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Implications of the Genitourinary Microbiota in Prostatic Disease

  • Petar BajicEmail author
  • Ryan A. Dornbier
  • Chirag P. Doshi
  • Alan J. Wolfe
  • Ahmer V. Farooq
  • Larissa Bresler
Benign Prostatic Hyperplasia (K McVary, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Benign Prostatic Hyperplasia

Abstract

Purpose of Review

To summarize recent investigation into associations between the genitourinary microbiota and prostatic disease.

Recent Findings

The genitourinary tract is not sterile. There are microbial communities (microbiota) in each niche of the genitourinary tract including the bladder, prostate, and urethra, which have been the subject of increasing scientific interest. Investigators have utilized several unique methods to study them, resulting in a highly heterogeneous body of literature. To characterize these genitourinary microbiota, diverse clinical specimens have been analyzed, including urine obtained by various techniques, seminal fluid, expressed prostatic secretions, and prostatic tissue. Recent studies have attempted to associate the microbiota detected from these samples with urologic disease and have implicated the genitourinary microbiota in many common conditions, including benign prostatic hyperplasia (BPH), prostate cancer, and chronic prostatitis/chronic pelvic pain syndrome (CP/CPPS).

Summary

In this review, we summarize the recent literature pertaining to the genitourinary microbiota and its relationship to the pathophysiology and management of three common prostatic conditions: BPH, prostate cancer, and CP/CPPS.

Keywords

Microbiota Microbiome Prostate BPH Prostate cancer Chronic prostatitis 

Notes

Acknowledgments

We would like to thank the members of the Loyola Urinary Education and Research Collaborative (LUEREC) for their contributions to the work described.

Funding

AJW has been supported by National Institutes of Health grants R01 DK104718, 2 U10 HD41250, U01 DK58229, R21 DK097435, R56 DK104718, and P20 DK108268, a translational grant from the Falk Foundation, and by RFC LU206998 from Loyola University Chicago. AJW also has received funding for an Investigator Initiated Study VESI-12D01 from Astellas Scientific and Medical Affairs, Inc. AVF and LB have been supported by Loyola University Chicago RFC LU207906. LB has also been supported by the Interstitial Cystitis Association.

Compliance with Ethical Standards

Conflict of Interest

Petar Bajic and Chirag P. Doshi each declare no potential conflicts of interest.

Ryan A. Dornbier, Ahmer V. Farooq, and Larissa Bresler report intramural funding from Loyola University Medical Center Research Committee.

Alan J. Wolfe reports grants from Astellas Scientific and Medical Affairs and Kimberly Clark Corporation.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Disclaimer

