Skip to main content

Advertisement

SpringerLink
Log in

Uncovering the role of urinary microbiota in urological tumors: a systematic review of literature

  • Original Article
  • Published:
World Journal of Urology Aims and scope Submit manuscript

Abstract

Purpose

Urinary microbiota has been found to play a key role in numerous urological diseases. The aim of this systematic review is to depict the role of urinary microbiota in the pathogenesis, diagnosis, prognosis, and treatment of urological tumors, including bladder cancer (BCa), prostate cancer (PCa) and renal cell carcinoma (RCC).

Methods

A systematic PubMed and Scopus search was undergone from inception through June 2021 for studies investigating urinary microbiota alterations in urological tumors. Study selection followed the PRISMA statement. Phylum, family, genus and species of each bacterium in cancer patients and controls were recorded.

Results

Twenty-one studies with 1194 patients (748 cancer patients and 446 controls) were included in our final analysis. Certain bacterial phylum, family, genus, and species were more predominant in each of BCa, PCa and RCC patients compared to controls. Abundance and specificity of urinary microbiota were prognosticators for: (1) recurrence, distinguishing recurrent from non-recurrent BCa, (2) disease stage, distinguishing non-muscle invasive from muscle invasive BCa, and (3) disease grade, distinguishing high- vs. low-grade PCa and BCa. Dietary, environmental and geographic patterns influenced urinary microbiota. Urinary microbiota of benign prostatic hyperplasia was different from PCa.

Conclusion

Urological cancer patients have an altered urinary microbiota compared to controls. This may predict recurrence, disease stage and disease grade of these tumors. Further prospective studies are needed to depict a potential influence on therapeutic outcomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The human microbiome project. Nature 449(7164):804–810

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Hilt EE, McKinley K, Pearce MM et al (2014) Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol 52(3):871–876

    Article  PubMed Central  PubMed  Google Scholar 

  3. Antunes-Lopes T, Vale L, Coelho AM et al (2020) The role of urinary microbiota in lower urinary tract dysfunction: a systematic review. Eur Urol Focus 6(2):361–369

    Article  PubMed  Google Scholar 

  4. Pearce MM, Zilliox MJ, Rosenfeld AB et al (2015) The female urinary microbiome in urgency urinary incontinence. Am J Obstet Gynecol 213(3):347.e1-347.e11

    Article  Google Scholar 

  5. Siddiqui H, Lagesen K, Nederbragt AJ, Jeansson SL, Jakobsen KS (2012) Alterations of microbiota in urine from women with interstitial cystitis. BMC Microbiol 12(1):205

    Article  PubMed Central  PubMed  Google Scholar 

  6. Khasriya R, Sathiananthamoorthy S, Ismail S et al (2013) Spectrum of bacterial colonization associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol 51(7):2054–2062

    Article  PubMed Central  PubMed  Google Scholar 

  7. Shoskes DA, Altemus J, Polackwich AS, Tucky B, Wang H, Eng C (2016) 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 92:26–32

    Article  PubMed  Google Scholar 

  8. Nicolaro M, Portal DE, Shinder B, Patel HV, Singer EA (2020) The human microbiome and genitourinary malignancies. Ann Transl Med 8(19):1245–1245

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Markowski MC, Boorjian SA, Burton JP et al (2019) The microbiome and genitourinary cancer: a collaborative review. Eur Urol 75(4):637–646

    Article  PubMed  Google Scholar 

  10. Pederzoli F, Bandini M, Raggi D et al (2021) Is there a detrimental effect of antibiotic therapy in patients with muscle-invasive bladder cancer treated with neoadjuvant pembrolizumab? Eur Urol S0302–2838(21):00387

    Google Scholar 

  11. Pak S, Kim S-Y, Kim SH et al (2021) Association between antibiotic treatment and the efficacy of intravesical BCG therapy in patients with high-risk non-muscle invasive bladder cancer. Front Oncol 11:570077

    Article  PubMed Central  PubMed  Google Scholar 

  12. Ueda K, Yonekura S, Ogasawara N et al (2019) The impact of antibiotics on prognosis of metastatic renal cell carcinoma in Japanese patients treated with immune checkpoint inhibitors. Anticancer Res 39(11):6265–6271

    Article  CAS  PubMed  Google Scholar 

  13. Bučević Popović V, Šitum M, Chow C-ET, Chan LS, Roje B, Terzić J (2018) The urinary microbiome associated with bladder cancer. Sci Rep 8(1):12157

