenbaum, H. (2014) · Innate Immunity · doi:10.1177/1753425914523459 · Cited by 43 · see citing works
Neutrophil Dysfunction and Host Susceptibility to Periodontal Inflammation: Current State of Knowledge
Sima, C., & Glogauer, M. (2014) · Current Oral Health Reports · doi:10.1007/s40496-014-0015-x · Cited by 43 · see citing works
Porphyromonas gingivalis Lipid A Phosphatase Activity Is Critical for Colonization and Increasing the Commensal Load in the Rabbit Ligature Model
Zenobia, C., Hastürk, H., Nguyen, D., Dyke, T. E. V., Kantarcı, A., & Darveau, R. P. (2013) · Infection and Immunity · doi:10.1128/iai.01136-13 · Cited by 43 · see citing works
Porphyromonas gingivalis lipopolysaccharide increases lipid accumulation by affecting CD36 and ATP-binding cassette transporter A1 in macrophages
Li, X., Wang, C., Xiang, X., Chen, F., YANG, C.-M., & Wu, J. (2013) · Oncology Reports · doi:10.3892/or.2013.2600 · Cited by 42 · see citing works
Oral Microbiology and Immunology
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Secondary Lymphoid Organ Homing Phenotype of Human Myeloid Dendritic Cells Disrupted by an Intracellular Oral Pathogen
Miles, B., Zakhary, I., El‐Awady, A., Scisci, E., Carrion, J. A., O'Neill, J. C., Rawlings, A., Stern, J. K., Susin, C., & Cutler, C. W. (2013) · Infection and Immunity · doi:10.1128/iai.01157-13 · Cited by 32 · see citing works
Smoking and the Subgingival Ecosystem: A Pathogen-Enriched Community
Kumar, P. (2012) · Future Microbiology · doi:10.2217/fmb.12.71 · Cited by 29 · see citing works
Acquisition of Complement Inhibitor Serine Protease Factor I and Its Cofactors C4b-Binding Protein and Factor H by Prevotella intermedia
Malm, S., Jusko, M., Eick, S., Potempa, J., Riesbeck, K., & Blom, A. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034852 · Cited by 26 · see citing works
Anticardiolipin in Porphyromonas gingivalis Antisera Causes Fetal Loss in Mice
Schenkein, H. A., Bradley, J. L., & Purkall, D. B. (2013) · Journal of Dental Research · doi:10.1177/0022034513497959 · Cited by 26 · see citing works
Anti-citrullinated protein antibodies (ACPA) in early rheumatoid arthritis
Suwannalai, P., Trouw, L. A., Toes, R. E. M., & Huizinga, T. W. J. (2011) · Modern Rheumatology · doi:10.1007/s10165-011-0486-8 · Cited by 26 · see citing works
Anti-citrullinated protein antibodies (ACPA) in early rheumatoid arthritis
Suwannalai, P., Trouw, L. A., Toes, R. E. M., & Huizinga, T. W. J. (2012) · Modern Rheumatology · doi:10.3109/s10165-011-0486-8 · Cited by 26 · see citing works
A periodontal pathogen Treponema denticola hijacks the Fusobacterium nucleatum‐driven host response
Shin, J. E., Baek, K. J., Choi, Y. S., & Choi, Y. (2013) · Immunology and Cell Biology · doi:10.1038/icb.2013.35 · Cited by 25 · see citing works
Porphyromonas gingivalis neutrophil manipulation: risk factor for periodontitis?
