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01-12-2019 | Erectile Dysfunction | Female Sexual Dysfunction and Disorders (A Pastuszak and N Thirumavalavan, Section Editors)

The Gut Microbiome and Men’s Sexual Health

Authors: Mohamad M. Osman, Farouk M. El-Khatib, Natalie H. Roberts, Linda M. Huynh, Faysal A. Yafi

Published in: Current Sexual Health Reports | Issue 4/2019

Abstract

Purpose of Review

Currently, there is no literature assessing for a potential relationship between the gut microbiome and men’s sexual health. The purpose of this paper is to review the literature on the gut microbiome and its effect on human health, in healthy and diseased states. We also aim to review the literature on men’s sexual health and then extrapolate a potential relationship between the gut microbiome and sexual health diseases.

Recent Findings

Many studies have suggested a correlation between the gut microbiome and components of the metabolic syndrome, cardiovascular disease, and inflammation. Men’s sexual health diseases, such as erectile dysfunction and hypogonadism, have also been associated with components of the metabolic syndrome and cardiovascular disease.

Summary

Due to the bidirectional relationships seen between the gut microbiome and men’s sexual health, with the metabolic syndrome, cardiovascular disease, and inflammation, it is highly likely that an association between men’s sexual health and the gut microbiome exists also. Future studies should begin looking at this potential relationship with the aim of developing gut microbiome targeted diagnostic and therapeutic tools for the treatment of men’s sexual health diseases.

Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474:1823–36. https://doi.org/10.1042/BCJ20160510.CrossRefPubMed

Barko PC, McMichael MA, Swanson KS, Williams DA. The gastrointestinal microbiome: a review. J Vet Intern Med. 2018;32:9–25. https://doi.org/10.1111/jvim.14875.CrossRefPubMed

Sidhu M, Van der Poorten D. The gut microbiome. Aust Fam Physician. 2017;46:206–11.PubMed

• Arnold JW, Roach J, Azcarate-Peril MA. Emerging technologies for gut microbiome research. Trends Microbiol. 2016;24:887–901. https://doi.org/10.1016/j.tim.2016.06.008This paper highlights the recent advancements in quality and ease of gut microbiome analysis. CrossRefPubMedPubMedCentral

Ahmadmehrabi S, Tang WHW. Gut microbiome and its role in cardiovascular diseases. Curr Opin Cardiol. 2017;32:761. https://doi.org/10.1097/HCO.0000000000000445.CrossRefPubMedPubMedCentral

Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67:1716–25. https://doi.org/10.1136/gutjnl-2018-316723.CrossRefPubMed

Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90:859–904. https://doi.org/10.1152/physrev.00045.2009.CrossRefPubMed

Shabsigh R. Hypogonadism and erectile dysfunction: the role for testosterone therapy. Int J Impot Res. 2003;15:9–13. https://doi.org/10.1038/sj.ijir.3901030.CrossRef

Buvat J, Bou JG. Significance of hypogonadism in erectile dysfunction. World J Urol. 2006;24:657–67. https://doi.org/10.1007/s00345-006-.CrossRefPubMed

10.

Ferrini MG, Gonzalez-Cadavid NF, Rajfer J. Aging related erectile dysfunction—potential mechanism to halt or delay its onset. Transl Androl Urol. 2017;6:20–7. https://doi.org/10.21037/tau.2016.11.18.CrossRefPubMedPubMedCentral

11.

Althof SE. Quality of life and erectile dysfunction. Urology. 2002;59:803–10. https://doi.org/10.1016/S0090-4295(02)01606-0.CrossRefPubMed

12.

Cunningham GR. Testosterone and metabolic syndrome. Asian J Androl. 2015;17:192–6. https://doi.org/10.4103/1008-682X.148068.CrossRefPubMedPubMedCentral

13.

Traish AM, Haider A, Doros G, Saad F. Long-term testosterone therapy in hypogonadal men ameliorates elements of the metabolic syndrome: an observational, long-term registry study. Int J Clin Pract. 2014;68:314–29. https://doi.org/10.1111/ijcp.12319.CrossRefPubMed

14.

• Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14. https://doi.org/10.1371/journal.pbio.1002533The importance of this paper is that it provides an updated estimate of the number of microbes found in the gut. The sheer number alone is preliminary evidence that these microbes have an effect on multiple systems and functions of their host organism. CrossRefPubMedPubMedCentral

15.

Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;13:220–30. https://doi.org/10.1038/nature11550.CrossRef

16.

Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;10:1635–8. https://doi.org/10.1126/science.1110591.CrossRef

17.

Bull MJ, Plummer NT. Part 1: The Human human Gut gut Microbiome microbiome in Health health and Diseasedisease. Integr Med (Encinitas). 2014;13:17–22.

18.

Björkstén B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol. 2001;108:516–20. https://doi.org/10.1067/mai.2001.118130.CrossRefPubMed

19.

LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24:160–8. https://doi.org/10.1016/j.copbio.2012.08.005.CrossRefPubMed

20.

Gallo A, Passaro G, Gasbarrini A, Landolfi R, Montalto M. Modulation of microbiota as treatment for intestinal inflammatory disorders: an uptodate. World J Gastroenterol. 2016;28:7186–202. https://doi.org/10.3748/wjg.v22.i32.7186.CrossRef

21.

Scheperjans F. Gut microbiota, 1013 new pieces in the Parkinson's Parkinson’s disease puzzle. Curr Opin Neurol. 2016;29:773–80. https://doi.org/10.1097/WCO.0000000000000389.CrossRefPubMed

22.

Hoeppli RE, Wu D, Cook L, Levings MK. The environment of regulatory T cell biology: cytokines, metabolites, and the microbiome. Front Immunol. 2015;6:61. https://doi.org/10.3389/fimmu.2015.00061.CrossRefPubMedPubMedCentral

23.

Umu ÖCO, Rudi K, Diep DB. Modulation of the gut microbiota by prebiotic fibres and bacteriocins. Microb Ecol Health Dis. 2017;28. https://doi.org/10.1080/16512235.2017.1348886.CrossRefPubMedPubMedCentral

24.

Smith M. PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73. https://doi.org/10.1126/science.1241165.CrossRefPubMed

25.

Dodd D, Spitzer MH, Van Treuren W, Merrill BD, Hryckowian AJ, Higginbottom SK, et al. A gut bacterial pathway metabolizes aromatic amino acids into nine circulating metabolites. Nature. 2017;551:648–52. https://doi.org/10.1038/nature24661.CrossRefPubMedPubMedCentral

26.

Bollrath J, Powrie F. Immunology. Feed your Tregs more fiber. Science. 2013;2:463–4. https://doi.org/10.1126/science.1242674.CrossRef

27.

Zhang LJ, Gallo RL. Antimicrobial peptides. Curr Biol. 2016;26:14–9. https://doi.org/10.1016/j.cub.2015.11.017.CrossRef

28.

Shamloul R, Ghanem H. Erectile dysfunction. Lancet. 2013;12:153–65. https://doi.org/10.1016/S0140-6736(12)60520-0.CrossRef

29.

• Mulhall JP, Trost LW, Brannigan RE, Kurtz EG, Redmon JB, Chiles KA, et al. Evaluation and management of testosterone deficiency: AUA guideline. J Urol. 2018;200:423–32. https://doi.org/10.1016/j.juro.2018.03.115Low testosterone is a highly likely to be associated with gut microbiome dysbiosis. These updates guidelines are important in defining low testosterone. CrossRefPubMed

30.

El-Sakka AI. Prevalence of Peyronie’'s disease among patients with erectile dysfunction. Eur Urol. 2006;49:564–9. https://doi.org/10.1016/j.eururo.2005.10.026.CrossRefPubMed

31.

Dibenedetti DB, Nguyen D, Zografos L, Ziemiecki R, Zhou X. A population-based study of Peyronie’'s disease: prevalence and treatment patterns in the United States. Adv Urol. 2011;2011. https://doi.org/10.1155/2011/282503.CrossRef

32.

