The microbiota of sexual intercourse and its effect on prostatitis

La microbiota vaginal como un factor protector contra la prostatitis

It is estimated that microorganisms colonize 90% of the body surface. In some tracts, such as the genitourinary tract, the microbiota varies throughout life, influenced by hormonal stimulation and sexual practices. This study evaluated the semen differences and presence of Lactobacillus crispatus, Lactobacillus iners, Gardnerella vaginalis and Atopobium vaginae in semen samples from patients with symptoms of chronic prostatitis and men asymptomatic for urogenital infections. Fifty-three semen samples were included: 22 samples from men with symptoms of chronic prostatitis and 31 asymptomatic men (control group). In addition to the presence of L. crispatus, L. iners, G. vaginalis and A. vaginae, semen parameters, total antioxidant capacity of seminal plasma, prostatic antigen and some proinflammatory cytokines were evaluated in each semen sample. Volunteers with symptoms of chronic prostatitis presented a lower percentage of sperm morphology (4.3% vs. control group 6.0%, p = 0.004); in the semen samples of volunteers in the group asymptomatic for urogenital infections, microorganisms associated with the vaginal microbiota were detected more frequently. The presence of bacteria in the vaginal microbiota can also benefit male reproductive health, which undergoes various modifications related to lifestyle habits that are susceptible to modification. Microorganisms associated with the vaginal microbiota, such as L. crispatus, L. iners, G. vaginalis and A. vaginae, may have a protective role against the development of male genitourinary diseases such as prostatitis.

Resumen

Se estima que el 90% de la superficie corporal está colonizada por microorganismos. En algunos tractos como el genitourinario, la microbiota varia a lo largo de la vida influenciada por factores como el estímulo hormonal y las prácticas sexuales. Los objetivos de este trabajo fueron comparar los parametros seminales y evaluar la presencia de Lactobacillus crispatus, Lactobacillus iners, Gardnerella vaginalis y Atopobium vaginae de muestras de semen de pacientes con síntomas de prostatitis crónica y de hombres asintomáticos para infecciones urogenitales. Se incluyeron 53 muestras de semen: 22 muestras de hombres con síntomas de prostatitis crónica (grupo prostatitis) y 31 de hombres asintomáticos (grupo control). En cada muestra de semen se evaluó además de la presencia de L. crispatus, L. iners, G. vaginalis y A. vaginae, los parámetros seminales convencionales y funcionales, además de la capacidad antioxidante total del plasma seminal. Los voluntarios con síntomas de prostatitis crónica presentaron menor porcentaje de morfología espermática (4.3% vs grupo control 6.0%, p = 0.004), en las muestras de semen de los voluntarios del grupo asintomático para infecciones urogenitales se detectaron con mayor frecuencia los microorganismos asociados a la microbiota vaginal. La presencia de bacterias de la microbiota vaginal puede ser también benéfico para la salud reproductiva masculina, esta sufre diversas modificaciones en relación con los hábitos de vida que son susceptibles de modificación. Los microorganismos asociados a la microbiota vaginal como L. crispatus, L. iners, G. vaginalis y A. vaginae pueden tener un papel protector frente al desarrollo de enfermedades genitourinarias masculinas como la prostatitis.

Microbiota; Sexual intercourse; Lactobacillus crispatus; Lactobacillus iners; Gard-nerella vaginalis; Atopobium vaginae; Prostatitis

Palabras Clave

Microbiota; Relaciones sexuales; Lactobacillus crispatus; Lactobacillus iners; Gardnerella vaginalis; Atopobium vaginae; Prostatitis

[1] Mändar R. Microbiota of male genital tract: impact on the health of man and his partner. Pharmacological Research. 2013; 69: 32–41.

[2] Aragón IM, Herrera-Imbroda B, Queipo-Ortuño MI, Castillo E, Del Moral JS, Gómez-Millán J, et al. The urinary tract microbiome in health and disease. European Urology Focus. 2018; 4: 128–138.

[3] Restrepo Arenas V, Velásquez Rivera V, Puerta Suárez J, Cardona Maya WD. Vaginal flow and semen: the microbiote of sexual relations. Colombian Urology Journal. 2021; 30: 140–144.

[4] Mändar R, Punab M, Borovkova N, Lapp E, Kiiker R, Korrovits P, et al. Complementary seminovaginal microbiome in couples. Research in Microbiology. 2015; 166: 440–447.

[5] Ding C, Yu Y, Zhou Q. Bacterial vaginosis: effects on reproduction and its therapeutics. Journal of Gynecology Obstetrics and Human Reproduction. 2021; 50: 102174.

[6] Puhr M, De Marzo A, Isaacs W, Lucia MS, Sfanos K, Yegnasubramanian S, et al. Inflammation, microbiota, and prostate cancer. European Urology Focus. 2016; 2: 374–382.

[7] Cano-Cháves A, Galarzo-Pardo S, Puerta-Suárez J, Giraldo M, Cadavid ÁP, Cardona-Maya WD. Effect of uropathogenic bacteria and soluble factors produced by their metabolism on sperm quality: Escherichia coli and Enterococcus faecalis. Clínica e Investigación en Ginecología y Obstetricia. 2017; 44: 106–112.

[8] Puerta Suárez J, Cardona Maya WD. Prevalence of Chlamydia trachomatis, Neisseria gonorrhoeae and Ureaplasma urealyticum in semen samples: effects on sperm quality. Urología Colombiana. 2016; 25: 219–224.

[9] Castrillón-Duque EX, Puera Suárez J, Cardona Maya WD. Yeast and fertility: effects of in vitro activity of Candida spp. on sperm quality. Journal of Reproduction & Infertility. 2018; 19: 49–55.

