The effects of nitrate on the oral microbiome: a systematic review investigating prebiotic potential

References

• Shannon OM, Easton C, Shepherd AI, et al. Dietary nitrate and population health: a narrative review of the translational potential of existing laboratory studies. BMC Sports Sci Med Rehabil. 2021;13(1):1–14. doi: 10.1186/s13102-021-00292-2
   PubMed Web of Science ®Google Scholar
• Martin K. Dietary nitrates, nitrites, and food safety: Risks versus benefits. Act Scie Nutr. 2021;5(6):65–76. doi: 10.31080/ASNH.2020.05.0884
   Google Scholar
• Stanaway L, Rutherfurd-Markwick K, Page R, et al. Performance and health benefits of dietary nitrate supplementation in older adults: a systematic review. Nutrients. 2017;9(11):1171. doi: 10.3390/nu9111171
   PubMed Web of Science ®Google Scholar
• Bryan NS, Burleigh MC, Easton C. The oral microbiome, nitric oxide and exercise performance. Nitric Oxide. 2022;125-126:23–30. doi: 10.1016/j.niox.2022.05.004
   PubMed Web of Science ®Google Scholar
• McDonagh STJ, Wylie LJ, Thompson C, et al. Potential benefits of dietary nitrate ingestion in healthy and clinical populations: a brief review. Eur J Sport Sci. 2019;19(1):15–29. doi: 10.1080/17461391.2018.1445298
   PubMed Web of Science ®Google Scholar
• Rosier BT, Takahashi N, Zaura E, et al. The importance of nitrate reduction for oral health. J Dent Res. 2022;101(8):887–897. doi: 10.1177/00220345221080982
   PubMed Web of Science ®Google Scholar
• Rosier BT, Buetas E, Moya-Gonzalvez EM, et al. Nitrate as a potential prebiotic for the oral microbiome. Sci Rep. 2020;10(1). doi: 10.1038/s41598-020-69931-x
   PubMed Web of Science ®Google Scholar
• Morou-Bermúdez E, Torres-Colón JE, Bermúdez NS, et al. Pathways linking oral bacteria, nitric oxide metabolism, and health. J Dent Res. 2022;101(6):623–631. doi: 10.1177/00220345211064571
   PubMed Web of Science ®Google Scholar
• Nazir MA. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci (Qassim). 2017;11(2):72–80.
   PubMedGoogle Scholar
• Saleem HG, Seers CA, Sabri AN, et al. Dental plaque bacteria with reduced susceptibility to chlorhexidine are multidrug resistant. BMC Microbiol. 2016;16(1):1–9. doi: 10.1186/s12866-016-0833-1
   PubMedGoogle Scholar
• Paul O, Arora P, Mayer M, et al. Inflammation in periodontal disease: possible link to vascular disease. Front Physiol. 2021;11. doi: 10.3389/fphys.2020.609614
   PubMed Web of Science ®Google Scholar
• Verspecht T, Rodriguez Herrero E, Khodaparast L, et al. Development of antiseptic adaptation and cross-adaptation in selected oral pathogens in vitro. Sci Rep. 2019;9(1). doi: 10.1038/s41598-019-44822-y
   PubMedGoogle Scholar
• Murray CJL, Ikuta KS, Sharara F, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet (London, England). 2022;399(10325):629–655.
