Skip to main content
Erschienen in: Acta Diabetologica 5/2019

19.03.2019 | Original Article

Understanding the gut–kidney axis among biopsy-proven diabetic nephropathy, type 2 diabetes mellitus and healthy controls: an analysis of the gut microbiota composition

verfasst von: Sibei Tao, Lingzhi Li, Ling Li, Yuan Liu, Qian Ren, Min Shi, Jing Liu, Jing Jiang, Huichao Ma, Zhuo Huang, Zijing Xia, Jing Pan, Tiantian Wei, Yan Wang, Peiyun Li, Tian Lan, Xi Tang, Xiaoxi Zeng, Song Lei, Huairong Tang, Liang Ma, Ping Fu

Erschienen in: Acta Diabetologica | Ausgabe 5/2019

Einloggen, um Zugang zu erhalten

Abstract

Aims

Type 2 diabetes mellitus (T2DM) has a rising prevalence and gut microbiota involvement is increasingly recognized. Diabetic nephropathy (DN) is a major complication of T2DM. The aim of the study was to understand the gut–kidney axis by an analysis of gut microbiota composition among biopsy-proven DN, T2DM without kidney disease, and healthy control.

Methods

Fecal samples were collected from 14 DNs, 14 age/gender-matched T2DMs without renal diseases (DM), 14 age and gender-matched healthy controls (HC) and household contacts (HH) of DM group. The microbiota composition was analyzed by 16sRNA microbial profiling approach.

Results

Substantial differences were found in the richness of gut microbiota and the variation of bacteria population in DM compared to HC, and DN compared to DM, respectively. DM could be accurately distinguished from age/gender-matched healthy controls by the variable of genus g_Prevotella_9 (AUC = 0.9), and DN patients could be accurately distinguished from age/gender-matched DM by the variables of two genera (g_Escherichia-Shigella and g_Prevotella_9, AUC = 0.86). The microbiota composition of HH group was close to that of HC group, and was different from DM group. Under the same diet, DM could be more accurately detected by the same genus (g_Prevotella_9, AUC = 0.92).