The funding sources have had no role in design or conduct of the studies; collection, management, analysis, and interpretation of the data; or in preparation, review, or approval of this or any other manuscript.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Hollingsworth JM, Wei JT. Economic impact of surgical intervention in the treatment of benign prostatic hyperplasia. Rev Urol. 2006;8(Suppl 3):S9–S15.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Auffenberg GB, Helfand BT, McVary KT. Established medical therapy for benign prostatic hyperplasia. Urol Clin North Am. 2009;36:443–59.PubMedGoogle Scholar
  3. 3.
    U.S. Department of Health and Human Services, Centers for Disease Control and Prevention and National Cancer Institute. U.S. Cancer Statistics Working Group. U.S. Cancer Statistics Data Visualizations Tool, based on November 2017 submission data (1999–2015). 2018. Available at: www.cdc.gov/cancer/dataviz. Accessed 16 Mar 2019.
  4. 4.
    Bowen DK, Dielubanza E, Schaeffer AJ. Chronic bacterial prostatitis and chronic pelvic pain syndrome. BMJ Clin Evid. 2015;2015:1802.Google Scholar
  5. 5.
    Ficarra V, Rossanese M, Zazzara M, Giannarini G, Abbinante M, Bartoletti R, et al. The role of inflammation in lower urinary tract symptoms (LUTS) due to benign prostatic hyperplasia (BPH) and its potential impact on medical therapy. Curr Urol Rep. 2014;15:463.PubMedGoogle Scholar
  6. 6.
    Gandaglia G, Zaffuto E, Fossati N, Cucchiara V, Mirone V, Montorsi F, et al. The role of prostatic inflammation in the development and progression of benign and malignant diseases. Curr Opin Urol. 2017;27:99–106.PubMedGoogle Scholar
  7. 7.
    •• Shrestha E, White JR, Yu SH, Kulac I, Ertunc O, de Marzo AM, et al. Profiling the urinary microbiome in men with positive versus negative biopsies for prostate cancer. J Urol. 2018;199:161–71 A recent study demonstrating increase in uropathogenic bacteria in cancerous prostate tissue. This study leads to additional hypotheses regarding the nature of bacterial inflammation as a determinant of prostate cancer. PubMedGoogle Scholar
  8. 8.
    Sfanos KS, Isaacs WB, De Marzo AM. Infections and inflammation in prostate cancer. Am J Clin Exp Urol. 2013;1:3–11.PubMedPubMedCentralGoogle Scholar
  9. 9.
    De Marzo AM, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer. 2007;7:256–69.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Sfanos KS, De Marzo AM. Prostate cancer and inflammation: the evidence. Histopathology. 2012;60:199–215.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Sfanos KS, Yegnasubramanian S, Nelson WG, De Marzo AM. The inflammatory microenvironment and microbiome in prostate cancer development. Nat Rev Urol. 2018;15:11–24.PubMedGoogle Scholar
  12. 12.
    Mani RS, Amin MA, Li X, Kalyana-Sundaram S, Veeneman BA, Wang L, et al. Inflammation-induced oxidative stress mediates gene fusion formation in prostate cancer. Cell Rep. 2016;17:2620–31.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Sfanos KS, Joshu CE. IBD as a risk factor for prostate cancer: what is the link? Nat Rev Urol. 2019.  https://doi.org/10.1038/s41585-019-0157-7.PubMedGoogle Scholar
  14. 14.
    Massari F, Mollica V, di Nunno V, Gatto L, Santoni M, Scarpelli M, et al. The human microbiota and prostate cancer: friend or foe? Cancers (Basel). 2019;11(4):E459.  https://doi.org/10.3390/cancers11040459 PubMedCentralGoogle Scholar
  15. 15.
    Nickel JC, et al. Leukocytes and bacteria in men with chronic prostatitis/chronic pelvic pain syndrome compared to asymptomatic controls. J Urol. 2003;170:818–22.PubMedGoogle Scholar
  16. 16.
    Breser ML, Salazar FC, Rivero VE, Motrich RD. Immunological mechanisms underlying chronic pelvic pain and prostate inflammation in chronic pelvic pain syndrome. Front Immunol. 2017;8:898.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Porter CM, Shrestha E, Peiffer LB, Sfanos KS. The microbiome in prostate inflammation and prostate cancer. Prostate Cancer Prostatic Dis. 2018;21:345–54.PubMedGoogle Scholar
  18. 18.
    Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9:577–89.PubMedGoogle Scholar
  19. 19.
