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Characterization of gut microbiota in patients with stage 3–4 chronic kidney disease: a retrospective cohort study

  • Nephrology - Original Paper
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Abstract

Purpose

Multiple factors, such as dietary patterns, pharmaceutical interventions, and exposure to harmful substances, possess the capacity to influence gut microbiota composition. Gut microbiota dysbiosis has emerged as a significant contributor to the progression of chronic kidney disease (CKD) and its associated complications. By comprehending the intricacies of the intestinal microbiota, this research endeavor holds the potential to offer novel perspectives on potential strategies for mitigating CKD progression.

Methods

In this retrospective analysis, we assessed gut microbiota composition in CKD patients. Fecal samples were collected from a cohort of 44 patients with stage 3–4 CKD, alongside a control group consisting of 132 healthy volunteers. Subsequently, 16 s rDNA sequencing was conducted to examine the composition of the gut microbiota.

Results

Our findings revealed significant alterations in the diversity of intestinal microbiota in fecal samples between patients with stage 3–4 CKD and healthy subjects. Among the 475 bacterial genera, 164 were shared, while 242 dominant genera were exclusive to healthy subjects and 69 to CKD stages 3–4 samples. Notably, healthy volunteers exhibited a prevalence of intestinal Firmicutes and Bacteroidetes, whereas stage 3–4 CKD patients displayed higher abundance of Proteobacteria and Actinobacteria. The presence of uncultured Coprobacillus sp. notably contributed to distinguishing between the two groups. ROC curve analysis identified distinct microbiota with superior diagnostic efficacy for discriminating stage 3–4 CKD patients from healthy individuals. Metabolic pathway analysis revealed differing dominant pathways between the two groups—the NADH dehydrogenase pathway in healthy individuals and the phosphate acetyltransferase pathway in stage 3–4 CKD patients. Moreover, the CKD cohort displayed a higher proportion of Gram-negative bacteria and facultative anaerobes.

Conclusions

In conclusion, our study underscores the profound influence of gut microbiota dysbiosis on CKD progression. The distinct microbial profiles observed in CKD patients highlight the potential efficacy of microbiota-based interventions in mitigating CKD advancement.

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Data availability

All data presented in this study are available from the corresponding author upon reasonable request.

References

  1. Yang C, Wang H, Zhao X, Matsushita K, Coresh J, Zhang L, Zhao MH (2020) CKD in China: evolving spectrum and public health implications. Am J Kidney Dis 76:258–264. https://doi.org/10.1053/j.ajkd.2019.05.032

    Article  PubMed  Google Scholar 

  2. Chen TK, Knicely DH, Grams ME (2019) Chronic kidney disease diagnosis and management: a review. JAMA 322:1294–1304. https://doi.org/10.1001/jama.2019.14745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Webster AC, Nagler EV, Morton RL, Masson P (2017) Chronic kidney disease. Lancet (London, England) 389:1238–1252. https://doi.org/10.1016/s0140-6736(16)32064-5

    Article  PubMed  Google Scholar 

  4. Hill NR, Fatoba ST, Oke JL, Hirst JA, O’Callaghan CA, Lasserson DS, Hobbs FD (2016) Global prevalence of chronic kidney disease—a systematic review and meta-analysis. PLoS ONE 11:e0158765. https://doi.org/10.1371/journal.pone.0158765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Levin A, Stevens PE, Bilous RW, Coresh J, De Francisco AL, De Jong PE, Griffith KE, Hemmelgarn BR, Iseki K, Lamb EJ (2013) Kidney Disease: Improving Global Outcomes (KDIGO) CKD Work Group. KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney int Suppl 3:1–150

    Google Scholar 

  6. Stevens PE, Levin A (2013) Evaluation and management of chronic kidney disease: synopsis of the kidney disease: improving global outcomes 2012 clinical practice guideline. Ann Intern Med 158:825–830. https://doi.org/10.7326/0003-4819-158-11-201306040-00007

    Article  PubMed  Google Scholar 

  7. Ammirati AL (2020) Chronic kidney disease. Rev Assoc Med Bras 66(1):03–09. https://doi.org/10.1590/1806-9282.66.s1.3

    Article  Google Scholar 

  8. KDOQI Clinical Practice Guideline for Diabetes and CKD (2012) 2012 Update. Am J Kidney Dis 60:850–886. https://doi.org/10.1053/j.ajkd.2012.07.005

