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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Review Article

Subversion of the Oral Microbiota and Induction of Immune-Mediated Systemic Inflammation with Special Reference to Periodontitis: Current Knowledge and Perspectives

Author(s): Luigi Santacroce*, Eleonora Lo Muzio*, Lucrezia Bottalico, Francesca Spirito, Ioannis Alexandros Charitos, Pier Carmine Passarelli and Emilio Jirillo

Volume 23, Issue 4, 2023

Published on: 27 October, 2022

Page: [470 - 484] Pages: 15

DOI: 10.2174/1871530322666220629101357

Price: $65

Abstract

Under steady-state circumstances, the oral microbiota is in equilibrium with host tissues, thus contributing to local and systemic health. Any interruption of such equilibrium leads to a condition of dysbiosis with the proliferation of oral pathogens able to cause gingivitis and periodontal disease. The mechanisms of periodontitis will be described, mostly emphasizing the noxious effects exerted by oral pathogens on the periodontium either directly or indirectly via the release of an array of mediators, even including pro-inflammatory cytokines, chemokines, and enzymes. The persistence of local inflammation ultimately leads to systemic inflammation; therefore, the link between periodontitis and obesity, diabetes and cardiovascular disease will be elucidated. Some natural compounds, such as polyphenols, prebiotics, and probiotics, will be discussed for their ability to exert anti-inflammatory and anti-oxidant activities in the context of the inflamed buccal cavity and systemically, as well as for their modulation of the altered gum-gut microbiota.

Keywords: Inflammation, Immunity, Microbiota, Natural Products, Oral Cavity, Periodontitis, Gut/mouth axis

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[1]
Weyrich, L.S. The evolutionary history of the human oral microbiota and its implications for modern health. Periodontol. 2000, 2021, 85(1), 90-100.
[http://dx.doi.org/10.1111/prd.12353] [PMID: 33226710]
[2]
Baker, J.L.; Bor, B.; Agnello, M.; Shi, W.; He, X. Ecology of the oral microbiome: Beyond bacteria. Trends Microbiol., 2017, 25(5), 362-374.
[http://dx.doi.org/10.1016/j.tim.2016.12.012] [PMID: 28089325]
[3]
Sedghi, L.; DiMassa, V.; Harrington, A.; Lynch, S.V.; Kapila, Y.L. The oral microbiome: Role of key organisms and complex networks in oral health and disease. Periodontol. 2000, 2021, 87(1), 107-131.
[http://dx.doi.org/10.1111/prd.12393] [PMID: 34463991]
[4]
Santacroce, L. Comment on “Could health only be defined by an equilibrated microbiome? A COVID-19 reappraisal” by P. Charlier. Ethics Med. Public Health, 2021, 19, 100720.
[http://dx.doi.org/10.1016/j.jemep.2021.100720]
[5]
Seneviratne, C.J.; Balan, P.; Suriyanarayanan, T.; Lakshmanan, M.; Lee, D.Y.; Rho, M.; Jakubovics, N.; Brandt, B.; Crielaard, W.; Zaura, E. Oral microbiome-systemic link studies: Perspectives on current limitations and future artificial intelligence-based approaches. Crit. Rev. Microbiol., 2020, 46(3), 288-299.
[http://dx.doi.org/10.1080/1040841X.2020.1766414] [PMID: 32434436]
[6]
Perez-Muñoz, M.E.; Arrieta, M.C.; Ramer-Tait, A.E.; Walter, J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: Implications for research on the pioneer infant microbiome. Microbiome, 2017, 5(1), 48.
[http://dx.doi.org/10.1186/s40168-017-0268-4]
[7]
Aagaard, K.; Ma, J.; Antony, K.M.; Ganu, R.; Petrosino, J.; Versalovic, J. The placenta harbors a unique microbiome. Sci. Transl. Med., 2014, 6(237), 237ra65.
[http://dx.doi.org/10.1126/scitranslmed.3008599] [PMID: 24848255]
[8]
Tuominen, H.; Collado, M.C.; Rautava, J.; Syrjänen, S.; Rautava, S. Composition and maternal origin of the neonatal oral cavity microbiota. J. Oral Microbiol., 2019, 11(1), 1663084.
[http://dx.doi.org/10.1080/20002297.2019.1663084] [PMID: 31528268]
[9]
Cobb, C.M.; Kelly, P.J.; Williams, K.B.; Babbar, S.; Angolkar, M.; Derman, R.J. The oral microbiome and adverse pregnancy outcomes. Int. J. Womens Health, 2017, 9, 551-559.
[http://dx.doi.org/10.2147/IJWH.S142730] [PMID: 28848365]
[10]
Northridge, M.E.; Kumar, A.; Kaur, R. Disparities in access to oral health care. Annu. Rev. Public Health, 2020, 41, 513-535.
[http://dx.doi.org/10.1146/annurev-publhealth-040119-094318] [PMID: 31900100]
[11]
Vander Haar, E.L.; So, J.; Gyamfi-Bannerman, C.; Han, Y.W. Fusobacterium nucleatum and adverse pregnancy outcomes: Epidemiological and mechanistic evidence. Anaerobe, 2018, 50, 55-59.
[http://dx.doi.org/10.1016/j.anaerobe.2018.01.008] [PMID: 29409815]
[12]
Nelson-Filho, P.; Borba, I.G.; Mesquita, K.S.; Silva, R.A.; Queiroz, A.M.; Silva, L.A. Dynamics of microbial colonization of the oral cavity in newborns. Braz. Dent. J., 2013, 24(4), 415-419.
[http://dx.doi.org/10.1590/0103-6440201302266] [PMID: 24173267]
[13]
Könönen, E. Development of oral bacterial flora in young children. Ann. Med., 2000, 32(2), 107-112.
[http://dx.doi.org/10.3109/07853890009011759] [PMID: 10766401]
[14]
Li, W.; Ma, Z.S. FBA ecological guild: Trio of firmicutes-bacteroidetes alliance against actinobacteria in human oral microbiome. Sci. Rep., 2020, 10(1), 287.
[http://dx.doi.org/10.1038/s41598-019-56561-1] [PMID: 31937838]
[15]
Mason, M.R.; Chambers, S.; Dabdoub, S.M.; Thikkurissy, S.; Kumar, P.S. Characterizing oral microbial communities across dentition states and colonization niches. Microbiome, 2018, 6(1), 67.
[http://dx.doi.org/10.1186/s40168-018-0443-2] [PMID: 29631628]
[16]
Boix-Amorós, A.; Collado, M.C.; Mira, A. Relationship between milk microbiota, bacterial load, macronutrients, and human cells during lactation. Front. Microbiol., 2016, 7, 492.
[http://dx.doi.org/10.3389/fmicb.2016.00492] [PMID: 27148183]
[17]
Sampaio-Maia, B.; Monteiro-Silva, F. Acquisition and maturation of oral microbiome throughout childhood: An update. Dent. Res. J. (Isfahan), 2014, 11(3), 291-301.
[PMID: 25097637]
[18]
Yost, S.; Stashenko, P.; Choi, Y.; Kukuruzinska, M.; Genco, C.A.; Salama, A.; Weinberg, E.O.; Kramer, C.D.; Frias-Lopez, J. Increased virulence of the oral microbiome in oral squamous cell carcinoma revealed by metatranscriptome analyses. Int. J. Oral Sci., 2018, 10(4), 32.
[http://dx.doi.org/10.1038/s41368-018-0037-7] [PMID: 30420594]
[19]
Li, K.; Bihan, M.; Methé, B.A. Analyses of the stability and core taxonomic memberships of the human microbiome. PLoS One, 2013, 8(5), e63139.
[http://dx.doi.org/10.1371/journal.pone.0063139] [PMID: 23671663]
[20]
Van Hoogmoed, C.G.; Geertsema-Doornbusch, G.I.; Teughels, W.; Quirynen, M.; Busscher, H.J.; Van der Mei, H.C. Reduction of periodontal pathogens adhesion by antagonistic strains. Oral Microbiol. Immunol., 2008, 23(1), 43-48.
[http://dx.doi.org/10.1111/j.1399-302X.2007.00388.x] [PMID: 18173797]
[21]
Wu, J.; Xie, H. Role of arginine deiminase of Streptococcus cristatus in Porphyromonas gingivalis colonization. Antimicrob. Agents Chemother., 2010, 54(11), 4694-4698.
[http://dx.doi.org/10.1128/AAC.00284-10] [PMID: 20660674]
[22]
Lin, D.; Yang, L.; Wen, L.; Lu, H.; Chen, Q.; Wang, Z. Crosstalk between the oral microbiota, mucosal immunity, and the epithelial barrier regulates oral mucosal disease pathogenesis. Mucosal Immunol., 2021, 14(6), 1247-1258.