    Frank DN, Zhu W, Sartor RB, Li E. Investigating the biological and clinical significance of human dysbioses. Trends Microbiol. 2011;19:427–34.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Gajer P, et al. Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 2012;4:132ra52.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, et al. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol. 2014;52:871–6.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Brubaker L, Nager CW, Richter HE, Visco A, Nygaard I, Barber MD, et al. Urinary bacteria in adult women with urgency urinary incontinence. Int Urogynecol J. 2014;25:1179–84.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K, Fok C, et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. MBio. 2014;5:e01283–14.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, FitzGerald M, et al. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50:1376–83.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Nienhouse V, Gao X, Dong Q, Nelson DE, Toh E, McKinley K, et al. Interplay between bladder microbiota and urinary antimicrobial peptides: mechanisms for human urinary tract infection risk and symptom severity. PLoS One. 2014;9:e114185.PubMedPubMedCentralGoogle Scholar
  26. 26.
    •• Bajic P, van Kuiken ME, Burge BK, Kirshenbaum EJ, Joyce CJ, Wolfe AJ, et al. Male bladder microbiome relates to lower urinary tract symptoms. Eur Urol Focus. 2018.  https://doi.org/10.1016/j.euf.2018.08.001 This study is the first study to demonstrate an association between the urinary microbiome in men and lower urinary tract symptoms. Also important in establishing the difference between voided and catheterized urine collection in men. It lays groundwork for additional investigation in the the male urinary microbiome.
  27. 27.
    Khasriya R, Sathiananthamoorthy S, Ismail S, Kelsey M, Wilson M, Rohn JL, et al. Spectrum of bacterial colonization associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol. 2013;51:2054–62.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Fouts DE, Pieper R, Szpakowski S, Pohl H, Knoblach S, Suh MJ, 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.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Karstens L, et al. Does the urinary microbiome play a role in urgency urinary incontinence and its severity? Front Cell Infect Microbiol. 2016;6:78.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Brubaker L, Wolfe A. The urinary microbiota: a paradigm shift for bladder disorders? Curr Opin Obstet Gynecol. 2016;28:407–12.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Brubaker L, Wolfe AJ. The female urinary microbiota, urinary health and common urinary disorders. Ann Transl Med. 2017;5:34.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Pearce MM, et al. The female urinary microbiome in urgency urinary incontinence. Am J Obstet Gynecol. 2015;213(347):e1–11.Google Scholar
  33. 33.
    • Price TK, Dune T, Hilt EE, Thomas-White KJ, Kliethermes S, Brincat C, et al. The clinical urine culture: enhanced techniques improve detection of clinically relevant microorganisms. J Clin Microbiol. 2016;54:1216–22 This study further expands our knowledge of urine culture protocols and the expanded quantitative urine culture (EQUC) to identify and isolate live bacteria that would not otherwise be detected by standard clinical cultures. PubMedPubMedCentralGoogle Scholar
  34. 34.
    Thomas-White KJ, Hilt EE, Fok C, Pearce MM, Mueller ER, Kliethermes S, et al. Incontinence medication response relates to the female urinary microbiota. Int Urogynecol J. 2016;27:723–33.PubMedGoogle Scholar
  35. 35.
    Nelson DE, Dong Q, van der Pol B, Toh E, Fan B, Katz BP, et al. Bacterial communities of the coronal sulcus and distal urethra of adolescent males. PLoS One. 2012;7:e36298.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Dong Q, Nelson DE, Toh E, Diao L, Gao X, Fortenberry JD, et al. The microbial communities in male first catch urine are highly similar to those in paired urethral swab specimens. PLoS One. 2011;6:e19709.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Nelson DE, van der Pol B, Dong Q, Revanna KV, Fan B, Easwaran S, et al. Characteristic male urine microbiomes associate with asymptomatic sexually transmitted infection. PLoS One. 2010;5:e14116.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Nickel JC, Stephens A, Landis JR, Chen J, Mullins C, van Bokhoven A, et al. Search for microorganisms in men with urologic chronic pelvic pain syndrome: a culture-independent analysis in the MAPP research network. J Urol. 2015;194:127–35.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Lewis DA, Brown R, Williams J, White P, Jacobson SK, Marchesi JR, et al. The human urinary microbiome; bacterial DNA in voided urine of asymptomatic adults. Front Cell Infect Microbiol. 2013;3:41.PubMedPubMedCentralGoogle Scholar
