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Le sperme « inflammatoire »: ses relations avec la fertilité

“Inflammatory” sperm: relationship with fertility

Andrologie volume 19, pages 35–44 (2009)Cite this article

Résumé

Objectifs

L’inflammation du sperme résulte d’une infection bactérienne ou virale du tractus urogénital male (TUGM); elle est souvent cliniquement silencieuse. Le dilemme existe quant aux rapports de cause à effet entre leucocytes, marqueurs de l’inflammation et mauvaise qualité du sperme. Nous nous sommes intéressés aux modifications des spermatozoïdes à l’échelon moléculaire en rapport avec l’inflammation.

Matériel et méthodes

Cette étude repose sur une revue de la littérature et des résultats personnels. Chez 200 hommes, partenaires de couples infertiles au spermogramme normal, nous avons étudié la condensation nucléaire et les dérivés actifs de l’oxygène (DAO) déterminés par cytométrie en flux après marquage à l’acridine orange et au dihydroéthidium en fonction des taux d’élastase du plasma séminal.

Résultats

Dans la littérature, on a décrit une relation positive entre infection et exacerbation de l’apoptose des spermatozoïdes avec augmentation de la nécrose et diminution du potentiel de membrane mitochondriale. Nous avons retrouvé une corrélation positive entre le taux de spermatozoïdes avec ADN dénaturé et celui d’élastase. Ce taux passait de 8,6 % à un taux d’élastase entre 0 et 100 μg/l à 15,7 % pour un taux d’élastase entre 100 et 250 μg/l, cette augmentation ne dépendant pas de la sécrétion de DAO. Le taux de spermatozoïdes avec ADN dénaturé se normalisait pour des taux d’élastase supérieurs à 600 μg/l.

Discussion et conclusion

Les modifications de l’ADN ou des membranes des spermatozoïdes n’influencent pas automatiquement les caractéristiques classiques du sperme ni ne réduisent la fertilité male. Elles peuvent cependant retentir négativement sur la capacitation et la réaction acrosomique, avec absence de fécondation ou mauvais développement embryonnaire. Avant de traiter, on tiendra compte du lieu et de la durée de l’inflammation ainsi que des lésions occasionnées sur les spermatozoïdes.

Abstract

Objectives

Sperm inflammation is caused by bacterial or viral infection of the male genitourinary tract; it is often clinically asymptomatic. There is a dilemma about the causal relationship between leukocytes as markers of inflammation and poor semen quality. We were interested in sperm changes at molecular level caused by inflammation.

Material and methods

This study was based on a literature review and personal data. In 200 male partners of infertile couples with normal semen analysis, the percentage of sperm with DNA denaturation and the level of reactive oxygen species (ROS) were determined by flow cytometric analysis, after acridine orange and dihydroethidium stainings, and correlated with seminal plasma elastase levels.

Results

In the literature, a positive relationship between inflammation and increased sperm apoptosis was found with increased necrosis and decreased mitochondrial membrane potential. We found a positive correlation between the percentage of sperm with denatured DNA and elastase levels. The percentage increased from 8.6% at elastase level 0–100 μg/l to 15.7% at elastase level 100–250 μg/l; this increase was not dependent on ROS production. The percentage of sperm with denatured DNA normalized at elastase levels above 600 μg/l.

Discussion and conclusion

Changes in sperm DNA or membranes do not necessarily affect classical semen characteristics or reduce fertility in males. They can, however, have a negative effect on capacitation and acrosomal reaction, resulting in failed fertilization or poor embryo development. Before treatment, we must take into account the location and the duration of the inflammation as well as the damage done to sperm.

