Bladder Microbiota Are Associated with Clinical Conditions That Extend beyond the Urinary Tract
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
TUH, 00064190
Ministry of Health
PubMed
35630319
PubMed Central
PMC9147640
DOI
10.3390/microorganisms10050874
PII: microorganisms10050874
Knihovny.cz E-resources
- Keywords
- aging, antibiotics, chronic kidney disease, diabetes mellitus, dyslipidemia, erectile dysfunction, smoking, urinary microbiota,
- Publication type
- Journal Article MeSH
BACKGROUND: Since the discovery of the human urinary microbiota (UM), alterations in microbial community composition have been associated with various genitourinary conditions. The aim of this exploratory study was to examine possible associations of UM with clinical conditions beyond the urinary tract and to test some of the conclusions from previous studies on UM. METHODS: Catheterised urine samples from 87 men were collected prior to endoscopic urological interventions under anaesthesia. The composition of the bacterial community in urine was characterized using the hypervariable V4 region of the 16S rRNA gene. Samples from 58 patients yielded a sufficient amount of bacterial DNA for analysis. Alpha diversity measures (number of operational taxonomic units, ACE, iChao2, Shannon and Simpson indices) were compared with the Kruskal-Wallis test. Beta diversity (differences in microbial community composition) was assessed using non-metric dimensional scaling in combination with the Prevalence in Microbiome Analysis algorithm. RESULTS: Differences in bacterial richness and diversity were observed for the following variables: age, diabetes mellitus, dyslipidemia, smoking status and single-dose preoperative antibiotics. Differences in microbial community composition were observed in the presence of chronic kidney disease, lower urinary tract symptoms and antibiotic prophylaxis. CONCLUSIONS: UM appears to be associated with certain clinical conditions, including those unrelated to the urinary tract. Further investigation is needed before conclusions can be drawn for diagnostics and treatment.
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Peterson J., Garges S., Giovanni M., McInnes P., Wang L., Schloss J.A., NIH HMP Working Group The NIH Human Microbiome Project. Genome Res. 2009;19:2317–2323. PubMed PMC
Loke Y.L., Chew M.T., Ngeow Y.F., Lim W.W.D., Peh S.C. Colon Carcinogenesis: The Interplay Between Diet and Gut Microbiota. Front. Cell. Infect. Microbiol. 2020;10:603086. doi: 10.3389/fcimb.2020.603086. PubMed DOI PMC
Belkaid Y., Hand T.W. Role of the Microbiota in Immunity and Inflammation. Cell. 2014;157:121–141. doi: 10.1016/j.cell.2014.03.011. PubMed DOI PMC
Łaniewski P., Ilhan Z.E., Herbst-Kralovetz M.M. The microbiome and gynaecological cancer development, prevention and therapy. Nat. Rev. Urol. 2020;17:232–250. doi: 10.1038/s41585-020-0286-z. PubMed DOI PMC
Siddiqui H., Nederbragt A.J., Lagesen K., Jeansson S.L., Jakobsen K.S. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol. 2011;11:244. doi: 10.1186/1471-2180-11-244. PubMed DOI PMC
