Colonisation of the male reproductive tract in asymptomatic infertile men: Effects on semen quality
Corresponding Author
Ernesto Veiga
Central Laboratory/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Correspondence
Ernesto Veiga, Hospital Clínico Universitario de Santiago de Compostela. Unidad de Reproducción Humana Asistida (URHA). Planta 0. Travesia da Choupana s/n, 15706 Santiago de Compostela, A Coruña, Spain.
Email: ernesto.veiga.alvarez@sergas.es
Search for more papers by this authorMercedes Treviño
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorAna B. Romay
Obstetrics Service/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
HM Fertility Center, A Coruña, Spain
Search for more papers by this authorDaniel Navarro
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorRocío Trastoy
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorManuel Macía
Obstetrics Service/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorCorresponding Author
Ernesto Veiga
Central Laboratory/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Correspondence
Ernesto Veiga, Hospital Clínico Universitario de Santiago de Compostela. Unidad de Reproducción Humana Asistida (URHA). Planta 0. Travesia da Choupana s/n, 15706 Santiago de Compostela, A Coruña, Spain.
Email: ernesto.veiga.alvarez@sergas.es
Search for more papers by this authorMercedes Treviño
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorAna B. Romay
Obstetrics Service/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
HM Fertility Center, A Coruña, Spain
Search for more papers by this authorDaniel Navarro
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorRocío Trastoy
Microbiology Service, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorManuel Macía
Obstetrics Service/Assisted Human Reproduction Unit, Complexo Hospitalario Universitario de Santiago de Compostela (CHUS), SERGAS, Santiago de Compostela, Spain
Search for more papers by this authorFunding information
This work was carried out with part of the data of the doctoral thesis of E.V. of the Faculty of Medical and Health Sciences, University of Santiago de Compostela, Spain. No funds were required for the tests, included in the infertility study of our Hospital. This study was funded by University Clinical Hospital of Santiago de Compostela.
Abstract
The objective was to explore presence/detection of microorganisms in the male reproductive tract (PMMRT) in asymptomatic patients undergoing infertility treatment and their effects on semen quality in our region. This study enrolled 205 men (mean age, 35.9 years) in a single-centre, tertiary university hospital from December 2015 to December 2016. We used the modified Meares–Stamey test, real-time polymerase chain reaction (rt-PCR) and the National Institutes of Health Chronic Prostatitis Sympton Index (NHI-CPSI) questionnaire to address this issue. No patient met the prostatitis criteria by the modified Meares–Stamey 4-sample test, 33 (16.1%) were positive for rt-PCR in the first-voided urine for any of the Mycoplasma (Ureaplasma urealyticum/parvum, Mycoplasma hominis/genitalium) and C. trachomatis was detected in two cases (1%), and three for rt-PCR in semen for HPV high-risk genotypes non-16/18 (1.5%). Significant statistical differences were reported among patients with and without PMMRT in terms of lower rate of progressive spermatozoa (PR) (p < .034), total motile sperm count (p < .028), normal morphologic forms, especially in the sperm head (p < .001) and highest viscosity (p < .012). It was concluded that PMMRT, specially Mycoplasmas, in asymptomatic infertility men, affects semen quality. The NIH-CPSI questionnaire was not a valid initial screening to subsequently evaluate the presence of prostatitis/PMMRT.
CONFLICT OF INTEREST
The authors report no financial or other conflict of interest relevant to this study.
Supporting Information
Filename | Description |
---|---|
and13637-sup-0001-FigS1.docxWord document, 1.3 MB | Fig S1 |
and13637-sup-0002-FigS2.docxWord document, 25.1 KB | Fig S2 |
and13637-sup-0003-TableS1-S3.docxWord document, 23.3 KB | Table S1-S3 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Abeysundara, P. K., Dissanayake, D., Wijesinghe, P. S., Perera, R., & Nishad, A. (2013). Efficacy of two sperm preparation techniques in reducing non-specific bacterial species from human semen. Journal of Human Reproductive Sciences, 6, 152–157. https://doi.org/10.4103/0974-1208.117169
- Askienazy-Elbhar, M. (2005). Male genital tract infection: The point of view of the bacteriologist. Gynecologie, Obstetrique and Fertilite, 33, 691–697.
