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Periodontitis: from microbial immune subversion to systemic inflammation
Open accessAbstract
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 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]
In the citing paper
“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]
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“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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BackgroundInfluentialInhibition of METTL3 Alleviates NLRP3 Inflammasome Activation via Increasing Ubiquitination of NEK7
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“…including vasodilation and increased permeability of blood vessels (Preshaw et al., 2004) facilitates the transfer of biofilm bacterial components into the bloodstream via the damaged and inflamed periodontium (Hajishengallis et al., 2011; Hajishengallis and Lamont, 2012; Hajishengallis, 2015).”
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“This non-communicable disease results from an accumulation of oral biofilm around the teeth, causing an exacerbated reaction from the immune system that destroys the periodontium [23].”
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“However, the exact specific roles of different microbes in the dental plaque 115 that lead to the development of periodontal disease remains an enigma (7, 23).”
BackgroundFeng, Y., Chen, Z., Tu, S.-Q., Wei, J.-M., Hou, Y., Kuang, Z., Kang, X.-N., & Ai, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.862415 · Cited by 62
The impact of periodontitis on vascular endothelial dysfunction
Li, Q., Ouyang, X., & Jiang, L. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.998313 · Cited by 63
“To date, there are three plausible hypotheses, including the bacteriological, inflammatory, and immunological theories (Hajishengallis, 2015; Febbraio et al., 2022).”
BackgroundEffect of topical administration of propolis in chronic periodontitis
Nakao, R., Senpuku, H., Ohnishi, M., Takai, H., & Ogata, Y. (2020) · Odontology · doi:10.1007/s10266-020-00500-4 · Cited by 59
Yuh, D., Maekawa, T., Li, X., Kajikawa, T., Bdeir, K. H., Chavakis, T., & Hajishengallis, G. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.013024 · Cited by 58
“The importance of these homeostatic functions of DEL-1 becomes phenotypically evident in DEL-1– deficient (Del1) mice in the setting of periodontitis, a prevalent inflammatory disease that affects the integrity of the tissues that surround and support the dentition, such as the gingiva and the underlying alveolar bone…”
BackgroundSelf-citationActive gingival inflammation is linked to hypertension
Pietropaoli, D., Monaco, A., D’Aiuto, F., Muñoz Aguilera, E., Ortu, E., Giannoni, M., Czesnikiewicz-Guzik, M., Guzik, T. J., Ferri, C., & Del Pinto, R. (2020) · Journal of Hypertension · doi:10.1097/hjh.0000000000002514 · Cited by 56
“The unique contribution of specific and diverse inflammatory pathways in the acute and the chronic settings might be a possible explanation for the observed differences between gingivitis and stable/unstable periodontitis in the reported association [42,43].”
BackgroundA concerted probiotic activity to inhibit periodontitis-associated bacteria
Jansen, P. M., Abdelbary, M. M. H., & Conrads, G. (2021) · PLoS ONE · doi:10.1371/journal.pone.0248308 · Cited by 58
“Several bacterial species such as Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Porphyromonas gingivalis, Prevotella intermedia, and fastidious anaerobes including Tannerella forsythia and Treponema denticola are implicated in these shifts [3].”
BackgroundPeriodontal bacteria in the brain—Implication for Alzheimer's disease: A systematic review
Parra‐Torres, V., Melgar‐Rodríguez, S., Muñoz‐Manríquez, C., Sanhueza, B., Cafferata, E. A., Paula-Lima, A. C., & Díaz‐Zúñiga, J. (2021) · Oral Diseases · doi:10.1111/odi.14054 · Cited by 60
Erythrocyte-Mimicking Nanovesicle Targeting Porphyromonas gingivalis for Periodontitis
Tang, Y., Qi, Y., Yang, C., Wang, Y., Zhang, C., Sun, Y., Huang, C., & Zhang, X. (2024) · ACS Nano · doi:10.1021/acsnano.4c02316 · Cited by 57
Interkingdom networking within the oral microbiome
Nobbs, A. H., & Jenkinson, H. F. (2015) · Microbes and Infection · doi:10.1016/j.micinf.2015.03.008 · Cited by 57
Complement inhibition in pre-clinical models of periodontitis and prospects for clinical application
Hajishengallis, G., Hajishengallis, E., Kajikawa, T., Wang, B., Yancopoulou, D., Ricklin, D., & Lambris, J. D. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.006 · Cited by 57
Self-citationT Helper 17 Cells as Pathogenic Drivers of Periodontitis
Dutzan, N., & Abusleme, L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-28524-1_9 · Cited by 60
Lähteenmäki, H., Umeizudike, K. A., Heikkinen, A. M., Räisänen, I. T., Rathnayake, N., Johannsen, G., Tervahartiala, T. I., Nwhator, S. O., & Sorsa, T. A. (2020) · Diagnostics · doi:10.3390/diagnostics10080562 · Cited by 58
“For example, the inflamed periodontal tissues release pro-inflammatory cytokines and tissue destruction mediators into the circulation system increasing the systemic inflammatory burden [31].”