Conclusion

Gut microbiota composition was explored to be related to the occurrence of biopsy-proven DN from DM. DM could be distinguished from HC by detecting g_Prevotella_9 level in feces, while DN was different from DM by the variables of g_Escherichia-Shigella and g_Prevotella_9, which potentially contributed to the physiopathological diagnosis of DN from DM.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Demmer RT, Zuk AM, Rosenbaum M, Desvarieux M (2013) Prevalence of diagnosed and undiagnosed type 2 diabetes mellitus among US adolescents: results from the continuous NHANES, 1999–2010. Am J Epidemiol 178(7):1106–1113PubMedPubMedCentral Demmer RT, Zuk AM, Rosenbaum M, Desvarieux M (2013) Prevalence of diagnosed and undiagnosed type 2 diabetes mellitus among US adolescents: results from the continuous NHANES, 1999–2010. Am J Epidemiol 178(7):1106–1113PubMedPubMedCentral
2.
Zurück zum Zitat Ma RC, Lin X, Jia W (2014) Causes of type 2 diabetes in China. Lancet Diabetes Endocrinol 2(12):980–991PubMed Ma RC, Lin X, Jia W (2014) Causes of type 2 diabetes in China. Lancet Diabetes Endocrinol 2(12):980–991PubMed
3.
Zurück zum Zitat Pitts-Tucker T (2012) Asian and Afro-Caribbean Britons have double the risk of type 2 diabetes. Br Med J 345:e6135 Pitts-Tucker T (2012) Asian and Afro-Caribbean Britons have double the risk of type 2 diabetes. Br Med J 345:e6135
4.
Zurück zum Zitat Schellenberg ES, Dryden DM, Vandermeer B, Ha C, Korownyk C (2013) Lifestyle interventions for patients with and at risk for type 2 diabetes: a systematic review and meta-analysis. Ann Intern Med 159(8):543–551PubMed Schellenberg ES, Dryden DM, Vandermeer B, Ha C, Korownyk C (2013) Lifestyle interventions for patients with and at risk for type 2 diabetes: a systematic review and meta-analysis. Ann Intern Med 159(8):543–551PubMed
5.
Zurück zum Zitat Karlsson FH, Tremaroli V, Nookaew I et al (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498(7452):99–103PubMed Karlsson FH, Tremaroli V, Nookaew I et al (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498(7452):99–103PubMed
6.
Zurück zum Zitat Qin J, Li Y, Cai Z et al (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490(7418):55–60PubMed Qin J, Li Y, Cai Z et al (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490(7418):55–60PubMed
7.
Zurück zum Zitat Zhang X, Shen D, Fang Z et al (2013) Human gut microbiota changes reveal the progression of glucose intolerance. PLoS One 8(8):e71108PubMedPubMedCentral Zhang X, Shen D, Fang Z et al (2013) Human gut microbiota changes reveal the progression of glucose intolerance. PLoS One 8(8):e71108PubMedPubMedCentral
8.
Zurück zum Zitat de Vos WM, Nieuwdorp M (2013) Genomics. A gut prediction. Nature 498(7452):48–49PubMed de Vos WM, Nieuwdorp M (2013) Genomics. A gut prediction. Nature 498(7452):48–49PubMed
9.
Zurück zum Zitat Lau E, Carvalho D, Pina-Vaz C, Barbosa JA, Freitas P (2015) Beyond gut microbiota: understanding obesity and type 2 diabetes. Hormones 14(3):358–369PubMed Lau E, Carvalho D, Pina-Vaz C, Barbosa JA, Freitas P (2015) Beyond gut microbiota: understanding obesity and type 2 diabetes. Hormones 14(3):358–369PubMed
10.
Zurück zum Zitat Barsoum RS (2006) Chronic kidney disease in the developing world. N Engl J Med 354(10):997–999PubMed Barsoum RS (2006) Chronic kidney disease in the developing world. N Engl J Med 354(10):997–999PubMed
11.
Zurück zum Zitat Du P, Fan B, Han H et al (2013) NOD2 promotes renal injury by exacerbating inflammation and podocyte insulin resistance in diabetic nephropathy. Kidney Int 84(2):265–276PubMed Du P, Fan B, Han H et al (2013) NOD2 promotes renal injury by exacerbating inflammation and podocyte insulin resistance in diabetic nephropathy. Kidney Int 84(2):265–276PubMed
12.
Zurück zum Zitat Zhang L, Long J, Jiang W et al (2016) Trends in chronic kidney disease in China. N Engl J Med 375(9):905–906PubMed Zhang L, Long J, Jiang W et al (2016) Trends in chronic kidney disease in China. N Engl J Med 375(9):905–906PubMed
13.
Zurück zum Zitat de Boer IH, Rue TC, Hall YN, Heagerty PJ, Weiss NS, Himmelfarb J (2011) Temporal trends in the prevalence of diabetic kidney disease in the United States. JAMA 305(24):2532–2539PubMedPubMedCentral de Boer IH, Rue TC, Hall YN, Heagerty PJ, Weiss NS, Himmelfarb J (2011) Temporal trends in the prevalence of diabetic kidney disease in the United States. JAMA 305(24):2532–2539PubMedPubMedCentral