Humphries KH, Izadnegahdar M, Sedlak T, Saw J, Johnston N, Schenck-Gustafsson K, et al. Sex differences in cardiovascular disease - impact on care and outcomes. Front Neuroendocrinol. 2017;46:46–70. https://doi.org/10.1016/j.yfrne.2017.04.001.CrossRefPubMedPubMedCentral

33.

Thompson IM, Tangen CM, Goodman PJ, Probstfield JL, Moinpour CM, Coltman CA. Erectile dysfunction and subsequent cardiovascular disease. JAMA. 2005;294:2996–3002. https://doi.org/10.1001/jama.294.23.2996.CrossRefPubMed

34.

Lane-Cordova AD, Kershaw K, Liu K, Herrington D, Lloyd-Jones DM. Association between cardiovascular health and endothelial function with future erectile dysfunction: the multi-ethnic study of atherosclerosis. Am J Hypertens. 2017;30:815–21. https://doi.org/10.1093/ajh/hpx060.CrossRefPubMedPubMedCentral

35.

Banks E, Joshy G, Abhayaratna WP, Kritharides L, Macdonald PS, Korda RJ, et al. Erectile dysfunction severity as a risk marker for cardiovascular disease hospitalisation and all-cause mortality: a prospective cohort study. PLoS Med. 2013;10. https://doi.org/10.1371/journal.pmed.1001372.CrossRefPubMedPubMedCentral

36.

Ponholzer A, Gutjahr G, Temml C, Madersbacher S. Is erectile dysfunction a predictor of cardiovascular events or stroke? A prospective study using a validated questionnaire. Int J Impot Res. 2010;22:25–9. https://doi.org/10.1038/ijir.2009.40.CrossRefPubMed

37.

Hotaling JM, Walsh TJ, Macleod LC, Heckbert S, Pocobelli G, Wessells H, et al. Erectile dysfunction is not independently associated with cardiovascular death: data from the vitamins and lifestyle (VITAL) study. J Sex Med. 2012;9:2104–10. https://doi.org/10.1111/j.1743-6109.2012.02826.CrossRefPubMed

38.

Mäkinen JI, Perheentupa A, Irjala K, Pöllänen P, Mäkinen J, Huhtaniemi I, et al. Endogenous testosterone and brachial artery endothelial function in middle-aged men with symptoms of late-onset hypogonadism. Aging Male. 2011;14:237–42. https://doi.org/10.3109/13685538.2011.593655.CrossRefPubMed

39.

Empen K, Lorbeer R, Dörr M, Haring R, Nauck M, Gläser S, et al. Association of testosterone levels with endothelial function in men: results from a population-based study. Arterioscler Thromb Vasc Biol. 2012;32:481–6. https://doi.org/10.1161/ATVBAHA.111.232876.CrossRefPubMed

40.

Akishita M, Hashimoto M, Ohike Y, Ogawa S, Iijima K, Eto M, et al. Low testosterone level is an independent determinant of endothelial dysfunction in men. Hypertens Res. 2007;30:1029–34. https://doi.org/10.1291/hypres.30.1029.CrossRefPubMed

41.

Corrigan FE, Al Mheid I, Eapen DJ, Hayek SS, Sher S, Martin GS, et al. Low testosterone in men predicts impaired arterial elasticity and microvascular function. Int J Cardiol. 2015;194:94–9. https://doi.org/10.1016/j.ijcard.2015.05.065.CrossRefPubMedPubMedCentral

42.

Khazai B, Golden SH, Colangelo LA, Swerdloff R, Wang C, Honoris L, et al. Association of endogenous testosterone with subclinical atherosclerosis in men: the multi-ethnic study of atherosclerosis. Clin Endocrinol (Oxf). 2016;84:700–7. https://doi.org/10.1111/cen.12997.CrossRef

43.

Lai J, Ge Y, Shao Y, Xuan T, Xia S, Li M. Low serum testosterone level was associated with extensive coronary artery calcification in elderly male patients with stable coronary artery disease. Coron Artery Dis. 2015;26:437–41. https://doi.org/10.1097/MCA.0000000000000260.CrossRefPubMed

44.