[10] Puerta Suárez J, Carlos Hernandez J, Cardona Maya WD. Molecular analysis of microorganisms in the semen and their impact on semen parameters. Archives of Italian Urology and Andrology. 2022; 94: 199–205.

[11] Rivera VV, Cardona Maya WD, Puerta-Suárez J. The relationship between sexually transmitted microorganisms and seminal quality in asymptomatic men. Asian Journal of Urology. 2022; 9: 473–479.

[12] Puerta Suárez J, Velázquez Rivera V, Morales M, Alvarez AM, Carvajal A, Cardona Maya WD. Chronic prostatitis: impact of lifestyle, infection, and inflammation on semen parameters. Open Access Macedonian Journal of Medical Sciences. 2022; 10: 543–553.

[13] Puerta Suárez J, Cardona Maya WD. Microbiota, prostatitis, and fertility: bacterial diversity as a possible health ally. Advances in Urology. 2021; 2021: 1–8.

[14] Borovkova N, Korrovits P, Ausmees K, Türk S, Jõers K, Punab M, et al. Influence of sexual intercourse on genital tract microbiota in infertile couples. Anaerobe. 2011; 17: 414–418.

[15] Farahani L, Tharakan T, Yap T, Ramsay JW, Jayasena CN, Minhas S. The semen microbiome and its impact on sperm function and male fertility: a systematic review and meta-analysis. Andrology. 2021; 9: 115–144.

[16] Campisciano G, Iebba V, Zito G, Luppi S, Martinelli M, Fischer L, et al. Lactobacillus iners and gasseri, Prevotella bivia and HPV belong to the microbiological signature negatively affecting human reproduction. Microorganisms. 2020; 9: 39.

[17] Litwin MS, McNaughton-Collins M, Fowler FJ Jr, Nickel JC, Calhoun EA, Pontari MA, et al. The national institutes of health chronic prostatitis symptom index: development and validation of a new outcome measure. Chronic Prostatitis Collaborative Research Network. The Journal of urology. 1999; 162: 369–375.

[18] World Health Organization. WHO laboratory manual for the examination and processing of human semen. 6th edn. World Health Organization: Geneva. 2021.

[19] Cardona-Maya W, Berdugo J, Cadavid A. Comparing the sperm concentration determined by the Makler and the Neubauer chambers. Actas Urológicas Españolas. 2008; 32: 443–445. (In Spanish)

[20] Mayorga-Torres BJ, Cardona-Maya W, Cadavid Á, Camargo M. Evaluation of sperm functional parameters in normozoospermic infertile individuals. Actas Urológicas Españolas. 2013; 37: 221–227.

[21] Martínez-Pastor F, Mata-Campuzano M, Álvarez-Rodríguez M, Álvarez M, Anel L, De Paz P. Probes and techniques for sperm evaluation by flow cytometry. Reproduction in Domestic Animals. 2010; 45: 67–78.

[22] Aitken RJ, Wingate JK, De Iuliis GN, McLaughlin EA. Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Molecular Human Reproduction. 2007; 13: 203–211.

[23] Gil-Villa AM, Cardona-Maya W, Agarwal A, Sharma R, Cadavid Á. Assessment of sperm factors possibly involved in early recurrent pregnancy loss. Fertility and Sterility. 2010; 94: 1465–1472.

[24] Serafini M, Maiani G, Ferro-Luzzi A. Alcohol-free red wine enhances plasma antioxidant capacity in humans. The Journal of Nutrition. 1998; 128: 1003–1007.

[25] Kusters JG, Reuland EA, Bouter S, Koenig P, Dorigo-Zetsma JW. A multiplex real-time PCR assay for routine diagnosis of bacterial vaginosis. European Journal of Clinical Microbiology & Infectious Diseases. 2015; 34: 1779–1785.

[26] Goldstein EJC, Tyrrell KL, Citron DM. Lactobacillus species: taxonomic complexity and controversial susceptibilities. Clinical Infectious Diseases. 2015; 60: S98–S107.

[27] Hou D, Zhou X, Zhong X, Settles ML, Herring J, Wang L, et al. Microbiota of the seminal fluid from healthy and infertile men. Fertility and Sterility. 2013; 100: 1261–1269.e3.

[28] Mändar R, Punab M, Korrovits P, Türk S, Ausmees K, Lapp E, et al. Seminal microbiome in men with and without prostatitis. International Journal of Urology. 2017; 24: 211–216.

[29] Berg E, Houska P, Nesheim N, Schuppe H-C, Pilatz A, Fijak M, et al. Chronic prostatitis/chronic pelvic pain syndrome leads to impaired semen parameters, increased sperm DNA fragmentation and unfavorable changes of sperm protamine mRNA ratio. International Journal of Molecular Sciences. 2021; 22: 7854.

[30] Rees J, Abrahams M, Doble A, Cooper A; Prostatitis Expert Reference Group (PERG). Diagnosis and treatment of chronic bacterial prostatitis and chronic prostatitis/chronic pelvic pain syndrome: a consensus guideline. BJU International. 2015; 116: 509–525.

[31] Smith KB, Pukall CF, Tripp DA, Nickel JC. Sexual and relationship functioning in men with chronic prostatitis/chronic pelvic pain syndrome and their partners. Archives of Sexual Behavior. 2007; 36: 301–311.

[32] Larsen B, Monif GRG. Understanding the bacterial flora of the female genital tract. Clinical Infectious Diseases. 2001; 32: e69–e77.

[33] Baud D, Pattaroni C, Vulliemoz N, Castella V, Marsland BJ, Stojanov M. Sperm microbiota and its impact on semen parameters. Frontiers in Microbiology. 2019; 10: 234.