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Published in: Endocrine 3/2020

01-06-2020 | Oral Microbiota | Original Article

The oral microbiome profile and biomarker in Chinese type 2 diabetes mellitus patients

Authors: Bin Chen, Zhe Wang, Jingwen Wang, Xinhuan Su, Junjie Yang, Qunye Zhang, Lei Zhang

Published in: Endocrine | Issue 3/2020

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Abstract

Purpose

Oral microbiota maintains a dynamic ecological balance with the host. However, a disruption in this balance can lead to oral diseases such as dental caries and periodontitis. Several studies suggest differences in microbial composition in the oral cavity between patients with T2DM and nondiabetic patients. However, there is inadequate oral microbiome-related data from Chinese patients with T2DM, and the difference in microbiome profile between Chinese patients with T2DM and other ethnicities needs to be investigated further.

Method

Oral swab samples were collected from 280 adult patients with T2DM and 162 healthy controls. Illumina sequencing was performed on oral samples targeting V1–V2 region of 16S rRNA gene and sequence analysis was carried in the QIIME.

Results

Patients with T2DM and healthy cohorts exhibited distinct oral microbial clusters based on principal coordinate analysis (PCoA). The Firmicutes/Bacteroidetes ratio increased in T2DM and T2DM patients presented significantly higher numbers of Neisseria, Streptococcus, Haemophilus, and Pseudomonas genera, and lower numbers of Acinetobacteria compared with healthy controls. When compared with the available published data of oral and gut microbiome associated with T2DM patients, we found the ratio of Firmicutes/Bacteroidetes and the abundance of Haemophilus could be a specific microbial biomarker in Chinese patients with T2DM.