  40. 40.
    • Thomas-White KJ, Gao X, Lin H, Fok CS, Ghanayem K, Mueller ER, et al. Urinary microbes and postoperative urinary tract infection risk in urogynecologic surgical patients. Int Urogynecol J. 2018;29:1797–805 In this study, the authors showed that certain preoperative urinary microbiome profiles in women lead to increased risk of postoperative, symptomatic UTI. Moreover, abundance of Lactobacillus iners was associated with protection against UTI development. This may have an important corollary in men in that dysbiosis of the urinary microbiome may lead to increased risk of disease. PubMedGoogle Scholar
  41. 41.
    Fok CS, et al. Urinary symptoms are associated with certain urinary microbes in urogynecologic surgical patients. Int Urogynecol J. 2018;29:1765–71.PubMedGoogle Scholar
  42. 42.
    Kass EH. Pyelonephritis and bacteriuria. Ann Intern Med. 1962;56:46.PubMedGoogle Scholar
  43. 43.
    Coorevits L, Heytens S, Boelens J, Claeys G. The resident microflora of voided midstream urine of healthy controls: standard versus expanded urine culture protocols. Eur J Clin Microbiol Infect Dis. 2017;36:635–9.PubMedGoogle Scholar
  44. 44.
    Gottschick C, Deng ZL, Vital M, Masur C, Abels C, Pieper DH, et al. The urinary microbiota of men and women and its changes in women during bacterial vaginosis and antibiotic treatment. Microbiome. 2017;5:99.PubMedPubMedCentralGoogle Scholar
  45. 45.
    • Yu H, et al. Urinary microbiota in patients with prostate cancer and benign prostatic hyperplasia. Arch Med Sci. 2015;11:385–94 In this study, investigators showed a difference in bacterial flora in men with and without prostate cancer. This study utilized expressed prostatic secretions as a sample type, introducing a less invasive way to detect prostatic microbiota outside of invasive tissue sampling. PubMedPubMedCentralGoogle Scholar
  46. 46.
    Alanee S, el-Zawahry A, Dynda D, Dabaja A, McVary K, Karr M, et al. 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. 2019;79:81–7.PubMedGoogle Scholar
  47. 47.
    • Cavarretta I, et al. The microbiome of the prostate tumor microenvironment. Eur Urol. 2017;72:625–31 This study examines the difference in microbial communities of various prostatic pathologies in patients with prostate cancer. In doing so, it suggests the microbiota to be a possible source of carcinogenesis and a potential therapeutic target. PubMedGoogle Scholar
  48. 48.
    Miyake M, Ohnishi K, Hori S, Nakano A, Nakano R, Yano H, et al. Mycoplasma genitalium infection and chronic inflammation in human prostate cancer: detection using prostatectomy and needle biopsy specimens. Cells. 2019;8:212.PubMedCentralGoogle Scholar
  49. 49.
    • Feng Y, et al. Metagenomic and metatranscriptomic analysis of human prostate microbiota from patients with prostate cancer. BMC Genomics. 2019;20:146 The importance of this study relates to the use of advanced miciobial detection methods with metagenomic and metascriptomic profiling for detecting the non-“sterile” environment in the prostate and prostate tumor tissue. PubMedPubMedCentralGoogle Scholar
  50. 50.
    •• Mändar R, Punab M, Korrovits P, Türk S, Ausmees K, Lapp E, et al. Seminal microbiome in men with and without prostatitis. Int J Urol. 2017;24:211–6 In this study, the authors demonstrate a different microbial profile in patients with CP/CPPS compared to controls. Importantly, there was a relative depletion of the genus Lactobacillus. These findings are similar to previous studies in women suggesting the importance of Lactobacillus in the genitourinary microbiome. PubMedGoogle Scholar
  51. 51.
    • Shoskes DA, Altemus J, Polackwich AS, 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 Additional evidence suggesting a difference in microbiota composition in patients with and without CP/CPPS. This study used voided urine. PubMedGoogle Scholar
  52. 52.
    Russo GI, Urzì D, Cimino S. Epidemiology of LUTS and BPH. Lower Urinary Tract Symptoms and Benign Prostatic Hyperplasia; 2018. p. 1–14.  https://doi.org/10.1016/b978-0-12-811397-4.00001-9.CrossRefGoogle Scholar
  53. 53.
    McConnell JD, et al. The long-term effect of doxazosin, finasteride, and combination therapy on the clinical progression of benign prostatic hyperplasia. N Engl J Med. 2003;349:2387–98.Google Scholar
  54. 54.