    Article  Google Scholar 

  9. Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D (2017) Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res 179:24–37. https://doi.org/10.1016/j.trsl.2016.04.007

    Article  CAS  PubMed  Google Scholar 

  10. Cresci GA, Bawden E (2015) Gut microbiome: what we do and don’t know. Nut in Clin Prac 30:734–746. https://doi.org/10.1177/0884533615609899

    Article  CAS  Google Scholar 

  11. Heintz-Buschart A, Wilmes P (2018) Human gut microbiome: function matters. Trends Microbiol 26:563–574. https://doi.org/10.1016/j.tim.2017.11.002

    Article  CAS  PubMed  Google Scholar 

  12. Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I (2015) Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7:2839–2849. https://doi.org/10.3390/nu7042839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ikeda T, Nishida A, Yamano M, Kimura I (2022) Short-chain fatty acid receptors and gut microbiota as therapeutic targets in metabolic, immune, and neurological diseases. Pharmacol Ther 239:108273. https://doi.org/10.1016/j.pharmthera.2022.108273

    Article  CAS  PubMed  Google Scholar 

  14. Schmidt TSB, Raes J, Bork P (2018) The human gut microbiome: from association to modulation. Cell 172:1198–1215. https://doi.org/10.1016/j.cell.2018.02.044

    Article  CAS  PubMed  Google Scholar 

  15. Guven G, Hilty MP, Ince C (2020) Microcirculation: physiology, pathophysiology, and clinical application. Blood Purif 49:143–150. https://doi.org/10.1159/000503775

    Article  CAS  PubMed  Google Scholar 

  16. Vasylyeva TL, Singh R (2016) Gut microbiome and kidney disease in pediatrics: does connection exist? Front Microbiol 7:235. https://doi.org/10.3389/fmicb.2016.00235

    Article  PubMed  PubMed Central  Google Scholar 

  17. Muskiet MH, Smits MM, Morsink LM, Diamant M (2014) The gut-renal axis: do incretin-based agents confer renoprotection in diabetes? Nat Rev Nephrol 10:88–103. https://doi.org/10.1038/nrneph.2013.272

    Article  CAS  PubMed  Google Scholar 

  18. Evenepoel P, Poesen R, Meijers B (2017) The gut-kidney axis. Pediatric Nephrol (Berlin, Germany) 32:2005–2014. https://doi.org/10.1007/s00467-016-3527-x

    Article  Google Scholar 

  19. Yang T, Richards EM, Pepine CJ, Raizada MK (2018) The gut microbiota and the brain-gut-kidney axis in hypertension and chronic kidney disease. Nat Rev Nephrol 14:442–456. https://doi.org/10.1038/s41581-018-0018-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Shi N, Li N, Duan X, Niu H (2017) Interaction between the gut microbiome and mucosal immune system. Mil Med Res 4:14. https://doi.org/10.1186/s40779-017-0122-9

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lohia S, Vlahou A, Zoidakis J (2022) Microbiome in chronic kidney disease (CKD): an omics perspective. Toxins. https://doi.org/10.3390/toxins14030176

    Article  PubMed  PubMed Central  Google Scholar 

  22. Plata C, Cruz C, Cervantes LG, Ramírez V (2019) The gut microbiota and its relationship with chronic kidney disease. Int Urol Nephrol 51:2209–2226. https://doi.org/10.1007/s11255-019-02291-2

    Article  PubMed  Google Scholar 

  23. Stedman A, Nigro G, Sansonetti PJ (2016) Microbiota-intestinal stem cells dialog: a key element for intestinal regeneration. Med Sci 32:983–990. https://doi.org/10.1051/medsci/20163211014

    Article  Google Scholar 

  24. Fakhoury HMA, Kvietys PR, AlKattan W, Anouti FA, Elahi MA, Karras SN, Grant WB (2020) Vitamin D and intestinal homeostasis: Barrier, microbiota, and immune modulation. J Steroid Biochem Mol Biol 200:105663. https://doi.org/10.1016/j.jsbmb.2020.105663

    Article  CAS  PubMed  Google Scholar 

  25. Wang X, Yang S, Li S, Zhao L, Hao Y, Qin J, Zhang L, Zhang C, Bian W, Zuo L et al (2020) Aberrant gut microbiota alters host metabolome and impacts renal failure in humans and rodents. Gut 69:2131–2142. https://doi.org/10.1136/gutjnl-2019-319766