Darveau, R. P. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.06.006 · Cited by 22 · see citing works
Porphyromonas gingivalis cell-induced hemagglutination and platelet aggregation
Nakayama, K. (2010) · Periodontology 2000 · doi:10.1111/j.1600-0757.2010.00351.x · Cited by 21 · see citing works
Individuals With Chronic Obstructive Pulmonary Disease (COPD) May Be More Likely to Have More Severe Periodontal Disease Than Individuals Without COPD
Scannapieco, F. A. (2014) · Journal of Evidence Based Dental Practice · doi:10.1016/j.jebdp.2014.04.012 · Cited by 16 · see citing works

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Rheumatoid arthritis
Smolen, J. S., Aletaha, D., Barton, A. C., Burmester, G. R., Emery, P., Firestein, G. S., Kavanaugh, A., McInnes, I. B., Solomon, D. H., Strand, V., et al. (2018) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2018.1 · Cited by 2,480 · see citing works
The Oral Microbiota: Dynamic Communities and Host Interactions
Lamont, R. J., Koo, H., & Hajishengallis, G. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0089-x · Cited by 2,217 · see citing works
Self-citation
Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities
Hajishengallis, G., & Chavakis, T. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-020-00488-6 · Cited by 1,871 · see citing works
Self-citation
Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation
Agler, M. T., Ruhe, J., Kroll, S., Morhenn, C., Kim, S., Weigel, D., & Kemen, E. M. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002352 · Cited by 1,400 · see citing works
The immune response to Prevotella bacteria in chronic inflammatory disease
Larsen, J. M. (2017) · Immunology · doi:10.1111/imm.12760 · Cited by 1,343 · see citing works
Periodontitis: facts, fallacies and the future
Slots, J. (2017) · Periodontology 2000 · doi:10.1111/prd.12221 · Cited by 1,157 · see citing works
Association between periodontal pathogens and systemic disease
Bui, F. Q., Almeida-da-Silva, C. L. C., Huynh, B. C., Trinh, A., Liu, J., Woodward, J., Asadi, H., & Ojcius, D. M. (2019) · Biomedical Journal · doi:10.1016/j.bj.2018.12.001 · Cited by 832 · see citing works
Osteoimmunology: evolving concepts in bone–immune interactions in health and disease
Tsukasaki, M., & Takayanagi, H. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0178-8 · Cited by 789 · see citing works
Oral microbiomes: more and more importance in oral cavity and whole body
Gao, L., Xu, T., Huang, G., Jiang, S., Gu, Y., & Chen, F. (2018) · Protein & Cell · doi:10.1007/s13238-018-0548-1 · Cited by 770 · see citing works
The gut microbiome: connecting spatial organization to function
Tropini, C., Earle, K. A., Huang, K. C., & Sonnenburg, J. L. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.03.010 · Cited by 685 · see citing works
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
Polydopamine Nanoparticles as Efficient Scavengers for Reactive Oxygen Species in Periodontal Disease
Bao, X., Zhao, J., Sun, J., Hu, M., & Yang, X. (2018) · ACS Nano · doi:10.1021/acsnano.8b04022 · Cited by 722 · see citing works
The cytokine network involved in the host immune response to periodontitis
Pan, W., Wang, Q., & Chen, Q. (2019) · International Journal of Oral Science · doi:10.1038/s41368-019-0064-z · Cited by 709 · see citing works
Global Prevalence of Periodontal Disease and Lack of Its Surveillance
Nazir, M. A., Al‐Ansari, A. A., Al‐Khalifa, K. S., Alhareky, M. S., Gaffar, B. O., & Almas, K. (2020) · The Scientific World JOURNAL · doi:10.1155/2020/2146160 · Cited by 678 · see citing works
“Aging is known to impair the immune and inflammatory responses which contribute to periodontal tissue destruction in older subjects [38].”
Background
Rheumatoid Arthritis: Pathogenic Roles of Diverse Immune Cells
Jang, S., Kwon, E.-J., & Lee, J. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020905 · Cited by 621 · see citing works
Extensive transmission of microbes along the gastrointestinal tract
Schmidt, T. S., Hayward, M. R., Coelho, L. P., Li, S. S., Costea, P. I., Voigt, A. Y., Wirbel, J., Maistrenko, O. M., Alves, R. J., Bergsten, E., et al. (2019) · eLife · doi:10.7554/elife.42693 · Cited by 596 · see citing works
The Gut Microbiome Alterations and Inflammation-Driven Pathogenesis of Alzheimer’s Disease—a Critical Review
Sochocka, M., Donskow-Łysoniewska, K., Diniz, B. S., Kurpas, D., Brzozowska, E., & Leszek, J. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1188-4 · Cited by 584 · see citing works
Human oral mucosa cell atlas reveals a stromal-neutrophil axis regulating tissue immunity
Williams, D. W., Greenwell‐Wild, T., Brenchley, L., Dutzan, N., Overmiller, A. M., Sawaya, A. P., Webb, S., Martı́n, D., Hajishengallis, G., Divaris, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.05.013 · Cited by 523 · see citing works
Self-citation
Periodontal Inflammation and Systemic Diseases: An Overview
Martínez-García, M., & Lemus, E. H. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.709438 · Cited by 520 · see citing works
“This may happen via periodontitis-associated inflammatory cascades: locally produced pro-inflammatory mediators enter into systemic circulation, thus becoming able to affect distant organs disrupting inflammatory state equilibria (Hajishengallis, 2015).”
