Skip to main content

Advertisement

SpringerLink
Log in

The influence of gut microbiome on progression of overactive bladder symptoms: a community-based 3-year longitudinal study in Aomori, Japan

  • Urology - Original Paper
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Purpose

To assess the influence of gut microbiome on overactive bladder (OAB) symptoms progression.

Methods

This was a 3-year longitudinal study, Hirosaki in Japan. We assessed OAB symptoms and reviewed the medication records of each subject in 2016. We extracted 16S rRNA genes from fecal samples and analyzed gut microbiomes via next-generation sequencing. We evaluated the changes in urinary urgency (UU) and/or urgent urinary incontinence (UUI) from 2016 to 2019. We defined UU/UUI-progression as exacerbation of UU and/or UUI. We compared the clinical backgrounds and microbiota structure between UU/UUI-progression subjects and non-progression (controls). We assessed the impact of gut microbiome on the UU/UUI-progression via multivariate logistic regression analyses.

Results

Of 669 subjects, 126 were UU/UUI-progression subjects. These subjects had a higher age and prevalence of proton pump inhibitor (PPI) use (14% vs. 5.4%, P = 0.003), irritable bowel syndrome, sleep disturbance, and metabolic syndrome than those without. We found the different microbiota structures between subjects with UU/UUI-progression and those without. A higher relative abundance of genus Streptococcus (harmful bacterial genus for human health) appeared in UU/UUI-progression subjects (3.8% vs. 2.3%, P < 0.001). Multivariate analysis revealed that age ≥ 65 years, current smoking, sleep disturbance, metabolic syndrome, and genus Streptococcus (Odds ratio: 1.05, P = 0.029) were independent risk factors for UU/UUI-progression. PPI use turned to be a significant risk factor on a multivariate analysis without including genus Streptococcus.

Conclusions

Gut microbiome might be associated with a risk for OAB symptoms progression. PPI use might cause gut dysbiosis and increase this risk.

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

Data availability

The datasets generated during and/or analyzed during this study are available from the corresponding author on reasonable request.

References

  1. Leron E, Weintraub AY, Mastrolia SA, Schwarzman P (2018) Overactive bladder syndrome: evaluation and management. Curr Urol 11(3):117–125. https://doi.org/10.1159/000447205

    Article  PubMed  PubMed Central  Google Scholar 

  2. Barlow GM, Yu A, Mathur R (2015) Role of the gut microbiome in obesity and diabetes mellitus. Nutr Clin Pract 30(6):787–797. https://doi.org/10.1177/0884533615609896

    Article  CAS  PubMed  Google Scholar 

  3. Yin J, Liao S-X, He Y et al (2015) Dysbiosis of gut microbiota with reduced trimethylamine-N-Oxide level in patients with large-artery atherosclerotic stroke or transient ischemic attack. J Am Heart Assoc. https://doi.org/10.1161/JAHA.115.002699

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kanbay M, Onal EM, Afsar B et al (2018) The crosstalk of gut microbiota and chronic kidney disease: role of inflammation, proteinuria, hypertension, and diabetes mellitus. Int Urol Nephrol 50(8):1453–1466. https://doi.org/10.1007/s11255-018-1873-2

    Article  PubMed  Google Scholar 

  5. Matsumoto H, Shiotani A, Katsumata R et al (2021) Mucosa-associated microbiota in patients with irritable bowel syndrome: a comparison of subtypes. Digestion 102(1):49–56. https://doi.org/10.1159/000512167

    Article  CAS  PubMed  Google Scholar 

  6. Okamoto T, Hatakeyama S, Imai A et al (2020) Altered gut microbiome associated with overactive bladder and daily urinary urgency. World J Urol (Published Online). https://doi.org/10.1007/s00345-020-03243-7

    Article  Google Scholar 

  7. Matsuo S, Imai E, Horio M et al (2009) Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53(6):982–992. https://doi.org/10.1053/j.ajkd.2008.12.034

    Article  CAS  PubMed  Google Scholar 

  8. Kanazawa M, Palsson OS, Thiwan SIM et al (2008) Contributions of pain sensitivity and colonic motility to IBS symptom severity and predominant bowel habits. Am J Gastroenterol 103(10):2550–2561. https://doi.org/10.1111/j.1572-0241.2008.02066.x

    Article  PubMed  Google Scholar 

  9. Urashima M, Wada T, Fukumoto T et al (2005) Prevalence of metabolic syndrome in a 22, 892 Japanese Population and Japan. Med Assoc J 48(9):441–450

    Google Scholar 

  10. Kido K, Hatakeyama S, Imai A et al (2018) Sleep disturbance has a higher impact on general and mental quality of life reduction than nocturia: results from the community health survey in Japan. Eur Urol Focus. https://doi.org/10.1016/j.euf.2018.04.017

    Article  PubMed  Google Scholar 

  11. Radloff LS (1977) The CES-D scale. Appl Psychol Meas 1(3):385–401. https://doi.org/10.1177/014662167700100306

    Article  Google Scholar 

  12. Vilagut G, Forero CG, Barbaglia G, Alonso J (2016) Screening for depression in the general population with the center for epidemiologic studies depression (CES-D): a systematic review with meta-analysis. PLoS ONE 11(5):e0155431. https://doi.org/10.1371/journal.pone.0155431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Homma Y, Yoshida M, Seki N et al (2006) Symptom assessment tool for overactive bladder syndrome—overactive bladder symptom score. Urology 68(2):318–323. https://doi.org/10.1016/j.urology.2006.02.042