- Baud, D., Pattaroni, C., Vulliemoz, N., Castella, V., Marsland, B. J., & Stojanov, M. (2019). Sperm microbiota and its impact on semen parameters. Frontiers in Microbiology, 10, 234. https://doi.org/10.3389/fmicb.2019.00234
- Benelli, A., Hossain, H., Pilatz, A., & Weidner, W. (2017). Prostatitis and its management. European Urology Supplements, 16, 132–137. https://doi.org/10.1016/j.eursup.2016.03.001
- Boeri, L., Pederzoli, F., Ventimiglia, E., Capogrosso, P., Cazzaniga, W., Frego, N., … Salonia, A. (2017). 582—Heavy cigarette smoking is the most detrimental factor for sperm DNA fragmentation – results of a cross-sectional study in primary infertile men. European Urology Supplements, 16, e1013. https://doi.org/10.1016/S1569-9056(17)30639-5
10.1016/S1569-9056(17)30639-5 Google Scholar
- Budía, A., Luis Palmero, J., Broseta, E., Tejadillos, S., Benedicto, A., Queipo, J. A., … Fernando Jiménez Cruz, J. (2006). Value of semen culture in the diagnosis of chronic bacterial prostatitis: A simplified method. Scandinavian Journal of Urology and Nephrology, 40, 326–331. https://doi.org/10.1080/00365590600748247
- Collins, M. M., O'Zleary, M. P., Calhoun, E. A., Pontari, M. A., Adler, A., Eremenco, S., , … Litwin, M. S.; Chronic Prostatitis Collaborative Research Network (2001). The Spanish National Institutes of Health-Chronic Prostatitis Symptom Index: Translation and linguistic validation. The Journal of Urology, 166, 1800–1803. https://doi.org/10.1016/S0022-5347(05)65678-9
- Comhaire, F. H., Mahmoud, A. M., Depuydt, C. E., Zalata, A. A., & Christophe, A. B. (1999). Mechanisms and effects of male genital tract infection on sperm quality and fertilizing potential: The andrologist's viewpoint. Human Reproduction Update, 5, 393–398. https://doi.org/10.1093/humupd/5.5.393
- Courcol, R. (2010). Rémic 2010: Référentiel en microbiologie médicale (4e édition). Paris: Société Française de Microbiologie - SFM.
- Esteves, S. C., Agarwal, A., Sharma, R., & Harlev, A. (2017). Reply to Eugenio Ventimiglia, Montorsi Francesco, and Andrea Salonia’s Letter to the Editor re: Reecha Sharma, Avi Harlev, Ashok Agarwal, Sandro C. Esteves. Cigarette Smoking and Semen Quality: A New Meta-analysis Examining the Effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. Eur Urol 2016;70:635–45. European Urology, 71, e21–e22.
- European Centre for Disease Prevention and Control. (2016). Guidance on chlamydia control in Europe, 2015. Luxembourg: Publications Office.
- Fode, M., Fusco, F., Lipshultz, L., & Weidner, W. (2016). Sexually transmitted disease and male infertility: A systematic review. European Urology Focus, 2, 383–393. https://doi.org/10.1016/j.euf.2016.08.002
- Garolla, A., Engl, B., Pizzol, D., Ghezzi, M., Bertoldo, A., Bottacin, A., … Foresta, C. (2016). Spontaneous fertility and in vitro fertilization outcome: New evidence of human papillomavirus sperm infection. Fertility and Sterility, 105, 65–72.e1.
- Guzick, D. S., Overstreet, J. W., Factor-Litvak, P., Brazil, C. K., Nakajima, S. T., Coutifaris, C., … Vogel, D. L. (2001). Sperm morphology, motility, and concentration in fertile and infertile men. The New England Journal of Medicine, 345, 1388–1393. https://doi.org/10.1056/NEJMoa003005
- Haahr, T., Jensen, J. S., Thomsen, L., Duus, L., Rygaard, K., & Humaidan, P. (2016). Abnormal vaginal microbiota may be associated with poor reproductive outcomes: A prospective study in IVF patients. Human Reproduction (Oxford, England), 31, 795–803. https://doi.org/10.1093/humrep/dew026
- Hamilton, J. A. M., Cissen, M., Brandes, M., Smeenk, J. M. J., de Bruin, J. P., Kremer, J. A. M., … Hamilton, C. J. C. M. (2015). Total motile sperm count: A better indicator for the severity of male factor infertility than the WHO sperm classification system. Human Reproduction (Oxford, England), 30, 1110–1121. https://doi.org/10.1093/humrep/dev058
- Jungwirth, A., Diemer, T., Krausz, C., Minhas, S., & Tournaye, H. (2018). EAU Guidelines on Male Infertility. Arnhem, The Netherlands: EAU Guidelines Office.
