The gut microbiota profile of adults with kidney disease and kidney stones: a systematic review of the literature

Jordan Stanford, Karen Charlton, Anita Stefoska-Needham, Rukayat Ibrahim, Kelly Lambert, Jordan Stanford, Karen Charlton, Anita Stefoska-Needham, Rukayat Ibrahim, Kelly Lambert

Abstract

Background: There is mounting evidence that individuals with kidney disease and kidney stones have an abnormal gut microbiota composition. No studies to date have summarised the evidence to categorise how the gut microbiota profile of these individuals may differ from controls. Synthesis of this evidence is essential to inform future clinical trials. This systematic review aims to characterise differences of the gut microbial community in adults with kidney disease and kidney stones, as well as to describe the functional capacity of the gut microbiota and reporting of diet as a confounder in these studies.

Methods: Included studies were those that investigated the gut microbial community in adults with kidney disease or kidney stones and compared this to the profile of controls. Six scientific databases (CINHAL, Medline, PubMed, Scopus, Web of Science and Cochrane Library), as well as selected grey literature sources, were searched. Quality assessment was undertaken independently by three authors. The system of evidence level criteria was employed to quantitatively evaluate the alteration of microbiota by strictly considering the number, methodological quality and consistency of the findings. Additional findings relating to altered functions of the gut microbiota, dietary intakes and dietary methodologies used were qualitatively summarised.

Results: Twenty-five articles met the eligibility criteria and included data from a total of 892 adults with kidney disease or kidney stones and 1400 controls. Compared to controls, adults with kidney disease had increased abundances of several microbes including Enterobacteriaceae, Streptococcaceae, Streptococcus and decreased abundances of Prevotellaceae, Prevotella, Prevotella 9 and Roseburia among other taxa. Adults with kidney stones also had an altered microbial composition with variations to Bacteroides, Lachnospiraceae NK4A136 group, Ruminiclostridium 5 group, Dorea, Enterobacter, Christensenellaceae and its genus Christensenellaceae R7 group. Differences in the functional potential of the microbial community between controls and adults with kidney disease or kidney stones were also identified. Only three of the 25 articles presented dietary data, and of these studies, only two used a valid dietary assessment method.

Conclusions: The gut microbiota profile of adults with kidney disease and kidney stones differs from controls. Future study designs should include adequate reporting of important confounders such as dietary intake to assist with interpretation of findings.

Keywords: Diet therapy; Gastrointestinal microbiome; Kidney diseases; Nephrolithiasis; Systematic review.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
PRISMA flow diagram
Fig. 2
Fig. 2
Altered taxa based on strong and moderate level of evidence for adults with kidney disease compared to controls. Figure includes data from studies that investigated adults with CKD, IgAN, DN, ESKD, KT recipients and individuals receiving dialysis therapy (HD and PD)
Fig. 3
Fig. 3
Sub-sample analysis of altered taxa based on strong and moderate level of evidence for adults with kidney disease receiving dialysis therapy compared to controls. Figure includes data only from the studies that investigated adults receiving HD or PD therapy
Fig. 4
Fig. 4
Altered taxa based on strong and moderate level of evidence for adults with kidney stones compared to controls

