Molecular analysis of microorganisms in the semen and their impact on semen parameters


Submitted: February 17, 2022
Accepted: April 7, 2022
Published: June 30, 2022
Abstract Views: 1127
pdf: 544
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Objective: Chronic genitourinary infections can alter male fertility and even promote carcinogenic processes. This study aimed to evaluate the effect of the presence in the semen of microorganisms on semen quality. Materials and methods: Clinical symptoms and conventional and functional seminal parameters of eleven fertile donors and ten volunteers with prostatitis-like symptoms were evaluated. Nitric oxide, antioxidant capacity, and pro-inflammatory cytokines in semen and seminal plasma samples were also quantified. Finally, the expression of the ROR-γT, FoxP3, and T-bet genes in semen and the presence of DNA of microorganisms associated with prostatitis in urine and semen were evaluated. Results: When compared with fertile donors, volunteers with chronic prostatitis-like symptoms reported erectile dysfunction (0% vs. 10%, p = 0.2825) and premature ejaculation (0% vs. 40%; p = 0.0190). No statistically significant differences were observed in seminal parameters, cytokine measurement, antioxidant capacity, nitric oxide concentration and ROR-γT, FoxP3, T-bet. Microorganisms responsible for sexually transmitted infections and some bacteria associated with the microbiota and infections in the prostate gland were detected. In the semen from the subjects with prostatitis-like symptoms T. vaginalis DNA was detected; in addition, N. gonorrhoeae DNA was also detected in semen and urine samples. S. pyogenes was detected in the urine samples from the control group. Conclusions: Prostatitis-like symptoms are a common finding in young men that affect sexual and reproductive health, but not always the seminal parameters or fertility. The presence of prostatitis- like symptoms does not affect seminal quality. However, it appears to be associated with an increased likelihood of erectile dysfunction and premature ejaculation. Thus, affecting the quality of life and sexual and reproductive health.


Miyake M, Ohnishi K, Hori S, et al. Mycoplasma genitalium infection and chronic inflammation in human prostate cancer: detection using prostatectomy and needle biopsy specimens. Cells. 2019; 8:212. DOI: https://doi.org/10.3390/cells8030212

Xu C, Sun GF, Zhu YF, Wang YF. The correlation of Ureaplasma urealyticum infection with infertility. Andrologia. 1997; 29:219. DOI: https://doi.org/10.1111/j.1439-0272.1997.tb00319.x

Verze P, Cai T, Lorenzetti S. The role of the prostate in male fertility, health and disease. Nat Rev Urol. 2016; 13:379. DOI: https://doi.org/10.1038/nrurol.2016.89

Zhao Q, Yang F, Meng L, et al. Lycopene attenuates chronic prostatitis/chronic pelvic pain syndrome by inhibiting oxidative stress and inflammation via the interaction of NF-kappaB, MAPKs, and Nrf2 signaling pathways in rats. Andrology. 2020; 8:747. DOI: https://doi.org/10.1111/andr.12747

Fujita K, Ewing CM, Sokoll LJ, et al. Cytokine profiling of prostatic fluid from cancerous prostate glands identifies cytokines associated with extent of tumor and inflammation. Prostate. 2008; 68:872. DOI: https://doi.org/10.1002/pros.20755

Zhang Q, Liu S, Parajuli KR, et al. Interleukin-17 promotes prostate cancer via MMP7-induced epithelial-to-mesenchymal transition. Oncogene. 2017; 36:687. DOI: https://doi.org/10.1038/onc.2016.240

Chen J, Zhang H, Niu D, et al. The risk factors related to the severity of pain in patients with Chronic Prostatitis/Chronic Pelvic Pain Syndrome. BMC Urol. 2020; 20:154. DOI: https://doi.org/10.1186/s12894-020-00729-9

Farahani L, Tharakan T, Yap T, et al. The semen microbiome and its impact on sperm function and male fertility: A systematic review and meta-analysis. Andrology. 2021; 9:115. DOI: https://doi.org/10.1111/andr.12886