[http://dx.doi.org/10.1038/s41385-021-00413-7] [PMID: 34040155]
[23]
Kamarajan, P.; Hayami, T.; Matte, B.; Liu, Y.; Danciu, T.; Ramamoorthy, A.; Worden, F.; Kapila, S.; Kapila, Y. Nisin ZP, a bacteriocin and food preservative, inhibits head and neck cancer tumorigenesis and prolongs survival. PLoS One, 2015, 10(7), e0131008.
[http://dx.doi.org/10.1371/journal.pone.0131008] [PMID: 26132406]
[24]
Shin, J.M.; Gwak, J.W.; Kamarajan, P.; Fenno, J.C.; Rickard, A.H.; Kapila, Y.L. Biomedical applications of nisin. J. Appl. Microbiol., 2016, 120(6), 1449-1465.
[http://dx.doi.org/10.1111/jam.13033] [PMID: 26678028]
[25]
Bondonno, C.P.; Liu, A.H.; Croft, K.D.; Considine, M.J.; Puddey, I.B.; Woodman, R.J.; Hodgson, J.M. Antibacterial mouthwash blunts oral nitrate reduction and increases blood pressure in treated hypertensive men and women. Am. J. Hypertens., 2015, 28(5), 572-575.
[http://dx.doi.org/10.1093/ajh/hpu192] [PMID: 25359409]
[26]
Koch, C.D.; Gladwin, M.T.; Freeman, B.A.; Lundberg, J.O.; Weitzberg, E.; Morris, A. Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health. Free Radic. Biol. Med., 2017, 105, 48-67.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.12.015] [PMID: 27989792]
[27]
Senneby, A.; Davies, J.R.; Svensäter, G.; Neilands, J. Acid tolerance properties of dental biofilms in vivo. BMC Microbiol., 2017, 17(1), 165.
[http://dx.doi.org/10.1186/s12866-017-1074-7] [PMID: 28743239]
[28]
Chapple, I.L. Potential mechanisms underpinning the nutritional modulation of periodontal inflammation. J. Am. Dent. Assoc., 2009, 140(2), 178-184.
[http://dx.doi.org/10.14219/jada.archive.2009.0131] [PMID: 19188414]
[29]
Wu, J.; Peters, B.A.; Dominianni, C.; Zhang, Y.; Pei, Z.; Yang, L.; Ma, Y.; Purdue, M.P.; Jacobs, E.J.; Gapstur, S.M.; Li, H.; Alekseyenko, A.V.; Hayes, R.B.; Ahn, J. Cigarette smoking and the oral microbiome in a large study of American adults. ISME J., 2016, 10(10), 2435-2446.
[http://dx.doi.org/10.1038/ismej.2016.37] [PMID: 27015003]
[30]
Pitiphat, W.; Merchant, A.T.; Rimm, E.B.; Joshipura, K.J. Alcohol consumption increases periodontitis risk. J. Dent. Res., 2003, 82(7), 509-513.
[http://dx.doi.org/10.1177/154405910308200704] [PMID: 12821709]
[31]
Schirinzi, A.; Cazzolla, A.P.; Lovero, R.; Lo Muzio, L.; Testa, N.F.; Ciavarella, D.; Palmieri, G.; Pozzessere, P.; Procacci, V.; Di Serio, F.; Santacroce, L. New insights in laboratory testing for COVID-19 patients: Looking for the role and predictive value of human epididymis secretory protein 4 (HE4) and the innate immunity of the oral cavity and respiratory tract. Microorganisms, 2020, 8(11), 1718.
[http://dx.doi.org/10.3390/microorganisms8111718] [PMID: 33147871]
[32]
Rowińska, I.; Szyperska-Ślaska, A.; Zariczny, P.; Pasławski, R.; Kramkowski, K.; Kowalczyk, P. The influence of diet on oxidative stress and inflammation induced by bacterial biofilms in the human oral cavity. Materials (Basel), 2021, 14(6), 1444.
[http://dx.doi.org/10.3390/ma14061444] [PMID: 33809616]
[33]
Cugini, C.; Shanmugam, M.; Landge, N.; Ramasubbu, N. The role of exopolysaccharides in oral biofilms. J. Dent. Res., 2019, 98(7), 739-745.
[http://dx.doi.org/10.1177/0022034519845001] [PMID: 31009580]
[34]
Koo, H.; Xiao, J.; Klein, M.I.; Jeon, J.G. Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J. Bacteriol., 2010, 192(12), 3024-3032.
[http://dx.doi.org/10.1128/JB.01649-09] [PMID: 20233920]
[35]
Bowen, W.H.; Koo, H. Biology of Streptococcus mutans-derived glucosyltransferases: Role in extracellular matrix formation of cariogenic biofilms. Caries Res., 2011, 45(1), 69-86.
[http://dx.doi.org/10.1159/000324598] [PMID: 21346355]
[36]
Hajishengallis, G.; Lamont, R.J. Beyond the red complex and into more complexity: The Polymicrobial Synergy and Dysbiosis (PSD) model of periodontal disease etiology. Mol. Oral Microbiol., 2012, 27(6), 409-419.
[http://dx.doi.org/10.1111/j.2041-1014.2012.00663.x] [PMID: 23134607]
[37]
Hajishengallis, G.; Chavakis, T. Local and systemic mechanisms linking periodontal disease and inflammatory comorbidities. Nat. Rev. Immunol., 2021, 21(7), 426-440.
[http://dx.doi.org/10.1038/s41577-020-00488-6] [PMID: 33510490]
[38]
Hajishengallis, G. Periodontitis: From microbial immune subversion to systemic inflammation. Nat. Rev. Immunol., 2015, 15(1), 30-44.
[http://dx.doi.org/10.1038/nri3785] [PMID: 25534621]
[39]
Marsh, P.D. Dental plaque: Biological significance of a biofilm and community life-style. J. Clin. Periodontol., 2005, 32(Suppl. 6), 7-15.
[http://dx.doi.org/10.1111/j.1600-051X.2005.00790.x] [PMID: 16128825]
[40]
Scheres, N.; Crielaard, W. Gingival fibroblast responsiveness is differentially affected by Porphyromonas gingivalis: Implications for the pathogenesis of periodontitis. Mol. Oral Microbiol., 2013, 28(3), 204-218.
[http://dx.doi.org/10.1111/omi.12016] [PMID: 23279858]
[41]
White, D. J. Dental calculus: Recent insights into occurrence, formation, prevention, removal and oral health effects of supragingival and subgingival deposits. Eur. J. Oral Sci., 1997, 105(5 Pt 2), 508-522.
[http://dx.doi.org/10.1111/j.1600-0722.1997.tb00238.x] [PMID: 9395117]
[42]
Jin, Y.; Yip, H.K. Supragingival calculus: Formation and control. Crit. Rev. Oral Biol. Med., 2002, 13(5), 426-441.
[http://dx.doi.org/10.1177/154411130201300506] [PMID: 12393761]
[43]
Roberts-Harry, E.A.; Clerehugh, V. Subgingival calculus: Where are we now? A comparative review. J. Dent., 2000, 28(2), 93-102.
[http://dx.doi.org/10.1016/S0300-5712(99)00056-1] [PMID: 10666966]
[44]
Hajishengallis, G.; Liang, S.; Payne, M.A.; Hashim, A.; Jotwani, R.; Eskan, M.A.; McIntosh, M.L.; Alsam, A.; Kirkwood, K.L.; Lambris, J.D.; Darveau, R.P.; Curtis, M.A. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe, 2011, 10(5), 497-506.
[http://dx.doi.org/10.1016/j.chom.2011.10.006] [PMID: 22036469]
[45]
Meghil, M.M.; Cutler, C.W. Oral microbes and mucosal dendritic cells, “Spark and Flame” of local and distant inflammatory diseases. Int. J. Mol. Sci., 2020, 21(5), 1643.
[http://dx.doi.org/10.3390/ijms21051643] [PMID: 32121251]
[46]
Carrion, J.; Scisci, E.; Miles, B.; Sabino, G.J.; Zeituni, A.E.; Gu, Y.; Bear, A.; Genco, C.A.; Brown, D.L.; Cutler, C.W. Microbial carriage state of peripheral blood Dendritic Cells (DCs) in chronic periodontitis influences DC differentiation, atherogenic potential. J. Immunol., 2012, 189(6), 3178-3187.
[http://dx.doi.org/10.4049/jimmunol.1201053] [PMID: 22891282]
[47]
Miles, B.; Zakhary, I.; El-Awady, A.; Scisci, E.; Carrion, J.; O’Neill, J.C.; Rawlings, A.; Stern, J.K.; Susin, C.; Cutler, C.W. Secondary lymphoid organ homing phenotype of human myeloid dendritic cells disrupted by an intracellular oral pathogen. Infect. Immun., 2014, 82(1), 101-111.
[http://dx.doi.org/10.1128/IAI.01157-13] [PMID: 24126519]
[48]
Gui, T.; Burgering, B.M.T. FOXOs: Masters of the equilibrium. FEBS J., 2021.
