Enrichment of sulphate-reducers and depletion of butyrate-producers may be hyperglycaemia signatures in the diabetic oral microbiome

References

• Albandar JM, Susin C, Hughes FJ. Manifestations of systemic diseases and conditions that affect the periodontal attachment apparatus: case definitions and diagnostic considerations. J Periodontol. 2018;89(1):S183–S203.
   Google Scholar
• Jepsen S, Caton JG, Albandar JM, et al. Periodontal manifestations of systemic diseases and developmental and acquired conditions: consensus report of workgroup 3 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(1):S237–S248.
   Google Scholar
• Grisi D, Vieira I, Lima AK, et al. The complex interrelationship between diabetes mellitus, oral diseases and general health. Curr Diabetes Rev. 2021;18 (3):8–14
   Web of Science ®Google Scholar
• Marques RCR, JRd S, Vieira Lima CP, et al. Salivary parameters of adults with diabetes mellitus: a systematic review and meta-analysis. Oral Surg Oral Med Oral Pathol Oral Radiol. 2022 Available online 8 March 2022 doi:10.1016/j.oooo.2022.03.001 .
   Google Scholar
• Mauri-Obradors E, Estrugo-Devesa A, Jané-Salas E, et al. Oral manifestations of diabetes mellitus. A systematic review. Med Oral Patol Oral Cir Bucal. 2017;22:e586–e594.
   Web of Science ®Google Scholar
• Verhulst MJL, Loos BG, Gerdes VEA, et al. Evaluating all potential oral complications of diabetes mellitus. Front Endocrinol (Lausanne). 2019;10:56.
   PubMed Web of Science ®Google Scholar
• de Lima Aka, Amorim Dos Santos J, Stefani CM, et al. Diabetes mellitus and poor glycemic control increase the occurrence of coronal and root caries: a systematic review and meta-analysis. Clin Oral Investig. 2020;24:3801–3812.
   Web of Science ®Google Scholar
• Goodson JM, Hartman ML, Shi P, et al. The salivary microbiome is altered in the presence of a high salivary glucose concentration. PLoS One. 2017;12:e0170437.
   Web of Science ®Google Scholar
• Abikshyeet P, Ramesh V, Oza N. Glucose estimation in the salivary secretion of diabetes mellitus patients. Diabetes Metab Syndr Obes. 2012;5:149–154.
   PubMedGoogle Scholar
• Tiongco REG, Arceo ES, Rivera NS, et al. Estimation of salivary glucose, amylase, calcium, and phosphorus among non-diabetics and diabetics: potential identification of non-invasive diagnostic markers. Diabetes Metab Syndr. 2019;13(4):2601–2605.
   Web of Science ®Google Scholar
• Mascarenhas P, Fatela B, Barahona I. Effect of diabetes mellitus type 2 on salivary glucose – a systematic review and meta-analysis of observational studies. PLoS One. 2014;9(7):e101706.
   Web of Science ®Google Scholar
• Smriti K, Pai KM, Ravindranath V, et al. Salivary glucose as a diagnostic marker for diabetes mellitus. J Diabetes Sci Technol. 2016;10(4):991–992.
   Google Scholar
• Nyvad B, Takahashi N. Integrated hypothesis of dental caries and periodontal diseases. J Oral Microbiol. 2020;12(1):1710953.
   PubMed Web of Science ®Google Scholar
• Yang Y, Liu S, Wang Y, et al. Changes of saliva microbiota in the onset and after the treatment of diabetes in patients with periodontitis. Aging (Albany NY). 2020;12(13):13090–13114.
   Google Scholar
• Fujii S, Maeda T, Noge I, et al. Determination of acetone in saliva by reversed-phase liquid chromatography with fluorescence detection and the monitoring of diabetes mellitus patients with ketoacidosis. Clin Chim Acta. 2014;430:140–144.
   Web of Science ®Google Scholar
• Sabharwal A, Ganley K, Miecznikowski JC, et al. The salivary microbiome of diabetic and non-diabetic adults with periodontal disease. J Periodontol. 2019;90:26–34.