Conclusions

Our study revealed a significant difference in the oral microbiota between T2DM patients and healthy individuals. We identified 25 taxa, including 6 genera, with significant difference in abundance between T2DM and healthy controls.
Literature
1.
go back to reference N.H. Cho, J.E. Shaw, S. Karuranga, Y. Huang, R.F.J. Da, A.W. Ohlrogge, B. Malanda, IDF diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res. Clin. Pract. 138, 271 (2018)CrossRef N.H. Cho, J.E. Shaw, S. Karuranga, Y. Huang, R.F.J. Da, A.W. Ohlrogge, B. Malanda, IDF diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res. Clin. Pract. 138, 271 (2018)CrossRef
3.
go back to reference M.E. Cerf, Beta cell dysfunction and insulin resistance. Front. Endocrinol. 4, 37 (2013) M.E. Cerf, Beta cell dysfunction and insulin resistance. Front. Endocrinol. 4, 37 (2013)
4.
go back to reference K.N. Keane, E.K. Calton, R. Carlessi, P.H. Hart, P. Newsholme, The bioenergetics of inflammation: insights into obesity and type 2 diabetes. Eur. J. Clin. Nutr. 71(7), 904–912 (2017)CrossRef K.N. Keane, E.K. Calton, R. Carlessi, P.H. Hart, P. Newsholme, The bioenergetics of inflammation: insights into obesity and type 2 diabetes. Eur. J. Clin. Nutr. 71(7), 904–912 (2017)CrossRef
5.
go back to reference F. Llambés, S. Ariasherrera, R. Caffesse, Relationship between diabetes and periodontal infection. World J. Diabetes 6(7), 927–935 (2015)CrossRef F. Llambés, S. Ariasherrera, R. Caffesse, Relationship between diabetes and periodontal infection. World J. Diabetes 6(7), 927–935 (2015)CrossRef
6.
go back to reference P.M. Preshaw, A.L. Alba, D. Herrera, S. Jepsen, A. Konstantinidis, K. Makrilakis, R. Taylor, Periodontitis and diabetes: a two-way relationship. Diabetologia 55(1), 21–31 (2012)CrossRef P.M. Preshaw, A.L. Alba, D. Herrera, S. Jepsen, A. Konstantinidis, K. Makrilakis, R. Taylor, Periodontitis and diabetes: a two-way relationship. Diabetologia 55(1), 21–31 (2012)CrossRef
7.
go back to reference R.C. Casarin, A. Barbagallo, T. Meulman, V.R. Santos, E.A. Sallum, F.H. Nociti, P.M. Duarte, M.Z. Casati, R.B. Gonçalves, Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J. Periodontal Res. 48(1), 30–36 (2013)CrossRef R.C. Casarin, A. Barbagallo, T. Meulman, V.R. Santos, E.A. Sallum, F.H. Nociti, P.M. Duarte, M.Z. Casati, R.B. Gonçalves, Subgingival biodiversity in subjects with uncontrolled type-2 diabetes and chronic periodontitis. J. Periodontal Res. 48(1), 30–36 (2013)CrossRef
8.
go back to reference N. Makiura, M. Ojima, Y. Kou, N. Furuta, N. Okahashi, S. Shizukuishi, A. Amano, Relationship of Porphyromonas gingivalis with glycemic level in patients with type 2 diabetes following periodontal treatment. Oral. Microbiol. Immunol. 23(4), 348–351 (2010)CrossRef N. Makiura, M. Ojima, Y. Kou, N. Furuta, N. Okahashi, S. Shizukuishi, A. Amano, Relationship of Porphyromonas gingivalis with glycemic level in patients with type 2 diabetes following periodontal treatment. Oral. Microbiol. Immunol. 23(4), 348–351 (2010)CrossRef
9.
go back to reference F.E. Dewhirst, T. Chen, J. Izard, B.J. Paster, A.C. Tanner, W.H. Yu, A. Lakshmanan, W.G. Wade, The human oral microbiome. J. Bacteriol. 192(19), 5002 (2010)CrossRef F.E. Dewhirst, T. Chen, J. Izard, B.J. Paster, A.C. Tanner, W.H. Yu, A. Lakshmanan, W.G. Wade, The human oral microbiome. J. Bacteriol. 192(19), 5002 (2010)CrossRef
11.
go back to reference M. Kilian, I.L. Chapple, M. Hannig, P.D. Marsh, V. Meuric, A.M. Pedersen, M.S. Tonetti, W.G. Wade, E. Zaura, The oral microbiome—an update for oral healthcare professionals. Br. Dent. J. 221(10), 657 (2016) M. Kilian, I.L. Chapple, M. Hannig, P.D. Marsh, V. Meuric, A.M. Pedersen, M.S. Tonetti, W.G. Wade, E. Zaura, The oral microbiome—an update for oral healthcare professionals. Br. Dent. J. 221(10), 657 (2016)