BackgroundThe relationship between gastrointestinal cancers and the microbiota
LaCourse, K. D., Johnston, C. D., & Bullman, S. (2021) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(20)30362-9 · Cited by 58
Gualtero, D. F., Lafaurie, G. I., Buitrago, D. M., Castillo, Y., Sanchez, P. K. V., & Castillo, D. M. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1250263 · Cited by 62
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Li, H., Deng, Y., Tan, M., Feng, G., Kuang, Y., Li, J., & Song, J. (2020) · Stem Cell Research & Therapy · doi:10.1186/s13287-020-01732-5 · Cited by 56
Oral health and changes in lipid profile: A nationwide cohort study
Song, T., Kim, J., & Kim, J. (2020) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13373 · Cited by 56
Dannewitz, B., Sommerer, C., Stölzel, P., Baid‐Agrawal, S., Nadal, J., Bärthlein, B., Wanner, C., Eckardt, K., Zeier, M. G., Schlagenhauf, U., et al. (2019) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13208 · Cited by 55
Mental Disorders and Oral Diseases: Future Research Directions
Joury, E., Kisely, S. R., Watt, R. G., Ahmed, N., Morris, A. J., Fortune, F., & Bhui, K. S. (2022) · Journal of Dental Research · doi:10.1177/00220345221120510 · Cited by 59
Shahoumi, L. A., Saleh, M. H. A., & Meghil, M. M. (2023) · Microorganisms · doi:10.3390/microorganisms11010115 · Cited by 59
Shi, T., Wang, J., Dong, J., Hu, P., & Guo, Q. (2023) · Pathogens · doi:10.3390/pathogens12091110 · Cited by 55
Oral microbiome in human health and diseases
Tian, S., Ding, T., & Li, H. (2024) · mLife · doi:10.1002/mlf2.12136 · Cited by 65
“Evidence suggests that perio-dontitis can lead to immune system dysfunction and increase the incidence of other diseases, such as chronic obstructive pulmonary disease 141 , gastric cancer, pancreatic cancer 116 , and diabetes 77,98 .”
BackgroundSun, J., Li, D., Dong, Y., Zhu, C., Liu, J. Y., Li, J., Zhou, T., Gou, J., Li, A., & Zang, W. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.04.012 · Cited by 55
Zhu, B., Macleod, L. C., Newsome, E., Liu, J., & Xu, P. (2019) · Scientific Reports · doi:10.1038/s41598-019-41467-9 · Cited by 55
Palioto, D. B., Finoti, L. S., Kinane, D. F., & Benakanakere, M. R. (2019) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.13151 · Cited by 64
Malan‐Müller, S., Vidal, R., O’Shea, E., Montero, E., Figuero, E., Zorrilla, E. P., de Diego-Adeliño, J., Cano, M., García‐Portilla, M. P., González-Pinto, A. M., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-03122-4 · Cited by 56
“Periodontitis, a chronic bacterial infection affecting nearly half the global population [15], triggers systemic in fl ammation through pro-in fl ammatory cytokine release and invasion by periodontal keystone pathogens like Porphyromonas gingivalis ( P. gingivalis ) [16].”
Background
Metadata
- Authors
- Hajishengallis, G.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Hajishengallis, George
- Venue
- Nature Reviews Immunology
- Published
- 2014-12-23
- Volume
- 15
- Issue
- 1
- Pages
- 30-44
- ISSN
- 1474-1733 (ISSN-L)
- 1474-1741
- 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
- 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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