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Published in: International Urology and Nephrology 8/2020

01-08-2020 | Erectile Dysfunction | Urology - Original Paper

The association between gut microbiome and erectile dysfunction: a community-based cross-sectional study in Japan

Authors: Teppei Okamoto, Shingo Hatakeyama, Atsushi Imai, Hayato Yamamoto, Tohru Yoneyama, Kazuyuki Mori, Takahiro Yoneyama, Yasuhiro Hashimoto, Shigeyuki Nakaji, Chikara Ohyama

Published in: International Urology and Nephrology | Issue 8/2020

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Abstract

Purpose

We investigated the gut microbiome in subjects with erectile dysfunction (ED) in a community-based population.

Methods

This cross-sectional study surveyed comprehensive health status in 408 men who participated in the Iwaki Health Promotion Project in 2015 in Hirosaki, Japan. The gut microbiome was assessed by tag sequencing of the 16S rRNA gene, which we extracted from fecal samples. Erectile function was evaluated with the five-item International Index of Erectile Function (IIEF-5), and the men were divided into two groups: low-IIEF-5 (≤ 16) and high-IIEF-5 (> 16). Of those, we selected age-adjusted 192 men (96 each) for analysis. We investigated the association of gut microbiome with IIEF-5 between the two groups.

Results

Median age was 50 years. No significant difference was seen in the history of hypertension, DM, CKD, and CVD between the low-IIEF-5 and high-IIEF-5 groups. However, the relative abundance of Alistipes (related with anti-inflammation) and Clostoridium XVIII (related with bowel movement) was significantly different between the two groups. Multivariate logistic analysis demonstrated that the relative abundance of Clostridium XVIII (OR, 2.06; 95% CI, 1.20–3.55, P = 0.009) and Alistipes (OR, 0.81; 95% CI, 0.66–0.99, P = 0.040) and, with an IPSS ≥ 8, were independent factors for low IIEF-5.