    Article  CAS  PubMed  Google Scholar 

  26. Liu JR, Miao H, Deng DQ, Vaziri ND, Li P, Zhao YY (2021) Gut microbiota-derived tryptophan metabolism mediates renal fibrosis by aryl hydrocarbon receptor signaling activation. Cell Mol Life Sci CMLS 78:909–922. https://doi.org/10.1007/s00018-020-03645-1

    Article  CAS  PubMed  Google Scholar 

  27. Ward T, Larson J, Meulemans J, Hillmann B, Lynch J, Sidiropoulos D, Spear J, Caporaso G, Blekhman R, Knight R (2017) BugBase predicts organism level microbiome phenotypes. Genome Biol 62:1479

    Google Scholar 

  28. Al Bander Z, Nitert MD, Mousa A, Naderpoor N (2020) The gut microbiota and inflammation: an overview. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph17207618

    Article  PubMed  PubMed Central  Google Scholar 

  29. Virtue AT, McCright SJ, Wright JM, Jimenez MT, Mowel WK, Kotzin JJ, Joannas L, Basavappa MG, Spencer SP, Clark ML et al (2019) The gut microbiota regulates white adipose tissue inflammation and obesity via a family of microRNAs. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aav1892

    Article  PubMed  PubMed Central  Google Scholar 

  30. Mahmoodpoor F, Rahbar Saadat Y, Barzegari A, Ardalan M, Zununi Vahed S (2017) The impact of gut microbiota on kidney function and pathogenesis. Biomed Pharm 93:412–419. https://doi.org/10.1016/j.biopha.2017.06.066

    Article  CAS  Google Scholar 

  31. Hobby GP, Karaduta O, Dusio GF, Singh M, Zybailov BL, Arthur JM (2019) Chronic kidney disease and the gut microbiome. Am J Physiol Renal Physiol 316:F1211-f1217. https://doi.org/10.1152/ajprenal.00298.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Chaves LD, McSkimming DI, Bryniarski MA, Honan AM, Abyad S, Thomas SA, Wells S, Buck M, Sun Y, Genco RJ et al (2018) Chronic kidney disease, uremic milieu, and its effects on gut bacterial microbiota dysbiosis. Am J Physiol Renal Physiol 315:F487-f502. https://doi.org/10.1152/ajprenal.00092.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. 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 39:230–237. https://doi.org/10.1159/000360010

    Article  CAS  PubMed  Google Scholar 

  34. Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, DeSantis TZ, Ni Z, Nguyen TH, Andersen GL (2013) Chronic kidney disease alters intestinal microbial flora. Kidney Int 83:308–315. https://doi.org/10.1038/ki.2012.345

    Article  PubMed  Google Scholar 

  35. Yasuda G, Shibata K, Takizawa T, Ikeda Y, Tokita Y, Umemura S, Tochikubo O (2002) Prevalence of constipation in continuous ambulatory peritoneal dialysis patients and comparison with hemodialysis patients. Am J Kidney Dis 39:1292–1299. https://doi.org/10.1053/ajkd.2002.33407

    Article  PubMed  Google Scholar 

  36. Gibiino G, Lopetuso LR, Scaldaferri F, Rizzatti G, Binda C, Gasbarrini A (2018) Exploring bacteroidetes: metabolic key points and immunological tricks of our gut commensals. Dig Liver Dis 50:635–639. https://doi.org/10.1016/j.dld.2018.03.016

    Article  PubMed  Google Scholar 

  37. Wu R, Ruan XL, Ruan DD, Zhang JH, Wang HL, Zeng QZ, Lu T, Gan YM, Luo JW, Wu JB (2021) Differences in gut microbiota structure in patients with stages 4–5 chronic kidney disease. Am J Transl Res 13:10056–10074

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhu H, Cao C, Wu Z, Zhang H, Sun Z, Wang M, Xu H, Zhao Z, Wang Y, Pei G et al (2021) The probiotic L. casei Zhang slows the progression of acute and chronic kidney disease. Cell Metab. https://doi.org/10.1016/j.cmet.2021.06.014

    Article  PubMed  PubMed Central  Google Scholar 

  39. Pavan M (2016) Influence of prebiotic and probiotic supplementation on the progression of chronic kidney disease. Min Urol Nefrol Ital J Urol Nephrol 68:222–226