[http://dx.doi.org/10.1111/febs.16221] [PMID: 34610198]
[49]
Meghil, M.M.; Tawfik, O.K.; Elashiry, M.; Rajendran, M.; Arce, R.M.; Fulton, D.J.; Schoenlein, P.V.; Cutler, C.W. Disruption of immune homeostasis in human dendritic cells via regulation of autophagy and apoptosis by Porphyromonas gingivalis. Front. Immunol., 2019, 10, 2286.
[http://dx.doi.org/10.3389/fimmu.2019.02286] [PMID: 31608069]
[50]
Mangini, F.; Santacroce, L.; Bottalico, L. Periodontitis and systemic diseases. Clin. Ter., 2006, 157(6), 541-548.
[PMID: 17228854]
[51]
Santacroce, L.; Man, A.; Charitos, I.A.; Haxhirexha, K.; Topi, S. Current knowledge about the connection between health status and gut microbiota from birth to elderly. A narrative review. Front. Biosci., 2021, 26(6), 135-148.
[http://dx.doi.org/10.52586/4930] [PMID: 34162042]
[52]
Bottalico, L.; Tatullo, M.; Marrelli, M.; Santacroce, L. Lights and shadows of dental implants: Focus on mucositis and perimplantitis and their biological markers. J. Biol. Regul. Homeost. Agents, 2016, 30(3), 859-861.
[PMID: 27655511]
[53]
Cullinan, M.P.; Seymour, G.J. Periodontal disease and systemic illness: Will the evidence ever be enough? Periodontol. 2000, 2013, 62(1), 271-286.
[http://dx.doi.org/10.1111/prd.12007] [PMID: 23574472]
[54]
Pihlstrom, B.L.; Hodges, J.S.; Michalowicz, B.; Wohlfahrt, J.C.; Garcia, R.I. Promoting oral health care because of its possible effect on systemic disease is premature and may be misleading. J. Am. Dent. Assoc., 2018, 149(6), 401-403.
[http://dx.doi.org/10.1016/j.adaj.2018.03.030] [PMID: 29804570]
[55]
Isacco, C.G.; Ballini, A.; De Vito, D.; Nguyen, K.C.D.; Cantore, S.; Bottalico, L.; Quagliuolo, L.; Boccellino, M.; Di Domenico, M.; Santacroce, L.; Arrigoni, R.; Dipalma, G.; Inchingolo, F. Rebalancing the oral microbiota as an efficient tool in endocrine, metabolic and immune disorders. Endocr. Metab. Immune Disord. Drug Targets, 2021, 21(5), 777-784.
[http://dx.doi.org/10.2174/1871530320666200729142504] [PMID: 32727337]
[56]
Byrd, K.M.; Gulati, A.S. The “Gum-Gut” axis in inflammatory bowel diseases: A hypothesis-driven review of associations and advances. Front. Immunol., 2021, 12, 620124.
[http://dx.doi.org/10.3389/fimmu.2021.620124] [PMID: 33679761]
[57]
Mall, A.S.; Habte, H.; Mthembu, Y.; Peacocke, J.; de Beer, C. Mucus and Mucins: do they have a role in the inhibition of the human immunodeficiency virus? Virol. J., 2017, 14(1), 192.
[http://dx.doi.org/10.1186/s12985-017-0855-9] [PMID: 28985745]
[58]
Arimatsu, K.; Yamada, H.; Miyazawa, H.; Minagawa, T.; Nakajima, M.; Ryder, M.I.; Gotoh, K.; Motooka, D.; Nakamura, S.; Iida, T.; Yamazaki, K. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci. Rep., 2014, 4, 4828.
[http://dx.doi.org/10.1038/srep04828] [PMID: 24797416]
[59]
Kitamoto, S.; Nagao-Kitamoto, H.; Hein, R.; Schmidt, T.M.; Kamada, N. The bacterial connection between the oral cavity and the gut diseases. J. Dent. Res., 2020, 99(9), 1021-1029.
[http://dx.doi.org/10.1177/0022034520924633] [PMID: 32464078]
[60]
Dinakaran, V.; Mandape, S.N.; Shuba, K.; Pratap, S.; Sakhare, S.S.; Tabatabai, M.A.; Smoot, D.T.; Farmer-Dixon, C.M.; Kesavalu, L.N.; Adunyah, S.E.; Southerland, J.H.; Gangula, P.R. Identification of specific oral and gut pathogens in full thickness colon of colitis patients: Implications for colon motility. Front. Microbiol., 2019, 9, 3220.
[http://dx.doi.org/10.3389/fmicb.2018.03220] [PMID: 30666239]
[61]
Oz, H.S.; Chen, T.; Ebersole, J.L. A model for chronic mucosal inflammation in IBD and periodontitis. Dig. Dis. Sci., 2010, 55(8), 2194-2202.
[http://dx.doi.org/10.1007/s10620-009-1031-x] [PMID: 19902356]
[62]
Pietropaoli, D.; Del Pinto, R.; Corridoni, D.; Rodriguez-Palacios, A.; Di Stefano, G.; Monaco, A.; Weinberg, A.; Cominelli, F. Occurrence of spontaneous periodontal disease in the SAMP1/YitFc murine model of Crohn disease. J. Periodontol., 2014, 85(12), 1799-1805.
[http://dx.doi.org/10.1902/jop.2014.140316] [PMID: 25019175]
[63]
Atarashi, K.; Suda, W.; Luo, C.; Kawaguchi, T.; Motoo, I.; Narushima, S.; Kiguchi, Y.; Yasuma, K.; Watanabe, E.; Tanoue, T.; Thaiss, C.A.; Sato, M.; Toyooka, K.; Said, H.S.; Yamagami, H.; Rice, S.A.; Gevers, D.; Johnson, R.C.; Segre, J.A.; Chen, K.; Kolls, J.K.; Elinav, E.; Morita, H.; Xavier, R.J.; Hattori, M.; Honda, K. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation. Science, 2017, 358(6361), 359-365.
[http://dx.doi.org/10.1126/science.aan4526] [PMID: 29051379]
[64]
Scribano, M.L. Vedolizumab for inflammatory bowel disease: From randomized controlled trials to real-life evidence. World J. Gastroenterol., 2018, 24(23), 2457-2467.
[http://dx.doi.org/10.3748/wjg.v24.i23.2457] [PMID: 29930467]
[65]
Calderón-Gómez, E.; Bassolas-Molina, H.; Mora-Buch, R.; Dotti, I.; Planell, N.; Esteller, M.; Gallego, M.; Martí, M.; Garcia-Martín, C.; Martínez-Torró, C.; Ordás, I.; Singh, S.; Panés, J.; Benítez-Ribas, D.; Salas, A. Commensal-Specific CD4(+) cells from patients with Crohn’s disease have a T-Helper 17 inflammatory profile. Gastroenterology, 2016, 151(3), 489-500.e3.
[http://dx.doi.org/10.1053/j.gastro.2016.05.050] [PMID: 27267052]
[66]
Yachida, S.; Mizutani, S.; Shiroma, H.; Shiba, S.; Nakajima, T.; Sakamoto, T.; Watanabe, H.; Masuda, K.; Nishimoto, Y.; Kubo, M.; Hosoda, F.; Rokutan, H.; Matsumoto, M.; Takamaru, H.; Yamada, M.; Matsuda, T.; Iwasaki, M.; Yamaji, T.; Yachida, T.; Soga, T.; Kurokawa, K.; Toyoda, A.; Ogura, Y.; Hayashi, T.; Hatakeyama, M.; Nakagama, H.; Saito, Y.; Fukuda, S.; Shibata, T.; Yamada, T. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat. Med., 2019, 25(6), 968-976.
[http://dx.doi.org/10.1038/s41591-019-0458-7] [PMID: 31171880]
[67]
Thomas, A.M.; Manghi, P.; Asnicar, F.; Pasolli, E.; Armanini, F.; Zolfo, M.; Beghini, F.; Manara, S.; Karcher, N.; Pozzi, C.; Gandini, S.; Serrano, D.; Tarallo, S.; Francavilla, A.; Gallo, G.; Trompetto, M.; Ferrero, G.; Mizutani, S.; Shiroma, H.; Shiba, S.; Shibata, T.; Yachida, S.; Yamada, T.; Wirbel, J.; Schrotz-King, P.; Ulrich, C.M.; Brenner, H.; Arumugam, M.; Bork, P.; Zeller, G.; Cordero, F.; Dias-Neto, E.; Setubal, J.C.; Tett, A.; Pardini, B.; Rescigno, M.; Waldron, L.; Naccarati, A.; Segata, N. Metagenomic analysis of colorectal cancer datasets identifies cross-cohort microbial diagnostic signatures and a link with choline degradation. Nat. Med., 2019, 25(4), 667-678.
[http://dx.doi.org/10.1038/s41591-019-0405-7] [PMID: 30936548]
[68]
Kostic, A.D.; Chun, E.; Robertson, L.; Glickman, J.N.; Gallini, C.A.; Michaud, M.; Clancy, T.E.; Chung, D.C.; Lochhead, P.; Hold, G.L.; El-Omar, E.M.; Brenner, D.; Fuchs, C.S.; Meyerson, M.; Garrett, W.S. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe, 2013, 14(2), 207-215.