Puerta-Suárez J, Giraldo M, Cadavid A, Cardona-Maya W. Infecciones bacterianas del tracto reproductivo masculino y su papel en la fertilidad. Rev Chil Obstet Ginecol 2014; 79:209. DOI: https://doi.org/10.4067/S0717-75262014000300010

Galarzo S, Cano-Cháves A, Puerta Suárez J, et al. Efecto de los factores solubles de Staphylococcus aureus, Staphylococcus capitis y Staphylococcus epidermidis sobre la fisiología espermática. Aprobado para publicación Rev Chil Obstet Ginecol 2015; 80:316-323. DOI: https://doi.org/10.4067/S0717-75262015000400006

Cano-Cháves A, Galarzo-Pardo S, Puerta-Suárez J, et al. Efecto de las bacterias uropatógenas y de los factores solubles de su metabolismo sobre la calidad espermática: Escherichia coli y Enterococcus faecalis. Clínica e Investigación en Ginecología y Obstetricia. 2017;44:106-112. DOI: https://doi.org/10.1016/j.gine.2015.11.005

Guerrero Hurtado L, Puerta Suarez J, Cardona Maya W. Papel de los espermatozoides en la transmisión de bacterias uropatógenas: Escherichia coli y Enterococcus faecalis. Clínica e Investigación en Ginecología y Obstetricia 2018:45:2-6. DOI: https://doi.org/10.1016/j.gine.2016.03.003

Puerta Suárez J, Cardona Maya W. Evaluación in vitro del efecto de Neisseria gonorrhoeae y los factores solubles producto de su metabolismo sobre la calidad espermática. Revista chilena de obstetricia y ginecología. 2016;81:211. DOI: https://doi.org/10.4067/S0717-75262016000300007

Zuleta-Gonzalez MC, Zapata-Salazar ME, Guerrero-Hurtado LS, et al. Klebsiella pneumoniae and Streptococcus agalactiae: Passengers in the sperm travel. Arch Esp Urol. 2019; 72:939.

Mandar R, Punab M, Korrovits P, et al. Seminal microbiome in men with and without prostatitis. Int J Urol. 2017; 24:211. DOI: https://doi.org/10.1111/iju.13286

Videcnik Zorman J, Maticic M, Jeverica S, Smrkolj T. Diagnosis and treatment of bacterial prostatitis. Acta Dermatovenerol Alp Pannonica Adriat. 2015; 24:25. DOI: https://doi.org/10.15570/actaapa.2015.8

Kumar S, Dave A, Wolf B, Lerma EV. Urinary tract infections. Dis Mon. 2015; 61:45. DOI: https://doi.org/10.1016/j.disamonth.2014.12.002

Shang Y, Liu C, Cui D, et al. The effect of chronic bacterial prostatitis on semen quality in adult men: a meta-analysis of case-control studies. Sci Rep. 2014; 4:7233. DOI: https://doi.org/10.1038/srep07233

Litwin MS, McNaughton-Collins M, Fowler FJ, Jr., et al. The National Institutes of Health chronic prostatitis symptom index: development and validation of a new outcome measure. Chronic Prostatitis Collaborative Research Network. J Urol. 1999; 162:369. DOI: https://doi.org/10.1016/S0022-5347(05)68562-X

Collins MM, O'Leary MP, Calhoun EA, et al. The Spanish National Institutes of Health-Chronic Prostatitis Symptom Index: translation and linguistic validation. J Urol. 2001; 166:1800. DOI: https://doi.org/10.1016/S0022-5347(05)65678-9

Nickel JC, Downey J, Hunter D, Clark J. Prevalence of prostatitis-like symptoms in a population based study using the National Institutes of Health chronic prostatitis symptom index. J Urol 2001;165:842. DOI: https://doi.org/10.1016/S0022-5347(05)66541-X

World Health Organization. WHO laboratory manual for the examination and processing of human semen. 2010.