Michos ED, Vaidya D, Gapstur SM, Schreiner PJ, Golden SH, Wong ND, et al. Sex hormones, sex hormone binding globulin, and abdominal aortic calcification in women and men in the multi-ethnic study of atherosclerosis (MESA). Atherosclerosis. 2008;200:432–8. https://doi.org/10.1016/j.atherosclerosis.2007.12.032.CrossRefPubMedPubMedCentral

45.

Yaron M, Greenman Y, Rosenfeld JB, Izkhakov E, Limor R, Osher E, et al. Effect of testosterone replacement therapy on arterial stiffness in older hypogonadal men. Eur J Endocrinol. 2009;160:839–46. https://doi.org/10.1530/EJE-09-0052.CrossRefPubMed

46.

Vlachopoulos C, Ioakeimidis N, Miner M, Aggelis A, Pietri P, Terentes-Printzios D, et al. Testosterone deficiency: a determinant of aortic stiffness in men. Atherosclerosis. 2014;233:278–83. https://doi.org/10.1016/j.atherosclerosis.2013.12.010.CrossRefPubMed

47.

Dockery F, Bulpitt CJ, Agarwal S, Donaldson M, Rajkumar C. Testosterone suppression in men with prostate cancer leads to an increase in arterial stiffness and hyperinsulinaemia. Clin Sci (Lond). 2003;104:195–201. https://doi.org/10.1042/CS20020209.CrossRef

48.

Brand JS, den Ouden ME, Schuurmans MJ, Bots ML, van der Schouw YT. Endogenous sex hormones and subclinical atherosclerosis in middle-aged and older men. Int J Cardiol. 2013;168:574–6. https://doi.org/10.1016/j.ijcard.2013.01.242.CrossRefPubMed

49.

Vaidya D, Golden SH, Haq N, Heckbert SR, Liu K, Ouyang P. Association of sex hormones with carotid artery distensibility in men and postmenopausal women: multi-ethnic study of atherosclerosis. Hypertension. 2015;65:1020–5. https://doi.org/10.1161/HYPERTENSIONAHA.114.04826.CrossRefPubMed

50.

Dockery F, Bulpitt CJ, Donaldson M, Fernandez S, Rajkumar C. The relationship between androgens and arterial stiffness in older men. J Am Geriatr Soc. 2003;51:1627–32. https://doi.org/10.1046/j.1532-5415.2003.51515.x.CrossRefPubMed

51.

Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–5. https://doi.org/10.1161/CIRCULATIONAHA.109.192644.CrossRefPubMed

52.

Bjekic MD, Vlajinac HD, Sipetic SB, Marinkovic JM. Risk factors for Peyronie's Peyronie’s disease: a case-control study. BJU Int. 2006;97:570–4. https://doi.org/10.1111/j.1464-410X.2006.05969.x.CrossRefPubMed

53.

Kadioglu A, Tefekli A, Erol B, Oktar T, Tunc M, Tellaloglu S. A retrospective review of 307 men with Peyronie's Peyronie’s disease. J Urol. 2002;168:1075–9. https://doi.org/10.1097/01.ju.0000024040.55662.36.CrossRefPubMed

54.

La Pera G, Pescatori ES, Calabrese M, Boffini A, Colombo F, Andriani E, et al. Peyronie's Peyronie’s disease: prevalence and association with cigarette smoking. A multicenter population-based study in men aged 50-69 years. Eur Urol. 2001;40:525–30.CrossRefPubMed

55.

Carrieri MP, Serraino D, Palmiotto F, Nucci G, Sasso F. A case-control study on risk factors for Peyronie's Peyronie’s disease. J Clin Epidemiol. 1998;51:511–5. https://doi.org/10.1016/S0895-4356(98)00015-8.CrossRefPubMed

56.