References

    1. Ramezani A, Massy ZA, Meijers B, Evenepoel P, Vanholder R, et al. Role of the gut microbiome in uremia: a potential therapeutic target. Am J Kidney Dis. 2016;67:483–498.
    1. Wang B, Yao M, Lv L, Ling Z, Li L. The human microbiota in health and disease. Engineering. 2017;3:71–82.
    1. Fernandez-Prado R, Esteras R, Perez-Gomez MV, Gracia-Iguacel C, Gonzalez-Parra E, et al. Nutrients turned into toxins: microbiota modulation of nutrient properties in chronic kidney disease. Nutrients. 2017;9:489.
    1. Allaband C, McDonald D, Vazquez-Baeza Y, Minich JJ, Tripathi A, et al. Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clin Gastroenterol Hepatol. 2019;17:218–230.
    1. Fraher MH, O'Toole PW, Quigley E. Techniques used to characterize the gut microbiota: A guide for the clinician. 2012. pp. 312–322.
    1. Hamady M, Knight R. Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 2009;19:1141–1152.
    1. Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157:121–141.
    1. Vaziri ND. Effect of Synbiotic therapy on gut-derived uremic toxins and the intestinal microbiome in patients with CKD. Clin J Am Soc Nephrol. 2016;11:1–3.
    1. Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–1836.
    1. Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D. Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res. 2017;179:24–37.
    1. Koppe L, Fouque D, Soulage CO. The Role of Gut Microbiota and Diet on Uremic Retention Solutes Production in the Context of Chronic Kidney Disease. Toxins (Basel) 2018;10:155.
    1. Evenepoel P, Poesen R, Meijers B. The gut-kidney axis. Pediatr Nephrol. 2017;32:2005–2014.
    1. Felizardo RJF, Castoldi A, Andrade-Oliveira V, Câmara NOS. The microbiota and chronic kidney diseases: a double-edged sword. Clin Transl Immunol. 2016;5:e86.
    1. Wu IW, Hsu KH, Lee CC, Sun CY, Hsu HJ, et al. P-Cresyl sulphate and indoxyl sulphate predict progression of chronic kidney disease. Nephrol Dial Transplant. 2011;26:938–947.
    1. Poesen R, Claes K, Evenepoel P, de Loor H, Augustijns P, et al. Microbiota-derived Phenylacetylglutamine associates with overall mortality and cardiovascular disease in patients with CKD. J Am Soc Nephrol. 2016;27:3479.
    1. Poesen R, Viaene L, Verbeke K, Augustijns P, Bammens B, et al. Cardiovascular disease relates to intestinal uptake of p-cresol in patients with chronic kidney disease. BMC Nephrol. 2014;15:87.
    1. Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA, et al. Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res. 2015;116:448–455.
    1. Lisowska-Myjak B. Uremic toxins and their effects on multiple organ systems. Nephron Clin Pract. 2014;128:303–311.
    1. Kaufman DW, Kelly JP, Curhan GC, Anderson TE, Dretler SP, et al. Oxalobacter formigenes may reduce the risk of calcium oxalate kidney stones. J Am Soc Nephrol. 2008;19:1197–1203.
    1. Kumar R, Mukherjee M, Bhandari M, Kumar A, Sidhu H, et al. Role of Oxalobacter formigenes in calcium oxalate stone disease: a study from North India. Eur Urol. 2002;41:318–322.
    1. Abratt VR, Reid SJ. Chapter 3 - oxalate-degrading Bacteria of the human gut as probiotics in the Management of Kidney Stone Disease. Adv Appl Microbiol. 2010;72:63–87.
    1. Miller AW, Dearing D. The metabolic and ecological interactions of oxalate-degrading bacteria in the Mammalian gut. Pathogens (Basel, Switzerland) 2013;2:636–652.
    1. Siener R, Bangen U, Sidhu H, Hönow R, von Unruh G, et al. The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int. 2013;83:1144–1149.
    1. Sadaf H, Raza SI, Hassan SW. Role of gut microbiota against calcium oxalate. Microb Pathog. 2017;109:287–291.
    1. Wexler AG, Goodman AL. An insider’s perspective: Bacteroides as a window into the microbiome. Nat Microbiol. 2017;2:17026.
    1. Korpela K. Diet, microbiota, and metabolic health: trade-off between saccharolytic and proteolytic fermentation. Annu Rev Food Sci Technol. 2018;9:65–84.
    1. Nazar CMJ. Significance of diet in chronic kidney disease. J Nephropharmacol. 2013;2:37–43.
    1. Al Khodor S, Shatat IF. Gut microbiome and kidney disease: a bidirectional relationship. Pediatr Nephrol. 2017;32:921–931.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG, The PG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009;6:e1000097.
    1. GA Wells, B Shea, D O'Connell, J Peterson, V Welch, M Losos, P Tugwell,. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses n.d.. . Accessed 21 Mar 2019.
    1. Filippini T, Heck JE, Malagoli C, Del Giovane C, Vinceti M. A review and meta-analysis of outdoor air pollution and risk of childhood leukemia. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2015;33:36–66.