[http://dx.doi.org/10.1016/j.chom.2013.07.007] [PMID: 23954159]
[69]
Rubinstein, M.R.; Wang, X.; Liu, W.; Hao, Y.; Cai, G.; Han, Y.W. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe, 2013, 14(2), 195-206.
[http://dx.doi.org/10.1016/j.chom.2013.07.012] [PMID: 23954158]
[70]
Casasanta, M.A.; Yoo, C.C.; Udayasuryan, B.; Sanders, B.E.; Umaña, A.; Zhang, Y.; Peng, H.; Duncan, A.J.; Wang, Y.; Li, L.; Verbridge, S.S.; Slade, D.J. Fusobacterium nucleatum host-cell binding and invasion induces IL-8 and CXCL1 secretion that drives colorectal cancer cell migration. Sci. Signal., 2020, 13(641), eaba9157.
[http://dx.doi.org/10.1126/scisignal.aba9157] [PMID: 32694172]
[71]
Yu, T.; Guo, F.; Yu, Y.; Sun, T.; Ma, D.; Han, J.; Qian, Y.; Kryczek, I.; Sun, D.; Nagarsheth, N.; Chen, Y.; Chen, H.; Hong, J.; Zou, W.; Fang, J.Y. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell, 2017, 170(3), 548-563.e16.
[http://dx.doi.org/10.1016/j.cell.2017.07.008] [PMID: 28753429]
[72]
Abed, J.; Emgård, J.E.; Zamir, G.; Faroja, M.; Almogy, G.; Grenov, A.; Sol, A.; Naor, R.; Pikarsky, E.; Atlan, K.A.; Mellul, A.; Chaushu, S.; Manson, A.L.; Earl, A.M.; Ou, N.; Brennan, C.A.; Garrett, W.S.; Bachrach, G. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe, 2016, 20(2), 215-225.
[http://dx.doi.org/10.1016/j.chom.2016.07.006] [PMID: 27512904]
[73]
Rubinstein, M.R.; Baik, J.E.; Lagana, S.M.; Han, R.P.; Raab, W.J.; Sahoo, D.; Dalerba, P.; Wang, T.C.; Han, Y.W. Fusobacterium nucleatum promotes colorectal cancer by inducing Wnt/β-catenin modulator Annexin A1. EMBO Rep., 2019, 20(4), e47638.
[http://dx.doi.org/10.15252/embr.201847638] [PMID: 30833345]
[74]
Gur, C.; Ibrahim, Y.; Isaacson, B.; Yamin, R.; Abed, J.; Gamliel, M.; Enk, J.; Bar-On, Y.; Stanietsky-Kaynan, N.; Coppenhagen-Glazer, S.; Shussman, N.; Almogy, G.; Cuapio, A.; Hofer, E.; Mevorach, D.; Tabib, A.; Ortenberg, R.; Markel, G.; Miklić, K.; Jonjic, S.; Brennan, C.A.; Garrett, W.S.; Bachrach, G.; Mandelboim, O. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity, 2015, 42(2), 344-355.
[http://dx.doi.org/10.1016/j.immuni.2015.01.010] [PMID: 25680274]
[75]
Nakarai, H.; Yamashita, A.; Nagayasu, S.; Iwashita, M.; Kumamoto, S.; Ohyama, H.; Hata, M.; Soga, Y.; Kushiyama, A.; Asano, T.; Abiko, Y.; Nishimura, F. Adipocyte-macrophage interaction may mediate LPS-induced low-grade inflammation: Potential link with metabolic complications. Innate Immun., 2012, 18(1), 164-170.
[http://dx.doi.org/10.1177/1753425910393370] [PMID: 21239459]
[76]
Ballini, A.; Cantore, S.; Dedola, A.; Santacroce, L.; Laino, L.; Cicciù, M.; Mastrangelo, F. IL-1 haplotype analysis in periodontal disease. J. Biol. Regul. Homeost. Agents, 2018, 32(2), 433-437.
[PMID: 29577711]
[77]
Rojas, C.; García, M.P.; Polanco, A.F.; González-Osuna, L.; Sierra-Cristancho, A.; Melgar-Rodríguez, S.; Cafferata, E.A.; Vernal, R. Humanized mouse models for the study of periodontitis: An opportunity to elucidate unresolved aspects of its immunopathogenesis and analyze new immunotherapeutic strategies. Front. Immunol., 2021, 12, 663328.
[http://dx.doi.org/10.3389/fimmu.2021.663328] [PMID: 34220811]
[78]
Hatasa, M.; Ohsugi, Y.; Katagiri, S.; Yoshida, S.; Niimi, H.; Morita, K.; Tsuchiya, Y.; Shimohira, T.; Sasaki, N.; Maekawa, S.; Shiba, T.; Hirota, T.; Tohara, H.; Takahashi, H.; Nitta, H.; Iwata, T. Endotoxemia by Porphyromonas gingivalis alters endocrine functions in brown adipose tissue. Front. Cell. Infect. Microbiol., 2021, 10, 580577.
[http://dx.doi.org/10.3389/fcimb.2020.580577] [PMID: 33542905]
[79]
Aoyama, N.; Fujii, T.; Kida, S.; Nozawa, I.; Taniguchi, K.; Fujiwara, M.; Iwane, T.; Tamaki, K.; Minabe, M. Association of periodontal status, number of teeth, and obesity: A cross-sectional study in Japan. J. Clin. Med., 2021, 10(2), 208.
[http://dx.doi.org/10.3390/jcm10020208] [PMID: 33435628]
[80]
Santacroce, L.; Monea, A.; Marrelli, M.; Man, A. Oral candidiasis and inflammatory response: A potential synergic contribution to the onset of type-2 diabetes mellitus. Australas. Med. J., 2017, 10, 550-556.
[http://dx.doi.org/10.21767/AMJ.2017.3053]
[81]
Guzman, S.; Karima, M.; Wang, H.Y.; Van Dyke, T.E. Association between interleukin-1 genotype and periodontal disease in a diabetic population. J. Periodontol., 2003, 74(8), 1183-1190.
[http://dx.doi.org/10.1902/jop.2003.74.8.1183] [PMID: 14514232]
[82]
Zheng, J.; Chen, S.; Albiero, M.L.; Vieira, G.H.A.; Wang, J.; Feng, J.Q.; Graves, D.T. Diabetes activates periodontal ligament fibroblasts via NF-κB in vivo. J. Dent. Res., 2018, 97(5), 580-588.
[http://dx.doi.org/10.1177/0022034518755697] [PMID: 29439598]
[83]
Wu, Y.Y.; Xiao, E.; Graves, D.T. Diabetes mellitus related bone metabolism and periodontal disease. Int. J. Oral Sci., 2015, 7(2), 63-72.
[http://dx.doi.org/10.1038/ijos.2015.2] [PMID: 25857702]
[84]
Santacroce, L.; Carlaio, R.G.; Bottalico, L. Does it make sense that diabetes is reciprocally associated with periodontal disease? Endocr. Metab. Immune Disord. Drug Targets, 2010, 10(1), 57-70.
[http://dx.doi.org/10.2174/187153010790827975] [PMID: 20001897]
[85]
Ohtsu, A.; Takeuchi, Y.; Katagiri, S.; Suda, W.; Maekawa, S.; Shiba, T.; Komazaki, R.; Udagawa, S.; Sasaki, N.; Hattori, M.; Izumi, Y. Influence of Porphyromonas gingivalis in gut microbiota of streptozotocin-induced diabetic mice. Oral Dis., 2019, 25(3), 868-880.
[http://dx.doi.org/10.1111/odi.13044] [PMID: 30667148]
[86]
Man, A.; Ciurea, C.N.; Pasaroiu, D.; Savin, A.I.; Toma, F.; Sular, F.; Santacroce, L.; Mare, A. New perspectives on the nutritional factors influencing growth rate of Candida albicans in diabetics. An in vitro study. Mem. Inst. Oswaldo Cruz, 2017, 112(9), 587-592.
[http://dx.doi.org/10.1590/0074-02760170098] [PMID: 28902283]
[87]
Seyama, M.; Yoshida, K.; Yoshida, K.; Fujiwara, N.; Ono, K.; Eguchi, T.; Kawai, H.; Guo, J.; Weng, Y.; Haoze, Y.; Uchibe, K.; Ikegame, M.; Sasaki, A.; Nagatsuka, H.; Okamoto, K.; Okamura, H.; Ozaki, K. Outer membrane vesicles of Porphyromonas gingivalis attenuate insulin sensitivity by delivering gingipains to the liver. Biochim. Biophys. Acta Mol. Basis Dis., 2020, 1866(6), 165731.