14.
Zurück zum Zitat Afkarian M, Sachs MC, Kestenbaum B et al (2013) Kidney disease and increased mortality risk in type 2 diabetes. J Am Soc Nephrol 24(2):302–308PubMedPubMedCentral Afkarian M, Sachs MC, Kestenbaum B et al (2013) Kidney disease and increased mortality risk in type 2 diabetes. J Am Soc Nephrol 24(2):302–308PubMedPubMedCentral
15.
Zurück zum Zitat Fineberg D, Jandeleit-Dahm KA, Cooper ME (2013) Diabetic nephropathy: diagnosis and treatment. Nat Rev Endocrinol 9(12):713–723PubMed Fineberg D, Jandeleit-Dahm KA, Cooper ME (2013) Diabetic nephropathy: diagnosis and treatment. Nat Rev Endocrinol 9(12):713–723PubMed
16.
Zurück zum Zitat Li L, Ma L, Fu P (2017) Gut microbiota-derived short-chain fatty acids and kidney diseases. Drug Des Dev Ther 11:3531–3542 Li L, Ma L, Fu P (2017) Gut microbiota-derived short-chain fatty acids and kidney diseases. Drug Des Dev Ther 11:3531–3542
17.
Zurück zum Zitat Ramezani A, Raj DS (2014) The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol 25(4):657–670PubMed Ramezani A, Raj DS (2014) The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol 25(4):657–670PubMed
18.
Zurück zum Zitat Cai L, Wu H, Li D, Zhou K, Zou F (2015) Type 2 diabetes biomarkers of human gut microbiota selected via iterative sure independent screening method. PLoS One 10(10):e0140827PubMedPubMedCentral Cai L, Wu H, Li D, Zhou K, Zou F (2015) Type 2 diabetes biomarkers of human gut microbiota selected via iterative sure independent screening method. PLoS One 10(10):e0140827PubMedPubMedCentral
19.
Zurück zum Zitat Guo Z, Zhang J, Wang Z et al (2016) Intestinal microbiota distinguish gout patients from healthy humans. Sci Rep 6:20602PubMedPubMedCentral Guo Z, Zhang J, Wang Z et al (2016) Intestinal microbiota distinguish gout patients from healthy humans. Sci Rep 6:20602PubMedPubMedCentral
20.
Zurück zum Zitat Vaziri ND, Wong J, Pahl M et al (2013) Chronic kidney disease alters intestinal microbial flora. Kidney Int 83(2):308–315PubMed Vaziri ND, Wong J, Pahl M et al (2013) Chronic kidney disease alters intestinal microbial flora. Kidney Int 83(2):308–315PubMed
21.
Zurück zum Zitat Levey AS, de Jong PE, Coresh J et al (2011) The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report. Kidney Int 80(1):17–28PubMed Levey AS, de Jong PE, Coresh J et al (2011) The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report. Kidney Int 80(1):17–28PubMed
22.
Zurück zum Zitat Bakris GL, Agarwal R, Chan JC et al (2015) Effect of finerenone on albuminuria in patients with diabetic nephropathy: a randomized clinical trial. JAMA 314(9):884–894PubMed Bakris GL, Agarwal R, Chan JC et al (2015) Effect of finerenone on albuminuria in patients with diabetic nephropathy: a randomized clinical trial. JAMA 314(9):884–894PubMed
23.
Zurück zum Zitat Brenner D, Hiergeist A, Adis C et al (2018) The fecal microbiome of ALS patients. Neurobiol Aging 61:132–137PubMed Brenner D, Hiergeist A, Adis C et al (2018) The fecal microbiome of ALS patients. Neurobiol Aging 61:132–137PubMed
24.
Zurück zum Zitat Hiergeist A, Reischl U, Gessner A (2016) Multicenter quality assessment of 16S ribosomal DNA-sequencing for microbiome analyses reveals high inter-center variability. Int J Med Microbiol 306(5):334–342PubMed Hiergeist A, Reischl U, Gessner A (2016) Multicenter quality assessment of 16S ribosomal DNA-sequencing for microbiome analyses reveals high inter-center variability. Int J Med Microbiol 306(5):334–342PubMed
25.
Zurück zum Zitat Mcardle BH, Anderson MJ (2011) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82(1):290–297 Mcardle BH, Anderson MJ (2011) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82(1):290–297
26.
Zurück zum Zitat Zapala MA, Schork NJ (2006) Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc Natl Acad Sci USA 103(51):19430–19435PubMedPubMedCentral Zapala MA, Schork NJ (2006) Multivariate regression analysis of distance matrices for testing associations between gene expression patterns and related variables. Proc Natl Acad Sci USA 103(51):19430–19435PubMedPubMedCentral
27.