    1. Roever L, Resende ES, Diniz ALD, Penha-Silva N, O’Connell JL, et al. Metabolic syndrome and risk of stroke: protocol for an update systematic review and meta-analysis. Medicine. 2018;97:e9862.
    1. Scholten-Peeters GG, Verhagen AP, Bekkering GE, van der Windt DA, Barnsley L, et al. Prognostic factors of whiplash-associated disorders: a systematic review of prospective cohort studies. Pain. 2003;104:303–322.
    1. Mols F, Vingerhoets AJ, Coebergh JW, van de Poll-Franse LV. Quality of life among long-term breast cancer survivors: a systematic review. Eur J Cancer. 2005;41:2613–2619.
    1. Ariëns GA, van Mechelen W, Bongers PM, Bouter LM, van der Wal G. Physical risk factors for neck pain. Scand J Work Environ Health. 2000;26:7–19.
    1. Wong J, Piceno YM, DeSantis TZ, Pahl M, Andersen GL, et al. 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. 2014;39:230–237.
    1. Suryavanshi MV, Bhute SS, Gune RP, Shouche YS. Functional eubacteria species along with trans-domain gut inhabitants favour dysgenic diversity in oxalate stone disease. Sci Rep. 2018;8:16598.
    1. Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, et al. Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep. 2016;6:34712.
    1. De Angelis M, Montemurno E, Piccolo M, Vannini L, Lauriero G, et al. Microbiota and Metabolome associated with immunoglobulin a nephropathy (IgAN) PLoS One. 2014;9:e99006.
    1. Tao S, Li L, Li L, Liu Y, Ren Q, et al. Understanding the gut-kidney axis among biopsy-proven diabetic nephropathy, type 2 diabetes mellitus and healthy controls: an analysis of the gut microbiota composition. Acta Diabetol. 2019;56:581–592.
    1. Gradisteanu G, Stoica R, Petcu L, Picu A, Suceveanu A, et al. Microbiota signatures in type-2 diabetic patients with chronic kidney disease - a pilot study. J Mind Med Sci. 2019;6:130–136.
    1. Al-Obaide MAI, Singh R, Datta P, Rewers-Felkins KA, Salguero MV, et al. Gut microbiota-dependent Trimethylamine-N-oxide and serum biomarkers in patients with T2DM and advanced CKD. J Clin Med. 2017;6:86.
    1. Wang IK, Lai HC, Yu CJ, Liang CC, Chang CT, et al. Real-time PCR analysis of the intestinal microbiotas in peritoneal dialysis patients. Appl Environ Microbiol. 2012;78:1107–1112.
    1. Wang F, Jiang H, Shi K, Ren Y, Zhang P, et al. Gut bacterial translocation is associated with microinflammation in end-stage renal disease patients. Nephrology (Carlton) 2012;17:733–738.
    1. Miao Y-Y, Xu C-M, Xia M, Zhu H-Q, Chen Y-Q. Relationship between gut microbiota and phosphorus metabolism in hemodialysis patients: a preliminary exploration. Chin Med J. 2018;131:2792–2799.
    1. Guirong YE, Minjie Z, Lixin YU, Junsheng YE, Lin Y, et al. Gut microbiota in renal transplant recipients, patients with chronic kidney disease and healthy subjects. Nan Fang Yi Ke Da Xue Xue Bao. 2018;38:1401–1408.
    1. Jiang S, Xie S, Lv D, Zhang Y, Deng J, et al. A reduction in the butyrate producing species Roseburia spp. and Faecalibacterium prausnitzii is associated with chronic kidney disease progression. Antonie Van Leeuwenhoek. 2016;109:1389–1396.
    1. Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, et al. Chronic kidney disease alters intestinal microbial flora. Kidney Int. 2013;83:308–315.
    1. Tavasoli S, Alebouyeh M, Naji M, Shakiba Majd G, Shabani Nashtaei M, et al. Association of intestinal oxalate-degrading bacteria with recurrent calcium kidney stone formation and hyperoxaluria: a case-control study. BJU Int. 2019;125(1):133–143.
    1. Ticinesi A, Milani C, Guerra A, Allegri F, Lauretani F, et al. Understanding the gut–kidney axis in nephrolithiasis: an analysis of the gut microbiota composition and functionality of stone formers. Gut. 2018;67(12):2097–2106.
    1. Jiang S, Xie S, Lv D, Wang P, He H, et al. Alteration of the gut microbiota in Chinese population with chronic kidney disease. Sci Rep. 2017;7:2870.
    1. Li F, Wang M, Wang J, Li R, Zhang Y. Alterations to the gut microbiota and their correlation with inflammatory factors in chronic kidney disease. Front Cell Infect Microbiol. 2019;9:206.
    1. Tang R, Jiang Y, Tan A, Ye J, Xian X, et al. 16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones. Urolithiasis. 2018;46(6):503–514.
    1. Morgan XC, Huttenhower C. Chapter 12: human microbiome analysis. PLoS Comput Biol. 2012;8:e1002808.
    1. Shi K, Wang F, Jiang H, Liu H, Wei M, et al. Gut bacterial translocation may aggravate microinflammation in hemodialysis patients. Dig Dis Sci. 2014;59:2109–2117.
    1. Xu K-Y, Xia G-H, Lu J-Q, Chen M-X, Zhen X, et al. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci Rep. 2017;7:1445.
    1. Stadlbauer V, Horvath A, Ribitsch W, Schmerböck B, Schilcher G, et al. Structural and functional differences in gut microbiome composition in patients undergoing haemodialysis or peritoneal dialysis. Sci Rep. 2017;7:15601.
