Drift of the Subgingival Periodontal Microbiome during Chronic Periodontitis in Type 2 Diabetes Mellitus Patients
Abstract
:1. Introduction
2. Material and Methods
2.1. Subject Population and Study Design
2.2. Diagnostic and Inclusion Criteria
2.3. Collection and Sequencing of Plaque Samples
2.4. Bioinformatic and Statistical Analysis
3. Results
3.1. Description of the Demographic and Clinical Parameters of the Experimental Cohort
3.2. Characteristic of the Subgingival Periodontal Microbiota Based on 16S rRNA Gene Sequencing of the Collected Samples
3.3. Genome-Resolved Metagenomic Analysis of the Shotgun Sequencing Data of the Pooled Samples
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Cook, J.; Holmes, C.J.; Wixtrom, R.; Newman, M.I.; Pozner, J.N. Characterizing the Microbiome of the Contracted Breast Capsule Using Next Generation Sequencing. Aesthetic Surg. J. 2021, 41, 440–447. [Google Scholar] [CrossRef]
- Ziganshin, R.H.; Ivanova, O.M.; Lomakin, Y.A.; Belogurov, A.A.; Kovalchuk, S.I.; Azarkin, I.V.; Arapidi, G.P.; Anikanov, N.A.; Shender, V.O.; Piradov, M.A.; et al. The pathogenesis of the demyelinating form of guillain-barre syndrome (GBS): Proteopeptidomic and immunological profiling of physiological fluids. Mol. Cell Proteom. 2016, 15, 2366–2378. [Google Scholar] [CrossRef] [Green Version]
- Belogurov, A.A.; Ivanova, O.M.; Lomakin, Y.A.; Ziganshin, R.H.; Vaskina, M.I.; Knorre, V.D.; Klimova, E.A.; Gabibov, A.G.; Ivanov, V.T.; Govorun, V.M. Mediators and biomarkers of inflammation in meningitis: Cytokine and peptidome profiling of cerebrospinal fluid. Biochemistry 2016, 81, 1293–1302. [Google Scholar] [CrossRef]
- Ghurye, J.S.; Cepeda-Espinoza, V.; Pop, M. Metagenomic assembly: Overview, challenges and applications. Yale J. Biol. Med. 2016, 89, 353–362. [Google Scholar] [PubMed]
- Terekhov, S.S.; Smirnov, I.V.; Malakhova, M.V.; Samoilov, A.E.; Manolov, A.I.; Nazarov, A.S.; Danilov, D.V.; Dubiley, S.A.; Osterman, I.A.; Rubtsova, M.P.; et al. Ultrahigh-throughput functional profiling of microbiota communities. Proc. Natl. Acad. Sci. USA 2018, 115, 9551–9556. [Google Scholar] [CrossRef] [Green Version]
- Terekhov, S.S.; Mokrushina, Y.A.; Nazarov, A.S.; Zlobin, A.; Zalevsky, A.; Bourenkov, G.; Golovin, A.; Belogurov, A.; Osterman, I.A.; Kulikova, A.A.; et al. A kinase bioscavenger provides antibiotic resistance by extremely tight substrate binding. Sci. Adv. 2020, 6, eaaz9861. [Google Scholar] [CrossRef] [PubMed]
- Terekhov, S.S.; Smirnov, I.V.; Stepanova, A.V.; Bobik, T.V.; Mokrushina, Y.A.; Ponomarenko, N.A.; Belogurov, A.A.; Rubtsova, M.P.; Kartseva, O.V.; Gomzikova, M.O.; et al. Microfluidic droplet platform for ultrahigh-throughput single-cell screening of biodiversity. Proc. Natl. Acad. Sci. USA 2017, 114, 2550–2555. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aas, J.A.; Paster, B.J.; Stokes, L.N.; Olsen, I.; Dewhirst, F.E. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 2005, 43, 5721–5732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baker, J.L.; Bor, B.; Agnello, M.; Shi, W.; He, X. Ecology of the Oral Microbiome: Beyond Bacteria. Trends Microbiol. 2017, 25, 362–374. [Google Scholar] [CrossRef] [Green Version]