- Karlström, P. O., Hjelm, E., & Lundkvist, O. (1991). Comparison of the ability of two sperm preparation techniques to remove microbes. Human Reproduction (Oxford, England), 6, 386–389.
- Kastrop, P. M. M., de Graaf-Miltenburg, L. A. M., Gutknecht, D. R., & Weima, S. M. (2007). Microbial contamination of embryo cultures in an ART laboratory: Sources and management. Human Reproduction (Oxford, England), 22, 2243–2248. https://doi.org/10.1093/humrep/dem165
- Kliesch, S. (2014). Diagnosis of male infertility: Diagnostic work-up of the infertile man. European Urology Supplements, 13, 73–82. https://doi.org/10.1016/j.eursup.2014.08.002
- Kohn, T. P., Kohn, J. R., & Lamb, D. J. (2018). Role of sperm morphology in deciding between various assisted reproduction technologies. European Urology Focus, 4, 311–313. https://doi.org/10.1016/j.euf.2018.07.029
- Krieger, J. N., Lee, S. W. H., Jeon, J., Cheah, P. Y., Liong, M. L., & Riley, D. E. (2008). Epidemiology of prostatitis. International Journal of Antimicrobial Agents, 31(Suppl 1), S85–90. https://doi.org/10.1016/j.ijantimicag.2007.08.028
- Krieger, J. N., Nyberg, L., & Nickel, J. C. (1999). NIH consensus definition and classification of prostatitis. JAMA, 282, 236–237. https://doi.org/10.1001/jama.282.3.236
- La Vignera, S., Condorelli, R. A., Vicari, E., Salmeri, M., Morgia, G., Favilla, V., … Calogero, A. E. (2014). Microbiological investigation in male infertility: A practical overview. Journal of Medical Microbiology, 63, 1–14. https://doi.org/10.1099/jmm.0.062968-0
- La Vignera, S., Vicari, E., Condorelli, R. A., D’Agata, R., & Calogero, A. E. (2011). Male accessory gland infection and sperm parameters (review). International Journal of Andrology, 34, e330–347. https://doi.org/10.1111/j.1365-2605.2011.01200.x
- Laprise, C., Trottier, H., Monnier, P., Coutlée, F., & Mayrand, M.-H. (2014). Prevalence of human papillomaviruses in semen: A systematic review and meta-analysis. Human Reproduction (Oxford, England), 29, 640–651. https://doi.org/10.1093/humrep/det453
- Lipsky, B. A., Byren, I., & Hoey, C. T. (2010). Treatment of bacterial prostatitis. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 50, 1641–1652. https://doi.org/10.1086/652861
- Litwin, M. S., McNAUGHTON-COLLINS, M., Fowler, F. J., Nickel, J. C., Calhoun, E. A., Pontari, M. A., … O'leary, M. P. (1999). 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, 162, 369–375. https://doi.org/10.1016/S0022-5347(05)68562-X
- Meares, E. M., & Stamey, T. A. (1968). Bacteriologic localization patterns in bacterial prostatitis and urethritis. Investigative Urology, 5, 492–518.
- Nicholson, C. M., Abramsson, L., Holm, S. E., & Bjurulf, E. (2000). Bacterial contamination and sperm recovery after semen preparation by density gradient centrifugation using silane-coated silica particles at different g forces. Human Reproduction (Oxford, England), 15, 662–666. https://doi.org/10.1093/humrep/15.3.662
- Nickel, J. C. (1997). The Pre and Post Massage Test (PPMT): A simple screen for prostatitis. Techniques in Urology, 3, 38–43.