Cardona-Maya W, Berdugo J, Cadavid A. Comparación de la concentración espermática usando la cámara de Makler y la cámara de Neubauer. Actas Urológicas Españolas. 2008; 32:443. DOI: https://doi.org/10.1016/S0210-4806(08)73860-9

Mayorga-Torres BJ, Cardona-Maya W, Cadavid A, Camargo M. Evaluation of sperm functional parameters in normozoospermicinfertile individuals. Actas Urol Esp. 2013; 37:221. DOI: https://doi.org/10.1016/j.acuroe.2012.06.007

Martinez-Pastor F, Mata-Campuzano M, Alvarez-Rodriguez M et al. Probes and techniques for sperm evaluation by flow cytometry. Reprod Domest Anim. 2010; 45 Suppl 2:67. DOI: https://doi.org/10.1111/j.1439-0531.2010.01622.x

Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl. 2002; 23:25. DOI: https://doi.org/10.1002/j.1939-4640.2002.tb02599.x

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. DOI: https://doi.org/10.1093/molehr/gal119

Gil-Villa AM, Cardona-Maya W, Agarwal A, et al. Assessment of sperm factors possibly involved in early recurrent pregnancy loss. Fertil Steril. 2010; 94:1465. DOI: https://doi.org/10.1016/j.fertnstert.2009.05.042

Puerta Suárez J, Cardona Maya WD. Microbiota, Prostatitis, and Fertility: Bacterial Diversity as a Possible Health Ally. Advances in Urology. 2021; 2021:1007366. DOI: https://doi.org/10.1155/2021/1007366

Serafini M, Maiani G, Ferro-Luzzi A. Alcohol-free red wine enhances plasma antioxidant capacity in humans. J Nutr. 1998; 128:1003. DOI: https://doi.org/10.1093/jn/128.6.1003

Rueda C, Velilla PA, Chougnet CA, et al. HIV-induced T-cell activation/exhaustion in rectal mucosa is controlled only partially by antiretroviral treatment. PloS one. 2012; 7:e30307. DOI: https://doi.org/10.1371/journal.pone.0030307

Velásquez Rivera V, Cardona Maya WD, Puerta Suárez J. The relationship between sexually transmitted bacteria, microbiota and seminal quality in asymptomatic men. Asian J Urol (in press) 101016/jajur202109004. 2021. DOI: https://doi.org/10.1016/j.ajur.2021.09.004

Schmittgen TD, Zakrajsek BA, Mills AG, et al. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Annal Biochem. 2000; 285:194. DOI: https://doi.org/10.1006/abio.2000.4753

Gimenes F, Medina FS, Abreu AL, et al. Sensitive simultaneous detection of seven sexually transmitted agents in semen by multiplex-PCR and of HPV by single PCR. PloS one. 2014; 9:e98862. DOI: https://doi.org/10.1371/journal.pone.0098862

Lee C, Kim J, Shin SG, Hwang S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol. 2006; 123:273. DOI: https://doi.org/10.1016/j.jbiotec.2005.11.014

Anbazhagan D, Mui WS, Mansor M, et al. Development of conventional and real-time multiplex PCR assays for the detection of nosocomial pathogens. Braz J Microbiol. 2011; 42:448. DOI: https://doi.org/10.1590/S1517-83822011000200006

Fu CJ, Carter JN, Li Y, et al. Comparison of agar plate and realtime PCR on enumeration of Lactobacillus, Clostridium perfringens and total anaerobic bacteria in dog faeces. Lett Appl Microbiol. 2006; 42:490. DOI: https://doi.org/10.1111/j.1472-765X.2006.01893.x

Kulkarni G, Gohil K, Misra V, et al. Multilocus sequence typing of Ochrobactrum spp. isolated from gastric niche. J Infect Public Health. 2017; 10:201. DOI: https://doi.org/10.1016/j.jiph.2016.04.013

Vandecasteele SJ, Peetermans WE, Merckx R, Van Eldere J. Quantification of expression of Staphylococcus epidermidis housekeeping genes with Taqman quantitative PCR during in vitro growth and under different conditions. J Bacteriol. 2001; 183:7094. DOI: https://doi.org/10.1128/JB.183.24.7094-7101.2001

