Clinical and Experimental Reproductive Medicine

  • 제44권3호
  • /
  • Pages.132-140
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  • 2017
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  • 2233-8233(pISSN)
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  • 2233-8241(eISSN)
대한생식의학회 (The Korean Society for Reproductive Medicine)
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ICSI significantly improved the pregnancy rate of patients with a high sperm DNA fragmentation index

  • 투고 : 2016.12.24
  • 심사 : 2017.07.05
  • 발행 : 2017.09.26
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초록

Objective: Correlations between semen parameters and sperm DNA fragmentation index (DFI) were investigated to identify characteristics of sperm without DNA damage that could be used in selecting sperm for intracytoplasmic sperm injection (ICSI). Pregnancy outcomes were compared to determine whether in vitro fertilization (IVF) or ICSI is a better choice for patients who have sperm with a high-DFI. Methods: Semen analysis was carried out in 388 patients who visited our IVF center for the first time to investigate correlations between sperm DFI and semen parameters. In addition, 1,102 IVF cycles in 867 patients were carried out in the present study; 921 cycles in the low-DFI group (DFI < 30%) and 181 cycles in the high-DFI group ($DFI{\geq}30%$). Both the low- and high-DFI groups were subdivided into IVF and ICSI cycle groups. Results: Sperm DFI showed significant inverse correlations with sperm motility (r = -0.435, p< 0.001) and morphology (r = -0.153, p< 0.05). Sperm DFI also showed significant correlations with rapid motility (r = -0.436, p< 0.001), and the kinetic parameters of average-path velocity (r = -0.403) and linearity (r = -0.412). Although there was no significant difference in the pregnancy rates between IVF (48.6%) and ICSI (44.8%) in the low-DFI group, the pregnancy rate of ICSI cycles (44.8%, p< 0.05) was significantly higher than IVF cycles (25.0%) in the high-DFI group. No significant difference was observed in the abortion rates between the low-DFI (52 of 921, 5.6%) and high-DFI groups (7 of 181, 3.8%). Conclusion: ICSI is a better choice than IVF for improving the pregnancy outcomes of patients who have sperm with a high DFI.