   PubMed Web of Science ®Google Scholar
• Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health. 2015;109(7):309–318. doi: 10.1179/2047773215Y.0000000030
   PubMed Web of Science ®Google Scholar
• Burleigh M, Liddle L, Muggeridge DJ, et al. Dietary nitrate supplementation alters the oral microbiome but does not improve the vascular responses to an acute nitrate dose. Nitric Oxide. 2019;89:54–63. doi: 10.1016/j.niox.2019.04.010
   PubMed Web of Science ®Google Scholar
• Jockel-Schneider Y, Goßner SK, Petersen N, et al. Stimulation of the nitrate-nitrite-NO-metabolism by repeated lettuce juice consumption decreases gingival inflammation in periodontal recall patients: a randomized, double-blinded, placebo-controlled clinical trial. J Clinic Periodontol. 2016;43(7):603–608. doi: 10.1111/jcpe.12542
   PubMed Web of Science ®Google Scholar
• Jockel-Schneider Y, Schlagenhauf U, Stölzel P, et al. Nitrate-rich diet alters the composition of the oral microbiota in periodontal recall patients. J Periodontol. 2021;92(11):1536–1545. doi: 10.1002/JPER.20-0778
   PubMed Web of Science ®Google Scholar
• Hohensinn B, Haselgrübler R, Müller U, et al. Sustaining elevated levels of nitrite in the oral cavity through consumption of nitrate-rich beetroot juice in young healthy adults reduces salivary pH. Nitric Oxide. 2016;60:10–15. doi: 10.1016/j.niox.2016.08.006
   PubMed Web of Science ®Google Scholar
• PRISMA. PRISMA 2020 checklist; 2021 [cited 2022 Nov 1]. Available from: http://www.prisma-statement.org
   Google Scholar
• Scottish Intercollegiate Guidelines Network. Algorithm for classifying study design for questions of effectiveness; 2021 [cited 2022 Nov 2022]. Available from: https://www.sign.ac.uk/assets/study_design.pdf
   Google Scholar
• University of Strathclyde. Systematic Review Steps; 2022 [cited 2022 Nov 1]. Available from: https://guides.lib.strath.ac.uk/systematic/steps
   Google Scholar
• Centre for Evidence-Based Management. Critical Appraisal Of a Controlled Study; 2019 [cited 2022 Nov 2]. Available from: https://cebma.org/resources-and-tools/what-is-critical-appraisal/
   Google Scholar
• Critical Appraisal Skills Programme. CASP Randomised Controlled Trial Checklist; 2022 [cited 2022 Nov 2]. Available from: https://casp-uk.net/casp-tools-checklists/
   Google Scholar
• Greenhalgh T, Robert G, Bate P, et al. Diffusion of innovations in health service organisations a systematic literature review: appendix 2, critical appraisal checklists. London: BMJ. 2005.
   Google Scholar
• The Joanna Briggs Institute. Checklist For Quasi-Experimental Studies; 2022 [cited 2022 Nov 2]. Available from: https://jbi.global/critical-appraisal-tools
   Google Scholar
• Centre for Evidence-Based Management. Critical Appraisal Checklist For Cross-Sectional Study; 2014 [cited 2022 Nov 2]. Available from: https://cebma.org/wp-content/uploads/Critical-Appraisal-Questions-for-a-Cross-Sectional-Study-July-2014-1.pdf
   Google Scholar
• Strengthening the reporting of observational studies in epidemiology. STROBE Checklist For Cross-Sectional Studies; 2022 [cited 2022 Nov 2]. Available from: https://www.strobe-statement.org/checklists/
   Google Scholar
• University of Exeter Library. Checklist For In Vitro Studies; 2022 [cited 2022 Nov 2]. Available from: https://libguides.exeter.ac.uk/c.php?g=660317&p=4708597
   Google Scholar
• Sheth VH, Shah NP, Jain R, et al. Development and validation of a risk-of-bias tool for assessing in vitro studies conducted in dentistry: the QUIN. J Prosthet Dent. 2022. doi: 10.1016/j.prosdent.2022.05.019
   Google Scholar
• Velmurugan S, Gan JM, Rathod KS, et al. Dietary nitrate improves vascular function in patients with hypercholesterolemia: a randomized, double-blind, placebo-controlled study. Am J Clin Nutr. 2016;103(1):25–38. doi: 10.3945/ajcn.115.116244
   PubMed Web of Science ®Google Scholar
• Koopman JE, Buijs MJ, Brandt BW, et al. Nitrate and the origin of saliva influence composition and short chain fatty acid production of oral microcosms. Microb Ecol. 2016;72(2):479–492. doi: 10.1007/s00248-016-0775-z
   PubMed Web of Science ®Google Scholar
• Vanhatalo A, Blackwell JR, L’Heureux JE, et al. Nitrate-responsive oral microbiome modulates nitric oxide homeostasis and blood pressure in humans. Free Radic Biol Med. 2018;124:21–30. doi: 10.1016/j.freeradbiomed.2018.05.078