Conclusion

We observed significant association between the low-IIEF-5 and high-IIEF-5 groups in Alistipes and Clostoridium XVIII. Further study is necessary to access the causal relationship between the gut microbiome and ED.
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Literature
1.
go back to reference Otoole PW, Jeffery IB (2015) Gut microbiota and aging. Science (80-) 350:1214–1215 Otoole PW, Jeffery IB (2015) Gut microbiota and aging. Science (80-) 350:1214–1215
2.
go back to reference Barlow GM, Yu A, Mathur R (2015) Role of the gut microbiome in obesity and diabetes mellitus. Nutr Clin Pract 30:787–797PubMed Barlow GM, Yu A, Mathur R (2015) Role of the gut microbiome in obesity and diabetes mellitus. Nutr Clin Pract 30:787–797PubMed
3.
go back to reference Yin J, Liao S-X, He Y, Wang S, Xia G-H, Liu F-T 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 4:e002699PubMedPubMedCentral Yin J, Liao S-X, He Y, Wang S, Xia G-H, Liu F-T 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 4:e002699PubMedPubMedCentral
4.
go back to reference Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G et al (2017) Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 5:14PubMedPubMedCentral Li J, Zhao F, Wang Y, Chen J, Tao J, Tian G et al (2017) Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 5:14PubMedPubMedCentral
5.
go back to reference Kanbay M, Onal EM, Afsar B, Dagel T, Yerlikaya A, Covic A et al (2018) The crosstalk of gut microbiota and chronic kidney disease: role of inflammation, proteinuria, hypertension, and diabetes mellitus. Int Urol Nephrol 50:1453–1466PubMed Kanbay M, Onal EM, Afsar B, Dagel T, Yerlikaya A, Covic A et al (2018) The crosstalk of gut microbiota and chronic kidney disease: role of inflammation, proteinuria, hypertension, and diabetes mellitus. Int Urol Nephrol 50:1453–1466PubMed
6.
go back to reference Li N, Wang X, Sun C, Wu X, Lu M, Si Y et al (2019) Change of intestinal microbiota in cerebral ischemic stroke patients. BMC Microbiol 19:191PubMedPubMedCentral Li N, Wang X, Sun C, Wu X, Lu M, Si Y et al (2019) Change of intestinal microbiota in cerebral ischemic stroke patients. BMC Microbiol 19:191PubMedPubMedCentral
7.
go back to reference Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L (2016) Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 7:979PubMedPubMedCentral Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L (2016) Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 7:979PubMedPubMedCentral
8.
go back to reference van den Munckhof ICL, Kurilshikov A, Ter Horst R, Riksen NP, Joosten LAB, Zhernakova A et al (2018) Role of gut microbiota in chronic low-grade inflammation as potential driver for atherosclerotic cardiovascular disease: a systematic review of human studies. Obes Rev 19:1719–1734PubMed van den Munckhof ICL, Kurilshikov A, Ter Horst R, Riksen NP, Joosten LAB, Zhernakova A et al (2018) Role of gut microbiota in chronic low-grade inflammation as potential driver for atherosclerotic cardiovascular disease: a systematic review of human studies. Obes Rev 19:1719–1734PubMed
9.
go back to reference Walker A, Pfitzner B, Harir M, Schaubeck M, Calasan J, Heinzmann SS et al (2017) Sulfonolipids as novel metabolite markers of Alistipes and Odoribacter affected by high-fat diets. Sci Rep 7:11047PubMedPubMedCentral Walker A, Pfitzner B, Harir M, Schaubeck M, Calasan J, Heinzmann SS et al (2017) Sulfonolipids as novel metabolite markers of Alistipes and Odoribacter affected by high-fat diets. Sci Rep 7:11047PubMedPubMedCentral
10.
go back to reference Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J et al (2017) New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5:24PubMedPubMedCentral Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J et al (2017) New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5:24PubMedPubMedCentral
11.
go back to reference Zhang Z, Li H, Zhang X, Dai Y, Park HJ, Jiann B et al (2019) Efficacy and safety of tadalafil 5 mg once-daily in Asian men with both lower urinary tract symptoms associated with benign prostatic hyperplasia and erectile dysfunction: A phase 3, randomized, double-blind, parallel, placebo- and tamsulosin-controlled s. Int J Urol 26:192–200PubMed Zhang Z, Li H, Zhang X, Dai Y, Park HJ, Jiann B et al (2019) Efficacy and safety of tadalafil 5 mg once-daily in Asian men with both lower urinary tract symptoms associated with benign prostatic hyperplasia and erectile dysfunction: A phase 3, randomized, double-blind, parallel, placebo- and tamsulosin-controlled s. Int J Urol 26:192–200PubMed
12.