Zurück zum Zitat Chow J, Tang H, Mazmanian SK (2011) Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr Opin Immunol 23(4):473–480PubMedPubMedCentral Chow J, Tang H, Mazmanian SK (2011) Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr Opin Immunol 23(4):473–480PubMedPubMedCentral
28.
Zurück zum Zitat Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268–1273PubMedPubMedCentral Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268–1273PubMedPubMedCentral
29.
Zurück zum Zitat Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904PubMed Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904PubMed
30.
Zurück zum Zitat Forslund K, Hildebrand F, Nielsen T et al (2015) Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528(7581):262–266PubMedPubMedCentral Forslund K, Hildebrand F, Nielsen T et al (2015) Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528(7581):262–266PubMedPubMedCentral
31.
Zurück zum Zitat De Angelis M, Montemurno E, Piccolo M et al (2014) Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS One 9(6):e99006PubMedPubMedCentral De Angelis M, Montemurno E, Piccolo M et al (2014) Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS One 9(6):e99006PubMedPubMedCentral
32.
Zurück zum Zitat Jiang S, Xie S, Lv D et al (2017) Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep 7(1):2870PubMedPubMedCentral Jiang S, Xie S, Lv D et al (2017) Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep 7(1):2870PubMedPubMedCentral
33.
Zurück zum Zitat Poesen R, Windey K, Neven E et al (2016) The influence of CKD on colonic microbial metabolism. J Am Soc Nephrol 27(5):1389–1399PubMed Poesen R, Windey K, Neven E et al (2016) The influence of CKD on colonic microbial metabolism. J Am Soc Nephrol 27(5):1389–1399PubMed
34.
Zurück zum Zitat Nicholson JK, Holmes E, Kinross J et al (2012) Host–gut microbiota metabolic interactions. Science 336(6086):1262–1267PubMed Nicholson JK, Holmes E, Kinross J et al (2012) Host–gut microbiota metabolic interactions. Science 336(6086):1262–1267PubMed
35.
Zurück zum Zitat Chen T, Zhang X, Long Y et al (2012) The association of plasma free amino acids with liver enzymes in Type 2 diabetic patients. J Endocrinol Investig 35(8):772–775 Chen T, Zhang X, Long Y et al (2012) The association of plasma free amino acids with liver enzymes in Type 2 diabetic patients. J Endocrinol Investig 35(8):772–775
36.
Zurück zum Zitat Li M, Wang X, Aa J et al (2013) GC/TOFMS analysis of metabolites in serum and urine reveals metabolic perturbation of TCA cycle in db/db mice involved in diabetic nephropathy. Am J Physiol Renal Physiol 304(11):F1317–F1324PubMed Li M, Wang X, Aa J et al (2013) GC/TOFMS analysis of metabolites in serum and urine reveals metabolic perturbation of TCA cycle in db/db mice involved in diabetic nephropathy. Am J Physiol Renal Physiol 304(11):F1317–F1324PubMed
37.
Zurück zum Zitat Nakamura H, Jinzu H, Nagao K et al (2014) Plasma amino acid profiles are associated with insulin, C-peptide and adiponectin levels in type 2 diabetic patients. Nutr Diabetes 4:e133PubMedPubMedCentral Nakamura H, Jinzu H, Nagao K et al (2014) Plasma amino acid profiles are associated with insulin, C-peptide and adiponectin levels in type 2 diabetic patients. Nutr Diabetes 4:e133PubMedPubMedCentral
38.
Zurück zum Zitat Scanlan PD, Shanahan F, Clune Y et al (2008) Culture-independent analysis of the gut microbiota in colorectal cancer and polyposis. Environ Microbiol 10(3):789–798PubMed Scanlan PD, Shanahan F, Clune Y et al (2008) Culture-independent analysis of the gut microbiota in colorectal cancer and polyposis. Environ Microbiol 10(3):789–798PubMed
39.
Zurück zum Zitat Vitali B, Ndagijimana M, Cruciani F et al (2010) Impact of a synbiotic food on the gut microbial ecology and metabolic profiles. BMC Microbiol 10:4PubMedPubMedCentral Vitali B, Ndagijimana M, Cruciani F et al (2010) Impact of a synbiotic food on the gut microbial ecology and metabolic profiles. BMC Microbiol 10:4PubMedPubMedCentral
40.
Zurück zum Zitat Sun L, Ma L, Ma Y, Zhang F, Zhao C, Nie Y (2018) Insights into the role of gut microbiota in obesity: pathogenesis, mechanisms, and therapeutic perspectives. Protein Cell 9(5):397–403PubMedPubMedCentral Sun L, Ma L, Ma Y, Zhang F, Zhao C, Nie Y (2018) Insights into the role of gut microbiota in obesity: pathogenesis, mechanisms, and therapeutic perspectives. Protein Cell 9(5):397–403PubMedPubMedCentral