[http://dx.doi.org/10.1016/j.bbadis.2020.165731] [PMID: 32088316]
[88]
D’Aiuto, F.; Gkranias, N.; Bhowruth, D.; Khan, T.; Orlandi, M.; Suvan, J.; Masi, S.; Tsakos, G.; Hurel, S.; Hingorani, A.D.; Donos, N.; Deanfield, J.E. Systemic effects of periodontitis treatment in patients with type 2 diabetes: A 12 month, single-centre, investigator-masked, randomised trial. Lancet Diabetes Endocrinol., 2018, 6(12), 954-965.
[http://dx.doi.org/10.1016/S2213-8587(18)30038-X] [PMID: 30472992]
[89]
Brito, L.C.; DalBó, S.; Striechen, T.M.; Farias, J.M.; Olchanheski, L.R., Jr; Mendes, R.T.; Vellosa, J.C.; Fávero, G.M.; Sordi, R.; Assreuy, J.; Santos, F.A.; Fernandes, D. Experimental periodontitis promotes transient vascular inflammation and endothelial dysfunction. Arch. Oral Biol., 2013, 58(9), 1187-1198.
[http://dx.doi.org/10.1016/j.archoralbio.2013.03.009] [PMID: 23583017]
[90]
Miyajima, S.; Naruse, K.; Kobayashi, Y.; Nakamura, N.; Nishikawa, T.; Adachi, K.; Suzuki, Y.; Kikuchi, T.; Mitani, A.; Mizutani, M.; Ohno, N.; Noguchi, T.; Matsubara, T. Periodontitis-activated monocytes/macrophages cause aortic inflammation. Sci. Rep., 2014, 4, 5171.
[http://dx.doi.org/10.1038/srep05171] [PMID: 24893991]
[91]
Hasturk, H.; Abdallah, R.; Kantarci, A.; Nguyen, D.; Giordano, N.; Hamilton, J.; Van Dyke, T.E. Resolvin E1 (RvE1) attenuates atherosclerotic plaque formation in diet and inflammation-induced atherogenesis. Arterioscler. Thromb. Vasc. Biol., 2015, 35(5), 1123-1133.
[http://dx.doi.org/10.1161/ATVBAHA.115.305324] [PMID: 25792445]
[92]
Farrugia, C.; Stafford, G.P.; Potempa, J.; Wilkinson, R.N.; Chen, Y.; Murdoch, C.; Widziolek, M. Mechanisms of vascular damage by systemic dissemination of the oral pathogen Porphyromonas gingivalis. FEBS J., 2021, 288(5), 1479-1495.
[http://dx.doi.org/10.1111/febs.15486] [PMID: 32681704]
[93]
Gimbrone, M.A., Jr; García-Cardeña, G. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ. Res., 2016, 118(4), 620-636.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.306301] [PMID: 26892962]
[94]
Dominy, S.S.; Lynch, C.; Ermini, F.; Benedyk, M.; Marczyk, A.; Konradi, A.; Nguyen, M.; Haditsch, U.; Raha, D.; Griffin, C.; Holsinger, L.J.; Arastu-Kapur, S.; Kaba, S.; Lee, A.; Ryder, M.I.; Potempa, B.; Mydel, P.; Hellvard, A.; Adamowicz, K.; Hasturk, H.; Walker, G.D.; Reynolds, E.C.; Faull, R.L.M.; Curtis, M.A.; Dragunow, M.; Potempa, J. Porphyromonas gingivalis in Alzheimer’s disease brains: Evidence for disease causation and treatment with small-molecule inhibitors. Sci. Adv., 2019, 5(1), eaau3333.
[http://dx.doi.org/10.1126/sciadv.aau3333] [PMID: 30746447]
[95]
Kovacech, B.; Novak, M. Tau truncation is a productive posttranslational modification of neurofibrillary degeneration in Alzheimer’s disease. Curr. Alzheimer Res., 2010, 7(8), 708-716.
[http://dx.doi.org/10.2174/156720510793611556] [PMID: 20678071]
[96]
Long, J.M.; Holtzman, D.M. Alzheimer Disease: An update on pathobiology and treatment strategies. Cell, 2019, 179(2), 312-339.
[http://dx.doi.org/10.1016/j.cell.2019.09.001] [PMID: 31564456]
[97]
Muñoz, S.S.; Garner, B.; Ooi, L. Understanding the role of ApoE fragments in Alzheimer’s disease. Neurochem. Res., 2019, 44(6), 1297-1305.
[http://dx.doi.org/10.1007/s11064-018-2629-1] [PMID: 30225748]
[98]
Lönn, J.; Ljunggren, S.; Klarström-Engström, K.; Demirel, I.; Bengtsson, T.; Karlsson, H. Lipoprotein modifications by gingipains of Porphyromonas gingivalis. J. Periodontal Res., 2018, 53(3), 403-413.
[http://dx.doi.org/10.1111/jre.12527] [PMID: 29341140]
[99]
Hashimoto, Y.; Kondo, C.; Katunuma, N. An active 32-kDa Cathepsin L is secreted directly from HT 1080 fibrosarcoma cells and not via lysosomal exocytosis. PLoS One, 2015, 10(12), e0145067.
[http://dx.doi.org/10.1371/journal.pone.0145067]
[100]
Maresz, K.J.; Hellvard, A.; Sroka, A.; Adamowicz, K.; Bielecka, E.; Koziel, J.; Gawron, K.; Mizgalska, D.; Marcinska, K.A.; Benedyk, M.; Pyrc, K.; Quirke, A.M.; Jonsson, R.; Alzabin, S.; Venables, P.J.; Nguyen, K.A.; Mydel, P.; Potempa, J. Porphyromonas gingivalis facilitates the development and progression of destructive arthritis through its unique bacterial peptidylarginine deiminase (PAD). PLoS Pathog., 2013, 9(9), e1003627.
[http://dx.doi.org/10.1371/journal.ppat.1003627] [PMID: 24068934]
[101]
Gully, N.; Bright, R.; Marino, V.; Marchant, C.; Cantley, M.; Haynes, D.; Butler, C.; Dashper, S.; Reynolds, E.; Bartold, M. Porphyromonas gingivalis peptidylarginine deiminase, a key contributor in the pathogenesis of experimental periodontal disease and experimental arthritis. PLoS One, 2014, 9(6), e100838.
[http://dx.doi.org/10.1371/journal.pone.0100838] [PMID: 24959715]
[102]
González-Febles, J.; Sanz, M. Periodontitis and rheumatoid arthritis: What have we learned about their connection and their treatment? Periodontol. 2000, 2021, 87(1), 181-203.
[http://dx.doi.org/10.1111/prd.12385] [PMID: 34463976]
[103]
Potempa, J.; Mydel, P.; Koziel, J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat. Rev. Rheumatol., 2017, 13(10), 606-620.
[http://dx.doi.org/10.1038/nrrheum.2017.132] [PMID: 28835673]
[104]
Konig, M.F.; Abusleme, L.; Reinholdt, J.; Palmer, R.J.; Teles, R.P.; Sampson, K.; Rosen, A.; Nigrovic, P.A.; Sokolove, J.; Giles, J.T.; Moutsopoulos, N.M.; Andrade, F. Aggregatibacter actinomycetemcomitans-induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis. Sci. Transl. Med., 2016, 8(369), 369ra176.
[http://dx.doi.org/10.1126/scitranslmed.aaj1921] [PMID: 27974664]
[105]
Wegner, N.; Wait, R.; Sroka, A.; Eick, S.; Nguyen, K.A.; Lundberg, K.; Kinloch, A.; Culshaw, S.; Potempa, J.; Venables, P.J. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum., 2010, 62(9), 2662-2672.
[http://dx.doi.org/10.1002/art.27552] [PMID: 20506214]
[106]
Mikuls, T.R.; Payne, J.B.; Yu, F.; Thiele, G.M.; Reynolds, R.J.; Cannon, G.W.; Markt, J.; McGowan, D.; Kerr, G.S.; Redman, R.S.; Reimold, A.; Griffiths, G.; Beatty, M.; Gonzalez, S.M.; Bergman, D.A.; Hamilton, B.C., III; Erickson, A.R.; Sokolove, J.; Robinson, W.H.; Walker, C.; Chandad, F.; O’Dell, J.R. Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol., 2014, 66(5), 1090-1100.
[http://dx.doi.org/10.1002/art.38348] [PMID: 24782175]
[107]
Lübcke, P.M.; Ebbers, M.N.B.; Volzke, J.; Bull, J.; Kneitz, S.; Engelmann, R.; Lang, H.; Kreikemeyer, B.; Müller-Hilke, B. Periodontal treatment prevents arthritis in mice and methotrexate ameliorates periodontal bone loss. Sci. Rep., 2019, 9(1), 8128.
[http://dx.doi.org/10.1038/s41598-019-44512-9] [PMID: 31148565]
[108]
Liu, S.; Liu, G.; Luan, Q.; Ma, Y.; Yu, X. Porphyromonas gingivalis lipopolysaccharide-induced B cell differentiation by toll-like receptors 2 and 4. Protein Pept. Lett., 2022, 29(1), 46-56.