Hilt E.E., McKinley K., Pearce M.M., Rosenfeld A.B., Zilliox M.J., Mueller E.R., Brubaker L., Gai X., Wolfe A.J., Schreckenberger P.C. Urine Is Not Sterile: Use of Enhanced Urine Culture Techniques to Detect Resident Bacterial Flora in the Adult Female Bladder. J. Clin. Microbiol. 2014;52:871–876. doi: 10.1128/JCM.02876-13. PubMed DOI PMC
Fouts D.E., Pieper R., Szpakowski S., Pohl H., Knoblach S., Suh M.-J., Huang S.-T., Ljungberg I., Sprague B.M., Lucas S.K., et al. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J. Transl. Med. 2012;10:174. doi: 10.1186/1479-5876-10-174. PubMed DOI PMC
Bajic P., Van Kuiken M.E., Burge B.K., Kirshenbaum E.J., Joyce C., Wolfe A.J., Branch J.D., Bresler L., Farooq A.V. Male Bladder Microbiome Relates to Lower Urinary Tract Symptoms. Eur. Urol. Focus. 2020;15:376–382. doi: 10.1016/j.euf.2018.08.001. PubMed DOI
Burnett L.A., Hochstedler B.R., Weldon K., Wolfe A.J., Brubaker L. Recurrent urinary tract infection: Association of clinical profiles with urobiome composition in women. Neurourol. Urodyn. 2021;40:1479–1489. doi: 10.1002/nau.24707. PubMed DOI PMC
Siddiqui H., Lagesen K., Nederbragt A.J., Jeansson S.L., Jakobsen K.S. Alterations of microbiota in urine from women with interstitial cystitis. BMC Microbiol. 2012;12:205. doi: 10.1186/1471-2180-12-205. PubMed DOI PMC
Shoskes D.A., Altemus J., Polackwich A.S., Tucky B., Wang H., Eng C. The Urinary Microbiome Differs Significantly Between Patients with Chronic Prostatitis/Chronic Pelvic Pain Syndrome and Controls as Well as Between Patients with Different Clinical Phenotypes. Urology. 2016;92:26–32. doi: 10.1016/j.urology.2016.02.043. PubMed DOI
Wu P., Zhang G., Zhao J., Chen J., Chen Y., Huang W., Zeng J. Profiling the Urinary Microbiota in Male Patients with Bladder Cancer in China. Front. Cell. Infect. Microbiol. 2018;8:167. doi: 10.3389/fcimb.2018.00167. PubMed DOI PMC
Scher J.U., Sczesnak A., Longman R.S., Segata N., Ubeda C., Bielski C., Littman D.R. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202. doi: 10.7554/eLife.01202. PubMed DOI PMC
Lee Y.K., Menezes J.S., Umesaki Y., Mazmanian S.K. Proin fl ammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 2011;108((Suppl. 1)):4615–4622. doi: 10.1073/pnas.1000082107. PubMed DOI PMC
Dahlin M., Prast-Nielsen S. EBioMedicine The gut microbiome and epilepsy. EBioMedicine. 2019;44:741–746. doi: 10.1016/j.ebiom.2019.05.024. PubMed DOI PMC
Barandouzi Z.A., Starkweather A.R., Henderson W., Gyamfi A., Cong X.S. Altered Composition of Gut Microbiota in Depression: A Systematic Review. Front. Psychiatry. 2020;11:541. doi: 10.3389/fpsyt.2020.00541. PubMed DOI PMC
Wu P., Chen Y., Zhao J., Zhang G., Chen J., Wang J., Zhang H. Urinary Microbiome and Psychological Factors in Women with Overactive Bladder. Front. Cell. Infect. Microbiol. 2017;7:488. doi: 10.3389/fcimb.2017.00488. PubMed DOI PMC
Lewis D.A., Brown R., Williams J., White P., Jacobson S.K., Marchesi J.R., Drake M.J. The human urinary microbiome; bacterial DNA in voided urine of asymptomatic adults. Front. Cell. Infect. Microbiol. 2013;3:41. doi: 10.3389/fcimb.2013.00041. PubMed DOI PMC
Kramer H., Kuffel G., Thomas-White K., Wolfe A.J., Vellanki K., Leehey D.J., Bansal V.K., Brubaker L., Flanigan R., Koval J., et al. Diversity of the midstream urine microbiome in adults with chronic kidney disease. Int. Urol. Nephrol. 2018;50:1123–1130. doi: 10.1007/s11255-018-1860-7. PubMed DOI PMC
Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Lozupone C.A., Turnbaugh P.J., Fierer N., Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA. 2011;108((Suppl. 1)):4516–4522. doi: 10.1073/pnas.1000080107. PubMed DOI PMC
Větrovský T., Baldrian P., Morais D. SEED 2: A user-friendly platfomr for amplicon high-throughput sequencing data analyses. Bioinformatics. 2018;34:2292–2294. doi: 10.1093/bioinformatics/bty071. PubMed DOI PMC
Aronesty E. Comparison of Sequencing Utility Programs. Open Bioinform. J. 2013;7:1–8. doi: 10.2174/1875036201307010001. DOI
Edgar R.C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods. 2013;10:996–998. doi: 10.1038/nmeth.2604. PubMed DOI
Větrovský T., Baldrian P. Analysis of soil fungal communities by amplicon pyrosequencing: Current approaches to data analysis and the introduction of the pipeline SEED. Biol. Fertil. Soils. 2013;49:1027–1037. doi: 10.1007/s00374-013-0801-y. DOI
Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Glöckner F.O. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–596. doi: 10.1093/nar/gks1219. PubMed DOI PMC
Wright E.S. Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 2016;8:352–359. doi: 10.32614/RJ-2016-025. DOI
Kim B.-R., Shin J., Guevarra R.B., Lee J.H., Kim D.W., Seol K.-H., Lee J.-H., Kim H.B., Isaacson R.E. Deciphering Diversity Indices for a Better Understanding of Microbial Communities. J. Microbiol. Biotechnol. 2017;27:2089–2093. doi: 10.4014/jmb.1709.09027. PubMed DOI
Willis A. Rarefaction, Alpha Diversity, and Statistics. Front. Microbiol. 2019;10:2407. doi: 10.3389/fmicb.2019.02407. PubMed DOI PMC
Su X. Elucidating the Beta-Diversity of the Microbiome: From Global Alignment to Local Alignment. mSystems. 2021;6 doi: 10.1128/mSystems.00363-21. PubMed DOI PMC
Bylemans J., Gleeson D.M., Lintermans M., Hardy C.M., Beitzel M., Gilligan D.M., Furlan E.M. Package ‘vegan. Community Ecol. Packag. 2018;5:2017.
McMurdie P., Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE. 2013;8:e61217. doi: 10.1371/journal.pone.0061217. PubMed DOI PMC
R Core Team R: A Language and Environment for Statistical Computing. 2021. [(accessed on 22 September 2021)]. Available online: http://www.r-project.org/
Chiu C.-H., Wang Y.-T., Walther B.A., Chao A. An improved nonparametric lower bound of species richness via a modified good-turing frequency formula. Biometrics. 2014;70:671–682. doi: 10.1111/biom.12200. PubMed DOI
O’Hara R.B., O’Hara R. Species richness estimators: How many species can dance on the head of a pin? J. Anim. Ecol. 2005;74:375–386. doi: 10.1111/j.1365-2656.2005.00940.x. DOI
Roesch L.F.W., Dobbler P.T., Pylro V.S., Kolaczkowski B., Drew J.C., Triplett E.W. Pime: A package for discovery of novel differences among microbial communities. Mol. Ecol. Resour. 2020;20:415–428. doi: 10.1111/1755-0998.13116. PubMed DOI
Whiteside S.A., Razvi H., Dave S., Reid G., Burton J. The microbiome of the urinary tract—A role beyond infection. Nat. Rev. Urol. 2015;12:81–90. doi: 10.1038/nrurol.2014.361. PubMed DOI
Odamaki T., Kato K., Sugahara H., Hashikura N., Takahashi S., Xiao J.-Z., Abe F., Osawa R. Age-related changes in gut microbiota composition from newborn to centenarian: A cross-sectional study. BMC Microbiol. 2016;16:90. doi: 10.1186/s12866-016-0708-5. PubMed DOI PMC