41.
Zurück zum Zitat Andrade-Oliveira V, Amano MT, Correa-Costa M et al (2015) Gut bacteria products prevent AKI induced by ischemia-reperfusion. J Am Soc Nephrol 26(8):1877–1888PubMedPubMedCentral Andrade-Oliveira V, Amano MT, Correa-Costa M et al (2015) Gut bacteria products prevent AKI induced by ischemia-reperfusion. J Am Soc Nephrol 26(8):1877–1888PubMedPubMedCentral
42.
Zurück zum Zitat Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, Vaziri ND (2014) Expansion of urease- and uricase-containing, indole- and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am J Nephrol 39(3):230–237PubMed Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, Vaziri ND (2014) Expansion of urease- and uricase-containing, indole- and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am J Nephrol 39(3):230–237PubMed
43.
Zurück zum Zitat Furusawa Y, Obata Y, Fukuda S et al (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446–450PubMed Furusawa Y, Obata Y, Fukuda S et al (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446–450PubMed
44.
Zurück zum Zitat Finegold SM, Dowd SE, Gontcharova V et al (2010) Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 16(4):444–453PubMed Finegold SM, Dowd SE, Gontcharova V et al (2010) Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 16(4):444–453PubMed
45.
Zurück zum Zitat Rizzatti G, Lopetuso LR, Gibiino G et al (2017) Proteobacteria: a common factor in human diseases. Biomed Res Int 2017(9):1–7 Rizzatti G, Lopetuso LR, Gibiino G et al (2017) Proteobacteria: a common factor in human diseases. Biomed Res Int 2017(9):1–7
46.
Zurück zum Zitat Wassenaar TM, Zimmermann K (2018) Lipopolysaccharides in food, food supplements, and probiotics: should we be worried? Eur J Microbiol Immunol 8(3):63–69 Wassenaar TM, Zimmermann K (2018) Lipopolysaccharides in food, food supplements, and probiotics: should we be worried? Eur J Microbiol Immunol 8(3):63–69
47.
Zurück zum Zitat Carrero JJ, Stenvinkel P (2009) Persistent inflammation as a catalyst for other risk factors in chronic kidney disease: a hypothesis proposal. Clin J Am Soc Nephrol 4(Suppl 1):S49–S55PubMed Carrero JJ, Stenvinkel P (2009) Persistent inflammation as a catalyst for other risk factors in chronic kidney disease: a hypothesis proposal. Clin J Am Soc Nephrol 4(Suppl 1):S49–S55PubMed
48.
Zurück zum Zitat Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB (2013) Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26(4):822–880PubMedPubMedCentral Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB (2013) Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26(4):822–880PubMedPubMedCentral
49.
Zurück zum Zitat Clark DP (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 63(3):223–234 Clark DP (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 63(3):223–234
50.
Zurück zum Zitat Liu J (2014) Ethanol and liver: recent insights into the mechanisms of ethanol-induced fatty liver. World J Gastroenterol 20(40):14672–14685PubMedPubMedCentral Liu J (2014) Ethanol and liver: recent insights into the mechanisms of ethanol-induced fatty liver. World J Gastroenterol 20(40):14672–14685PubMedPubMedCentral
51.
Zurück zum Zitat Mahmoodpoor F, Rahbar Saadat Y, Barzegari A, Ardalan M, Zununi Vahed S (2017) The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharmacother 93:412–419PubMed Mahmoodpoor F, Rahbar Saadat Y, Barzegari A, Ardalan M, Zununi Vahed S (2017) The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharmacother 93:412–419PubMed
Metadaten
Titel
Understanding the gut–kidney axis among biopsy-proven diabetic nephropathy, type 2 diabetes mellitus and healthy controls: an analysis of the gut microbiota composition
verfasst von
Sibei Tao
Lingzhi Li
Ling Li
Yuan Liu
Qian Ren
Min Shi
Jing Liu
Jing Jiang
Huichao Ma
Zhuo Huang
Zijing Xia
Jing Pan
Tiantian Wei
Yan Wang
Peiyun Li
Tian Lan
Xi Tang
Xiaoxi Zeng
Song Lei
Huairong Tang
Liang Ma
Ping Fu
Publikationsdatum
19.03.2019
Verlag
Springer Milan
Erschienen in
Acta Diabetologica / Ausgabe 5/2019
Print ISSN: 0940-5429
Elektronische ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-019-01316-7

Weitere Artikel der Ausgabe 5/2019

Acta Diabetologica 5/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.