    Roehrborn CG, Siami P, Barkin J, Damião R, Major-Walker K, Nandy I, et al. The effects of combination therapy with dutasteride and tamsulosin on clinical outcomes in men with symptomatic benign prostatic hyperplasia: 4-year results from the CombAT study. Eur Urol. 2010;57:123–31.Google Scholar
  55. 55.
    McVary KT, Roehrborn CG, Avins AL, Barry MJ, Bruskewitz RC, Donnell RF, et al. Update on AUA guideline on the management of benign prostatic hyperplasia. J Urol. 2011;185:1793–803.Google Scholar
  56. 56.
    Djavan B. The correlation between inflammation, BPH and prostate cancer. Eur Urol Suppl. 2009;8:863–4.Google Scholar
  57. 57.
    Pisano F. The contribution of prostate infection and inflammation to BPH and cancer. Prostatitis and Its Management; 2016. p. 87–94.  https://doi.org/10.1007/978-3-319-25175-2_10.CrossRefGoogle Scholar
  58. 58.
    Kashyap M, Pore S, Wang Z, Gingrich J, Yoshimura N, Tyagi P. Inflammasomes are important mediators of prostatic inflammation associated with BPH. J Inflamm. 2015;12:37.Google Scholar
  59. 59.
    Jiang Y-H, Lin VC-H, Liao C-H, Kuo H-C. International prostatic symptom score — voiding/storage subscore ratio in association with total prostatic volume and maximum flow rate is diagnostic of bladder outlet-related lower urinary tract dysfunction in men with lower urinary tract symptoms. PLoS One. 2013;8:e59176.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Liao C-H, Kuo H-C. Use of the international prostate symptom score voiding-to-storage subscore ratio in assessing lower urinary tract symptoms. Tzu Chi Med J. 2014;26:61–3.Google Scholar
  61. 61.
    Chuang F-C, Hsiao S-M, Kuo H-C. The overactive bladder symptom score, international prostate symptom score–storage subscore, and urgency severity score in patients with overactive bladder and hypersensitive bladder: which scoring system is best? Int Neurourol J. 2018;22:99–106.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Roberts RO, Bergstralh EJ, Bass SE, Lieber MM, Jacobsen SJ. Prostatitis as a risk factor for prostate cancer. Epidemiology. 2004;15:93–9.PubMedGoogle Scholar
  63. 63.
    Dennis LK, Lynch CF, Torner JC. Epidemiologic association between prostatitis and prostate cancer. Urology. 2002;60:78–83.PubMedGoogle Scholar
  64. 64.
    Masood U, Sharma A, Lowe D, Khan R, Manocha D. Colorectal cancer associated with Streptococcus anginosus bacteremia and liver abscesses. Case Rep Gastroenterol. 2016;10:769–74.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Sasaki M, Yamaura C, Ohara-Nemoto Y, Tajika S, Kodama Y, Ohya T, et al. Streptococcus anginosus infection in oral cancer and its infection route. Oral Dis. 2005;11:151–6.PubMedGoogle Scholar
  66. 66.
    Shiga K, et al. Presence of Streptococcus infection in extra-oropharyngeal head and neck squamous cell carcinoma and its implication in carcinogenesis. Oncol Rep. 2001;8:245–8.PubMedGoogle Scholar
  67. 67.
    Domann E, Hong G, Imirzalioglu C, Turschner S, Kuhle J, Watzel C, et al. Culture-independent identification of pathogenic bacteria and polymicrobial infections in the genitourinary tract of renal transplant recipients. J Clin Microbiol. 2003;41:5500–10.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Williams GD. Two cases of urinary tract infection caused by Propionimicrobium lymphophilum. J Clin Microbiol. 2015;53:3077–80.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Glassing A, Dowd SE, Galandiuk S, Davis B, Chiodini RJ. Inherent bacterial DNA contamination of extraction and sequencing reagents may affect interpretation of microbiota in low bacterial biomass samples. Gut Pathog. 2016;8:24.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Mollerup S, Friis-Nielsen J, Vinner L, Hansen TA, Richter SR, Fridholm H, et al. Propionibacterium acnes: disease-causing agent or common contaminant? Detection in diverse patient samples by next-generation sequencing. J Clin Microbiol. 2016;54:980–7.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Yow MA, et al. Characterisation of microbial communities within aggressive prostate cancer tissues. Infect Agent Cancer. 2017;12:4.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Keay S, Zhang CO, Baldwin BR, Alexander RB. Polymerase chain reaction amplification of bacterial 16s rRNA genes in prostate biopsies from men without chronic prostatitis. Urology. 1999;53:487–91.PubMedGoogle Scholar
  73. 73.
    Krieger JN, et al. Bacterial dna sequences in prostate tissue from patients with prostate cancer and chronic prostatitis. J Urol. 2000;164:1221–8.PubMedGoogle Scholar