Références

  1. Riley FJ, Masters WH (1956) Problems of male fertility. III. Bacteriology of human semen. Fertil Steril 7:128–132

    PubMed  CAS  Google Scholar 

  2. Auroux M (1984) Non-spermatozoal cells in human semen: a study of 1,243 subfertile and 253 fertile men. Arch Androl 12:197–201

    Article  PubMed  CAS  Google Scholar 

  3. Comhaire F, Verschraegen G, Vermeulen L (1980) Diagnosis of accessory gland infection and its possible role in male infertility. Int J Androl 3:32–45

    Article  PubMed  CAS  Google Scholar 

  4. Aitken RJ, Clarkson JS (1987) Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 81:459–469

    Article  PubMed  CAS  Google Scholar 

  5. Barratt CL, Bolton AE, Cooke ID (1990) Functional significance of white blood cells in the male and female reproductive tract. Hum Reprod 5:639–648

    PubMed  CAS  Google Scholar 

  6. Jochum M, Pabst W, Schill WB (1986) Granulocyte elastase as a sensitive diagnostic parameter of silent male genital tract inflammation. Andrologia 18:413–419

    Article  PubMed  CAS  Google Scholar 

  7. Satta A, Stivala A, Garozzo A, et al (2006) Experimental Chlamydia trachomatis infection causes apoptosis in human sperm. Hum Reprod 21:134–137

    Article  PubMed  Google Scholar 

  8. Diaz-Garcia FJ, Herrera-Mendoza AP, Giono-Cerezo S, Guerra-Infanta FM (2006) Mycoplasma hominis attaches and locates intracellularly in human spermatozoa. Hum Reprod 21:1591–1598

    Article  PubMed  Google Scholar 

  9. Villegas J, Schulz M, Soto L, Sanchez R (2005) Bacteria induce expression of apoptosis in human spermatozoa. Apoptosis 10:105–110

    Article  PubMed  CAS  Google Scholar 

  10. Eggert-Kruse W, Rohr G, Kunt B, et al (2003) Prevalence of Chlamydia trachomatis in subfertile couples. Fertil Steril 80:660–663

    Article  PubMed  Google Scholar 

  11. Gdoura R, Kchaou W, Ammar-Keskes L, et al (2008) Assessment of Chlamydia trachomatis, Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis, and Mycoplasma genitalium in semen and first void urine specimens of asymptomatic male partners of infertile couples. J Androl 29:198–206

    Article  PubMed  CAS  Google Scholar 

  12. Gallegos G, Ramos B, Santiso R, Goyanes V (2008) Sperm DNA fragmentation in infertile men with genitourinary infection by Chlamydia trachomatis and Mycoplasma. Fertil Steril 90:328–334

    Article  PubMed  Google Scholar 

  13. Eggert-Kruse W, Rohr G, Demirakca T, et al (1997) Chlamydial serology in 1,303 asymptomatic subfertile couples. Hum Reprod 12:1464–1475

    Article  PubMed  CAS  Google Scholar 

  14. Idahl A, Abramsson L, Kumlin U, et al (2007) Male serum Chlamydia trachomatis IgA and IgG, but not heat shock protein 60 IgG, correlates with negatively affected semen characteristics and lower pregnancy rates in the infertile couple. Int J Androl 30:99–107

    Article  PubMed  CAS  Google Scholar 

  15. Joki-Korpela P, Sahrakorpi N, Halttunen M, et al (2008) The role of Chlamydia trachomatis infection in male infertility. Fertil Steril Aug 13 [Epub ahead of print]

  16. Rodin DM, Larone D, Goldstein M (2003) Relationship between semen cultures, leukospermia, and semen analysis in men undergoing fertility evaluation. Fertil Steril 79(Suppl 3): 1555–1558

    Article  PubMed  Google Scholar 

  17. Dejucq N, Jégou B (2001) Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev 65:208–231

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Nicopoullos JD, Almeida PA, Ramsay JW, Gilling-Smith C (2004) The effect of human immunodeficiency virus on sperm parameters and the outcome of intrauterine insemination following sperm washing. Hum Reprod 19:2289–2297

    Article  PubMed  Google Scholar 

  19. Garrido N, Meseguer M, Remohi J, et al (2005) Semen characteristics in human immunodeficiency virus (HIV) — and hepatitis C (HCV) — seropositive males: predictors of the success of viral removal after sperm washing. Hum Reprod 20:1028–1034