Beltrán-Sánchez H, Harhay MO, Harhay MM, McElligott S. Prevalence and trends of metabolic syndrome in the adult U.S. population, 1999-2010. J Am Coll Cardiol. 2013;62:697–703. https://doi.org/10.1016/j.jacc.2013.05.064.CrossRefPubMedPubMedCentral

57.

Antonio L, Wu FC, O’'Neill TW, Pye SR, Carter EL, Finn JD, et al. Associations between sex steroids and the development of metabolic syndrome: a longitudinal study in European men. J Clin Endocrinol Metab. 2015;100:1396–404. https://doi.org/10.1210/jc.2014-4184.CrossRefPubMed

58.

Laaksonen DE, Niskanen L, Punnonen K, Nyyssönen K, Tuomainen TP, Valkonen VP, et al. Testosterone and sex hormone-binding globulin predict the metabolic syndrome and diabetes in middle-aged men. Diabetes Care. 2004;27:1036–41. https://doi.org/10.2337/diacare.27.5.1036.CrossRefPubMed

59.

Laaksonen DE, Niskanen L, Punnonen K, Nyyssönen K, Tuomainen TP, Valkonen VP, et al. The metabolic syndrome and smoking in relation to hypogonadism in middle-aged men: a prospective cohort study. J Clin Endocrinol Metab. 2005;90:712–9. https://doi.org/10.1210/jc.2004-0970.CrossRefPubMed

60.

Chaudhary RK, Shamsi BH, Tan T, Chen HM, Xing JP. Study of the relationship between male erectile dysfunction and type 2 diabetes mellitus/metabolic syndrome and its components. J Int Med Res. 2016;44:735–41. https://doi.org/10.1177/0300060515623122.CrossRefPubMedPubMedCentral

61.

Weinberg AE, Eisenberg M, Patel CJ, Chertow GM, Leppert JT. Diabetes severity, metabolic syndrome, and the risk of erectile dysfunction. J Sex Med. 2013;10:3102–9. https://doi.org/10.1111/jsm.12318.CrossRefPubMedPubMedCentral

62.

Park JH, Cho IC, Kim YS, Kim SK, Min SK, Kye SS. Body mass index, waist-to-hip ratio, and metabolic syndrome as predictors of middle-aged men's men’s health. Korean J Urol. 2015;56:386–92. https://doi.org/10.4111/kju.2015.56.5.386.CrossRefPubMedPubMedCentral

63.

Arrabal-Polo MÁ, Arias-Santiago S, López-Carmona Pintado F, Merino-Salas S, Lahoz-García C, Zuluaga-Gómez A, et al. Metabolic syndrome, hormone levels, and inflammation in patients with erectile dysfunction. ScientificWorldJournal. 2012. https://doi.org/10.1100/2012/272769.CrossRef

64.

El-Sakka AI, Tayeb KA. Peyronie's Peyronie’s disease in diabetic patients being screened for erectile dysfunction. J Urol. 2005;17:1026–30. https://doi.org/10.1097/01.ju.0000170231.51306.32.CrossRef

65.

Arafa M, Eid H, El-Badry A, Ezz-Eldine K, Shamloul R. The prevalence of Peyronie's Peyronie’s disease in diabetic patients with erectile dysfunction. Int J Impot Res. 2007;19:213–7. https://doi.org/10.1038/sj.ijir.3901518.CrossRefPubMed

66.

Kendirci M, Trost L, Sikka SC, Hellstrom WJ. Diabetes mellitus is associated with severe Peyronie's Peyronie’s disease. BJU Int. 2007;99:383–6. https://doi.org/10.1111/j.1464-410X.2007.06611.x.CrossRefPubMed

67.

Tefekli A, Kandirali E, Erol B, Tunc M, Kadioglu A. Peyronie's Peyronie’s disease: a silent consequence of diabetes mellitus. Asian J Androl. 2006;8:75–9. https://doi.org/10.1111/j.1745-7262.2006.00099.x.CrossRefPubMed

68.

McKelvey KJ, Ariyakumar G, McCracken SA. Inflammatory and immune system markers. Methods Mol Biol. 1710;2018:85–101. https://doi.org/10.1007/978-1-4939-7498-6_7.CrossRef

69.