Thomas-White K.J., Kliethermes S., Rickey L., Lukacz E.S., Richter H.E., Moalli P., Zimmern P., Norton P., Kusek J.W., Wolfe A.J., et al. Evaluation of the urinary microbiota of women with uncomplicated stress urinary incontinence. Am. J. Obstet. Gynecol. 2017;216:55.e1–55.e16. doi: 10.1016/j.ajog.2016.07.049. PubMed DOI PMC
Harman S.M., Metter E.J., Tobin J.D., Pearson J., Blackman M.R. Longitudinal Effects of Aging on Serum Total and Free Testosterone Levels in Healthy Men. J. Clin. Endocrinol. Metab. 2001;86:724–731. doi: 10.1210/jcem.86.2.7219. PubMed DOI
Grishina I., Fenton A., Sankaran-Walters S. Gender differences, aging and hormonal status in mucosal injury and repair. Aging Dis. 2014;5:160–169. doi: 10.14336/AD.2014.0500160. PubMed DOI PMC
Ragonnaud E., Biragyn A. Gut microbiota as the key controllers of ‘healthy’ aging of elderly people. Immun. Ageing. 2021;18:2. doi: 10.1186/s12979-020-00213-w. PubMed DOI PMC
Yang T., Richards E.M., Pepine C.J., Raizada M.K. The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease. Nat. Rev. Nephrol. 2018;14:442–456. doi: 10.1038/s41581-018-0018-2. PubMed DOI PMC
Yang T., Santisteban M.M., Rodriguez V., Li E., Ahmari N., Carvajal J.M., Zadeh M., Gong M., Qi Y., Zubcevic J., et al. Gut Dysbiosis Is Linked to Hypertension. Hypertension. 2015;65:1331–1340. doi: 10.1161/HYPERTENSIONAHA.115.05315. PubMed DOI PMC
Li J., Zhao F., Wang Y., Chen J., Tao J., Tian G., Wu S., Liu W., Cui Q., Geng B., et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome. 2017;5:14. doi: 10.1186/s40168-016-0222-x. PubMed DOI PMC
Larsen N., Vogensen F.K., Berg F.W.J.V.D., Nielsen D.S., Andreasen A.S., Pedersen B.K., Abu Al-Soud W., 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. doi: 10.1371/journal.pone.0009085. PubMed DOI PMC
Liu F., Ling Z., Xiao Y., Lv L., Yang Q., Wang B., Lu H., Zheng L., Jiang P., Wang W., et al. Dysbiosis of urinary microbiota is positively correlated with Type 2 diabetes mellitus. Oncotarget. 2017;8:3798–3810. doi: 10.18632/oncotarget.14028. PubMed DOI PMC
Hu Z.B., Lu J., Chen P.P., Lu C.C., Zhang J.X., Li X.Q., Yuan B.Y., Huang S.J., Ruan X.Z., Liu B.C., et al. Dysbiosis of intestinal microbiota mediates tubulointerstitial injury in diabetic nephropathy via the disruption of cholesterol homeostasis. Theranostics. 2020;10:2803–2816. doi: 10.7150/thno.40571. PubMed DOI PMC
Ma W., Zhang W., Shen L., Liu J., Yang F., Maskey N., Wang H., Zhang J., Yan Y., Yao X. Can Smoking Cause Differences in Urine Microbiome in Male Patients with Bladder Cancer? A Retrospective Study. Front. Oncol. 2021;11:677605. doi: 10.3389/fonc.2021.677605. PubMed DOI PMC
Moynihan M.J., Sullivan T., Provenzano K., Rieger-Christ K. Urinary Microbiome Evaluation in Patients Presenting with Hematuria with a Focus on Exposure to Tobacco Smoke. Res. Rep. Urol. 2019;11:359–367. doi: 10.2147/RRU.S233386. PubMed DOI PMC
Reid G., Denstedt J.D., Kang Y.S., Lam D., Nause C. Microbial Adhesion and Biofilm Formation on Ureteral Stents in Vitro and in Vivo. J. Urol. 1992;148:1592–1594. doi: 10.1016/S0022-5347(17)36976-8. PubMed DOI