- Cho, I.; Blaser, M.J. The human microbiome: At the interface of health and disease. Nat. Rev. Genet. 2012, 13, 260–270. [Google Scholar] [CrossRef] [Green Version]
- Paster, B.J.; Boches, S.K.; Galvin, J.L.; Ericson, R.E.; Lau, C.N.; Levanos, V.A.; Sahasrabudhe, A.; Dewhirst, F.E. Bacterial diversity in human subgingival plaque. J. Bacteriol. 2001, 183, 3770–3783. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takahashi, N.; Sulijaya, B.; Yamada-Hara, M.; Tsuzuno, T.; Tabeta, K.; Yamazaki, K. Gingival epithelial barrier: Regulation by beneficial and harmful microbes. Tissue Barriers 2019, 7. [Google Scholar] [CrossRef] [PubMed]
- Graves, D.T.; Corrêa, J.D.; Silva, T.A. The Oral Microbiota Is Modified by Systemic Diseases. J. Dent. Res. 2019, 98, 148–156. [Google Scholar] [CrossRef] [PubMed]
- Bui, F.Q.; Almeida-da-Silva, C.L.C.; Huynh, B.; Trinh, A.; Liu, J.; Woodward, J.; Asadi, H.; Ojcius, D.M. Association between periodontal pathogens and systemic disease. Biomed. J. 2019, 42, 27–35. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Losada, F.D.L.; Jané-Salas, E.; Sabater-Recolons, M.D.M.; Estrugo-Devesa, A.; Segura-Egea, J.J.; López-López, J. Correlation between periodontal disease management and metabolic control of type 2 diabetes mellitus: A systematic literature review. Med. Oral Patol. Oral Y Cir. Bucal. 2016, 21, e440–e446. [Google Scholar] [CrossRef]
- Glurich, I.; Acharya, A. Updates from the Evidence Base Examining Association between Periodontal Disease and Type 2 Diabetes Mellitus: Current Status and Clinical Relevance. Curr. Diabetes Rep. 2019, 19. [Google Scholar] [CrossRef]
- Sanz, M.; Ceriello, A.; Buysschaert, M.; Chapple, I.; Demmer, R.T.; Graziani, F.; Herrera, D.; Jepsen, S.; Lione, L.; Madianos, P.; et al. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J. Clin. Periodontol. 2018, 45, 138–149. [Google Scholar] [CrossRef]
- Barnes, V.M.; Kennedy, A.D.; Panagakos, F.; Devizio, W.; Trivedi, H.M.; Jönsson, T.; Guo, L.; Cervi, S.; Scannapieco, F.A. Global metabolomic analysis of human saliva and plasma from healthy and diabetic subjects, with and without periodontal disease. PLoS ONE 2014, 9, e105181. [Google Scholar] [CrossRef]
- Patil, V.S.; Patil, V.P.; Gokhale, N.; Acharya, A.; Kangokar, P. Chronic periodontitis in type 2 diabetes mellitus: Oxidative stress as a common factor in periodontal tissue injury. J. Clin. Diagn. Res. 2016, 10, BC12–BC16. [Google Scholar] [CrossRef]
- Balmasova, I.P.; Lomakin, Y.A.; Babaev, E.A.; Tsarev, V.A.; Gabibov, A.G.; Smirnov, I.V.; Knorre, V.D.; Ovchinnikova, L.A.; Gnuchev, N.V.; Khurs, E.N.; et al. “Shielding” of cytokine induction by the periodontal microbiome in patients with periodontitis associated with type 2 diabetes mellitus. Acta Nat. 2019, 11, 79–87. [Google Scholar] [CrossRef]
- Matsha, T.E.; Prince, Y.; Davids, S.; Chikte, U.; Erasmus, R.T.; Kengne, A.P.; Davison, G.M. Oral Microbiome Signatures in Diabetes Mellitus and Periodontal Disease. J. Dent. Res. 2020, 99, 658–665. [Google Scholar] [CrossRef] [PubMed]