  74. 74.
    Sfanos KS, Sauvageot J, Fedor HL, Dick JD, de Marzo AM, Isaacs WB. A molecular analysis of prokaryotic and viral DNA sequences in prostate tissue from patients with prostate cancer indicates the presence of multiple and diverse microorganisms. Prostate. 2008;68:306–20.PubMedGoogle Scholar
  75. 75.
    Xiang J, Yan H, Li J, Wang X, Chen H, Zheng X. Transperineal versus transrectal prostate biopsy in the diagnosis of prostate cancer: a systematic review and meta-analysis. World J Surg Oncol. 2019;17:31.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Schaeffer AJ. Epidemiology and evaluation of chronic pelvic pain syndrome in men. Int J Antimicrob Agents. 2008;31(Suppl 1):S108–11.PubMedGoogle Scholar
  77. 77.
    Meares EM, Stamey TA. Bacteriologic localization patterns in bacterial prostatitis and urethritis. Investig Urol. 1968;5:492–518.Google Scholar
  78. 78.
    Schwager S, Agnoli K, Köthe M, Feldmann F, Givskov M, Carlier A, et al. Identification of Burkholderia cenocepacia strain H111 virulence factors using nonmammalian infection hosts. Infect Immun. 2013;81:143–53.PubMedPubMedCentralGoogle Scholar
  79. 79.
    Arzola JM, Hawley JS, Oakman C, Mora RV. A case of prostatitis due to Burkholderia pseudomallei. Nat Clin Pract Urol. 2007;4:111–4.PubMedGoogle Scholar
  80. 80.
    Organ M, Grantmyre J, Hutchinson J. Burkholderia cepacia infection of the prostate caused by inoculation of contaminated ultrasound gel during transrectal biopsy of the prostate. Can Urol Assoc J. 2010;4:E58–60.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Hütt P, et al. Characterisation of probiotic properties in human vaginal lactobacilli strains. Microb Ecol Health Dis. 2016;27:30484.PubMedGoogle Scholar
  82. 82.
    Miller EA, Beasley DE, Dunn RR, Archie EA. Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique? Front Microbiol. 2016;7:1936.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Shoskes DA, Wang H, Polackwich AS, Tucky B, Altemus J, Eng C. Analysis of gut microbiome reveals significant differences between men with chronic prostatitis/chronic pelvic pain syndrome and controls. J Urol. 2016;196:435–41.PubMedGoogle Scholar
  84. 84.
    Murphy SF, Schaeffer AJ, Done JD, Quick ML, Acar U, Thumbikat P. Commensal bacterial modulation of the host immune response to ameliorate pain in a murine model of chronic prostatitis. Pain. 2017;158:1517–27.PubMedPubMedCentralGoogle Scholar
  85. 85.
    Hetrick DC, et al. Musculoskeletal dysfunction in men with chronic pelvic pain syndrome type III: a case-control study. J Urol. 2003;170:828–31.PubMedGoogle Scholar
  86. 86.
    Berger RE, Ciol MA, Rothman I, Turner JA. Pelvic tenderness is not limited to the prostate in chronic prostatitis/chronic pelvic pain syndrome (CPPS) type IIIA and IIIB: comparison of men with and without CP/CPPS. BMC Urol. 2007;7:17.Google Scholar
  87. 87.
    Anderson RU, Wise D, Nathanson BH. Chronic prostatitis and/or chronic pelvic pain as a psychoneuromuscular disorder—a meta-analysis. Urology. 2018;120:23–9.PubMedGoogle Scholar
  88. 88.
    Shoskes DA, Nickel JC. Classification and treatment of men with chronic prostatitis/chronic pelvic pain syndrome using the UPOINT system. World J Urol. 2013;31:755–60.PubMedGoogle Scholar
  89. 89.
    Ackerman AL, Underhill DM. The mycobiome of the human urinary tract: potential roles for fungi in urology. Ann Transl Med. 2017;5:31.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Garretto A, Thomas-White K, Wolfe AJ, Putonti C. Detecting viral genomes in the female urinary microbiome. J Gen Virol. 2018;99:1141–6.PubMedGoogle Scholar
  91. 91.
    Miller-Ensminger T, Garretto A, Brenner J, Thomas-White K, Zambom A, Wolfe AJ, et al. Bacteriophages of the urinary microbiome. J Bacteriol. 2018;200(7):e00738–17.  https://doi.org/10.1128/JB.00738-17
  92. 92.
    Bang C, Schmitz RA. Archaea: forgotten players in the microbiome. Emerg Top Life Sci. 2018;2:459–68.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Petar Bajic
    • 1
    Email author
  • Ryan A. Dornbier
    • 1
  • Chirag P. Doshi
    • 1
  • Alan J. Wolfe
    • 2
  • Ahmer V. Farooq
    • 1
  • Larissa Bresler
    • 1
  1. 1.Department of UrologyLoyola University Chicago Stritch School of MedicineMaywoodUSA
  2. 2.Department of Microbiology and ImmunologyLoyola University Chicago Stritch School of MedicineMaywoodUSA

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