    Article  PubMed  Google Scholar 

  20. Bezold G, Politch JA, Kiviat NB, et al (2007) Prevalence of sexually transmissible pathogens in semen from asymptomatic male infertility patients with and without leukocytospermia. Fertil Steril 87:1087–1097

    Article  PubMed  PubMed Central  Google Scholar 

  21. Kapranos N, Petrakou E, Anastasiadou C, Kotronias D (2003) Detection of herpes simplex virus, cytomegalovirus, and Epstein-Barr virus in the semen of men attending an infertility clinic. Fertil Steril 79(Suppl 3):1566–1570

    Article  PubMed  Google Scholar 

  22. Ricci G, Presani G, Guaschino S, et al (2000) Leukocyte detection in human semen using flow cytometry. Hum Reprod 15:1329–1337

    Article  PubMed  CAS  Google Scholar 

  23. Sanocka D, Jedrzejczak P, Szumala-Kaekol A, et al (2003) Male genital tract inflammation: the role of selected interleukins in regulation of pro-oxidant and antioxidant enzymatic substances in seminal plasma. J Androl 24:448–455

    Article  PubMed  Google Scholar 

  24. Henkel R, Kierspel E, Stalf T, et al (2005) Effect of reactive oxygen species produced by spermatozoa and leukocytes on sperm functions in non-leukocytospermic patients. Fertil Steril 83:635–642

    Article  PubMed  CAS  Google Scholar 

  25. Trum JW, Mol BW, Pannekoek Y, et al (1998) Value of detecting leukocytospermia in the diagnosis of genital tract infection in subfertile men. Fertil Steril 70:315–319

    Article  PubMed  CAS  Google Scholar 

  26. Keck C, Gerber-Schäfer C, Clad A, et al (1998) Seminal tract infections: impact on male fertility and treatment options. Hum Reprod Update 4:891–903

    Article  PubMed  CAS  Google Scholar 

  27. Brinkmann V, Reichard U, Goosmann C, et al (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535

    Article  PubMed  CAS  Google Scholar 

  28. Fuchs TA, Abed U, Goosmann C, et al (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176:231–241

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  29. Eggert-Kruse W, Kiefer I, Beck C, et al (2007) Role for tumor necrosis factor alpha (TNF-α) and interleukin 1-beta (IL-1beta) determination in seminal plasma during infertility investigation. Fertil Steril 87:810–823

    Article  PubMed  CAS  Google Scholar 

  30. Zorn B, Virant-Klun I, Meden-Vrtovec H (2000) Semen granulocyte elastase: its relevance for the diagnosis and prognosis of silent genital tract inflammation. Hum Reprod 15:1978–1984

    Article  PubMed  CAS  Google Scholar 

  31. Bourgeon F, Evrard B, Brillard-Bourdet M, et al (2004) Involvement of semenogelin-derived peptides in the antibacterial activity of human seminal plasma. Biol Reprod 70:768–774

    Article  PubMed  CAS  Google Scholar 

  32. Linge HM, Collin M, Giwercman A, et al (2008) The antibacterial chemokine MIG/CXCL9 is constitutively expressed in epithelial cells of the male urogenital tract and is present in seminal plasma. J Interferon Cytokine Res 28:191–196

    Article  PubMed  CAS  Google Scholar 

  33. Rowe PJ, Comhaire FH, Hargreave TB, et al (2000) Objective criteria for diagnostic categories in the standardized management of male infertility: male accessory gland infection (MAGI). In: Rowe PJ, Comhaire FH, Hargreave TB, Mahmoud AMA (eds), WHO Manual for the Standardized Investigation, Diagnosis and Management of the Infertile Male. World Health Organization. Cambridge University Press, Cambridge, pp. 52–54

    Google Scholar 

  34. Koppers AJ, De Iuliis GN, Finnie JM, et al (2008) Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab 93:3199–3207

    Article  PubMed  CAS  Google Scholar 

  35. Burden HP, Holmes CH, Persad R, Whittington K (2005) Prostasomes their effects on human male reproduction and fertility. Hum Reprod Update 12:283–292