Background
Current understanding of periodontal disease pathogenesis and targets for host‐modulation therapy
Hajishengallis, G., Chavakis, T., & Lambris, J. D. (2020) · Periodontology 2000 · doi:10.1111/prd.12331 · Cited by 513 · see citing works
Self-citation
Host–microbiota interactions in immune-mediated diseases
Ruff, W. E., Greiling, T. M., & Kriegel, M. A. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0367-2 · Cited by 489 · see citing works
Novel mechanisms and functions of complement
Hajishengallis, G., Reis, E. S., Mastellos, D. C., Ricklin, D., & Lambris, J. D. (2017) · Nature Immunology · doi:10.1038/ni.3858 · Cited by 484 · see citing works
Self-citation
Chronic periodontitis, inflammatory cytokines, and interrelationship with other chronic diseases
Cardoso, E. M., Reis, C., & Manzanares‐Céspedes, M. C. (2017) · Postgraduate Medicine · doi:10.1080/00325481.2018.1396876 · Cited by 485 · see citing works
Exosomes from TNF-α-treated human gingiva-derived MSCs enhance M2 macrophage polarization and inhibit periodontal bone loss
Nakao, Y., Fukuda, T., Zhang, Q.-Z., Sanui, T., Shinjo, T., Kou, X., Chen, C., Liu, D.-W., Watanabe, Y., Hayashi, C., et al. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.12.046 · Cited by 442 · see citing works
“Periodontitis is the most common osteolytic inflammatory disease in human that adversely affects systemic disorders, such as atherosclerosis, rheumatoid arthritis, and diabetes [11].”
Background
The Bacterial Connection between the Oral Cavity and the Gut Diseases
Kitamoto, S., Nagao‐Kitamoto, H., Hein, R., Schmidt, T. M., & Kamada, N. (2020) · Journal of Dental Research · doi:10.1177/0022034520924633 · Cited by 444 · see citing works
“Furthermore, as described in Table 2, oral bacteria is known to invade and survive inside immune cells, such as dendritic cells and macrophages, indicating that oral bacteria may hijack host immune cells to serve as Trojan horses for dissemination from the oral mucosa to the gut mucosa (Hajishengallis 2015).”
Background
Interconnection of periodontal disease and comorbidities: Evidence, mechanisms, and implications
Hajishengallis, G. (2022) · Periodontology 2000 · doi:10.1111/prd.12430 · Cited by 449 · see citing works
Self-citation
Tissue-Specific Immunity at the Oral Mucosal Barrier
Moutsopoulos, N. M., & Konkel, J. E. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.08.005 · Cited by 401 · see citing works
The Structure of Dental Plaque Microbial Communities in the Transition from Health to Dental Caries and Periodontal Disease
Valm, A. M. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.016 · Cited by 425 · see citing works
Evidence of the Immune Relevance of Prevotella copri, a Gut Microbe, in Patients With Rheumatoid Arthritis
Pianta, A., Arvikar, S. L., Strle, K., Drouin, E. E., Wang, Q., Costello, C. E., & Steere, A. C. (2016) · Arthritis & Rheumatology · doi:10.1002/art.40003 · Cited by 405 · see citing works
Microenvironment-Responsive Metal-Phenolic Nanozyme Release Platform with Antibacterial, ROS Scavenging, and Osteogenesis for Periodontitis
Xu, Y., Luo, Y., Weng, Z., Xu, H., Zhang, W., Li, Q., Liu, H., Liu, L., Wang, Y., Liu, X., et al. (2023) · ACS Nano · doi:10.1021/acsnano.3c01940 · Cited by 402 · see citing works
A dysbiotic microbiome triggers T H 17 cells to mediate oral mucosal immunopathology in mice and humans
Dutzan, N., Kajikawa, T., Abusleme, L., Greenwell-Wild, T., Zuazo, C. E., Ikeuchi, T., Brenchley, L., Abe, T., Hurabielle, C., Martin, D., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aat0797 · Cited by 382 · see citing works
Self-citation
Periodontal Disease: The Good, The Bad, and The Unknown
Sedghi, L. M., Bacino, M. S., & Kapila, Y. L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.766944 · Cited by 385 · see citing works
“Putative periodontal pathogens are critical to eliciting disease and prompting host inflammation while continuing to perpetuate disease via immune subversion and manipulation of tissues (Maekawa et al., 2014;Hajishengallis, 2015;Malone et al., 2021).”