- Shi, B.; Lux, R.; Klokkevold, P.; Chang, M.; Barnard, E.; Haake, S.; Li, H. The subgingival microbiome associated with periodontitis in type 2 diabetes mellitus. ISME J. 2020, 14, 519–530. [Google Scholar] [CrossRef] [PubMed]
- Nakajima, M.; Arimatsu, K.; Minagawa, T.; Matsuda, Y.; Sato, K.; Takahashi, N.; Nakajima, T.; Yamazaki, K. Brazilian propolis mitigates impaired glucose and lipid metabolism in experimental periodontitis in mice. BMC Complement Altern. Med. 2016, 16. [Google Scholar] [CrossRef] [Green Version]
- Ohno, T.; Yamamoto, G.; Hayashi, J.I.; Nishida, E.; Goto, H.; Sasaki, Y.; Kikuchi, T.; Fukuda, M.; Hasegawa, Y.; Mogi, M.; et al. Angiopoietin-like protein 2 regulates Porphyromonas gingivalis lipopolysaccharide-induced inflammatory response in human gingival epithelial cells. PLoS ONE 2017, 12, e0184825. [Google Scholar] [CrossRef] [Green Version]
- Taylor, J.R.; Dietrich, E.; Powell, J.G. New and Emerging Pharmacologic Therapies for Type 2 Diabetes, Dyslipidemia, and Obesity. Clin. Ther. 2013, 35. [Google Scholar] [CrossRef] [PubMed]
- Graetz, C.; Mann, L.; Krois, J.; Sälzer, S.; Kahl, M.; Springer, C.; Schwendicke, F. Comparison of periodontitis patients’ classification in the 2018 versus 1999 classification. J. Clin. Periodontol. 2019, 46, 908–917. [Google Scholar] [CrossRef]
- Association, A.D. Diagnosis and classification of diabetes mellitus. Diabetes Care 2012, 35, S64–S71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A.; Holmes, S.P. DADA2, High-resolution sample inference from Illumina amplicon data. Nat. Methods 2016, 13, 581–583. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Callahan, B.J.; Sankaran, K.; Fukuyama, J.A.; McMurdie, P.J.; Holmes, S.P. Bioconductor Workflow for Microbiome Data Analysis: From raw reads to community analyses. F1000Research 2016, 5, 1492. [Google Scholar] [CrossRef] [PubMed]
- McMurdie, P.J.; Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 2013, 8, e61217. [Google Scholar] [CrossRef] [Green Version]
- Aitchison, J. On criteria for measures of compositional difference. Math. Geol. 1992, 24, 365–379. [Google Scholar] [CrossRef]
- Aitchison, J.; Pawlowsky-Glahn, V. The one-hour course in compositional data analysis or compositional data analysis is simple. Proc. IAMG 1997, 97, 3–35. [Google Scholar]
- Pawlowsky-Glahn, V.; Egozcue, J.J. Exploring Compositional Data with the CoDa-Dendrogram. Austrian J. Stat. 2011, 40. [Google Scholar] [CrossRef]
- Egozcue, J.; Pawlowsky-Glahn, V. Coda-dendrogram: A new exploratory tool. In Proceedings of the CoDaWork’05, Girona, Spain, 19–21 October 2005. [Google Scholar]
- Egozcue, J.J.; Pawlowsky-Glahn, V.; Gloor, G.B. Linear association in compositional data analysis. Austrian J. Stat. 2018, 47, 3–31. [Google Scholar] [CrossRef]