[http://dx.doi.org/10.2174/0929866528666211118085828] [PMID: 34791999]
[109]
Goodson, J.M. Principles of pharmacologic intervention. J. Clin. Periodontol., 1996, 23(3 Pt 2), 268-272.
[http://dx.doi.org/10.1111/j.1600-051X.1996.tb02087.x] [PMID: 8707988]
[110]
Kornman, K.S. Refractory periodontitis: Critical questions in clinical management. J. Clin. Periodontol., 1996, 23(3 Pt 2), 293-298.
[http://dx.doi.org/10.1111/j.1600-051X.1996.tb02092.x] [PMID: 8707993]
[111]
Drisko, C.H. The use of locally delivered doxycycline in the treatment of periodontitis. Clinical results. J. Clin. Periodontol., 1998, 25(11 Pt 2), 947-952.
[http://dx.doi.org/10.1111/j.1600-051X.1998.tb02396.x] [PMID: 9839851]
[112]
Attia, M.S.; Alblowi, J.A. Effect of subantimicrobial dose doxycycline treatment on gingival crevicular fluid levels of MMP-9 and MMP-13 in periodontitis stage 2, grade B in subjects with type 2 diabetes mellitus. J. Immunol. Res., 2020, 2020, 2807259.
[http://dx.doi.org/10.1155/2020/2807259] [PMID: 33294463]
[113]
Sinha, S.; Kumar, S.; Dagli, N.; Dagli, R.J. Effect of tetracycline HCl in the treatment of chronic periodontitis-A clinical study. J. Int. Soc. Prev. Community Dent., 2014, 4(3), 149-153.
[http://dx.doi.org/10.4103/2231-0762.142011] [PMID: 25374831]
[114]
Leiknes, T.; Leknes, K.N.; Böe, O.E.; Skavland, R.J.; Lie, T. Topical use of a metronidazole gel in the treatment of sites with symptoms of recurring chronic inflammation. J. Periodontol., 2007, 78(8), 1538-1544.
[http://dx.doi.org/10.1902/jop.2007.060501] [PMID: 17668973]
[115]
Bai, Y.L.; Zheng, T.J.; Zhang, Z.W.; Gan, Y.; Huang, J. Efficacy of minocycline hydrochloride combined with flap surgery for chronic periodontitis: A meta-analysis. Hua Xi Kou Qiang Yi Xue Za Zhi, 2018, 36(4), 421-427.
[http://dx.doi.org/10.7518/hxkq.2018.04.013]
[116]
Mitali, R.; Sabyasachi, S.; Reddy, V.K.; Shafaat, M.; Kumari, M. Mouthwashes-an overview of current knowledge. Int. J. Oral Health Res. Rev., 2013, 1, 24-28.
[117]
Bescos, R.; Ashworth, A.; Cutler, C.; Brookes, Z.L.; Belfield, L.; Rodiles, A.; Casas-Agustench, P.; Farnham, G.; Liddle, L.; Burleigh, M.; White, D.; Easton, C.; Hickson, M. Effects of chlorhexidine mouthwash on the oral microbiome. Sci. Rep., 2020, 10(1), 5254.
[http://dx.doi.org/10.1038/s41598-020-61912-4] [PMID: 32210245]
[118]
Zanatta, F.B.; Antoniazzi, R.P.; Rösing, C.K. Staining and calculus formation after 0.12% chlorhexidine rinses in plaque-free and plaque covered surfaces: A randomized trial. J. Appl. Oral Sci., 2010, 18(5), 515-521.
[http://dx.doi.org/10.1590/S1678-77572010000500015] [PMID: 21085810]
[119]
Bacali, C.; Vulturar, R.; Buduru, S.; Cozma, A.; Fodor, A.; Chiș, A.; Lucaciu, O.; Damian, L.; Moldovan, M.L. Oral Microbiome: Getting to know and befriend neighbors, a biological approach. Biomedicines, 2022, 10(3), 671.
[http://dx.doi.org/10.3390/biomedicines10030671] [PMID: 35327473]
[120]
Obersztyn, A.; Kolwinski, K.; Trykowski, J.; Starosciak, S. Effects of stannous fluoride and amine fluorides on caries incidence and enamel solubility in adults. Aust. Dent. J., 1979, 24(6), 395-397.
[http://dx.doi.org/10.1111/j.1834-7819.1979.tb03633.x] [PMID: 295205]
[121]
Kruse, A.B.; Schlueter, N.; Kortmann, V.K.; Frese, C.; Anderson, A.; Wittmer, A.; Hellwig, E.; Vach, K.; Al-Ahmad, A. Long-term use of oral hygiene products containing stannous and fluoride ions: Effect on viable salivary bacteria. Antibiotics (Basel), 2021, 10(5), 481.
[http://dx.doi.org/10.3390/antibiotics10050481] [PMID: 33921981]
[122]
Yasuda, K.; Hsu, T.; Gallini, C.A.; Mclver, L.J.; Schwager, E.; Shi, A.; DuLong, C.R.; Schwager, R.N.; Abu-Ali, G.S.; Franzosa, E.A.; Garrett, W.S.; Huttenhower, C.; Morgan, X.C. Fluoride depletes acidogenic taxa in oral but not gut microbial communities in mice. mSystems, 2017, 2(4), e00047-e17.
[http://dx.doi.org/10.1128/mSystems.00047-17] [PMID: 28808691]
[123]
DePaola, L.G.; Minah, G.E.; Overholser, C.D.; Meiller, T.F.; Charles, C.H.; Harper, D.S.; McAlary, M. Effect of an antiseptic mouthrinse on salivary microbiota. Am. J. Dent., 1996, 9(3), 93-95.
[PMID: 9002796]
[124]
Courtois, P. Oral peroxidases: From antimicrobial agents to ecological actors (Review). Mol. Med. Rep., 2021, 24(1), 500.
[http://dx.doi.org/10.3892/mmr.2021.12139] [PMID: 33982776]
[125]
Gilbert, R.J.; Williams, P.E. The oral retention and antiplaque efficacy of triclosan in human volunteers. Br. J. Clin. Pharmacol., 1987, 23(5), 579-583.
[http://dx.doi.org/10.1111/j.1365-2125.1987.tb03094.x] [PMID: 3593627]
[126]
Tanomaru, J.M.; Nascimento, A.P.; Watanabe, E.; Matoba-Júnior, F.; Tanomaru-Filho, M.; Ito, I.Y. Antibacterial activity of four mouthrinses containing triclosan against salivary Staphylococcus aureus. Braz. J. Microbiol., 2008, 39(3), 569-572.
[http://dx.doi.org/10.1590/S1517-83822008000300030] [PMID: 24031267]
[127]
Rosling, B.; Dahlén, G.; Volpe, A.; Furuichi, Y.; Ramberg, P.; Lindhe, J. Effect of triclosan on the subgingival microbiota of periodontitis-susceptible subjects. J. Clin. Periodontol., 1997, 24(12), 881-887.
[http://dx.doi.org/10.1111/j.1600-051X.1997.tb01206.x] [PMID: 9442424]
[128]
Nagy-Bota, M.C.; Man, A.; Santacroce, L.; Brinzaniuc, K.; Pap, Z.; Pacurar, M.; Pribac, M.; Ciurea, C.N.; Pintea-Simon, I.A.; Kovacs, M. Essential oils as alternatives for root-canal treatment and infection control against Enterococcus faecalis-A preliminary study. Appl. Sci. (Basel), 2021, 11(4), 1422.
[http://dx.doi.org/10.3390/app11041422]
[129]
Vlachojannis, C.; Al-Ahmad, A.; Hellwig, E.; Chrubasik, S. Listerine® products: An update on the efficacy and safety. Phytother. Res., 2016, 30(3), 367-373.
[http://dx.doi.org/10.1002/ptr.5555] [PMID: 26931615]
[130]
Mombelli, A.; Samaranayake, L.P. Topical and systemic antibiotics in the management of periodontal diseases. Int. Dent. J., 2004, 54(1), 3-14.
[http://dx.doi.org/10.1111/j.1875-595X.2004.tb00246.x] [PMID: 15005467]
[131]
Stelzel, M.; Florès-de-Jacoby, L. Topical metronidazole application compared with subgingival scaling. A clinical and microbiological study on recall patients. J. Clin. Periodontol., 1996, 23(1), 24-29.
[http://dx.doi.org/10.1111/j.1600-051X.1996.tb00500.x] [PMID: 8636453]
[132]
Paquette, D.W. Minocycline microspheres: A complementary medical-mechanical model for the treatment of chronic periodontitis. Compend. Contin. Educ. Dent., 2002, 23(Suppl. 5), 15-21.
[PMID: 12789964]
[133]
Vandekerckhove, B.N.; Quirynen, M.; van Steenberghe, D. The use of tetracycline-containing controlled-release fibers in the treatment of refractory periodontitis. J. Periodontol., 1997, 68(4), 353-361.