    Google Scholar 

  40. Huang H, Li K, Lee Y, Chen M (2021) Preventive effects of lactobacillus mixture against chronic kidney disease progression through enhancement of beneficial bacteria and downregulation of gut-derived uremic toxins. J Agric Food Chem 69:7353–7366. https://doi.org/10.1021/acs.jafc.1c01547

    Article  CAS  PubMed  Google Scholar 

  41. Sorbara MT, Pamer EG (2022) Microbiome-based therapeutics. Nat Rev Microbiol 20:365–380. https://doi.org/10.1038/s41579-021-00667-9

    Article  CAS  PubMed  Google Scholar 

  42. Sharma A, Das P, Buschmann M, Gilbert JA (2020) The future of microbiome-based therapeutics in clinical applications. Clin Pharmacol Ther 107:123–128. https://doi.org/10.1002/cpt.1677

    Article  CAS  PubMed  Google Scholar 

  43. Barba C, Soulage CO, Caggiano G, Glorieux G, Fouque D, Koppe L (2020) Effects of fecal microbiota transplantation on composition in mice with CKD. Toxins. https://doi.org/10.3390/toxins12120741

    Article  PubMed  PubMed Central  Google Scholar 

  44. Feng YL, Cao G, Chen DQ, Vaziri ND, Chen L, Zhang J, Wang M, Guo Y, Zhao YY (2019) Microbiome-metabolomics reveals gut microbiota associated with glycine-conjugated metabolites and polyamine metabolism in chronic kidney disease. Cell Mol Life Sci 76:4961–4978. https://doi.org/10.1007/s00018-019-03155-9

    Article  CAS  PubMed  Google Scholar 

  45. Ozkok A, Elcioglu OC, Cukadar T, Bakan A, Sasak G, Atilgan KG, Alisir S, Kanbay M, Covic A, Odabas AR (2013) Low serum pancreatic enzyme levels predict mortality and are associated with malnutrition-inflammation-atherosclerosis syndrome in patients with chronic kidney disease. Int Urol Nephrol 45:477–484. https://doi.org/10.1007/s11255-012-0237-6

    Article  CAS  PubMed  Google Scholar 

  46. Matsushita K, Ballew SH, Wang AY, Kalyesubula R, Schaeffner E, Agarwal R (2022) Epidemiology and risk of cardiovascular disease in populations with chronic kidney disease. Nat Rev Nephrol 18:696–707. https://doi.org/10.1038/s41581-022-00616-6

    Article  PubMed  Google Scholar 

  47. Patel N, Yaqoob MM, Aksentijevic D (2022) Cardiac metabolic remodelling in chronic kidney disease. Nat Rev Nephrol 18:524–537. https://doi.org/10.1038/s41581-022-00576-x

    Article  PubMed  Google Scholar 

  48. Speer T, Dimmeler S, Schunk SJ, Fliser D, Ridker PM (2022) Targeting innate immunity-driven inflammation in CKD and cardiovascular disease. Nat Rev Nephrol 18:762–778. https://doi.org/10.1038/s41581-022-00621-9

    Article  PubMed  Google Scholar 

  49. Kadatane SP, Satariano M, Massey M, Mongan K, Raina R (2023) The role of inflammation in CKD. Cells. https://doi.org/10.3390/cells12121581

    Article  PubMed  PubMed Central  Google Scholar 

  50. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108. https://doi.org/10.1126/science.1208344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Su G, Qin X, Yang C, Sabatino A, Kelly JT, Avesani CM, Carrero JJ (2022) Fiber intake and health in people with chronic kidney disease. Clin Kidney J 15:213–225. https://doi.org/10.1093/ckj/sfab169

    Article  CAS  PubMed  Google Scholar 

  52. Favero C, Carriazo S, Cuarental L, Fernandez-Prado R, Gomá-Garcés E, Perez-Gomez MV, Ortiz A, Fernandez-Fernandez B, Sanchez-Niño MD (2021) Phosphate, microbiota and CKD. Nutrients. https://doi.org/10.3390/nu13041273

    Article  PubMed  PubMed Central  Google Scholar 

  53. Naber T, Purohit S (2021) Chronic kidney disease: role of diet for a reduction in the severity of the disease. Nutrients. https://doi.org/10.3390/nu13093277