    1. Stern JM, Moazami S, Qiu Y, Kurland I, Chen Z, et al. Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis. 2016;44:399–407.
    1. Hajian-Tilaki K. Receiver operating characteristic (ROC) curve analysis for medical diagnostic test evaluation. Caspian J Intern Med. 2013;4:627–635.
    1. Lun H, Yang W, Zhao S, Jiang M, Xu M, et al. Altered gut microbiota and microbial biomarkers associated with chronic kidney disease. MicrobiologyOpen. 2019;8:e00678.
    1. Barrios C, Beaumont M, Pallister T, Villar J, Goodrich JK, et al. Gut-microbiota-metabolite Axis in early renal function decline. PLoS One. 2015;10:e0134311.
    1. Li Y, Su X, Zhang L, Liu Y, Shi M, et al. Dysbiosis of the gut microbiome is associated with CKD5 and correlated with clinical indices of the disease: a case-controlled study. J Transl Med. 2019;17:228.
    1. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489:220–230.
    1. Valdes AM, Walter J, Segal E, Spector TD. Role of the gut microbiota in nutrition and health. BMJ. 2018;361:k2179.
    1. Ramezani A, Raj DS. The gut microbiome, kidney disease, and targeted interventions. J Am Soc Nephrol. 2014;25:657–670.
    1. March DS, Graham-Brown MPM, Stover CM, Bishop NC, Burton JO. Intestinal Barrier Disturbances in Haemodialysis Patients: Mechanisms, Consequences, and Therapeutic Options. BioMed Res Int. 2017;2017:5765417.
    1. Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33:496–503.
    1. Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. Biomed Res Int. 2017;2017:7.
    1. Wang X, Quinn P. Endotoxins: Lipopolysaccharides of Gram-Negative Bacteria. 2010. pp. 3–25.
    1. Friedman JE. The maternal microbiome: cause or consequence of obesity risk in the next generation? Obesity. 2017;25:497–498.
    1. Chen H, Zhu J, Liu Y, Dong Z, Liu H, et al. Lipopolysaccharide induces chronic kidney injury and fibrosis through activation of mTOR signaling in macrophages. Am J Nephrol. 2015;42:305–317.
    1. Ivanov II, Honda K. Intestinal commensal microbes as immune modulators. Cell Host Microbe. 2012;12:496–508.
    1. van der Beek CM, Dejong CHC, Troost FJ, Masclee AAM, Lenaerts K. Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing. Nutr Rev. 2017;75:286–305.
    1. Ríos-Covián D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los Reyes-Gavilán CG, et al. Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health. Front Microbiol. 2016;7:185.
    1. McDaniel R, Licari P, Khosla C, et al. Process Development and Metabolic Engineering for the Overproduction of Natural and Unnatural Polyketides. In: Nielsen J, Eggeling L, Dynesen J, Gárdonyi M, Gill RT, de Graaf AA, et al., editors. Metabolic Engineering. Berlin: Springer Berlin Heidelberg; 2001. pp. 31–52.
    1. Mutka SC, Bondi SM, Carney JR, Da Silva NA, Kealey JT. Metabolic pathway engineering for complex polyketide biosynthesis in Saccharomyces cerevisiae. FEMS Yeast Res. 2006;6:40–47.
    1. Tebani A, Afonso C, Bekri S. Advances in metabolome information retrieval: turning chemistry into biology. Part I: analytical chemistry of the metabolome. J Inherit Metab Dis. 2018;41:379–391.
    1. Yang C-Y, Tarng D-C. Diet, gut microbiome and indoxyl sulphate in chronic kidney disease patients. Nephrology. 2018;23:16–20.
    1. Mehta M, Goldfarb DS, Nazzal L. The role of the microbiome in kidney stone formation. Int J Surg. 2016;36:607–612.
    1. Beerendrakumar N, Ramamoorthy L, Haridasan S. Dietary and fluid regime adherence in chronic kidney disease patients. J Caring Sci. 2018;7:17–20.
    1. Borges NA, Carmo FL, Stockler-Pinto MB, de Brito JS, Dolenga CJ, et al. Probiotic supplementation in chronic kidney disease: a double-blind, randomized, Placebo-controlled Trial. J Ren Nutr. 2018;28:28–36.
    1. Rossi M, Klein K, Johnson DW, Campbell KL. Pre-, pro-, and Synbiotics: do they have a role in reducing uremic toxins? A Systematic Review and Meta-Analysis. Int J Nephrol. 2012;2012:20.
    1. Rossi M, Johnson DW, Morrison M, Pascoe EM, Coombes JS, et al. Synbiotics easing renal failure by improving gut microbiology (SYNERGY): a randomized trial. Clin J Am Soc Nephrol. 2016;11:223.
    1. Koppe L, Mafra D, Fouque D. Probiotics and chronic kidney disease. Kidney Int. 2015;88:958–966.
    1. Singh RK, Chang H-W, Yan D, Lee KM, Ucmak D, et al. Influence of diet on the gut microbiome and implications for human health. J Transl Med. 2017;15:73.
    1. Tapsell LC, Neale EP, Satija A, Hu FB. Foods, nutrients, and dietary patterns: interconnections and implications for dietary guidelines. Adv Nutr. 2016;7:445–454.

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