12.
go back to reference F. Teng, F. Yang, S. Huang, C. Bo, Z. Xu, Prediction of early childhood caries via spatial-temporal variations of oral microbiota. Cell Host Microbe 18(3), 296–306 (2015)CrossRef F. Teng, F. Yang, S. Huang, C. Bo, Z. Xu, Prediction of early childhood caries via spatial-temporal variations of oral microbiota. Cell Host Microbe 18(3), 296–306 (2015)CrossRef
13.
go back to reference C. Chen, C. Hemme, J. Beleno, Z.J. Shi, D. Ning, Y. Qin, Q. Tu, M. Jorgensen, Z. He, L. Wu, Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy. ISME J. 12(5), 1210–1224 (2018)CrossRef C. Chen, C. Hemme, J. Beleno, Z.J. Shi, D. Ning, Y. Qin, Q. Tu, M. Jorgensen, Z. He, L. Wu, Oral microbiota of periodontal health and disease and their changes after nonsurgical periodontal therapy. ISME J. 12(5), 1210–1224 (2018)CrossRef
14.
go back to reference Y.W. Han, X. Wang, Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J. Dent. Res. 92(6), 485–491 (2013)CrossRef Y.W. Han, X. Wang, Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J. Dent. Res. 92(6), 485–491 (2013)CrossRef
15.
go back to reference W.D. Miller, The human mouth as a focus of infection. Lancet 138(3546), 340–342 (1891) W.D. Miller, The human mouth as a focus of infection. Lancet 138(3546), 340–342 (1891)
16.
go back to reference M.L. Metzker, Sequencing technologies—the next generation. Nat. Rev. Genet. 11(1), 31–46 (2010)CrossRef M.L. Metzker, Sequencing technologies—the next generation. Nat. Rev. Genet. 11(1), 31–46 (2010)CrossRef
17.
go back to reference E. Figuero, S. Cuesta-Frechoso, J.M. Tejerina, J.A. Del Castro, D. Herrera, M. Sanz, Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J. Periodontol. 82(10), 1469–1477 (2011)CrossRef E. Figuero, S. Cuesta-Frechoso, J.M. Tejerina, J.A. Del Castro, D. Herrera, M. Sanz, Detection of periodontal bacteria in atheromatous plaque by nested polymerase chain reaction. J. Periodontol. 82(10), 1469–1477 (2011)CrossRef
18.
go back to reference P.N. Madianos, Y.A. Bobetsis, S. Offenbacher, Adverse pregnancy outcomes (APOs) and periodontal disease: pathogenic mechanisms. J. Clin. Periodontol. 40(s14), S170–S180 (2013)PubMed P.N. Madianos, Y.A. Bobetsis, S. Offenbacher, Adverse pregnancy outcomes (APOs) and periodontal disease: pathogenic mechanisms. J. Clin. Periodontol. 40(s14), S170–S180 (2013)PubMed
19.
go back to reference J.M. Goodson, D. Groppo, S. Halem, E. Carpino, Is obesity an oral bacterial disease? J. Dent. Res. 88(6), 519–523 (2009)CrossRef J.M. Goodson, D. Groppo, S. Halem, E. Carpino, Is obesity an oral bacterial disease? J. Dent. Res. 88(6), 519–523 (2009)CrossRef
20.
go back to reference J.C.O. Sardi, C. Duque, G.A.C.G. Camargo, J.F. Hofling, R.B. Gonçalves, Periodontal conditions and prevalence of putative periodontopathogens and Candida spp. in insulin-dependent type 2 diabetic and non-diabetic patients with chronic periodontitis—a pilot study. Arch. Oral. Biol. 56(10), 1098–1105 (2011)CrossRef J.C.O. Sardi, C. Duque, G.A.C.G. Camargo, J.F. Hofling, R.B. Gonçalves, Periodontal conditions and prevalence of putative periodontopathogens and Candida spp. in insulin-dependent type 2 diabetic and non-diabetic patients with chronic periodontitis—a pilot study. Arch. Oral. Biol. 56(10), 1098–1105 (2011)CrossRef
21.