- Morton, J.T.; Marotz, C.; Washburne, A.; Silverman, J.; Zaramela, L.S.; Edlund, A.; Zengler, K.; Knight, R. Establishing microbial composition measurement standards with reference frames. Nat. Commun. 2019, 10, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Bolyen, E.; Rideout, J.R.; Dillon, M.R.; Bokulich, N.A.; Abnet, C.C.; Al-Ghalith, G.A.; Alexander, H.; Alm, E.J.; Arumugam, M.; Asnicar, F.; et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019, 37, 852–857. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Core Team: Vienna, Austria, 2018. [Google Scholar]
- Uritskiy, G.V.; Diruggiero, J.; Taylor, J. MetaWRAP-A flexible pipeline for genome-resolved metagenomic data analysis. Microbiome 2018, 6, 158. [Google Scholar] [CrossRef] [Green Version]
- Li, D.; Liu, C.-M.; Luo, R.; Sadakane, K.; Lam, T.-W. MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 2015, 31, 1674–1676. [Google Scholar] [CrossRef] [Green Version]
- Kang, D.D.; Li, F.; Kirton, E.; Thomas, A.; Egan, R.; An, H.; Wang, Z. MetaBAT 2: An adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 2019, 7, e7359. [Google Scholar] [CrossRef]
- Wu, Y.-W.; Simmons, B.A.; Singer, S.W. MaxBin 2.0: An automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 2016, 32, 605–607. [Google Scholar] [CrossRef]
- Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [Green Version]
- Escapa, I.F.; Chen, T.; Huang, Y.; Gajare, P.; Dewhirst, F.E.; Lemon, K.P. New Insights into Human Nostril Microbiome from the Expanded Human Oral Microbiome Database (eHOMD): A Resource for the Microbiome of the Human Aerodigestive Tract. MSystems 2018, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parks, D.H.; Imelfort, M.; Skennerton, C.T.; Hugenholtz, P.; Tyson, G.W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015, 25, 1043–1055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Von Meijenfeldt, F.A.B.; Arkhipova, K.; Cambuy, D.D.; Coutinho, F.H.; Dutilh, B.E. Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT. Genome Biol. 2019, 20, 217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lalla, E.; Papapanou, P.N. Diabetes mellitus and periodontitis: A tale of two common interrelated diseases. Nat. Rev. Endocrinol. 2011, 7, 738–748. [Google Scholar] [CrossRef]
- Preshaw, P.M.; Alba, A.L.; Herrera, D.; Jepsen, S.; Konstantinidis, A.; Makrilakis, K.; Taylor, R. Periodontitis and diabetes: A two-way relationship. Diabetologia 2012, 55, 21–31. [Google Scholar] [CrossRef] [Green Version]
- Bissett, S.; Pumerantz, A.; Preshaw, P. Periodontal disease and diabetes. J. Diabetes Nurs. 2015, 19, 134–140. [Google Scholar]
- Graziani, F.; Gennai, S.; Solini, A.; Petrini, M. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes an update of the EFP-AAP review. J. Clin. Periodontol. 2018, 45, 167–187. [Google Scholar] [CrossRef] [PubMed]
- Preshaw, P.M.; Bissett, S.M. Periodontitis and diabetes. Br. Dent. J. 2019, 227, 577–584. [Google Scholar] [CrossRef]
- Marsh, P.D.; Do, T.; Beighton, D.; Devine, D.A. Influence of saliva on the oral microbiota. Periodontol. 2000 2016, 70, 80–92. [Google Scholar] [CrossRef]
- Woldeamlak, B.; Yirdaw, K.; Biadgo, B. Role of Gut Microbiota in Type 2 Diabetes Mellitus and Its Complications: Novel Insights and Potential Intervention Strategies. Korean J. Gastroenterol. 2019, 74, 314–320. [Google Scholar] [CrossRef]