- Nickel, J. C., Nyberg, L. M., & Hennenfent, M. (1999). Research guidelines for chronic prostatitis: Consensus report from the first National Institutes of Health International Prostatitis Collaborative Network. Urology, 54, 229–233. https://doi.org/10.1016/S0090-4295(99)00205-8
- Pederzoli, F., Capogrosso, P., Ventimiglia, E., Boeri, L., Cazzaniga, W., Chierigo, F., … Salonia, A. (2018). P114—The impact of semen infections over sperm parameters in primary infertile men–results of a real-life, cross-sectional study. European Urology Supplements, 17, 238–239. https://doi.org/10.1016/S1569-9056(18)33175-0
10.1016/S1569-9056(18)33175-0 Google Scholar
- Pederzoli, F., Ventimiglia, E., Chierigo, F., Capogrosso, P., Boeri, L., Cazzaniga, W., … Salonia, A. (2018). 768 - Precise assessment of underlying etiological factors in infertile men: Results from a cross-sectional study. European Urology Supplements, 17, e1104. https://doi.org/10.1016/S1569-9056(18)31603-8
10.1016/S1569-9056(18)31603-8 Google Scholar
- Pergialiotis, V., Karampetsou, N., Perrea, D. N., Konstantopoulos, P., & Daskalakis, G. (2018). The impact of bacteriospermia on semen parameters: A meta-analysis. Journal of Family and Reproductive Health, 12, 73–83.
- Sharma, R., Harlev, A., Agarwal, A., & Esteves, S. C. (2016). Cigarette smoking and semen quality: A new meta-analysis Examining the Effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. European Urology, 70, 635–645. https://doi.org/10.1016/j.eururo.2016.04.010
- Teuchert, L. M., Velagala, S. R., Schuppe, H.-C., Steger, K., Weidner, W., Schagdarsurengin, U., & Wagenlehner, F. (2015). 300 Association of CP/CPPS with impaired semen parameters: Does chronic prostatitis affect male fertility? European Urology Supplements, 14, e300. https://doi.org/10.1016/S1569-9056(15)60297-4
10.1016/S1569-9056(15)60297-4 Google Scholar
- Thoma, M. E., McLain, A. C., Louis, J. F., King, R. B., Trumble, A. C., Sundaram, R., & Buck Louis, G. M. (2013). Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertility and Sterility, 99, 1324–1331.e1. https://doi.org/10.1016/j.fertnstert.2012.11.037
- Turner, J. A., Ciol, M. A., Von Korff, M., & Berger, R. (2003). Validity and responsiveness of the national institutes of health chronic prostatitis symptom index. The Journal of Urology, 169, 580–583. https://doi.org/10.1016/S0022-5347(05)63957-2
- Veiga, E., Treviño, M., Romay, A. B., Navarro, D., Trastoy, R., & Macía, M. (2019). Prevalence of genital Mycoplasma and response to eradication treatment in patients undergoing assisted reproductive techniques. Revista Espanola De Quimioterapia: Publicacion Oficial De La Sociedad Espanola De Quimioterapia, 32, 327–332.
- Ventimiglia, E., Montorsi, F., & Salonia, A. (2017). Re: Reecha Sharma, Avi Harlev, Ashok Agarwal, Sandro C. Esteves. Cigarette Smoking and Semen Quality: A New Meta-analysis Examining the Effect of the 2010 World Health Organization Laboratory Methods for the Examination of Human Semen. Eur Urol 2016;70:635–45. European Urology, 71, e19–e20.
- Ventimiglia, E., Pederzoli, F., Capogrosso, P., Cazzaniga, W., Boeri, L., Alfano, M., … Salonia, A. (2018). 762 - When to perform semen culture in asymptomatic infertile men? Hints from a cross sectional study. European Urology Supplements, 17, e1097. https://doi.org/10.1016/S1569-9056(18)31597-5
10.1016/S1569-9056(18)31597-5 Google Scholar
- Weidner, W., Pilatz, A., Diemer, T., Schuppe, H. C., Rusz, A., & Wagenlehner, F. (2013). Male urogenital infections: Impact of infection and inflammation on ejaculate parameters. World Journal of Urology, 31, 717–723. https://doi.org/10.1007/s00345-013-1082-7
- World Health Organization (Ed.) (2010). WHO laboratory manual for the examination and processing of human semen, 5th ed. Geneva: World Health Organization.