[http://dx.doi.org/10.1902/jop.1997.68.4.353] [PMID: 9150040]
[134]
Blot, S. Antiseptic mouthwash, the nitrate-nitrite-nitric oxide pathway, and hospital mortality: A hypothesis generating review. Intensive Care Med., 2021, 47(1), 28-38.
[http://dx.doi.org/10.1007/s00134-020-06276-z] [PMID: 33067640]
[135]
Bruckdorfer, R. The basics about nitric oxide. Mol. Aspects Med., 2005, 26(1-2), 3-31.
[http://dx.doi.org/10.1016/j.mam.2004.09.002] [PMID: 15722113]
[136]
Brookes, Z.L.S.; Belfield, L.A.; Ashworth, A.; Casas-Agustench, P.; Raja, M.; Pollard, A.J.; Bescos, R. Effects of chlorhexidine mouthwash on the oral microbiome. J. Dent., 2021, 113, 103768.
[http://dx.doi.org/10.1016/j.jdent.2021.103768] [PMID: 34418463]
[137]
Venturelli, M.; Pedrinolla, A.; Boscolo Galazzo, I.; Fonte, C.; Smania, N.; Tamburin, S.; Muti, E.; Crispoltoni, L.; Stabile, A.; Pistilli, A.; Rende, M.; Pizzini, F.B.; Schena, F. Impact of nitric oxide bioavailability on the progressive cerebral and peripheral circulatory impairments during aging and Alzheimer’s Disease. Front. Physiol., 2018, 9, 169.
[http://dx.doi.org/10.3389/fphys.2018.00169] [PMID: 29593548]
[138]
Sharma, J.N.; Al-Omran, A.; Parvathy, S.S. Role of nitric oxide in inflammatory diseases. Inflammopharmacology, 2007, 15(6), 252-259.
[http://dx.doi.org/10.1007/s10787-007-0013-x] [PMID: 18236016]
[139]
Signorini, L.; Ballini, A.; Arrigoni, R.; De Leonardis, F.; Saini, R.; Cantore, S.; De Vito, D.; Coscia, M.F.; Dipalma, G.; Santacroce, L.; Inchingolo, F. Evaluation of a nutraceutical product with probiotics, Vitamin D, plus banaba leaf extracts (Lagerstroemia speciosa) in glycemic control. Endocr. Metab. Immune Disord. Drug Targets, 2021, 21(7), 1356-1365.
[http://dx.doi.org/10.2174/1871530320666201109115415] [PMID: 33167849]
[140]
Magrone, T.; Magrone, M.; Russo, M.A.; Jirillo, E. Recent advances on the anti-inflammatory and antioxidant properties of red grape polyphenols: In vitro and in vivo studies. Antioxidants, 2019, 9(1), 35.
[http://dx.doi.org/10.3390/antiox9010035] [PMID: 31906123]
[141]
Arrigoni, R.; Ballini, A.; Santacroce, L.; Cantore, S.; Inchingolo, A.; Inchingolo, F.; Di Domenico, M.; Quagliuolo, L.; Boccellino, M. Another look at dietary polyphenols: Challenges in cancer prevention and treatment. Curr. Med. Chem., 2022, 29(6), 1061-1082.
[http://dx.doi.org/10.2174/0929867328666210810154732] [PMID: 34375181]
[142]
Nawrot-Hadzik, I.; Matkowski, A.; Kubasiewicz-Ross, P.; Hadzik, J. Proanthocyanidins and Flavan-3-ols in the prevention and treatment of periodontitis-immunomodulatory effects, animal and clinical studies. Nutrients, 2021, 13(1), 239.
[http://dx.doi.org/10.3390/nu13010239] [PMID: 33467650]
[143]
Jekabsone, A.; Sile, I.; Cochis, A.; Makrecka-Kuka, M.; Laucaityte, G.; Makarova, E.; Rimondini, L.; Bernotiene, R.; Raudone, L.; Vedlugaite, E.; Baniene, R.; Smalinskiene, A.; Savickiene, N.; Dambrova, M. Investigation of antibacterial and antiinflammatory activities of proanthocyanidins from Pelargonium sidoides DC root extract. Nutrients, 2019, 11(11), 2829.
[http://dx.doi.org/10.3390/nu11112829] [PMID: 31752295]
[144]
Gao, Y.; Meng, L.; Liu, H.; Wang, J.; Zheng, N. The compromised intestinal barrier induced by mycotoxins. Toxins (Basel), 2020, 12(10), 619.
[http://dx.doi.org/10.3390/toxins12100619] [PMID: 32998222]
[145]
La, V.D.; Howell, A.B.; Grenier, D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of A-type cranberry proanthocyanidins. Antimicrob. Agents Chemother., 2010, 54(5), 1778-1784.
[http://dx.doi.org/10.1128/AAC.01432-09] [PMID: 20176905]
[146]
Labrecque, J.; Bodet, C.; Chandad, F.; Grenier, D. Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis. J. Antimicrob. Chemother., 2006, 58(2), 439-443.
[http://dx.doi.org/10.1093/jac/dkl220] [PMID: 16735419]
[147]
Ikai, H.; Nakamura, K.; Kanno, T.; Shirato, M.; Meirelles, L.; Sasaki, K.; Niwano, Y. Synergistic effect of proanthocyanidin on the bactericidal action of the photolysis of H2O2. Biocontrol Sci., 2013, 18(3), 137-141.
[http://dx.doi.org/10.4265/bio.18.137] [PMID: 24077536]
[148]
Feldman, M.; Grenier, D. Cranberry proanthocyanidins act in synergy with licochalcone A to reduce Porphyromonas gingivalis growth and virulence properties, and to suppress cytokine secretion by macrophages. J. Appl. Microbiol., 2012, 113(2), 438-447.
[http://dx.doi.org/10.1111/j.1365-2672.2012.05329.x] [PMID: 22563853]
[149]
Houle, M.A.; Grenier, D.; Plamondon, P.; Nakayama, K. The collagenase activity of Porphyromonas gingivalis is due to Arg-gingipain. FEMS Microbiol. Lett., 2003, 221(2), 181-185.
[http://dx.doi.org/10.1016/S0378-1097(03)00178-2] [PMID: 12725924]
[150]
Lagha, A.B.; Groeger, S.; Meyle, J.; Grenier, D. Green tea polyphenols enhance gingival keratinocyte integrity and protect against invasion by Porphyromonas gingivalis. Pathog. Dis., 2018, 76(4)
[http://dx.doi.org/10.1093/femspd/fty030] [PMID: 29635433]
[151]
Sakanaka, S.; Okada, Y. Inhibitory effects of green tea polyphenols on the production of a virulence factor of the periodontal-disease-causing anaerobic bacterium Porphyromonas gingivalis. J. Agric. Food Chem., 2004, 52(6), 1688-1692.
[http://dx.doi.org/10.1021/jf0302815] [PMID: 15030231]
[152]
Ben Lagha, A.; Azelmat, J.; Vaillancourt, K.; Grenier, D. A polyphenolic cinnamon fraction exhibits anti-inflammatory properties in a monocyte/macrophage model. PLoS One, 2021, 16(1), e0244805.
[http://dx.doi.org/10.1371/journal.pone.0244805] [PMID: 33439867]
[153]
Bhargava, P.; Mahanta, D.; Kaul, A.; Ishida, Y.; Terao, K.; Wadhwa, R.; Kaul, S.C. Experimental evidence for therapeutic potentials of propolis. Nutrients, 2021, 13(8), 2528.
[http://dx.doi.org/10.3390/nu13082528] [PMID: 34444688]
[154]
Stähli, A.; Schröter, H.; Bullitta, S.; Serralutzu, F.; Dore, A.; Nietzsche, S.; Milia, E.; Sculean, A.; Eick, S. In vitro activity of propolis on oral microorganisms and biofilms. Antibiotics (Basel), 2021, 10(9), 1045.
[http://dx.doi.org/10.3390/antibiotics10091045] [PMID: 34572627]
[155]
Das, M.; Das, A.C.; Panda, S.; Greco Lucchina, A.; Mohanty, R.; Manfredi, B.; Rovati, M.; Giacomello, M.S.; Colletti, L.; Mortellaro, C.; Satpathy, A.; Del Fabbro, M. Clinical efficacy of grape seed extract as an adjuvant to scaling and root planing in treatment of periodontal pockets. J. Biol. Regul. Homeost. Agents, 2021, 35(2)(Suppl. 1), 89-96.
[http://dx.doi.org/10.23812/21-2supp1-8] [PMID: 34281305]
[156]
Taalab, M.R.; Mahmoud, S.A.; Moslemany, R.M.E.; Abdelaziz, D.M. Intrapocket application of tea tree oil gel in the treatment of stage 2 periodontitis. BMC Oral Health, 2021, 21(1), 239.