- Wang, J.; Qin, J.; Li, Y.; Cai, Z.; Li, S.; Zhu, J.; Zhang, F.; Liang, S.; Zhang, W.; Guan, Y.; et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012, 490, 55–60. [Google Scholar] [CrossRef]
- Karlsson, F.H.; Tremaroli, V.; Nookaew, I.; Bergström, G.; Behre, C.J.; Fagerberg, B.; Nielsen, J.; Bäckhed, F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 2013, 498, 99–103. [Google Scholar] [CrossRef]
- Wu, X.; Ma, C.; Han, L.; Nawaz, M.; Gao, F.; Zhang, X.; Yu, P.; Zhao, C.; Li, L.; Zhou, A.; et al. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr. Microbiol. 2010, 61, 69–78. [Google Scholar] [CrossRef] [PubMed]
- Larsen, N.; Vogensen, F.K.; Van Den Berg, F.W.J.; Nielsen, D.S.; Andreasen, A.S.; Pedersen, B.K.; Al-Soud, W.A.; Sørensen, S.J.; Hansen, L.H.; Jakobsen, M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 2010, 5, e9085. [Google Scholar] [CrossRef]
- Delzenne, N.M.; Cani, P.D. Gut microbiota and the pathogenesis of insulin resistance. Curr. Diabetes Rep. 2011, 11, 154–159. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kootte, R.S.; Vrieze, A.; Holleman, F.; Dallinga-Thie, G.M.; Zoetendal, E.G.; de Vos, W.M.; Groen, A.K.; Hoekstra, J.B.L.; Stroes, E.S.; Nieuwdorp, M. The therapeutic potential of manipulating gut microbiota in obesity and type 2 diabetes mellitus. Diabetes Obes. Metab. 2012, 14, 112–120. [Google Scholar] [CrossRef] [PubMed]
- Sohail, M.U.; Althani, A.; Anwar, H.; Rizzi, R.; Marei, H.E. Role of the Gastrointestinal Tract Microbiome in the Pathophysiology of Diabetes Mellitus. J. Diabetes Res. 2017, 2017. [Google Scholar] [CrossRef] [PubMed]
- Goodrich, J.K.; Waters, J.L.; Poole, A.C.; Sutter, J.L.; Koren, O.; Blekhman, R.; Beaumont, M.; Van Treuren, W.; Knight, R.; Bell, J.T.; et al. Human genetics shape the gut microbiome. Cell 2014, 159, 789–799. [Google Scholar] [CrossRef] [Green Version]
- Arimatsu, K.; Yamada, H.; Miyazawa, H.; Minagawa, T.; Nakajima, M.; Ryder, M.I.; Gotoh, K.; Motooka, D.; Nakamura, S.; Iida, T.; et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci. Rep. 2014, 4. [Google Scholar] [CrossRef] [Green Version]
- Nakajima, M.; Arimatsu, K.; Kato, T.; Matsuda, Y.; Minagawa, T.; Takahashi, N.; Ohno, H.; Yamazaki, K. Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver. PLoS ONE 2015, 10, e0134234. [Google Scholar] [CrossRef] [Green Version]
- Soffientini, U.; Caridis, A.M.; Dolan, S.; Graham, A. Intracellular cholesterol transporters and modulation of hepatic lipid metabolism: Implications for diabetic dyslipidaemia and steatosis. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2014, 1841, 1372–1382. [Google Scholar] [CrossRef] [Green Version]
- Griffen, A.L.; Beall, C.J.; Campbell, J.H.; Firestone, N.D.; Kumar, P.S.; Yang, Z.K.; Podar, M.; Leys, E.J. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 2012, 6, 1176–1185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kistler, J.O.; Booth, V.; Bradshaw, D.J.; Wade, W.G. Bacterial Community Development in Experimental Gingivitis. PLoS ONE 2013, 8, e71227. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wolcott, R.; Costerton, J.W.; Raoult, D.; Cutler, S.J. The polymicrobial nature of biofilm infection. Clin. Microbiol. Infect. 2013, 19, 107–112. [Google Scholar] [CrossRef] [Green Version]