Bocchio M, Desideri G, Scarpelli P, Necozione S, Properzi G, Spartera C, et al. Endothelial cell activation in men with erectile dysfunction without cardiovascular risk factors and overt vascular damage. J Urol. 2004;171:1601–4. https://doi.org/10.1097/01.ju.0000116325.06572.85.CrossRefPubMed

70.

Sullivan ME, Miller MA, Bell CR, Jagroop IA, Thompson CS, Khan MA, et al. Fibrinogen, lipoprotein (a) and lipids in patients with erectile dysfunction. A preliminary study. Int Angiol. 2001;20:195–9.PubMed

71.

Billups KL, Kaiser DR, Kelly AS, Wetterling RA, Tsai MY, Hanson N, et al. Relation of C-reactive protein and other cardiovascular risk factors to penile vascular disease in men with erectile dysfunction. Int J Impot Res. 2003;15:231–6. https://doi.org/10.1038/sj.ijir.3901012.CrossRefPubMed

72.

Chiurlia E, D'Amico D’Amico R, Ratti C, Granata AR, Romagnoli R, Modena MG. Subclinical coronary artery atherosclerosis in patients with erectile dysfunction. J Am Coll Cardiol. 2005;46(8):1503–6. https://doi.org/10.1016/j.jacc.2005.06.068.CrossRefPubMed

73.

Long T, Liu G, Wang Y, Chen Y, Zhang Y, Qin D. TNF-α, erectile dysfunction, and NADPH oxidase-mediated ROS generation in corpus cavernosum in high-fat diet/streptozotocin-induced diabetic rats. J Sex Med. 2012;9:1801–14. https://doi.org/10.1111/j.1743-6109.2012.02739.x.CrossRefPubMed

74.

Matos G, Hirotsu C, Alvarenga TA, Cintra F, Bittencourt L, Tufik S, et al. The association between TNF-α and erectile dysfunction complaints. Andrology. 2013;1:872–8. https://doi.org/10.1111/j.2047-2927.2013.00136.x.CrossRefPubMed

75.

Tremellen K, McPhee N, Pearce K. Metabolic endotoxaemia related inflammation is associated with hypogonadism in overweight men. Basic Clin Androl. 2017;27:5. https://doi.org/10.1186/s12610-017-0049-8.CrossRefPubMedPubMedCentral

76.

Wickramatilake CM, Mohideen MR, Withanawasam BP, Pathirana C. Testosterone and high-sensitive C-reactive protein in coronary artery disease patients awaiting coronary artery bypass graft. Andrologia. 2015;47:493–8. https://doi.org/10.1111/and.12290.CrossRefPubMed

77.

Tsilidis KK, Rohrmann S, McGlynn KA, Nyante SJ, Lopez DS, Bradwin G, et al. Association between endogenous sex steroid hormones and inflammatory biomarkers in US men. Andrology. 2013;1:919–28. https://doi.org/10.1111/j.2047-2927.2013.00129.x.CrossRefPubMed

78.

Bobjer J, Katrinaki M, Tsatsanis C, Lundberg Giwercman Y, Giwercman A. Negative association between testosterone concentration and inflammatory markers in young men: a nested cross-sectional study. PLoS One. 2013;8. https://doi.org/10.1371/journal.pone.0061466.CrossRefPubMedPubMedCentral

79.

Kalinchenko SY, Tishova YA, Mskhalaya GJ, Gooren LJ, Giltay EJ, Saad F. Effects of testosterone supplementation on markers of the metabolic syndrome and inflammation in hypogonadal men with the metabolic syndrome: the double-blinded placebo-controlled Moscow study. Clin Endocrinol (Oxf). 2010;73:602–12. https://doi.org/10.1111/j.1365-2265.2010.03845.x.CrossRef

80.

Malkin CJ, Pugh PJ, Jones RD, Kapoor D, Channer KS, Jones TH. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J Clin Endocrinol Metab. 2004;89:3313–8. https://doi.org/10.1210/jc.2003-031069.CrossRefPubMed

81.