    Article  PubMed Central  PubMed  Google Scholar 

  14. Wu P, Zhang G, Zhao J et al (2018) Profiling the urinary microbiota in male patients with bladder cancer in China. Front Cell Infect Microbiol 8:167

    Article  PubMed Central  PubMed  Google Scholar 

  15. Bi H, Tian Y, Song C et al (2019) Urinary microbiota—a potential biomarker and therapeutic target for bladder cancer. J Med Microbiol 68(10):1471–1478

    Article  CAS  PubMed  Google Scholar 

  16. Pederzoli F, Ferrarese R, Amato V et al (2020) Sex-specific alterations in the urinary and tissue microbiome in therapy-naïve urothelial bladder cancer patients. Eur Urol Oncol 3(6):784–788

    Article  PubMed  Google Scholar 

  17. Mansour B, Monyók Á, Makra N et al (2020) Bladder cancer-related microbiota: examining differences in urine and tissue samples. Sci Rep 10(1):11042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Mai G, Chen L, Li R, Liu Q, Zhang H, Ma Y (2019) Common core bacterial biomarkers of bladder cancer based on multiple datasets. Biomed Res Int 2019:4824909

    PubMed  PubMed Central  Google Scholar 

  19. Zeng J, Zhang G, Chen C et al (2020) Alterations in urobiome in patients with bladder cancer and implications for clinical outcome: a single-institution study. Front Cell Infect Microbiol 10:555508

    Article  PubMed Central  PubMed  Google Scholar 

  20. Liu F, Liu A, Lu X et al (2019) Dysbiosis signatures of the microbial profile in tissue from bladder cancer. Cancer Med 8(16):6904–6914

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Nadler N, Kvich L, Bjarnsholt T, Jensen JB, Gögenur I, Azawi N (2021) The discovery of bacterial biofilm in patients with muscle invasive bladder cancer. APMIS 129(5):265–270

    Article  CAS  PubMed  Google Scholar 

  22. Moynihan M, Sullivan T, Provenzano K, Rieger-Christ K (2019) Urinary microbiome evaluation in patients presenting with hematuria with a focus on exposure to tobacco smoke. Res Rep Urol 11:359–367

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hussein AA, Elsayed AS, Durrani M et al (2021) Investigating the association between the urinary microbiome and bladder cancer: an exploratory study. Urol Oncol. https://doi.org/10.1016/j.urolonc.2020.12.011

    Article  PubMed  Google Scholar 

  24. Oresta B, Braga D, Lazzeri M et al (2021) The microbiome of catheter collected urine in males with bladder cancer according to disease stage. J Urol 205(1):86–93

    Article  PubMed  Google Scholar 

  25. Chipollini J, Wright JR, Nwanosike H et al (2020) Characterization of urinary microbiome in patients with bladder cancer: results from a single-institution, feasibility study. Urol Oncol 38(7):615–621

    Article  CAS  PubMed  Google Scholar 

  26. Hourigan SK, Zhu W, Wong WS et al (2020) Studying the urine microbiome in superficial bladder cancer: samples obtained by midstream voiding versus cystoscopy. BMC Urol 20(1):5

    Article  PubMed Central  PubMed  Google Scholar 

  27. Alexeyev O, Bergh J, Marklund I et al (2006) Association between the presence of bacterial 16S RNA in prostate specimens taken during transurethral resection of prostate and subsequent risk of prostate cancer (Sweden). Cancer Causes Control 17(9):1127–1133

    Article  CAS  PubMed  Google Scholar 

  28. Shrestha E, White JR, Yu S-H et al (2018) Profiling the urinary microbiome in men with positive versus negative biopsies for prostate cancer. J Urol 199(1):161–171

    Article  PubMed  Google Scholar 

  29. Alanee S, El-Zawahry A, Dynda D et al (2019) A prospective study to examine the association of the urinary and fecal microbiota with prostate cancer diagnosis after transrectal biopsy of the prostate using 16sRNA gene analysis. Prostate 79(1):81–87

    Article  CAS  PubMed  Google Scholar 

  30. Yu H, Meng H, Zhou F, Ni X, Shen S, Das UN (2015) Urinary microbiota in patients with prostate cancer and benign prostatic hyperplasia. Arch Med Sci 11(2):385–394

    Article  PubMed Central  PubMed  Google Scholar 

  31. Cavarretta I, Ferrarese R, Cazzaniga W et al (2017) The microbiome of the prostate tumor microenvironment. Eur Urol 72(4):625–631