go back to reference Okamoto T, Hatakeyama S, Imai A, Konishi S, Okita K, Yamamoto H et al (2019) The relationship between gait function and erectile dysfunction: results from a community-based cross-sectional study in Japan. J Sex Med 16:1922–1929PubMed Okamoto T, Hatakeyama S, Imai A, Konishi S, Okita K, Yamamoto H et al (2019) The relationship between gait function and erectile dysfunction: results from a community-based cross-sectional study in Japan. J Sex Med 16:1922–1929PubMed
13.
go back to reference Cao S, Gan Y, Dong X, Liu J, Lu Z (2014) Association of quantity and duration of smoking with erectile dysfunction: a dose-response meta-analysis. J Sex Med 11:2376–2384PubMed Cao S, Gan Y, Dong X, Liu J, Lu Z (2014) Association of quantity and duration of smoking with erectile dysfunction: a dose-response meta-analysis. J Sex Med 11:2376–2384PubMed
14.
go back to reference Kałka D, Domagała Z, Dworak J, Womperski K, Rusiecki L, Marciniak W et al (2013) Association between physical exercise and quality of erection in men with ischaemic heart disease and erectile dysfunction subjected to physical training. Kardiol Pol 71:573–580PubMed Kałka D, Domagała Z, Dworak J, Womperski K, Rusiecki L, Marciniak W et al (2013) Association between physical exercise and quality of erection in men with ischaemic heart disease and erectile dysfunction subjected to physical training. Kardiol Pol 71:573–580PubMed
15.
go back to reference Calogero AE, Burgio G, Condorelli RA, Cannarella R, La Vignera S (2019) Epidemiology and risk factors of lower urinary tract symptoms/benign prostatic hyperplasia and erectile dysfunction. Aging Male 22:12–19PubMed Calogero AE, Burgio G, Condorelli RA, Cannarella R, La Vignera S (2019) Epidemiology and risk factors of lower urinary tract symptoms/benign prostatic hyperplasia and erectile dysfunction. Aging Male 22:12–19PubMed
16.
go back to reference Malavige LS, Levy JC (2009) Erectile dysfunction in diabetes mellitus. J Sex Med 6:1232–1247PubMed Malavige LS, Levy JC (2009) Erectile dysfunction in diabetes mellitus. J Sex Med 6:1232–1247PubMed
17.
go back to reference Navaneethan SD, Vecchio M, Johnson DW, Saglimbene V, Graziano G, Pellegrini F et al (2010) Prevalence and correlates of self-reported sexual dysfunction in CKD: a meta-analysis of observational studies. Am J Kidney Dis 56:670–685PubMed Navaneethan SD, Vecchio M, Johnson DW, Saglimbene V, Graziano G, Pellegrini F et al (2010) Prevalence and correlates of self-reported sexual dysfunction in CKD: a meta-analysis of observational studies. Am J Kidney Dis 56:670–685PubMed
18.
go back to reference Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB (1994) Impotence and its medical and psychosocial correlates: results of the Massachusetts male aging study. J Urol 151:54–61PubMed Feldman HA, Goldstein I, Hatzichristou DG, Krane RJ, McKinlay JB (1994) Impotence and its medical and psychosocial correlates: results of the Massachusetts male aging study. J Urol 151:54–61PubMed
19.
go back to reference Ponholzer A, Temml C, Obermayr R, Wehrberger C, Madersbacher S (2005) Is erectile dysfunction an indicator for increased risk of coronary heart disease and stroke? Eur Urol 48:512–518PubMed Ponholzer A, Temml C, Obermayr R, Wehrberger C, Madersbacher S (2005) Is erectile dysfunction an indicator for increased risk of coronary heart disease and stroke? Eur Urol 48:512–518PubMed
20.
go back to reference Fode M, Sønksen J (2014) Sexual function in elderly men receiving androgen deprivation therapy (ADT). Sex Med Rev 2:36–46PubMed Fode M, Sønksen J (2014) Sexual function in elderly men receiving androgen deprivation therapy (ADT). Sex Med Rev 2:36–46PubMed
21.
go back to reference Schauer I, Keller E, Müller A, Madersbacher S (2015) Have rates of erectile dysfunction improved within the past 17 years after radical prostatectomy? A systematic analysis of the control arms of prospective randomized trials on penile rehabilitation. Andrology 3:661–665PubMed Schauer I, Keller E, Müller A, Madersbacher S (2015) Have rates of erectile dysfunction improved within the past 17 years after radical prostatectomy? A systematic analysis of the control arms of prospective randomized trials on penile rehabilitation. Andrology 3:661–665PubMed
22.
go back to reference Pinkawa M, Gagel B, Piroth MD, Fischedick K, Asadpour B, Kehl M et al (2009) Erectile dysfunction after external beam radiotherapy for prostate cancer. Eur Urol 55:227–236PubMed Pinkawa M, Gagel B, Piroth MD, Fischedick K, Asadpour B, Kehl M et al (2009) Erectile dysfunction after external beam radiotherapy for prostate cancer. Eur Urol 55:227–236PubMed
23.