   PubMed Web of Science ®Google Scholar
• Ashworth A, Cutler C, Farnham G, et al. Dietary intake of inorganic nitrate in vegetarians and omnivores and its impact on blood pressure, resting metabolic rate and the oral microbiome. Free Radic Biol Med. 2019;138:63–72. doi: 10.1016/j.freeradbiomed.2019.05.010
   PubMed Web of Science ®Google Scholar
• Liddle L, Burleigh MC, Monaghan C, et al. Variability in nitrate-reducing oral bacteria and nitric oxide metabolites in biological fluids following dietary nitrate administration: An assessment of the critical difference. Nitric Oxide. 2019;83:1–10. doi: 10.1016/j.niox.2018.12.003
   PubMed Web of Science ®Google Scholar
• Rosier BT, Moya-Gonzalvez EM, Corell-Escuin P, et al. Isolation and Characterization of Nitrate-Reducing Bacteria as Potential Probiotics for Oral and Systemic Health. Front Microbiol. 11. doi: 10.3389/fmicb.2020.555465
   Web of Science ®Google Scholar
• Vanhatalo A, L’Heureux JE, Kelly J, et al. Network analysis of nitrate-sensitive oral microbiome reveals interactions with cognitive function and cardiovascular health across dietary interventions. Redox Biol. 2021;41:101933. doi: 10.1016/j.redox.2021.101933
   PubMed Web of Science ®Google Scholar
• Sinha R, Zhao N, Goedert JJ, et al. Effects of processed meat and drinking water nitrate on oral and fecal microbial populations in a controlled feeding study. Environ Res. 2021;197:111084. doi:10.1016/j.envres.2021.111084
   PubMed Web of Science ®Google Scholar
• Rosier BT, Palazón C, García-Esteban S, et al. A single dose of nitrate increases resilience against acidification derived from sugar fermentation by the oral microbiome. Front Cell Infect Microbiol. 2021;11:692883. doi: 10.3389/fcimb.2021.692883
   PubMed Web of Science ®Google Scholar
• López-Ibáñez J, Martín LT, Chagoyen M, et al. Bacterial feature finder (BaFF)-a system for extracting features overrepresented in sets of prokaryotic organisms. Bioinformatics (Oxford Academia). 2019;35(18):3482–3483. doi: 10.1093/bioinformatics/btz099
   PubMed Web of Science ®Google Scholar
• Pignatelli P, Fabietti G, Ricci A, et al. How periodontal disease and presence of nitric oxide reducing oral bacteria can affect blood pressure. Int J Mol Sci. 2020;21(20):7538. doi: 10.3390/ijms21207538
   PubMed Web of Science ®Google Scholar
• Radaic A, Kapila YL. The oralome and its dysbiosis: new insights into oral microbiome-host interactions. Computat Struct Biotechnol J. 2021;19:1335–1360. doi: 10.1016/j.csbj.2021.02.010
   PubMed Web of Science ®Google Scholar
• Miyoshi T, Oge S, Nakata S, et al. Gemella haemolysans inhibits the growth of the periodontal pathogen porphyromonas gingivalis. Sci Rep. 2021;11(1). doi: 10.1038/s41598-021-91267-3
   Web of Science ®Google Scholar
• Zhou P, Manoil D, Belibasakis GN, et al. Veillonellae: beyond bridging species in oral biofilm ecology. Front Oral Health. 2021;2. doi: 10.3389/froh.2021.774115
   PubMedGoogle Scholar
• Acar B, Çağlayan F, İnkaya AÇ, et al. Actinomyces-associated lesions located in the gingiva: case report of rare gingival lesions. Contemp Clin Dent. 2017;8(1):182–184. doi: 10.4103/0976-237X.205067
   PubMedGoogle Scholar
• Bescos R, Ashworth A, Cutler C, et al. Effects of chlorhexidine mouthwash on the oral microbiome. Sci Rep. 2020;10(1). doi: 10.1038/s41598-020-61912-4
   PubMed Web of Science ®Google Scholar
• Liu T, Chen Y-C, Jeng S-L, et al. Short-term effects of chlorhexidine mouthwash and Listerine on oral microbiome in hospitalized patients. Front Cell Infect Microbiol. 2023;13:13. doi: 10.3389/fcimb.2023.1056534
   Web of Science ®Google Scholar
• Burleigh MC, Sculthorpe N, Henriquez FL, et al. Nitrate-rich beetroot juice offsets salivary acidity following carbohydrate ingestion before and after endurance exercise in healthy male runners. PLoS One. 2020;15(12):e0243755. doi: 10.1371/journal.pone.0243755
   PubMed Web of Science ®Google Scholar
• Mashima I, Nakazawa F, O’Toole GA. The interaction between streptococcus spp. And veillonella tobetsuensis in the early stages of oral biofilm formation. J Bacteriol. 2015;197(13):2104–2111. doi: 10.1128/JB.02512-14