- Tam, J.; Hoffmann, T.; Fischer, S.; Bornstein, S.; Gräler, J.; Noack, B. Obesity alters composition and diversity of the oral microbiota in patients with type 2 diabetes mellitus independently of glycemic control. PLoS ONE 2018, 13, e0204724. [Google Scholar] [CrossRef]
- Yamashita, Y.; Takeshita, T. The oral microbiome and human health. J. Oral Sci. 2017, 59, 201–206. [Google Scholar] [CrossRef] [Green Version]
- Abusleme, L.; Dupuy, A.K.; Dutzan, N.; Silva, N.; Burleson, J.A.; Strausbaugh, L.D.; Gamonal, J.; Diaz, P.I. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013, 7, 1016–1025. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ge, X.; Rodriguez, R.; Trinh, M.; Gunsolley, J.; Xu, P. Oral Microbiome of Deep and Shallow Dental Pockets In Chronic Periodontitis. PLoS ONE 2013, 8, 65520. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; He, J.; He, Z.; Zhou, Y.; Yuan, M.; Xu, X.; Sun, F.; Liu, C.; Li, J.; Xie, W.; et al. Phylogenetic and functional gene structure shifts of the oral microbiomes in periodontitis patients. ISME J. 2014, 8, 1879–1891. [Google Scholar] [CrossRef] [Green Version]
- Kirst, M.E.; Li, E.C.; Alfant, B.; Chi, Y.Y.; Walker, C.; Magnusson, I.; Wanga, G.P. Dysbiosis and alterations in predicted functions of the subgingival microbiome in chronic periodontitis. Appl. Environ. Microbiol. 2015, 81, 783–793. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Faller, L.L.; Klitgord, N.; Mazumdar, V.; Ghodsi, M.; Sommer, D.D.; Gibbons, T.R.; Treangen, T.J.; Chang, Y.C.; Li, S.; et al. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS ONE 2012, 7, e37919. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Qi, J.; Zhao, H.; He, S.; Zhang, Y.; Wei, S.; Zhao, F. Metagenomic sequencing reveals microbiota and its functional potential associated with periodontal disease. Sci. Rep. 2013, 3. [Google Scholar] [CrossRef] [PubMed]
- Zhou, M.; Rong, R.; Munro, D.; Zhu, C.; Gao, X.; Zhang, Q.; Dong, Q. Investigation of the Effect of Type 2 Diabetes Mellitus on Subgingival Plaque Microbiota by High-Throughput 16S rDNA Pyrosequencing. PLoS ONE 2013, 8, e61516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pearce, M.A.; Devine, D.A.; Dixon, R.A.; Van Steenbergen, T.J.M. Genetic heterogeneity in Prevotella intermedia, Prevotella nigrescens, Prevotella corporis and related species isolated from oral and nonoral sites. Oral Microbiol. Immunol. 2000, 15, 89–95. [Google Scholar] [CrossRef] [PubMed]
- Luong, T.T.; Tirgar, R.; Reardon-Robinson, M.E.; Joachimiak, A.; Osipiuk, J.; Ton-That, H. Structural basis of a thiol-disulfide oxidoreductase in the hedgehog-forming actinobacterium Corynebacterium matruchotii. J. Bacteriol. 2018, 200. [Google Scholar] [CrossRef] [Green Version]
Parameters | Study Group (Subjects) | One-Way ANOVA | ||||
---|---|---|---|---|---|---|
CPT2DM (n = 15) | CP (n = 15) | Control (n = 16) | F | p | ||
Sex | Male | 7 | 7 | 8 | 0.080 | 0.786 |
Female | 8 | 8 | 8 | |||