go back to reference Okihara K, Yorozu A, Saito S, Tanaka N, Koga H, Higashide S et al (2017) Assessment of sexual function in Japanese men with prostate cancer undergoing permanent brachytherapy without androgen deprivation therapy: analysis from the Japanese prostate cancer outcome study of permanent iodine-125 seed implantation database. Int J Urol 24:518–524PubMed Okihara K, Yorozu A, Saito S, Tanaka N, Koga H, Higashide S et al (2017) Assessment of sexual function in Japanese men with prostate cancer undergoing permanent brachytherapy without androgen deprivation therapy: analysis from the Japanese prostate cancer outcome study of permanent iodine-125 seed implantation database. Int J Urol 24:518–524PubMed
24.
go back to reference Ainsworth BE, Haskell WL, Leon AS, Jacobs DR, Montoye HJ, Sallis JF et al (1993) Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 25:71–80PubMed Ainsworth BE, Haskell WL, Leon AS, Jacobs DR, Montoye HJ, Sallis JF et al (1993) Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 25:71–80PubMed
25.
go back to reference Jenkinson C, Coulter A, Wright L (1993) Short form 36 (SF36) health survey questionnaire: normative data for adults of working age. BMJ 306:1437–1440PubMedPubMedCentral Jenkinson C, Coulter A, Wright L (1993) Short form 36 (SF36) health survey questionnaire: normative data for adults of working age. BMJ 306:1437–1440PubMedPubMedCentral
26.
go back to reference Matsukawa Y, Majima T, Matsuo K, Funahashi Y, Kato M, Yamamoto T et al (2018) Effects of tadalafil on storage and voiding function in patients with male lower urinary tract symptoms suggestive of benign prostatic hyperplasia: A urodynamic-based study. Int J Urol 25:246–250PubMed Matsukawa Y, Majima T, Matsuo K, Funahashi Y, Kato M, Yamamoto T et al (2018) Effects of tadalafil on storage and voiding function in patients with male lower urinary tract symptoms suggestive of benign prostatic hyperplasia: A urodynamic-based study. Int J Urol 25:246–250PubMed
27.
go back to reference Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K et al (2009) Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53:982–992PubMed Matsuo S, Imai E, Horio M, Yasuda Y, Tomita K, Nitta K et al (2009) Revised equations for estimated GFR from serum creatinine in Japan. Am J Kidney Dis 53:982–992PubMed
28.
go back to reference Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Peña BM (1999) Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 11:319–326PubMed Rosen RC, Cappelleri JC, Smith MD, Lipsky J, Peña BM (1999) Development and evaluation of an abridged, 5-item version of the International Index of Erectile Function (IIEF-5) as a diagnostic tool for erectile dysfunction. Int J Impot Res 11:319–326PubMed
29.
go back to reference Eiko T, Minoru Y, Toshio N, Hideki Y (2009) Relation between the desire to the treatment of erectile dysfunction and IIEF5 score. Kenko Igaku 19:556–559 Eiko T, Minoru Y, Toshio N, Hideki Y (2009) Relation between the desire to the treatment of erectile dysfunction and IIEF5 score. Kenko Igaku 19:556–559
30.
go back to reference Nagashima K, Hisada T, Sato M, Mochizuki J (2003) Application of new primer-enzyme combinations to terminal restriction fragment length polymorphism profiling of bacterial populations in human feces. Appl Environ Microbiol 69:1251–1262PubMedPubMedCentral Nagashima K, Hisada T, Sato M, Mochizuki J (2003) Application of new primer-enzyme combinations to terminal restriction fragment length polymorphism profiling of bacterial populations in human feces. Appl Environ Microbiol 69:1251–1262PubMedPubMedCentral
31.
go back to reference Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and Archaea using next-generation sequencing. Bourtzis K editor. PLoS ONE 9:e105592PubMedPubMedCentral Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M (2014) Development of a prokaryotic universal primer for simultaneous analysis of bacteria and Archaea using next-generation sequencing. Bourtzis K editor. PLoS ONE 9:e105592PubMedPubMedCentral
32.
go back to reference Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transplant 48:452–458PubMed Kanda Y (2013) Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transplant 48:452–458PubMed
33.
go back to reference Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60PubMedPubMedCentral Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60PubMedPubMedCentral
34.
go back to reference Maeda J, Nishida M, Takikawa H, Yoshida H, Azuma T, Yoshida M et al (2010) Inhibitory effects of sulfobacin B on DNA polymerase and inflammation. Int J Mol Med 26:751–758PubMed Maeda J, Nishida M, Takikawa H, Yoshida H, Azuma T, Yoshida M et al (2010) Inhibitory effects of sulfobacin B on DNA polymerase and inflammation. Int J Mol Med 26:751–758PubMed
35.