go back to reference R. Anbalagan, P. Srikanth, M. Mani, R. Barani, K.G. Seshadri, R. Janarthanan, Next generation sequencing of oral microbiota in type 2 diabetes mellitus prior to and after neem stick usage and correlation with serum monocyte chemoattractant-1. Diabetes Res. Clin. Pract. 130, 204 (2017)CrossRef R. Anbalagan, P. Srikanth, M. Mani, R. Barani, K.G. Seshadri, R. Janarthanan, Next generation sequencing of oral microbiota in type 2 diabetes mellitus prior to and after neem stick usage and correlation with serum monocyte chemoattractant-1. Diabetes Res. Clin. Pract. 130, 204 (2017)CrossRef
22.
go back to reference T. Ogawa, M. Hondaogawa, K. Ikebe, Y. Notomi, Y. Iwamoto, I. Shirobayashi, S. Hata, M. Kibi, S. Masayasu, S. Sasaki, Characterizations of oral microbiota in elderly nursing home residents with diabetes. J. Oral. Sci. 60(4), 549–555 (2017)CrossRef T. Ogawa, M. Hondaogawa, K. Ikebe, Y. Notomi, Y. Iwamoto, I. Shirobayashi, S. Hata, M. Kibi, S. Masayasu, S. Sasaki, Characterizations of oral microbiota in elderly nursing home residents with diabetes. J. Oral. Sci. 60(4), 549–555 (2017)CrossRef
23.
go back to reference M. Zhou, R. Rong, D. Munro, C. Zhu, X. Gao, Q. Zhang, Q. Dong, Investigation of the effect of type 2 diabetes mellitus on subgingival plaque microbiota by high-throughput 16S rDNA pyrosequencing. PLoS ONE 8(4), e61516 (2013)CrossRef M. Zhou, R. Rong, D. Munro, C. Zhu, X. Gao, Q. Zhang, Q. Dong, Investigation of the effect of type 2 diabetes mellitus on subgingival plaque microbiota by high-throughput 16S rDNA pyrosequencing. PLoS ONE 8(4), e61516 (2013)CrossRef
24.
go back to reference E.J. Ohlrich, M.P. Cullinan, J.W. Leichter, Diabetes, periodontitis, and the subgingival microbiota. J. Oral. Microbiol. 2(2010), 10 (2010)PubMedCentral E.J. Ohlrich, M.P. Cullinan, J.W. Leichter, Diabetes, periodontitis, and the subgingival microbiota. J. Oral. Microbiol. 2(2010), 10 (2010)PubMedCentral
25.
go back to reference F. Fouhy, A.G. Clooney, C. Stanton, M.J. Claesson, P.D. Cotter, 16S rRNA gene sequencing of mock microbial populations- impact of DNA extraction method, primer choice and sequencing platform. BMC Microbiol. 16(1), 123 (2016)CrossRef F. Fouhy, A.G. Clooney, C. Stanton, M.J. Claesson, P.D. Cotter, 16S rRNA gene sequencing of mock microbial populations- impact of DNA extraction method, primer choice and sequencing platform. BMC Microbiol. 16(1), 123 (2016)CrossRef
26.
go back to reference T. Magoč, S.L. Salzberg, FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21), 2957–2963 (2011)CrossRef T. Magoč, S.L. Salzberg, FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21), 2957–2963 (2011)CrossRef
27.
go back to reference R.C. Edgar, Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19), 2460 (2010)CrossRef R.C. Edgar, Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19), 2460 (2010)CrossRef
28.
go back to reference J.R. Cole, Q. Wang, E. Cardenas, J. Fish, B. Chai, R.J. Farris, A.S. Kulamsyedmohideen, D.M. Mcgarrell, T. Marsh, G.M. Garrity, The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141–D145 (2009) J.R. Cole, Q. Wang, E. Cardenas, J. Fish, B. Chai, R.J. Farris, A.S. Kulamsyedmohideen, D.M. Mcgarrell, T. Marsh, G.M. Garrity, The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141–D145 (2009)
29.
go back to reference N. Segata, J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W.S. Garrett, C. Huttenhower, Metagenomic biomarker discovery and explanation. Genome Biol. 12(6), R60 (2011)CrossRef N. Segata, J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W.S. Garrett, C. Huttenhower, Metagenomic biomarker discovery and explanation. Genome Biol. 12(6), R60 (2011)CrossRef
30.
go back to reference L. Dong, J. Yin, J. Zhao, S. Ma, H. Wang, M. Wang, W. Chen, W. Wei, Microbial similarity and preference for specific sites in healthy oral cavity and esophagus. Front. Microbiol. 9, 1603 (2018)CrossRef L. Dong, J. Yin, J. Zhao, S. Ma, H. Wang, M. Wang, W. Chen, W. Wei, Microbial similarity and preference for specific sites in healthy oral cavity and esophagus. Front. Microbiol. 9, 1603 (2018)CrossRef