Somers KD, Dawson DM. Fibrin deposition in Peyronie's Peyronie’s disease plaque. J Urol. 1997;157:311–5.CrossRefPubMed

82.

El-Sakka AI, Hassan MU, Nunes L, Bhatnagar RS, Yen TS, Lue TF. Histological and ultrastructural alterations in an animal model of Peyronie's Peyronie’s disease. Br J Urol 1998:Mar81:445-52.

83.

Davis CJ Jr. The microscopic pathology of Peyronie's Peyronie’s disease. J Urol. 1997;157:282–4.CrossRefPubMed

84.

Vernet D, Nolazco G, Cantini L, Magee TR, Qian A, Rajfer J, et al. Evidence that osteogenic progenitor cells in the human tunica albuginea may originate from stem cells: implications for peyronie disease. Biol Reprod. 2005;73:1199–210. https://doi.org/10.1095/biolreprod.105.041038.CrossRefPubMed

85.

Halfvarson J, Brislawn CJ, Lamendella R, Vázquez-Baeza Y, Walters WA, Bramer LM, et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol. 2017;2:17004. https://doi.org/10.1038/nmicrobiol.2017.4.CrossRefPubMedPubMedCentral

86.

Yan Q, Gu Y, Li X, Yang W, Jia L, Chen C, et al. Alterations of the gut microbiome in hypertension. Front Cell Infect Microbiol. 2017;7:381. https://doi.org/10.3389/fcimb.2017.00381.CrossRefPubMedPubMedCentral

87.

Richards EM, Pepine CJ, Raizada MK, Kim S. The gut, its microbiome, and hypertension. Curr Hypertens Rep. 2017;19:36. https://doi.org/10.1007/s11906-017-0734-1.CrossRefPubMedPubMedCentral

88.

Jie Z, Xia H, Zhong SL, Feng Q, Li S, Liang S, et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat Commun. 2017;8:845. https://doi.org/10.1038/s41467-017-00900-1.CrossRefPubMedPubMedCentral

89.

Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57–63. https://doi.org/10.1038/nature09922.CrossRefPubMedPubMedCentral

90.

Li XS, Obeid S, Klingenberg R, Gencer B, Mach F, Räber L, et al. Gut microbiota-dependent trimethylamine N-oxide in acute coronary syndromes: a prognostic marker for incident cardiovascular events beyond traditional risk factors. Eur Heart J. 2017;38:814–24. https://doi.org/10.1093/eurheartj/ehw582.CrossRefPubMedPubMedCentral

91.

Janeiro MH, Ramírez MJ, Milagro FI, Martínez JA, Solas M. Implication of trimethylamine N-Oxide oxide (TMAO) in disease: potential biomarker or new therapeutic target. Nutrients. 2018;10:1398. https://doi.org/10.3390/nu10101398.CrossRefPubMedCentral

92.

Seldin MM, Meng Y, Qi H, Zhu W, Wang Z, Hazen SL, et al. Trimethylamine N-Oxide oxide promotes vascular inflammation through signaling of mitogen-activated protein kinase and nuclear factor-κB. J Am Heart Assoc. 2016;5. https://doi.org/10.1161/JAHA.115.002767.

93.

Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575–84. https://doi.org/10.1056/NEJMoa1109400.CrossRefPubMedPubMedCentral

94.

Wang Z, Roberts AB, Buffa JA, Levison BS, Zhu W, Org E, et al. Non-lethal inhibition of gut microbial trimethylamine production for the treatment of atherosclerosis. Cell. 2015;163:1585–95. https://doi.org/10.1016/j.cell.2015.11.055.CrossRefPubMedPubMedCentral

95.

Gregory JC, Buffa JA, Org E, Wang Z, Levison BS, Zhu W, et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J Biol Chem. 2015;290:5647–60. https://doi.org/10.1074/jbc.M114.618249.CrossRefPubMed

96.

Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341. https://doi.org/10.1126/science.1241214.CrossRefPubMed

97.