   PubMed Web of Science ®Google Scholar
• Saeb ATM, Al-Rubeaan KA, Aldosary K, et al. Relative reduction of biological and phylogenetic diversity of the oral microbiota of diabetes and pre-diabetes patients. Microb Pathog. 2019;128:215–229.
   Web of Science ®Google Scholar
• Ogawa T, Honda-Ogawa M, Ikebe K, et al. Characterizations of oral microbiota in elderly nursing home residents with diabetes. J Oral Sci. 2017;59(4):549–555.
   PubMed Web of Science ®Google Scholar
• Sun X, Li M, Xia L, et al. Alteration of salivary microbiome in periodontitis with or without type-2 diabetes mellitus and metformin treatment. Sci Rep. 2020;10(1):15363.
   Web of Science ®Google Scholar
• Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60.
   PubMed Web of Science ®Google Scholar
• Tanase DM, Gosav EM, Neculae E, et al. Role of gut microbiota on onset and progression of microvascular complications of type 2 diabetes (T2DM). Nutrients. 2020;12(12):3719.
   Web of Science ®Google Scholar
• Martínez JE, Vargas A, Pérez-Sánchez T, et al. Human microbiota network: unveiling potential crosstalk between the different microbiota ecosystems and their role in health and disease. Nutrients.2021;13(9):2905.
   Web of Science ®Google Scholar
• Ribeiro BA, Vieira Lima CP, Alves LS, et al. Impact of detection criteria on coronal and root caries estimates in adults with and without type 2 diabetes mellitus. Clin Oral Investig. 2022;26(4):3687-3695.
   Web of Science ®Google Scholar
• Vandenbroucke JP, von Elm E, Altman DG, et al. Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration. Int J Surg. 2014;12:1500–1524.
   PubMed Web of Science ®Google Scholar
• Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol. 2018;89(1):S173–S182.
   Google Scholar
• Côrtes D, de Cena Jsa, Marconatto L, et al. Clinical parameters of individuals with periodontitis and Diabetes Mellitus reveals signatures of the minority microbiota in saliva. Preprint ed. Scielo Preprints; 2021 https://doi.org/10.1590/SciELOPreprints.3093
   Google Scholar
• Nyvad B, Baelum V. Nyvad criteria for caries lesion activity and severity assessment: a validated approach for clinical management and research. Caries Res. 2018;52:397–405.
   Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583.
   PubMed Web of Science ®Google Scholar
• R Core Team. R: a language and environment for statistical computing. Vol. 3 6.1 Vienna Austria: R Foundation for Statistical Computing; 2021. https://www.R-project.org/
   Google Scholar
• Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
   PubMed Web of Science ®Google Scholar
• McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and. Graphics of Microbiome Census Data; 2013.
   Google Scholar
• Lahti L, Shetty S, Al. E. Tools for microbiome analysis in R, v3.14. 2017. http://microbiome.github.com/microbiome.
   Google Scholar
• Oksanen J, Blanchet G, Friendly M, et al. vegan R package, v2.5–7. https://cran.r-project.org,https://github.com/vegandevs/vegan
   Google Scholar
• Slowikowski K, Schep A, Hughes S, et al. ggrepel R package, v0.9.1. 2021. https://cran.r-project.org/web/packages/ggrepel/index.html.
   Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
   PubMed Web of Science ®Google Scholar
• Peschel S, Müller CL, von Mutius E, et al., NetCoMi: network construction and comparison for microbiome data in R. Brief Bioinform 22. 2021;
   Web of Science ®Google Scholar
• Wang J, Jia H. Metagenome-wide association studies: fine-mining the microbiome. Nat Rev Microbiol. 2016;14:508–522.
   PubMed Web of Science ®Google Scholar
• Demmer RT, Trinh P, Rosenbaum M, et al. Subgingival microbiota and longitudinal glucose change: the oral infections, glucose intolerance and insulin resistance study (ORIGINS). J Dent Res. 2019;98:1488–1496.
   Web of Science ®Google Scholar
• Palmas V, Pisanu S, Madau V, et al. Gut microbiota markers associated with obesity and overweight in Italian adults. Sci Rep. 2021;11:5532.