Background
Current concepts in the pathogenesis of periodontitis: from symbiosis to dysbiosis
Abdulkareem, A. A., Al-Taweel, F. B. H., Al-Sharqi, A. J. B., Gul, S. S., Sha, A. M., & Chapple, I. (2023) · Journal of Oral Microbiology · doi:10.1080/20002297.2023.2197779 · Cited by 402 · see citing works
“severe and destructive form, periodontitis [1]].”
Photocatalytic Antimicrobials: Principles, Design Strategies, and Applications
Ran, B., Ran, L., Wang, Z., Liao, J., Li, D., Chen, K., Cai, W., Hou, J., & Peng, X. (2023) · Chemical Reviews · doi:10.1021/acs.chemrev.3c00326 · Cited by 362 · see citing works
The Oral Microbiome and Cancer
Irfan, M., Delgado, R. Z. R., & Frias-Lopez, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.591088 · Cited by 341 · see citing works
Clinical promise of next-generation complement therapeutics
Mastellos, D. C., Ricklin, D., & Lambris, J. D. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0031-6 · Cited by 346 · see citing works
Bacteria in cancer initiation, promotion and progression
Tekle, G. E., & Garrett, W. S. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00594-2 · Cited by 349 · see citing works
Maladaptive innate immune training of myelopoiesis links inflammatory comorbidities
Li, X., Wang, H., Yu, X., Saha, G., Kalafati, L., Ioannidis, C., Mitroulis, I., Netea, M. G., Chavakis, T., & Hajishengallis, G. (2022) · Cell · doi:10.1016/j.cell.2022.03.043 · Cited by 337 · see citing works
Self-citation
Host defense against oral microbiota by bone-damaging T cells
Tsukasaki, M., Komatsu, N., Nagashima, K., Nitta, T., Pluemsakunthai, W., Shukunami, C., Iwakura, Y., Nakashima, T., Okamoto, K., & Takayanagi, H. (2018) · Nature Communications · doi:10.1038/s41467-018-03147-6 · Cited by 324 · see citing works
The oral–gut microbiome axis in health and disease
Kunath, B. J., Rudder, C. D., Laczny, C. C., Letellier, E., & Wilmes, P. (2024) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01075-5 · Cited by 342 · see citing works
“A growing number of studies have demonstrated correlations between alterations in the oral microbiome and other health conditions 14,15 .”
Hematopoietic progenitor cells as integrative hubs for adaptation to and fine-tuning of inflammation
Chavakis, T., Mitroulis, I., & Hajishengallis, G. (2019) · Nature Immunology · doi:10.1038/s41590-019-0402-5 · Cited by 318 · see citing works
Self-citation
The Type IX Secretion System (T9SS): Highlights and Recent Insights into Its Structure and Function
Lasica, A. M., Ksiazek, M., Madej, M., & Potempa, J. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00215 · Cited by 312 · see citing works
DEL-1 promotes macrophage efferocytosis and clearance of inflammation
Kourtzelis, I., Li, X., Mitroulis, I., Grosser, D., Kajikawa, T., Wang, B., Grzybek, M., von Renesse, J., Czogalla, A., Troullinaki, M., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0249-1 · Cited by 310 · see citing works
Self-citation
Antibiotics/antimicrobials: systemic and local administration in the therapy of mild to moderately advanced periodontitis
Jepsen, K., & Jepsen, S. (2016) · Periodontology 2000 · doi:10.1111/prd.12121 · Cited by 306 · see citing works
Oral microbial biofilms: an update
Mosaddad, S. A., Tahmasebi, E., Yazdanian, A., Rezvani, M. B., Seifalian, A. M., Yazdanıan, M., & Tebyanian, H. (2019) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-019-03641-9 · Cited by 306 · see citing works
Characterization of the human immune cell network at the gingival barrier
Dutzan, N., Konkel, J. E., Greenwell-Wild, T., & Moutsopoulos, N. M. (2016) · Mucosal Immunology · doi:10.1038/mi.2015.136 · Cited by 305 · see citing works
Polarized Macrophages in Periodontitis: Characteristics, Function, and Molecular Signaling
Sun, X., Gao, J., Meng, X. L., Lu, X., Zhang, L., & Chen, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.763334 · Cited by 294 · see citing works
“In periodontal tissue, macrophage polarization to the M1 type is primarily induced by Th1 production of IFN-g and LPSdominated microbial-related factors (6).”