    Article  PubMed  Google Scholar 

  36. Saez F, Motta C, Boucher D, Grizard G (2000) Prostasomes inhibit the NADPH-oxidase activity of human neutrophils. Mol Hum Reprod 6:883–891

    Article  PubMed  CAS  Google Scholar 

  37. Vignon F, Clavert A, Cranz C, et al (1993) Alterations in the lipid composition of seminal plasma in patients with a chronic infection of the urogenital tract. Urol Int 50:36–38

    Article  PubMed  CAS  Google Scholar 

  38. Zhou CX, Zhang YL, Xiao L, et al (2004) An epididymis-specific beta-defensin is important for the initiation of sperm maturation. Nat Cell Biol 6:458–464

    Article  PubMed  CAS  Google Scholar 

  39. World Health Organization, WHO (1999) Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction. 4th ed. Cambridge University Press, Cambridge

    Google Scholar 

  40. Ziyyat A, Barraud-Lange V, Sifer C, et al (2008) Paradoxical increase of sperm motility and seminal carnitine associated with moderate leukocytospermia in infertile patients. Fertil Steril 90:2257–2263

    Article  PubMed  Google Scholar 

  41. Elzanaty S, Richthoff J, Malm J, Giwercman A (2002) The impact of epididymal and accessory gland function on sperm motility. Hum Reprod 17:2904–2911

    Article  PubMed  CAS  Google Scholar 

  42. Modrich RD, Maccioni M, Molina R, et al (2005) Reduced semen quality in chronic prostatitis patients that have cellular autoimmune response to prostate antigens. Hum Reprod 20:2567–2572

    Article  Google Scholar 

  43. Alvarez JG, Sharma RK, Ollero M, et al (2002) Increased DNA damage in sperm from leukocytospermic semen samples as determined by the sperm chromatin structure assay. Fertil Steril 78:319–329

    Article  PubMed  Google Scholar 

  44. Armstrong JS, Rajasekaran M, Chamulitrat W, et al (1999) Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radic Biol Med 26:869–880

    Article  PubMed  CAS  Google Scholar 

  45. Wang X, Sharma RK, Gupta A, et al (2003) Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil Steril 80(Suppl 2):844–850

    Article  PubMed  Google Scholar 

  46. Perdichizzi A, Nicoletti A, La Vignera S, et al (2007) Effects of tumor necrosis factor alpha on human sperm motility and apoptosis. J Clin Immunol 27:152–162

    Article  PubMed  CAS  Google Scholar 

  47. Krause W (2008) Male accessory gland infection. Andrologia 40:113–116

    Article  PubMed  CAS  Google Scholar 

  48. Grunewald S, Said TM, Paasch U, et al (2008) Relationship between sperm apoptosis signaling and oocyte penetration capacity. Int J Androl 31:325–330

    Article  PubMed  CAS  Google Scholar 

  49. Agarwal A, Allamaneni SSR, Nallella KP, et al (2005) Correlation of reactive oxygen species levels with the fertilization rate after in vitro fertilization: a qualified meta-analysis. Fertil Steril 84:228–231

    Article  PubMed  CAS  Google Scholar 

  50. Jedrzejczak P, Fraczek M, Szumala-Kakol A, et al (2005) Consequences of semen inflammation on fertilization capacity of spermatozoa in in vitro conditions. Int J Androl 28:275–283

    Article  PubMed  CAS  Google Scholar 

  51. Zorn B, Virant-Klun I, Vidmar G, et al (2004) Seminal elastase-inhibitor complex, a marker of genital tract inflammation, and negative IVF outcome measures: a role for a silent inflammation? Int J Androl 27:368–374

    Article  PubMed  CAS  Google Scholar 

  52. Zorn B, Vidmar G, Meden-Vrtovec H (2003) Seminal reactive oxygen species as predictors of fertilization, embryo quality and pregnancy rates after conventional in vitro fertilization and intracytoplasmic sperm injection. Int J Androl 26:279–285