Age | Male | 57.8 ± 6.3 | 55.7 ± 9.6 | 48.2 ± 5.7 | 2.739 | 0.142 |
Female | 57.9 ± 6.4 | 56.2 ± 8.6 | 48.9 ± 6.7 | |||
BMI * | 25.0–29.9 kg/m2 | 4 * | 12 | 10 | 5.942 | 0.019 * |
30.0–34.9 kg/m2 | 5 * | 3 | 5 | |||
35.0–45.9 kg/m2 | 6 * | 0 | 1 |
Variable | Study Group, Median (Min; Max) | Wilcoxon Rank Sum Test p-Value | |||
---|---|---|---|---|---|
CPT2DM (n = 15) | CP (n = 15) | Control (n = 16) | |||
Dental status indices | PHP | 0.7 (0; 2.1) | 1.3 (0.6; 2.1) | 0.2 (0; 0.7) | p(CP2DM-CP) = 0.234 p(CPT2DM-Control) = 0.085 p(CP-Control) < 0.010 * |
OHI-S | 1.4 (0.4; 4.5) | 1.4 (0.4; 3.3) | 1.8 (0.5; 3.1) | p(CP2DM-CP) = 0.718 p(CPT2DM-Control) = 0.627 p(CP-Control) = 0.958 | |
CAL | 3.9 (3.0; 4.5) | 3.8 (3.4; 4.3) | 0.8 (0; 1.1) | p(CP2DM-CP) = 0.697 p(CPT2DM-Control) < 0.001 * p(CP-Control) < 0.001 * | |
MMI | 0.8 (0; 2.0) | 0.5 (0; 2.0) | 0 (0; 1.0) | p(CP2DM-CP) = 0.409 p(CPT2DM-Control) = 0.056 p(CP-Control) = 0.122 | |
TL | 0 (0; 0) | 0.05 (0; 1.0) | 0 (0; 0) | p(CP2DM-CP) = 0.697 p(CPT2DM-Control) = 0.998 p(CP-Control) = 0.874 | |
PBI | 0.34 (0; 0.90) | 0.30 (0.10; 0.90) | 0.38 (0; 0.84) | p(CP2DM-CP) = 0.697 p(CPT2DM-Control) = 0.584 p(CP-Control) = 0.874 | |
Diabetes criteria | Glucose (mmol/L) | 5.7 (5.0; 7.8) | 5.6 (5.1; 6.1) | 5.4 (4.4; 6.6) | p(CP2DM-CP) = 0.748 p(CPT2DM-Control) = 0.665 p(CP-Control) = 0.589 |
Glycosylated hemoglobin (HbA1c) | 7.5 (6.5; 8.0) | 4.5 (3.0; 6.0) | 3.5 (3.0; 5.0) | p(CP2DM-CP) < 0.001 * p(CPT2DM-Control) < 0.001 * p(CP-Control) = 0.067 |
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Balmasova, I.P.; Olekhnovich, E.I.; Klimina, K.M.; Korenkova, A.A.; Vakhitova, M.T.; Babaev, E.A.; Ovchinnikova, L.A.; Lomakin, Y.A.; Smirnov, I.V.; Tsarev, V.N.; et al. Drift of the Subgingival Periodontal Microbiome during Chronic Periodontitis in Type 2 Diabetes Mellitus Patients. Pathogens 2021, 10, 504. https://doi.org/10.3390/pathogens10050504
Balmasova IP, Olekhnovich EI, Klimina KM, Korenkova AA, Vakhitova MT, Babaev EA, Ovchinnikova LA, Lomakin YA, Smirnov IV, Tsarev VN, et al. Drift of the Subgingival Periodontal Microbiome during Chronic Periodontitis in Type 2 Diabetes Mellitus Patients. Pathogens. 2021; 10(5):504. https://doi.org/10.3390/pathogens10050504
Chicago/Turabian StyleBalmasova, Irina P., Evgenii I. Olekhnovich, Ksenia M. Klimina, Anna A. Korenkova, Maria T. Vakhitova, Elmar A. Babaev, Leyla A. Ovchinnikova, Yakov A. Lomakin, Ivan V. Smirnov, Victor N. Tsarev, and et al. 2021. "Drift of the Subgingival Periodontal Microbiome during Chronic Periodontitis in Type 2 Diabetes Mellitus Patients" Pathogens 10, no. 5: 504. https://doi.org/10.3390/pathogens10050504
APA StyleBalmasova, I. P., Olekhnovich, E. I., Klimina, K. M., Korenkova, A. A., Vakhitova, M. T., Babaev, E. A., Ovchinnikova, L. A., Lomakin, Y. A., Smirnov, I. V., Tsarev, V. N., Mkrtumyan, A. M., Belogurov, A. A., Jr., Gabibov, A. G., Ilina, E. N., & Arutyunov, S. D. (2021). Drift of the Subgingival Periodontal Microbiome during Chronic Periodontitis in Type 2 Diabetes Mellitus Patients. Pathogens, 10(5), 504. https://doi.org/10.3390/pathogens10050504