    Article  PubMed  PubMed Central  Google Scholar 

  54. Meléndez Oliva E, Villafañe JH, Alonso Pérez JL, Alonso Sal A, Molinero Carlier G, Quevedo García A, Turroni S, Martínez-Pozas O, Valcárcel Izquierdo N, Sánchez Romero EA (2022) Effect of exercise on inflammation in hemodialysis patients: a systematic review. J Personal Med. https://doi.org/10.3390/jpm12071188

    Article  Google Scholar 

  55. Suzuki K (2019) Chronic inflammation as an immunological abnormality and effectiveness of exercise. Biomolecules. https://doi.org/10.3390/biom9060223

    Article  PubMed  PubMed Central  Google Scholar 

  56. Wegierska AE, Charitos IA, Topi S, Potenza MA, Montagnani M, Santacroce L (2022) The connection between physical exercise and gut microbiota: implications for competitive sports athletes. Sports Med 52:2355–2369. https://doi.org/10.1007/s40279-022-01696-x

    Article  PubMed  PubMed Central  Google Scholar 

  57. König RS, Albrich WC, Kahlert CR, Bahr LS, Löber U, Vernazza P, Scheibenbogen C, Forslund SK (2021) The gut microbiome in myalgic encephalomyelitis (ME)/chronic fatigue syndrome (CFS). Front Immunol 12:628741. https://doi.org/10.3389/fimmu.2021.628741

    Article  CAS  PubMed  Google Scholar 

  58. Li F, Wang M, Wang J, Li R, Zhang Y (2019) Alterations to the gut microbiota and their correlation with inflammatory factors in chronic kidney disease. Front Cell Infect Microbiol 9:206. https://doi.org/10.3389/fcimb.2019.00206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by Youth Natural Science Foundation of Jiangxi Province (Grant No. 20171BAB215011), Foundation of Zhaoyang Talent Plan of Shanghai East Hospital (Grant No. DFZY-6) and Youth Research Development Foundation of The First Affiliated Hospital of Xiamen University (XYY2017021).

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Author notes

  1. Xiali Yang and Shiying Cai have contributed equally to this work.

Authors and Affiliations

  1. Department of Nephrology, The First Affiliated Hospital of Xiamen University, Xiamen, 361003, Fujian Province, People’s Republic of China

    Xiali Yang, Jinsheng Gong, Jun Zhang, Minling Lian, Rufu Chen, Linghui Zhou, Peijin Bai, Bo Liu & Minting Zhuang

  2. Department of Nursing, Shenzhen Hospital of Southern Medical University, Shenzhen, 518101, People’s Republic of China

    Shiying Cai

  3. School of Nursing, Southern Medical University, Guangzhou, 510515, People’s Republic of China

    Shiying Cai

  4. Department of VIP Clinic, Shanghai East Hospital, Tongji University School of Medicine, No.150 Jimo Road, Shanghai, 200120, People’s Republic of China

    Honghong Tan

  5. Department of Rehabilitation Medicine, The First Affiliated Hospital of Xiamen University, No.55 Zhenhai Road, Xiamen, 361003, Fujian Province, People’s Republic of China

    Juan Xu

  6. Department of Nutrition, The First Affiliated Hospital of Xiamen University, No.55 Zhenhai Road, Xiamen, 361003, Fujian Province, People’s Republic of China

    Meizhen Li

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  1. Xiali Yang
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Contributions

HT, JX, ML, XY, and SC: conceptualization, methodology, supervision, and revision. XY, and SC: original draft preparation. XY, SC, JG, JZ, ML, RC, LZ, PB, BL, and MZ: investigation and visualization. All the authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Honghong Tan, Juan Xu or Meizhen Li.

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The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of First Affiliated Hospital of Xiamen University.

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Informed consents have been obtained from all the patients involved in this study.

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11255_2023_3893_MOESM1_ESM.jpg

Supplementary file1 Supplementary Figure. 1 Relative abundance of gut microbiota in patients with stage 3-4 CKD and healthy controls at class, order, family and genus levels (JPG 945 kb)

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Yang, X., Cai, S., Gong, J. et al. Characterization of gut microbiota in patients with stage 3–4 chronic kidney disease: a retrospective cohort study. Int Urol Nephrol 56, 1751–1762 (2024). https://doi.org/10.1007/s11255-023-03893-7

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