    Article  PubMed  CAS  Google Scholar 

  53. Naber KG, Bergman B, Bishop MC, et al (2001) EAU guidelines for the management of urinary and male genital tract infections. Urinary Tract Infection (UTI) Working Group of the Health Care Office (HCO) of the European Association of Urology (EAU). Eur Urol 40:576–588

    Article  PubMed  CAS  Google Scholar 

  54. Vicari E, La Vignera S, Calogero AE (2002) Antioxidant treatment with carnitines is effective in infertile patients with prostatovesiculoepididymitis and elevated seminal leukocyte concentrations after treatment with non-steroidal ant-inflammatory compounds. Fertil Steril 78:1203–1208

    Article  PubMed  Google Scholar 

  55. Skau PA, Folstad I (2003) Do bacterial infections cause reduced ejaculate quality? A meta-analysis of antibiotic treatment of male infertility. Behav Ecol 14:40–47

    Article  Google Scholar 

  56. Henkel R, Schill WB (1998) Sperm separation in patients with urogenital infections. Andrologia 30(Suppl 1):91–97

    PubMed  Google Scholar 

  57. De Geyter C, De Geyter M, Behre HM, et al (1994) Peroxidasepositive round cells and microorganisms in human semen together with antibiotic treatment adversely influence the outcome of in vitro fertilization and embryo transfer. Int J Androl 17:127–134

    Article  PubMed  Google Scholar 

  58. Liversedge NH, Jenkins JM, Keay SD, et al (1996) Antibiotic treatment-based on seminal cultures from asymptomatic male partners in in vitro fertilization is unnecessary and may be detrimental. Hum Reprod 11:1227–1231

    Article  PubMed  CAS  Google Scholar 

  59. Kastrop PM, de Graaf-Miltenburg LA, Gutknecht DR, Weima SM (2007) Microbial contamination of embryo cultures in an ART laboratory: sources and management. Hum Reprod 22:2243–2248

    Article  PubMed  Google Scholar 

  60. Grunewald S, Baumann T, Paasch U, Glander HJ (2006) Capacitation and acrosome reaction in non-apoptotic spermatozoa. Ann NY Acad Sci 1090:138–146

    Article  PubMed  Google Scholar 

  61. Cohen DR, Basu S, Randall JM, et al (2004) Sperm motility in men with spinal cord injuries is enhanced by inactivating cytokines in the seminal plasma. J Androl 25:922–925

    Article  PubMed  Google Scholar 

  62. Fabiani R, Johansson L, Lundkvist O, Ronquist G (1994) Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim-up medium. Hum Reprod 9:1485–1489

    PubMed  CAS  Google Scholar 

  63. Chi HJ, Kim JH, Ryu CS, et al (2008) Protective effect of antioxidant supplementation in sperm preparation medium against oxidative stress in human spermatozoa. Hum Reprod 23:1023–1028

    Article  PubMed  CAS  Google Scholar 

  64. Chan PJ, Jacobson JD, Corselli JU, Patton WC (2006) A simple zeta method for sperm selection-based on membrane charge. Fertil Steril 85:481–486

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Service de gynécologie-obstétrique, centre d’andrologie, Centre médical universitaire de Ljubljana, 3, Šlajmerjeva, 1000, Ljubljana, Slovénie

    B. Zorn

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Correspondence to B. Zorn.

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Zorn, B. Le sperme « inflammatoire »: ses relations avec la fertilité. Basic Clin. Androl. 19, 35–44 (2009). https://doi.org/10.1007/s12610-008-0005-8

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Mots clés

  • ADN
  • Analyse microbienne
  • Dérivés actifs de l’oxygène
  • Élastase
  • Leucocytes
  • Mitochondries
  • Prostasomes
  • Spermogramme
  • Tests fonctionnels

Keywords

  • DNA
  • Elastase
  • Functional tests
  • Leukocytes
  • Microbial analysis
  • Mitochondria
  • Prostasomes
  • Reactive oxygen species
  • Semen analysis

Basic and Clinical Andrology

ISSN: 2051-4190