   Web of Science ®Google Scholar
• Yang Q, Lin SL, Kwok MK, et al. The Roles of 27 genera of human gut microbiota in ischemic heart disease, type 2 diabetes mellitus, and their risk factors: a Mendelian randomization study. Am J Epidemiol. 2018;187:1916–1922.
   Web of Science ®Google Scholar
• Gheibi S, Samsonov AP, Vazquez AB, et al. Regulation of carbohydrate metabolism by nitric oxide and hydrogen sulfide: implications in diabetes. Biochem Pharmacol. 2020;176:113819.
   Web of Science ®Google Scholar
• Bełtowski J, Wójcicka G, Jamroz-Wiśniewska A. Hydrogen sulfide in the regulation of insulin secretion and insulin sensitivity: implications for the pathogenesis and treatment of diabetes mellitus. Biochem Pharmacol. 2018;149:60–76.
   PubMed Web of Science ®Google Scholar
• Cross KL, Chirania P, Xiong W, et al., Insights into the evolution of host association through the isolation and characterization of a novel human periodontal pathobiont. mBio 9. 2018
   Google Scholar
• Abu Fanas S, Brigi C, Varma SR, et al. The prevalence of novel periodontal pathogens and bacterial complexes in Stage II generalized periodontitis based on 16S rRNA next generation sequencing. J Appl Oral Sci. 2021;29:e20200787.
   PubMed Web of Science ®Google Scholar
• Rivière A, Selak M, Lantin D, et al. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 2016;7:979.
   PubMed Web of Science ®Google Scholar
• Larsen N, Vogensen FK, van den Berg Fw, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5:e9085.
   PubMed Web of Science ®Google Scholar
• Li Q, Chang Y, Zhang K, et al. Implication of the gut microbiome composition of type 2 diabetic patients from northern China. Sci Rep. 2020;10:5450.
   PubMed Web of Science ®Google Scholar
• Zaura E, Keijser BJ, Huse SM, et al. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 2009;9:259.
   PubMed Web of Science ®Google Scholar
• Radaic A, Kapila YL. The oralome and its dysbiosis: new insights into oral microbiome-host interactions. Comput Struct Biotechnol J. 2021;19:1335–1360.
   PubMed Web of Science ®Google Scholar
• Kumar PS, Monteiro MF, Dabdoub SM, et al. Subgingival host-microbial interactions in hyperglycemic individuals. J Dent Res. 2020;99:650–657.
   Web of Science ®Google Scholar
• Marangoni A, Ceccarani C, Camboni T, et al. Pharyngeal microbiome alterations during Neisseria gonorrhoeae infection. PLoS One. 2020;15:e0227985.
   Web of Science ®Google Scholar
• Johansson I, Witkowska E, Kaveh B, et al. The microbiome in populations with a low and high prevalence of caries. J Dent Res. 2016;95:80–86.
   PubMed Web of Science ®Google Scholar
• Socransky SS, Haffajee AD, Cugini MA, et al. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–144.
   PubMed Web of Science ®Google Scholar
• Gross EL, Leys EJ, Gasparovich SR, et al. Bacterial 16S sequence analysis of severe caries in young permanent teeth. J Clin Microbiol. 2010;48:4121–4128.
   PubMed Web of Science ®Google Scholar
• Wei YS, Hsiao YC, Su GW, et al. Identification of hyperglycemia-associated microbiota alterations in saliva and gingival sulcus. Arch Biochem Biophys. 2020;682:108278.
   Web of Science ®Google Scholar
• Dame-Teixeira Ndl AKAD, Stefani T, CM. Meta-Analysis using NGS data: the veillonella species in dental caries. Frontiers in Oral Health. 2021
   Google Scholar
• Diaz PI. Microbial diversity and interactions in subgingival biofilm communities. Periodontal Disease. 2011;15:17–40.
   Google Scholar
• Cena J, Zhang J, Deng D, et al. Low-abundant microorganisms: the human microbiome’s dark matter, a scoping review. Frontiers in Cellular and Infection Microbiology. 2021;11.
   Web of Science ®Google Scholar