Kong F, Ma L, Gilbert GL. Simultaneous detection and serotype identification of Streptococcus agalactiae using multiplex PCR and reverse line blot hybridization. J Med Microbiol. 2005; 54:1133. DOI: https://doi.org/10.1099/jmm.0.46244-0

Kais M, Spindler C, Kalin M, et al. Quantitative detection of Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis in lower respiratory tract samples by real-time PCR. Diagn Microbiol Infect Dis. 2006; 55:169. DOI: https://doi.org/10.1016/j.diagmicrobio.2006.01.007

Zhao X, He X, Li H, et al. Detection of Streptococcus pyogenes using rapid visual molecular assay. FEMS Microbiology Letters. 2015; 362. DOI: https://doi.org/10.1093/femsle/fnv148

Frank JA, Reich CI, Sharma S, et al. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 2008; 74:2461. DOI: https://doi.org/10.1128/AEM.02272-07

Rivera Tapia J, Centeno Torres M, Santellan Olea M, Rodríguez Preval N. Prevalencia de Ureaplasma urealyticum en mujeres. Rev Mex Patol Clin. 2004; 51:33.

Lundy SD, Sangwan N, Parekh NV, et al. Functional and taxonomic dysbiosis of the gut, urine, and semen microbiomes in male infertility. Eur Urol. 2021; 79:826-836 DOI: https://doi.org/10.1016/j.eururo.2021.01.014

Mouraviev V, McDonald M. An implementation of next generation sequencing for prevention and diagnosis of urinary tract infection in urology. Can J Urol. 2018; 25:9349.

Eslahi A, Farpour H, Hosseini A, et al. Evaluation of the sympathetic skin response in men with chronic prostatitis: a case-control study. Res Rep Urol. 2020; 12:239. DOI: https://doi.org/10.2147/RRU.S253101

Gimenes F, Souza RP, Bento JC, et al. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol. 2014; 11:672. DOI: https://doi.org/10.1038/nrurol.2014.285

Manente L, Gargiulo U, Gargiulo P, Dovinola G. Propionibacterium acnes in urine and semen samples from men with urinary infection. Arch Ital Urol Androl. 2022; 94:62. DOI: https://doi.org/10.4081/aiua.2022.1.62

Aglamis E, Ceylan C, Akin MM. Is there a correlation between the aggressiveness of chronic asymptomatic prostatitis National Institutes of Health category IV and the Gleason score in patients with prostate cancer? Can Urol Assoc J. 2020; 14:E568. DOI: https://doi.org/10.5489/cuaj.6284

Perletti G, Monti E, Magri V, et al. The association between prostatitis and prostate cancer. Systematic review and meta-analysis. Arch Ital Urol Androl. 2017; 89:259. DOI: https://doi.org/10.4081/aiua.2017.4.259

Cai T, Gallelli L, Cione E, et al. The use of Lactobacillus casei DG® prevents symptomatic episodes and reduces the antibiotic use in patients affected by chronic bacterial prostatitis: results from a phase IV study. World J Urol. 2021; 39:3433-3440. DOI: https://doi.org/10.1007/s00345-020-03580-7

Zhang M, Liu Y, Chen J, et al. Single-cell multi-omics analysis presents the landscape of peripheral blood T-cell subsets in human chronic prostatitis/chronic pelvic pain syndrome. J Cell Mol Med. 2020; 24:14099. DOI: https://doi.org/10.1111/jcmm.16021

Li HJ, Kang DY. Prevalence of sexual dysfunction in men with chronic prostatitis/chronic pelvic pain syndrome: a meta-analysis. World J Urol. 2016; 34:1009. DOI: https://doi.org/10.1007/s00345-015-1720-3

Puerta Suárez, J. ., Hernandez, J. C., & Cardona Maya, W. D. (2022). Molecular analysis of microorganisms in the semen and their impact on semen parameters. Archivio Italiano Di Urologia E Andrologia, 94(2), 199–205. https://doi.org/10.4081/aiua.2022.2.199

Downloads

Download data is not yet available.

Citations