Background
An injectable and thermosensitive hydrogel: Promoting periodontal regeneration by controlled-release of aspirin and erythropoietin
Xu, X., Gu, Z., Chen, X., Shi, C., Liu, C., Liu, M., Wang, L., Sun, M., Zhang, K., Liu, Q., et al. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.01.001 · Cited by 293 · see citing works
Dental resin composites: A review on materials to product realizations
Cho, K., Rajan, G., Farrar, P., Prentice, L. H., & Prusty, B. G. (2021) · Composites Part B Engineering · doi:10.1016/j.compositesb.2021.109495 · Cited by 288 · see citing works
Polymicrobial communities in periodontal disease: Their quasi‐organismal nature and dialogue with the host
Hajishengallis, G., & Lamont, R. J. (2021) · Periodontology 2000 · doi:10.1111/prd.12371 · Cited by 302 · see citing works
Self-citation
The role of the local microbial ecosystem in respiratory health and disease
Piters, W. A. A. D. S., Sanders, E. A. M., & Bogaert, D. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0294 · Cited by 283 · see citing works
Surface treatments on titanium implants via nanostructured ceria for antibacterial and anti-inflammatory capabilities
Li, X., Qi, M., Sun, X., Weir, M. D., Tay, F. R., Oates, T. W., Dong, B., Zhou, Y., Wang, L., & Xu, H. H. K. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.06.023 · Cited by 281 · see citing works
Aging, inflammation, immunity and periodontal disease
Ebersole, J. L., Graves, C. L., González, O. A., Dawson, D. R., Morford, L. A., Emecen‐Huja, P., Hartsfield, J. K., Huja, S. S., Pandruvada, S. N. M., & Wallet, S. M. (2016) · Periodontology 2000 · doi:10.1111/prd.12135 · Cited by 308 · see citing works
Pathogenesis of Important Virulence Factors of Porphyromonas gingivalis via Toll-Like Receptors
Lü, J., Han, N., Du, J., Guo, L., Luo, Z., & Liu, Y. F. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00262 · Cited by 284 · see citing works
Linkage of Periodontitis and Rheumatoid Arthritis: Current Evidence and Potential Biological Interactions
de Molon, R. S., Rossa, C., Thurlings, R. M., Cirelli, J. A., & Koenders, M. I. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184541 · Cited by 262 · see citing works
Regulation of host-microbe interactions at oral mucosal barriers by type 17 immunity
Gaffen, S., & Moutsopoulos, N. (2020) · Science immunology · doi:10.1126/sciimmunol.aau4594 · Cited by 230 · see citing works
On-going Mechanical Damage from Mastication Drives Homeostatic Th17 Cell Responses at the Oral Barrier
Dutzan, N., Abusleme, L., Bridgeman, H., Greenwell-Wild, T., Zangerle-Murray, T., Fife, M. E., Bouladoux, N., Linley, H., Brenchley, L., Wemyss, K., et al. (2017) · Immunity · doi:10.1016/j.immuni.2016.12.010 · Cited by 252 · see citing works
“…2012; Moutsopoulos et al., 2014) are causative in periodontitis, as are dysbiotic microbial communities that stimulate aberrant inﬂammatory responses promoting the disease in mouse models (Hajishengallis et al., 2011) and in susceptible patients (Darveau, 2010; Lamont and Hajishengallis, 2015).”