go back to reference Kamiyama T, Umino T, Satoh T, Sawairi S, Shirane M, Ohshima S et al (1995) Sulfobacins A and B, novel von Willebrand factor receptor antagonists. I. Production, isolation, characterization and biological activities. J Antibiot (Tokyo) 48:924–928 Kamiyama T, Umino T, Satoh T, Sawairi S, Shirane M, Ohshima S et al (1995) Sulfobacins A and B, novel von Willebrand factor receptor antagonists. I. Production, isolation, characterization and biological activities. J Antibiot (Tokyo) 48:924–928
36.
go back to reference Vlachopoulos C, Rokkas K, Ioakeimidis N, Stefanadis C (2007) Inflammation, metabolic syndrome, erectile dysfunction, and coronary artery disease: common links. Eur Urol 52:1590–1600PubMed Vlachopoulos C, Rokkas K, Ioakeimidis N, Stefanadis C (2007) Inflammation, metabolic syndrome, erectile dysfunction, and coronary artery disease: common links. Eur Urol 52:1590–1600PubMed
37.
go back to reference Jie Z, Xia H, Zhong S-L, Feng Q, Li S, Liang S et al (2017) The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun 8:845PubMedPubMedCentral Jie Z, Xia H, Zhong S-L, Feng Q, Li S, Liang S et al (2017) The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun 8:845PubMedPubMedCentral
38.
go back to reference Shimozato A, Sasaki M, Ogasawara N, Funaki Y, Ebi M, Goto C et al (2017) Transglucosidase improves the bowel movements in type 2 diabetes mellitus patients: a preliminary randomized double-blind, placebo-controlled study. United Eur Gastroenterol J 5:898–907 Shimozato A, Sasaki M, Ogasawara N, Funaki Y, Ebi M, Goto C et al (2017) Transglucosidase improves the bowel movements in type 2 diabetes mellitus patients: a preliminary randomized double-blind, placebo-controlled study. United Eur Gastroenterol J 5:898–907
39.
go back to reference Rajilić-Stojanović M, Biagi E, Heilig HGHJ, Kajander K, Kekkonen RA, Tims S et al (2011) Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 141:1792–1801PubMed Rajilić-Stojanović M, Biagi E, Heilig HGHJ, Kajander K, Kekkonen RA, Tims S et al (2011) Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 141:1792–1801PubMed
40.
go back to reference Hsu C-Y, Lin C-L, Kao C-H (2015) Irritable bowel syndrome is associated not only with organic but also psychogenic erectile dysfunction. Int J Impot Res 27:233–238PubMed Hsu C-Y, Lin C-L, Kao C-H (2015) Irritable bowel syndrome is associated not only with organic but also psychogenic erectile dysfunction. Int J Impot Res 27:233–238PubMed
41.
go back to reference Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H et al (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500:232–236PubMed Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H et al (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500:232–236PubMed
42.
go back to reference Gonzalez-Sanchez B, Cendejas-Gomez J, Alejandro Rivera-Ramirez J, Herrera-Caceres JO, Olvera-Posada D, Villeda-Sandoval CI et al (2016) The correlation between lower urinary tract symptoms (LUTS) and erectile dysfunction (ED): results from a survey in males from Mexico City (MexiLUTS). World J Urol 34:979–983PubMed Gonzalez-Sanchez B, Cendejas-Gomez J, Alejandro Rivera-Ramirez J, Herrera-Caceres JO, Olvera-Posada D, Villeda-Sandoval CI et al (2016) The correlation between lower urinary tract symptoms (LUTS) and erectile dysfunction (ED): results from a survey in males from Mexico City (MexiLUTS). World J Urol 34:979–983PubMed
43.
go back to reference Matsumoto T, Hatakeyama S, Imai A, Tanaka T, Hagiwara K, Konishi S et al (2019) Relationship between oxidative stress and lower urinary tract symptoms: results from a community health survey in Japan. BJU Int 123:877–884PubMed Matsumoto T, Hatakeyama S, Imai A, Tanaka T, Hagiwara K, Konishi S et al (2019) Relationship between oxidative stress and lower urinary tract symptoms: results from a community health survey in Japan. BJU Int 123:877–884PubMed
44.
go back to reference Soma O, Hatakeyama S, Imai A, Matsumoto T, Hamano I, Fujita N, et al. (2019). Relationship between frailty and lower urinary tract symptoms among community‐dwelling adults. LUTS Low Urin Tract Symptoms. :luts.12292. Soma O, Hatakeyama S, Imai A, Matsumoto T, Hamano I, Fujita N, et al. (2019). Relationship between frailty and lower urinary tract symptoms among community‐dwelling adults. LUTS Low Urin Tract Symptoms. :luts.12292.
Metadata
Title
The association between gut microbiome and erectile dysfunction: a community-based cross-sectional study in Japan
Authors
Teppei Okamoto
Shingo Hatakeyama
Atsushi Imai
Hayato Yamamoto
Tohru Yoneyama
Kazuyuki Mori
Takahiro Yoneyama
Yasuhiro Hashimoto
Shigeyuki Nakaji
Chikara Ohyama
Publication date
01-08-2020
Publisher
Springer Netherlands
Published in
International Urology and Nephrology / Issue 8/2020
Print ISSN: 0301-1623
Electronic ISSN: 1573-2584
DOI
https://doi.org/10.1007/s11255-020-02443-9

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