31.
go back to reference J. Qin, Y. Li, Z. Cai, S. Li, J. Zhu, F. Zhang, S. Liang, W. Zhang, Y. Guan, D. Shen, Y. Peng, D. Zhang, Z. Jie, W. Wu, Y. Qin, W. Xue, J. Li, L. Han, D. Lu, P. Wu, Y. Dai, X. Sun, Z. Li, A. Tang, S. Zhong, X. Li, W. Chen, R. Xu, M. Wang, Q. Feng, M. Gong, J. Yu, Y. Zhang, M. Zhang, T. Hansen, G. Sanchez, J. Raes, G. Falony, S. Okuda, M. Almeida, E. LeChatelier, P. Renault, N. Pons, J.M. Batto, Z. Zhang, H. Chen, R. Yang, W. Zheng, S. Li, H. Yang, J. Wang, S.D. Ehrlich, R. Nielsen, O. Pedersen, K. Kristiansen, J. Wang, A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490(7418), 55–60 (2012). https://doi.org/10.1038/nature11450 CrossRefPubMed J. Qin, Y. Li, Z. Cai, S. Li, J. Zhu, F. Zhang, S. Liang, W. Zhang, Y. Guan, D. Shen, Y. Peng, D. Zhang, Z. Jie, W. Wu, Y. Qin, W. Xue, J. Li, L. Han, D. Lu, P. Wu, Y. Dai, X. Sun, Z. Li, A. Tang, S. Zhong, X. Li, W. Chen, R. Xu, M. Wang, Q. Feng, M. Gong, J. Yu, Y. Zhang, M. Zhang, T. Hansen, G. Sanchez, J. Raes, G. Falony, S. Okuda, M. Almeida, E. LeChatelier, P. Renault, N. Pons, J.M. Batto, Z. Zhang, H. Chen, R. Yang, W. Zheng, S. Li, H. Yang, J. Wang, S.D. Ehrlich, R. Nielsen, O. Pedersen, K. Kristiansen, J. Wang, A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490(7418), 55–60 (2012). https://​doi.​org/​10.​1038/​nature11450 CrossRefPubMed
32.
go back to reference N. Qin, F. Yang, A. Li, E. Prifti, Y. Chen, L. Shao, J. Guo, C.E. Le, J. Yao, L. Wu, Alterations of the human gut microbiome in liver cirrhosis. Nature 513(7516), 59–64 (2014)CrossRef N. Qin, F. Yang, A. Li, E. Prifti, Y. Chen, L. Shao, J. Guo, C.E. Le, J. Yao, L. Wu, Alterations of the human gut microbiome in liver cirrhosis. Nature 513(7516), 59–64 (2014)CrossRef
33.
go back to reference X. Zhang, D. Zhang, H. Jia, Q. Feng, D. Wang, D. Liang, X. Wu, J. Li, L. Tang, Y. Li, Z. Lan, B. Chen, Y. Li, H. Zhong, H. Xie, Z. Jie, W. Chen, S. Tang, X. Xu, X. Wang, X. Cai, S. Liu, Y. Xia, J. Li, X. Qiao, J.Y. Al-Aama, H. Chen, L. Wang, Q.J. Wu, F. Zhang, W. Zheng, Y. Li, M. Zhang, G. Luo, W. Xue, L. Xiao, J. Li, W. Chen, X. Xu, Y. Yin, H. Yang, J. Wang, K. Kristiansen, L. Liu, T. Li, Q. Huang, Y. Li, J. Wang, The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat. Med. 21(8), 895–905 (2015). https://doi.org/10.1038/nm.3914 CrossRefPubMed X. Zhang, D. Zhang, H. Jia, Q. Feng, D. Wang, D. Liang, X. Wu, J. Li, L. Tang, Y. Li, Z. Lan, B. Chen, Y. Li, H. Zhong, H. Xie, Z. Jie, W. Chen, S. Tang, X. Xu, X. Wang, X. Cai, S. Liu, Y. Xia, J. Li, X. Qiao, J.Y. Al-Aama, H. Chen, L. Wang, Q.J. Wu, F. Zhang, W. Zheng, Y. Li, M. Zhang, G. Luo, W. Xue, L. Xiao, J. Li, W. Chen, X. Xu, Y. Yin, H. Yang, J. Wang, K. Kristiansen, L. Liu, T. Li, Q. Huang, Y. Li, J. Wang, The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat. Med. 21(8), 895–905 (2015). https://​doi.​org/​10.​1038/​nm.​3914 CrossRefPubMed
35.
go back to reference M. Remely, E. Aumueller, D. Jahn, B. Hippe, H. Brath, A.G. Haslberger, Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity. Benef. Microbes 5(1), 33–43 (2014)CrossRef M. Remely, E. Aumueller, D. Jahn, B. Hippe, H. Brath, A.G. Haslberger, Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity. Benef. Microbes 5(1), 33–43 (2014)CrossRef
36.