Background
Oral microbiota and cancer development
Tuominen, H., & Rautava, J. (2021) · Pathobiology · doi:10.1159/000510979 · Cited by 238 · see citing works
Gold nanoparticles modulate the crosstalk between macrophages and periodontal ligament cells for periodontitis treatment
Ni, C., Zhou, J., Kong, N., Bian, T., Zhang, Y., Huang, X., Xiao, Y., Yang, W. R., & Yan, F. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.03.039 · Cited by 245 · see citing works
Revisiting the Page & Schroeder model: the good, the bad and the unknowns in the periodontal host response 40 years later
Hajishengallis, G., & Korostoff, J. M. (2017) · Periodontology 2000 · doi:10.1111/prd.12181 · Cited by 245 · see citing works
Self-citation
Oral Bacteria and Intestinal Dysbiosis in Colorectal Cancer
Koliarakis, I., Messaritakis, I., Νikolouzakis, Τ. Κ., Hamilos, G., Souglakos, J., & Tsiaoussis, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174146 · Cited by 248 · see citing works
ZIF-8 modified multifunctional injectable photopolymerizable GelMA hydrogel for the treatment of periodontitis
Liu, Y., Li, T., Sun, M., Cheng, Z., Jia, W., Jiao, K., Wang, S., Jiang, K., Yang, Y., Dai, Z., et al. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.03.046 · Cited by 237 · see citing works
Local drug delivery systems in the management of periodontitis: A scientific review
Rajeshwari, H., Dhamecha, D. L., Jagwani, S., Rao, M. D. S., Jadhav, K. V., Shaikh, S., Puzhankara, L., & Jalalpure, S. S. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.06.038 · Cited by 236 · see citing works
The Effect of Inflammation on Bone
Epsley, S., Tadros, S., Farid, A., Kargilis, D., Mehta, S., & Rajapakse, C. S. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2020.511799 · Cited by 242 · see citing works
“Periodontitis is a dysbiotic disease in which the oral microbiota become dysregulated and lead to an increased risk of systemic inflammatory diseases, such as Rheumatoid arthritis (RA) (Hajishengallis, 2015).”
Background
Host modulation: controlling the inflammation to control the infection
Bartold, P. M., & Dyke, T. E. V. (2017) · Periodontology 2000 · doi:10.1111/prd.12169 · Cited by 231 · see citing works
Streptococcus Sanguinis Biofilm Formation & Interaction with Oral Pathogens
Zhu, B., Macleod, L. C., Kitten, T. O., & Xu, P. (2018) · Future Microbiology · doi:10.2217/fmb-2018-0043 · Cited by 228 · see citing works
Immunomodulation in the Treatment of Periodontitis: Progress and Perspectives
Yang, B., Pang, X., Li, Z., Chen, Z., & Wang, Y. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.781378 · Cited by 230 · see citing works
Periodontal disease and adverse pregnancy outcomes
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Mechanism of alveolar bone destruction in periodontitis — Periodontal bacteria and inflammation
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Authors: Hajishengallis, G.
Affiliations: University of Pennsylvania (US)
Corresponding author: Hajishengallis, George
ORCID: Hajishengallis, George
Venue: Nature Reviews Immunology
Publisher: Springer Science and Business Media LLC
Published: 2014-12-23
Volume: 15
Issue: 1
Pages: 30-44
ISSN: 1474-1733 (ISSN-L)
1474-1741
DOI: 10.1038/nri3785
PMC: PMC4276050
OpenAlex: W2021838232
Cited by: 3,046
References: 175
Citations by year: 2026: 400 · 2025: 359 · 2024: 348 · 2023: 394 · 2022: 291 · 2021: 318 · 2020: 262 · 2019: 215 · 2018: 135 · 2017: 144 · 2016: 131 · 2015: 46 · 2013: 1
FWCI: 18.04
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute of Allergy and Infectious Diseases (AI 068730, P01AI068730)
National Institute of Dental and Craniofacial Research (DE-015254, DE017138, R01DE015254, R01DE024716, DE021685, R01DE021685, R01DE017138)
Topics: Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Dentistry › General Dentistry › Dental Research and COVID-19
Keywords: periodontitis, systemic inflammation, rheumatoid arthritis, oral dysbiosis, oral microbiota, oral-systemic disease link, host-pathogen interaction
MeSH terms: Animals, Antibiosis, Arthritis, Rheumatoid, Cardiovascular Diseases, Female, Humans, Immunity, Periodontitis, Pregnancy, Pregnancy Outcome, Respiratory Tract Diseases, Symbiosis

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Periodontitis: from microbial immune subversion to systemic inflammation

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