[http://dx.doi.org/10.1186/s12903-021-01588-y] [PMID: 33952216]
[157]
Melo, J.G.A.; Sousa, J.P.; Firmino, R.T.; Matins, C.C.; Granville-Garcia, A.F.; Nonaka, C.F.W.; Costa, E.M.M.B. Different applications forms of green tea (Camellia sinensis (L.) Kuntze) for the treatment of periodontitis: A systematic review and meta-analysis. J. Periodontal Res., 2021, 56(3), 443-453.
[http://dx.doi.org/10.1111/jre.12871] [PMID: 33729563]
[158]
Nielsen, S.J.; Trak-Fellermeier, M.A.; Joshipura, K.; Dye, B.A. Dietary fiber intake is inversely associated with periodontal disease among US adults. J. Nutr., 2016, 146(12), 2530-2536.
[http://dx.doi.org/10.3945/jn.116.237065] [PMID: 27798338]
[159]
Merchant, A.T.; Pitiphat, W.; Franz, M.; Joshipura, K.J. Whole-grain and fiber intakes and periodontitis risk in men. Am. J. Clin. Nutr., 2006, 83(6), 1395-1400.
[http://dx.doi.org/10.1093/ajcn/83.6.1395] [PMID: 16762952]
[160]
Haas, A.N.; Furlaneto, F.; Gaio, E.J.; Gomes, S.C.; Palioto, D.B.; Castilho, R.M.; Sanz, M.; Messora, M.R. New tendencies in non-surgical periodontal therapy. Braz. Oral Res., 2021, 35(Suppl. 2), e095.
[http://dx.doi.org/10.1590/1807-3107bor-2021.vol35.0095] [PMID: 34586209]
[161]
Cani, P.D.; Lecourt, E.; Dewulf, E.M.; Sohet, F.M.; Pachikian, B.D.; Naslain, D.; De Backer, F.; Neyrinck, A.M.; Delzenne, N.M. Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. Am. J. Clin. Nutr., 2009, 90(5), 1236-1243.
[http://dx.doi.org/10.3945/ajcn.2009.28095] [PMID: 19776140]
[162]
Fang, W.; Xue, H.; Chen, X.; Chen, K.; Ling, W. Supplementation with sodium butyrate modulates the composition of the gut microbiota and ameliorates high-fat diet-induced obesity in mice. J. Nutr., 2019, 149(5), 747-754.
[http://dx.doi.org/10.1093/jn/nxy324] [PMID: 31004166]
[163]
Dodington, D.W.; Fritz, P.C.; Sullivan, P.J.; Ward, W.E. Higher intakes of fruits and vegetables, β-Carotene, Vitamin C, α-Tocopherol, EPA, and DHA Are positively associated with periodontal healing after nonsurgical periodontal therapy in nonsmokers but not in smokers. J. Nutr., 2015, 145(11), 2512-2519.
[http://dx.doi.org/10.3945/jn.115.211524] [PMID: 26423734]
[164]
Kondo, K.; Ishikado, A.; Morino, K.; Nishio, Y.; Ugi, S.; Kajiwara, S.; Kurihara, M.; Iwakawa, H.; Nakao, K.; Uesaki, S.; Shigeta, Y.; Imanaka, H.; Yoshizaki, T.; Sekine, O.; Makino, T.; Maegawa, H.; King, G.L.; Kashiwagi, A. A high-fiber, low-fat diet improves periodontal disease markers in high-risk subjects: A pilot study. Nutr. Res., 2014, 34(6), 491-498.
[http://dx.doi.org/10.1016/j.nutres.2014.06.001] [PMID: 25026916]
[165]
Zanatta, C.A.R.; Fritz, P.C.; Comelli, E.M.; Ward, W.E. Intervention with inulin prior to and during sanative therapy to further support periodontal health: Study protocol for a randomized controlled trial. Trials, 2021, 22(1), 527.
[http://dx.doi.org/10.1186/s13063-021-05504-1] [PMID: 34376241]
[166]
Sedghi, L.; Byron, C.; Jennings, R.; Chlipala, G.E.; Green, S.J.; Silo-Suh, L. Effect of dietary fiber on the composition of the murine dental microbiome. Dent. J., 2019, 7(2), 58.
[http://dx.doi.org/10.3390/dj7020058] [PMID: 31159370]
[167]
Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr., 1995, 125(6), 1401-1412.
[http://dx.doi.org/10.1093/jn/125.6.1401] [PMID: 7782892]
[168]
Bustamante, M.; Oomah, B.D.; Mosi-Roa, Y.; Rubilar, M.; Burgos-Díaz, C. Probiotics as an adjunct therapy for the treatment of halitosis, dental caries and periodontitis. Probiotics Antimicrob. Proteins, 2020, 12(2), 325-334.
[http://dx.doi.org/10.1007/s12602-019-9521-4] [PMID: 30729452]
[169]
Mu, Q.; Tavella, V.J.; Luo, X.M. Role of Lactobacillus reuteri in human health and diseases. Front. Microbiol., 2018, 9, 757.
[http://dx.doi.org/10.3389/fmicb.2018.00757] [PMID: 29725324]
[170]
Reid, G.; Burton, J. Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect., 2002, 4(3), 319-324.
[http://dx.doi.org/10.1016/S1286-4579(02)01544-7] [PMID: 11909742]
[171]
Silva, J.; Carvalho, A.S.; Teixeira, P.; Gibbs, P.A. Bacteriocin production by spray-dried lactic acid bacteria. Lett. Appl. Microbiol., 2002, 34(2), 77-81.
[http://dx.doi.org/10.1046/j.1472-765x.2002.01055.x] [PMID: 11849498]
[172]
Tachedjian, G.; Aldunate, M.; Bradshaw, C.S.; Cone, R.A. The role of lactic acid production by probiotic Lactobacillus species in vaginal health. Res. Microbiol., 2017, 168(9-10), 782-792.
[http://dx.doi.org/10.1016/j.resmic.2017.04.001] [PMID: 28435139]
[173]
Nguyen, T.; Brody, H.; Radaic, A.; Kapila, Y. Probiotics for periodontal health-Current molecular findings. Periodontol. 2000, 2021, 87(1), 254-267.
[http://dx.doi.org/10.1111/prd.12382] [PMID: 34463979]
[174]
Giudice, G.; Cutrignelli, D.A.; Sportelli, P.; Limongelli, L.; Tempesta, A.; Gioia, G.D.; Santacroce, L.; Maiorano, E.; Favia, G. Rhinocerebral mucormycosis with orosinusal involvement: Diagnostic and surgical treatment guidelines. Endocr. Metab. Immune Disord. Drug Targets, 2016, 16(4), 264-269.
[http://dx.doi.org/10.2174/1871530316666161223145055] [PMID: 28017141]
[175]
Morales, A.; Carvajal, P.; Silva, N.; Hernandez, M.; Godoy, C.; Rodriguez, G.; Cabello, R.; Garcia-Sesnich, J.; Hoare, A.; Diaz, P.I.; Gamonal, J. Clinical effects of lactobacillus rhamnosus in non-surgical treatment of chronic periodontitis: A randomized placebo-controlled trial with 1-year follow-up. J. Periodontol., 2016, 87(8), 944-952.
[http://dx.doi.org/10.1902/jop.2016.150665] [PMID: 26944407]
[176]
Iwasaki, K.; Maeda, K.; Hidaka, K.; Nemoto, K.; Hirose, Y.; Deguchi, S. Daily intake of heat-killed Lactobacillus plantarum L-137 decreases the probing depth in patients undergoing supportive periodontal therapy. Oral Health Prev. Dent., 2016, 14(3), 207-214.
[http://dx.doi.org/10.3290/j.ohpd.a36099] [PMID: 27175447]
[177]
Alkaya, B.; Laleman, I.; Keceli, S.; Ozcelik, O.; Cenk Haytac, M.; Teughels, W. Clinical effects of probiotics containing Bacillus species on gingivitis: A pilot randomized controlled trial. J. Periodontal Res., 2017, 52(3), 497-504.
[http://dx.doi.org/10.1111/jre.12415] [PMID: 27859252]
[178]
Alanzi, A.; Honkala, S.; Honkala, E.; Varghese, A.; Tolvanen, M.; Söderling, E. Effect of Lactobacillus rhamnosus and Bifidobacterium lactis on gingival health, dental plaque, and periodontopathogens in adolescents: A randomised placebo-controlled clinical trial. Benef. Microbes, 2018, 9(4), 593-602.
[http://dx.doi.org/10.3920/BM2017.0139] [PMID: 29633646]
[179]
Santacroce, L.; Charitos, I.A.; Bottalico, L. A successful history: Probiotics and their potential as antimicrobials. Expert Rev. Anti Infect. Ther., 2019, 17(8), 635-645.
[http://dx.doi.org/10.1080/14787210.2019.1645597] [PMID: 31318576]
[180]
Magrone, T.; Jirillo, E. The new era of nutraceuticals: Beneficial effects of polyphenols in various experimental and clinical settings. Curr. Pharm. Des., 2018, 24(44), 5229-5231.
[http://dx.doi.org/10.2174/138161282444190329154418] [PMID: 30973101]

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