go back to reference K. Forslund, F. Hildebrand, T. Nielsen, G. Falony, E. Le Chatelier, S. Sunagawa, E. Prifti, S. Vieira-Silva, V. Gudmundsdottir, H.K. Pedersen, M. Arumugam, K. Kristiansen, A.Y. Voigt, H. Vestergaard, R. Hercog, P.I. Costea, J.R. Kultima, J. Li, T. Jorgensen, F. Levenez, J. Dore, H.I.Tc Meta, H.B. Nielsen, S. Brunak, J. Raes, T. Hansen, J. Wang, S.D. Ehrlich, P. Bork, O. Pedersen, Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528(7581), 262–266 (2015). https://doi.org/10.1038/nature15766 CrossRefPubMedPubMedCentral K. Forslund, F. Hildebrand, T. Nielsen, G. Falony, E. Le Chatelier, S. Sunagawa, E. Prifti, S. Vieira-Silva, V. Gudmundsdottir, H.K. Pedersen, M. Arumugam, K. Kristiansen, A.Y. Voigt, H. Vestergaard, R. Hercog, P.I. Costea, J.R. Kultima, J. Li, T. Jorgensen, F. Levenez, J. Dore, H.I.Tc Meta, H.B. Nielsen, S. Brunak, J. Raes, T. Hansen, J. Wang, S.D. Ehrlich, P. Bork, O. Pedersen, Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528(7581), 262–266 (2015). https://​doi.​org/​10.​1038/​nature15766 CrossRefPubMedPubMedCentral
37.
go back to reference A. Rodriguez-Hernandez, L. Marquez-Corono, A.-P. Pontigo-Loyola, L.A. Ximenez-Fyvie, Subgingival microbiota of an indigenous mexican population with chronic periodontitis and T2DM, 7(2), 00238 (2017) A. Rodriguez-Hernandez, L. Marquez-Corono, A.-P. Pontigo-Loyola, L.A. Ximenez-Fyvie, Subgingival microbiota of an indigenous mexican population with chronic periodontitis and T2DM, 7(2), 00238 (2017)
38.
go back to reference K. Kampoo, Bacteriological Investigations of the Human Oral Microbiota in Health and Disease, Doctoral dissertation, University of Manchester (2011) K. Kampoo, Bacteriological Investigations of the Human Oral Microbiota in Health and Disease, Doctoral dissertation, University of Manchester (2011)
42.
go back to reference H. Wu, E. Esteve, V. Tremaroli, M.T. Khan, R. Caesar, L. Manneras-Holm, M. Stahlman, L.M. Olsson, M. Serino, M. Planas-Felix, G. Xifra, J.M. Mercader, D. Torrents, R. Burcelin, W. Ricart, R. Perkins, J.M. Fernandez-Real, F. Backhed,, Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat. Med. 23(7), 850–858 (2017). https://doi.org/10.1038/nm.4345 CrossRefPubMed H. Wu, E. Esteve, V. Tremaroli, M.T. Khan, R. Caesar, L. Manneras-Holm, M. Stahlman, L.M. Olsson, M. Serino, M. Planas-Felix, G. Xifra, J.M. Mercader, D. Torrents, R. Burcelin, W. Ricart, R. Perkins, J.M. Fernandez-Real, F. Backhed,, Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat. Med. 23(7), 850–858 (2017). https://​doi.​org/​10.​1038/​nm.​4345 CrossRefPubMed
43.
go back to reference R. Pryor, P. Norvaisas, G. Marinos, L. Best, L.B. Thingholm, L.M. Quintaneiro, W. De Haes, D. Esser, S. Waschina, C. Lujan, R.L. Smith, T.A. Scott, D. Martinez-Martinez, O. Woodward, K. Bryson, M. Laudes, W. Lieb, R.H. Houtkooper, A. Franke, L. Temmerman, I. Bjedov, H.M. Cocheme, C. Kaleta, F. Cabreiro, Host-microbe-drug-nutrient screen identifies bacterial effectors of metformin therapy. Cell 178(6), 1299–1312.e29 (2019). https://doi.org/10.1016/j.cell.2019.08.003 CrossRefPubMedPubMedCentral R. Pryor, P. Norvaisas, G. Marinos, L. Best, L.B. Thingholm, L.M. Quintaneiro, W. De Haes, D. Esser, S. Waschina, C. Lujan, R.L. Smith, T.A. Scott, D. Martinez-Martinez, O. Woodward, K. Bryson, M. Laudes, W. Lieb, R.H. Houtkooper, A. Franke, L. Temmerman, I. Bjedov, H.M. Cocheme, C. Kaleta, F. Cabreiro, Host-microbe-drug-nutrient screen identifies bacterial effectors of metformin therapy. Cell 178(6), 1299–1312.e29 (2019). https://​doi.​org/​10.​1016/​j.​cell.​2019.​08.​003 CrossRefPubMedPubMedCentral
Metadata
Title
The oral microbiome profile and biomarker in Chinese type 2 diabetes mellitus patients
Authors
Bin Chen
Zhe Wang
Jingwen Wang
Xinhuan Su
Junjie Yang
Qunye Zhang
Lei Zhang
Publication date
01-06-2020
Publisher
Springer US
Published in
Endocrine / Issue 3/2020
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-020-02269-6

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