   PubMed Web of Science ®Google Scholar
• López-Santacruz HD, López-López A, Revilla-Guarinos A, et al. Streptococcus dentisani is a common inhabitant of the oral microbiota worldwide and is found at higher levels in caries-free individuals. Int Microbiol. 2021;24(4):619–629. doi: 10.1007/s10123-021-00222-9
   PubMed Web of Science ®Google Scholar
• Mazurel D, Carda-Diéguez M, Langenburg T, et al. Nitrate and a nitrate-reducing Rothia aeria strain as potential prebiotic or synbiotic treatments for periodontitis. NPJ Biofilms Microbiomes. 2023;9(1):40. doi: 10.1038/s41522-023-00406-3
   PubMed Web of Science ®Google Scholar
• Pałka Ł, Nowakowska-Toporowska A, Dalewski B. Is chlorhexidine in Dentistry an Ally or a foe? A narrative review. Healthcare. 2022;10(5):764. doi: 10.3390/healthcare10050764
   Web of Science ®Google Scholar
• Brookes ZLS, Belfield LA, Ashworth A, et al. Effects of chlorhexidine mouthwash on the oral microbiome. J Dent. 2021;113:103768. doi: 10.1016/j.jdent.2021.103768
   PubMed Web of Science ®Google Scholar
• Chatzigiannidou I, Teughels W, Van de Wiele T, et al. Oral biofilms exposure to chlorhexidine results in altered microbial composition and metabolic profile. NPJ Biofilms Microbiomes. 2020;6(1):13. doi: 10.1038/s41522-020-0124-3
   PubMed Web of Science ®Google Scholar
• Kulik EM, Waltimo T, Weiger R, et al. Development of resistance of mutans streptococci and porphyromonas gingivalis to chlorhexidine digluconate and amine fluoride/stannous fluoride-containing mouthrinses, in vitro. Clin Oral Invest. 2015;19(6):1547–1553. doi: 10.1007/s00784-014-1379-y
   PubMed Web of Science ®Google Scholar
• Wang S, Wang H, Ren B, et al. Do quaternary ammonium monomers induce drug resistance in cariogenic, endodontic and periodontal bacterial species? Dental Mater. 2017;33(10):1127–1138. doi: 10.1016/j.dental.2017.07.001
   PubMed Web of Science ®Google Scholar
• Nambu T, Wang D, Mashimo C, et al. Nitric Oxide Donor Modulates a Multispecies Oral Bacterial Community—An In Vitro Study. Microorganisms. 2019;7(9):353. doi: 10.3390/microorganisms7090353
   PubMed Web of Science ®Google Scholar
• Backlund CJ, Sergesketter AR, Offenbacher S, et al. Antibacterial efficacy of exogenous nitric oxide on periodontal pathogens. J Dent Res. 2014;93(11):1089–1094. doi: 10.1177/0022034514529974
   PubMed Web of Science ®Google Scholar
• Naseem KM. The role of nitric oxide in cardiovascular diseases. Mol Aspect Med. 2005;26(1–2):33–65. doi: 10.1016/j.mam.2004.09.003
   PubMedGoogle Scholar
• Bondonno CP, Blekkenhorst LC, Liu AH, et al. Vegetable-derived bioactive nitrate and cardiovascular health. Mol Aspect Med. 2018;61:83–91. doi: 10.1016/j.mam.2017.08.001
   PubMed Web of Science ®Google Scholar
• Fadel PJ. Nitric oxide and cardiovascular regulation. Hypertension. 2017;69(5):778–779. doi: 10.1161/HYPERTENSIONAHA.117.08999
   PubMed Web of Science ®Google Scholar
• Infante T, Costa D, Napoli C. Novel insights regarding nitric oxide and cardiovascular diseases. Angiology. 2021;72(5):411–425. doi: 10.1177/0003319720979243
   PubMed Web of Science ®Google Scholar
• Webb AJ, Patel N, Loukogeorgakis S, et al. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension. 2008;51(3):784–790. doi: 10.1161/HYPERTENSIONAHA.107.103523
   PubMed Web of Science ®Google Scholar
• Kenjale AA, Ham KL, Stabler T, et al. Dietary nitrate supplementation enhances exercise performance in peripheral arterial disease. J Appl Physiol. 2011;110(6):1582–1591. doi: 10.1152/japplphysiol.00071.2011
   PubMed Web of Science ®Google Scholar
• Ivy JL. Inorganic Nitrate Supplementation for Cardiovascular Health. Methodist DeBakey Cardiovasc J. 2019;15(3):200–206. doi: 10.14797/mdcj-15-3-200
   PubMedGoogle Scholar
• Jovanovski E, Bosco L, Khan K, et al. Effect of spinach, a high dietary nitrate source, on arterial stiffness and related hemodynamic measures: a randomized, controlled trial in healthy adults. Clin Nutr Res. 2015;4(3):160–167. doi: 10.7762/cnr.2015.4.3.160
   PubMedGoogle Scholar
• Bedale W, Sindelar JJ, Milkowski AL. Dietary nitrate and nitrite: Benefits, risks, and evolving perceptions. Meat Sci. 2016;120:85–92. doi: 10.1016/j.meatsci.2016.03.009
   PubMed Web of Science ®Google Scholar