    Article  CAS  PubMed  Google Scholar 

  32. Wang J, Li X, Wu X et al (2021) Uncovering the microbiota in renal cell carcinoma tissue using 16S rRNA gene sequencing. J Cancer Res Clin Oncol 147(2):481–491

    Article  CAS  PubMed  Google Scholar 

  33. Heidler S, Lusuardi L, Madersbacher S, Freibauer C (2020) The microbiome in benign renal tissue and in renal cell carcinoma. Urol Int 104(3–4):247–252

    Article  CAS  PubMed  Google Scholar 

  34. McConnell MJ, Actis L, Pachón J (2013) Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol Rev 37(2):130–155

    Article  CAS  PubMed  Google Scholar 

  35. Sheweita SA, Alsamghan AS (2020) Molecular mechanisms contributing bacterial infections to the incidence of various types of cancer. Mediat Inflamm 2020:4070419

    Article  Google Scholar 

  36. Drott JB, Alexeyev O, Bergström P, Elgh F, Olsson J (2010) Propionibacterium acnes infection induces upregulation of inflammatory genes and cytokine secretion in prostate epithelial cells. BMC Microbiol 10:126

    Article  PubMed Central  PubMed  Google Scholar 

  37. Derosa L, Hellmann MD, Spaziano M et al (2018) Negative association of antibiotics on clinical activity of immune checkpoint inhibitors in patients with advanced renal cell and non-small-cell lung cancer. Ann Oncol 29(6):1437–1444

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Derosa L, Routy B, Fidelle M et al (2020) Gut bacteria composition drives primary resistance to cancer immunotherapy in renal cell carcinoma patients. Eur Urol 78(2):195–206

    Article  CAS  PubMed  Google Scholar 

  39. Hopkins AM, Kichenadasse G, Karapetis CS, Rowland A, Sorich MJ (2020) Concomitant antibiotic use and survival in urothelial carcinoma treated with atezolizumab. Eur Urol 78(4):540–543

    Article  CAS  PubMed  Google Scholar 

  40. Siddiqui H, Nederbragt AJ, Lagesen K, Jeansson SL, Jakobsen KS (2011) Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol 11:244

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Neugent ML, Hulyalkar NV, Nguyen VH, Zimmern PE, De Nisco NJ (2020) Advances in understanding the human urinary microbiome and its potential role in urinary tract infection. MBio 11(2):e00218-20

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgements

None.

Funding

This study did not receive any funding.

Author information

Author notes

  1. Aya Karam and Georges Mjaess are co-first authors.

  2. Yara El Daccache, Marialida Farah and Samah Daou contributed equally to the manuscript.

Authors and Affiliations

  1. Department of Internal Medicine, Faculty of Medicine, Hotel-Dieu de France, University of Saint Joseph, Beirut, Lebanon

    Aya Karam, Yara El Daccache, Marialida Farah, Samah Daou & Rebecca Hassoun

  2. Department of Urology, University Clinics of Brussels, Erasme Hospital, Université Libre de Bruxelles, Route de Lennik 808, 1070, Brussels, Belgium

    Georges Mjaess, Simone Albisinni, George Bou Kheir, Fouad Aoun & Thierry Roumeguère

  3. Department of Radiology, Saint Joseph Medical Center, Beirut, Lebanon

    Hanane Kazzi

  4. Department of Urology, Institut Jules Bordet, Brussels, Belgium

    Fouad Aoun & Thierry Roumeguère

Authors
  1. Aya Karam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Georges Mjaess
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simone Albisinni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yara El Daccache
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marialida Farah
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Samah Daou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hanane Kazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rebecca Hassoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. George Bou Kheir
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fouad Aoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Thierry Roumeguère
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AK, GM: study conception, protocol development, data analysis, manuscript writing. SA: study conception, protocol development, manuscript writing, supervision. YED, MF, SD: data collection, data analysis, manuscript writing. HK: data analysis, manuscript editing. RH: data collection, manuscript writing. GBK: study conception, manuscript editing. FA: protocol development, manuscript editing, supervision. TR: project leader, study conception, protocol development, manuscript editing, supervision.

Corresponding author

Correspondence to Georges Mjaess.

Ethics declarations

Ethical approval

This study was performed in line with the principles of the Declaration of Helsinki. No approval from the ethics committee was necessary.

Conflict of interests

All the authors have no conflict of interest to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karam, A., Mjaess, G., Albisinni, S. et al. Uncovering the role of urinary microbiota in urological tumors: a systematic review of literature. World J Urol 40, 951–964 (2022). https://doi.org/10.1007/s00345-021-03924-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00345-021-03924-x

Keywords

Search

Navigation