    Article  PubMed  Google Scholar 

  14. Holland B, Karr M, Delfino K et al (2019) The effect of the urinary and fecal microbiota on lower urinary tract symptoms measured by the international prostate symptom score: analysis utilizing next-generation sequencing. BJU Int. https://doi.org/10.1111/bju.14972

    Article  Google Scholar 

  15. Bruno G, Zaccari P, Rocco G et al (2019) Proton pump inhibitors and dysbiosis: Current knowledge and aspects to be clarified. World J Gastroenterol 25(22):2706–2719. https://doi.org/10.3748/wjg.v25.i22.2706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. De Jager CPC, Wever PC, Gemen EFA et al (2012) Proton pump inhibitor therapy predisposes to community-acquired Streptococcus pneumoniae pneumonia. Aliment Pharmacol Ther 36(10):941–949. https://doi.org/10.1111/apt.12069

    Article  PubMed  Google Scholar 

  17. Horvath A, Rainer F, Bashir M et al (2019) Biomarkers for oralization during long-term proton pump inhibitor therapy predict survival in cirrhosis. Sci Rep 9(1):1–9. https://doi.org/10.1038/s41598-019-48352-5

    Article  CAS  Google Scholar 

  18. Jie Z, Xia H, Zhong S-L et al (2017) The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun 8(1):845. https://doi.org/10.1038/s41467-017-00900-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Pittayanon R, Lau JT, Yuan Y et al (2019) Gut Microbiota in patients with irritable bowel syndrome-a systematic review. Gastroenterology 157(1):97–108. https://doi.org/10.1053/j.gastro.2019.03.049

    Article  PubMed  Google Scholar 

  20. Matsumoto S, Hashizume K, Wada N et al (2013) Relationship between overactive bladder and irritable bowel syndrome: a large-scale internet survey in Japan using the overactive bladder symptom score and Rome III criteria. BJU Int 111(4):647–652. https://doi.org/10.1111/j.1464-410X.2012.11591.x

    Article  PubMed  Google Scholar 

  21. Christianson JA, Liang R, Ustinova EE et al (2007) Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128(3):235–243. https://doi.org/10.1016/j.pain.2006.09.023

    Article  PubMed  Google Scholar 

  22. Esan OB, Perera R, McCarthy N, Violato M, Fanshawe TR (2020) Incidence, risk factors, and health service burden of sequelae of campylobacter and non-typhoidal salmonella infections in England, 2000–2015: a retrospective cohort study using linked electronic health records. J Infect 81(2):221–230. https://doi.org/10.1016/j.jinf.2020.05.027

    Article  CAS  PubMed  Google Scholar 

  23. Howden CW, Hunt RH (1987) Relationship between gastric secretion and infection. Gut 28(1):96–107. https://doi.org/10.1136/gut.28.1.96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wallace JL, Syer S, Denou E et al (2011) Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. https://doi.org/10.1053/j.gastro.2011.06.075

    Article  PubMed  Google Scholar 

  25. Chey WD, Mody RR, Wu EQ et al (2009) Treatment patterns and symptom control in patients with GERD: US community based survey. Curr Med Res Opin 25(8):1869–1878. https://doi.org/10.1185/03007990903035745

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to Dr. Atsushi Imai in Oyokyo Kidney Research Institute Hirosaki Hospital, Prof. Shigeyuki Nakaji and the entire staff of the Department of Social Medicine in Hirosaki University for their invaluable help with data collection. JST COI Grant Number JPMJCE1302 supported this work. The authors would also like to thank Enago (www.enago.jp) for the English language review.

Funding

None.

Author information

Authors and Affiliations

  1. Department of Urology, Hirosaki University Graduate School of Medicine, 5 Zaifu-chou, Hirosaki, 036-8562, Japan

    Yoshiharu Okuyama, Teppei Okamoto, Daichi Sasaki, Kai Ozaki, Shingo Hatakeyama & Chikara Ohyama

  2. Department of Digital Nutrition, Graduate School of Medicine, Hirosaki University Graduate School of Medicine, 5 Zaifu-chou, Hirosaki, 036-8562, Japan

    Jung Songee

  3. Innovation Center for Health Promotion, Hirosaki University Graduate School of Medicine, 5 Zaifu-chou, Hirosaki, 036-8562, Japan

    Tatsuya Mikami

  4. Department of Advanced Transplant and Regenerative Medicine, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

    Chikara Ohyama

Authors
  1. Yoshiharu Okuyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teppei Okamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daichi Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Ozaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jung Songee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shingo Hatakeyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tatsuya Mikami
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chikara Ohyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

1) Conception and design of the study: TO, SH, and CO, 2) analysis and interpretation of data: YO, DS, KO, SH and TO, 3) collection and assembly of data: JS, TM, SH, and CO, 4) drafting of the article: YO and TO, 5) critical revision of the article for important intellectual content: SH, and CO, all other authors have contributed to data collection and interpretation and critically reviewed the manuscript. All authors approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Teppei Okamoto.

Ethics declarations

Conflict of interest

The authors have no competing interests.

Ethical approval

Written informed consent was obtained from all subjects. The data we used from the Iwaki Health Promotion Project was approved by the Ethics Committee of Hirosaki University School of Medicine (authorization number 2021-003raH).

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 32387 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okuyama, Y., Okamoto, T., Sasaki, D. et al. The influence of gut microbiome on progression of overactive bladder symptoms: a community-based 3-year longitudinal study in Aomori, Japan. Int Urol Nephrol 54, 9–16 (2022). https://doi.org/10.1007/s11255-021-03044-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-021-03044-w

Keywords

Search

Navigation