Liou AP, Paziuk M, Luevano JM Jr, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med. 2013;5:178. https://doi.org/10.1126/scitranslmed.3005687.CrossRef

98.

Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3. https://doi.org/10.1038/4441022a.CrossRefPubMed

99.

Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331–40. https://doi.org/10.1161/HYPERTENSIONAHA.115.05315.CrossRefPubMed

100.

Nagpal R, Newman TM, Wang S, Jain S, Lovato JF, Yadav H. Obesity-linked gut microbiome dysbiosis associated with derangements in gut permeability and intestinal cellular homeostasis independent of diet. J Diabetes Res. 2018;2018. https://doi.org/10.1155/2018/3462092.CrossRef

101.

Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–6. https://doi.org/10.1053/j.gastro.2012.06.031.CrossRefPubMed

102.

Laakso M, Kuusisto J, Stančáková A, Kuulasmaa T, Pajukanta P, Lusis AJ, et al. The metabolic syndrome in men study: a resource for studies of metabolic and cardiovascular diseases. J Lipid Res. 2017;58:481–93. https://doi.org/10.1194/jlr.O072629.CrossRefPubMedPubMedCentral

103.

Warshakoon HJ, Burns MR, David SA. Structure-activity relationships of antimicrobial and lipoteichoic acid-sequestering properties in polyamine sulfonamides. Antimicrob Agents Chemother. 2009;53:57–62. https://doi.org/10.1128/AAC.00812-08.CrossRefPubMed

104.

Huang ZY, Stabler T, Pei FX, Kraus VB. Both systemic and local lipopolysaccharide (LPS) burden are associated with knee OA severity and inflammation. Osteoarthritis Cartilage. 2016;24:1769–75. https://doi.org/10.1016/j.joca.2016.05.008.CrossRefPubMedPubMedCentral

105.

Nicolucci AC, Hume MP, Martínez I, Mayengbam S, Walter J, Reimer RA. Prebiotics reduce body fat and alter intestinal microbiota in children who are overweight or with obesity. Gastroenterology. 2017;153:711–22. https://doi.org/10.1053/j.gastro.2017.05.055.CrossRefPubMed

106.

Morales P, Fujio S, Navarrete P, Ugalde JA, Magne F, Carrasco-Pozo C, et al. Impact of dietary lipids on colonic function and microbiota: an experimental approach involving orlistat-induced fat malabsorption in human volunteers. Clin Transl Gastroenterol. 2016;7. https://doi.org/10.1038/ctg.2016.20.CrossRefPubMedPubMedCentral

107.

Benjamin JL, Hedin CR, Koutsoumpas A, Ng SC, McCarthy NE, Hart AL, et al. Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn's Crohn’s disease. Gut. 2011;60:923–9. https://doi.org/10.1136/gut.2010.232025.CrossRefPubMed

108.

Lovat LB. Age related changes in gut physiology and nutritional status. Gut. 1996;38:306–9. https://doi.org/10.1136/gut.38.3.306.CrossRefPubMedPubMedCentral

109.

van Tongeren SP, Slaets JP, Harmsen HJ, Welling GW. Fecal microbiota composition and frailty. Appl Environ Microbiol. 2005;71:6438–42. https://doi.org/10.1128/AEM.71.10.6438-6442.2005.CrossRefPubMedPubMedCentral

Title: The Gut Microbiome and Men’s Sexual Health
Authors: Mohamad M. Osman
Farouk M. El-Khatib
Natalie H. Roberts
Linda M. Huynh
Faysal A. Yafi
Publication date: 01-12-2019
Publisher: Springer US
Keywords: Erectile Dysfunction
Hypogonadism
Testosterone
Published in: Current Sexual Health Reports / Issue 4/2019
Print ISSN: 1548-3584
Electronic ISSN: 1548-3592
DOI: https://doi.org/10.1007/s11930-019-00230-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The Gut Microbiome and Men’s Sexual Health

Abstract

Purpose of Review

Recent Findings

Summary

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose of Review

Recent Findings

Summary

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