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참고문헌

  1. Bianchi PG, Manicardi GC, Urner F, Campana A, Sakkas D. Chromatin packaging and morphology in ejaculated human spermatozoa: evidence of hidden anomalies in normal spermatozoa. Mol Hum Reprod 1996;2:139-44. https://doi.org/10.1093/molehr/2.3.139
  2. Muratori M, Tamburrino L, Marchiani S, Cambi M, Olivito B, Azzari C, et al. Investigation on the origin of sperm DNA fragmentation: role of apoptosis, immaturity and oxidative stress. Mol Med 2015;21:109-22. https://doi.org/10.1007/s00894-015-2655-8
  3. Gawecka JE, Marh J, Ortega M, Yamauchi Y, Ward MA, Ward WS. Mouse zygotes respond to severe sperm DNA damage by delaying paternal DNA replication and embryonic development. PLoS One 2013;8:e56385. https://doi.org/10.1371/journal.pone.0056385
  4. Chi HJ, Chung DY, Choi SY, Kim JH, Kim GY, Lee JS, et al. Integrity of human sperm DNA assessed by the neutral comet assay and its relationship to semen parameters and clinical outcomes for the IVF-ET program. Clin Exp Reprod Med 2011;38:10-7. https://doi.org/10.5653/cerm.2011.38.1.10
  5. Sharma R, Ahmad G, Esteves SC, Agarwal A. Terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay using bench top flow cytometer for evaluation of sperm DNA fragmentation in fertility laboratories: protocol, reference values, and quality control. J Assist Reprod Genet 2016;33:291-300. https://doi.org/10.1007/s10815-015-0635-7
  6. Evenson DP. The Sperm Chromatin Structure Assay (SCSA((R))) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim Reprod Sci 2016;169:56-75. https://doi.org/10.1016/j.anireprosci.2016.01.017
  7. Fernandez JL, Cajigal D, Lopez-Fernandez C, Gosalvez J. Assessing sperm DNA fragmentation with the sperm chromatin dispersion test. Methods Mol Biol 2011;682:291-301.
  8. Abad C, Amengual MJ, Gosalvez J, Coward K, Hannaoui N, Benet J, et al. Effects of oral antioxidant treatment upon the dynamics of human sperm DNA fragmentation and subpopulations of sperm with highly degraded DNA. Andrologia 2013;45:211-6. https://doi.org/10.1111/and.12003
  9. Li F, Yamaguchi K, Okada K, Matsushita K, Ando M, Chiba K, et al. Significant improvement of sperm DNA quality after microsurgical repair of varicocele. Syst Biol Reprod Med 2012;58:274-7. https://doi.org/10.3109/19396368.2012.692431
  10. Berkovitz A, Eltes F, Yaari S, Katz N, Barr I, Fishman A, et al. The morphological normalcy of the sperm nucleus and pregnancy rate of intracytoplasmic injection with morphologically selected sperm. Hum Reprod 2005;20:185-90. https://doi.org/10.1093/humrep/deh545
  11. Parmegiani L, Cognigni GE, Bernardi S, Troilo E, Ciampaglia W, Filicori M. “Physiologic ICSI”: hyaluronic acid (HA) favors selection of spermatozoa without DNA fragmentation and with normal nucleus, resulting in improvement of embryo quality. Fertil Steril 2010;93:598-604. https://doi.org/10.1016/j.fertnstert.2009.03.033
  12. Yagci A, Murk W, Stronk J, Huszar G. Spermatozoa bound to solid state hyaluronic acid show chromatin structure with high DNA chain integrity: an acridine orange fluorescence study. J Androl 2010;31:566-72. https://doi.org/10.2164/jandrol.109.008912
  13. Fleming SD, Ilad RS, Griffin AM, Wu Y, Ong KJ, Smith HC, et al. Prospective controlled trial of an electrophoretic method of sperm preparation for assisted reproduction: comparison with density gradient centrifugation. Hum Reprod 2008;23:2646-51. https://doi.org/10.1093/humrep/den330
  14. Enciso M, Iglesias M, Galan I, Sarasa J, Gosalvez A, Gosalvez J. The ability of sperm selection techniques to remove single- or double-strand DNA damage. Asian J Androl 2011;13:764-8. https://doi.org/10.1038/aja.2011.46
  15. Rougier N, Uriondo H, Papier S, Checa MA, Sueldo C, Alvarez Sedo C. Changes in DNA fragmentation during sperm preparation for intracytoplasmic sperm injection over time. Fertil Steril 2013;100:69-74. https://doi.org/10.1016/j.fertnstert.2013.03.005
  16. Sa R, Cunha M, Rocha E, Barros A, Sousa M. Sperm DNA fragmentation is related to sperm morphological staining patterns. Reprod Biomed Online 2015;31:506-15. https://doi.org/10.1016/j.rbmo.2015.06.019
  17. Said TM, Agarwal A, Grunewald S, Rasch M, Glander HJ, Paasch U. Evaluation of sperm recovery following annexin V magnetic-activated cell sorting separation. Reprod Biomed Online 2006;13:336-9. https://doi.org/10.1016/S1472-6483(10)61437-X
  18. Lee TH, Liu CH, Shih YT, Tsao HM, Huang CC, Chen HH, et al. Magnetic-activated cell sorting for sperm preparation reduces spermatozoa with apoptotic markers and improves the acrosome reaction in couples with unexplained infertility. Hum Reprod 2010;25:839-46. https://doi.org/10.1093/humrep/deq009
  19. Tavalaee M, Deemeh MR, Arbabian M, Nasr-Esfahani MH. Density gradient centrifugation before or after magnetic-activated cell sorting: which technique is more useful for clinical sperm selection? J Assist Reprod Genet 2012;29:31-8. https://doi.org/10.1007/s10815-011-9686-6
  20. Chi HJ, Kwak SJ, Kim SG, Kim YY, Park JY, Yoo CS, et al. Efficient isolation of sperm with high DNA integrity and stable chromatin packaging by a combination of density-gradient centrifugation and magnetic-activated cell sorting. Clin Exp Reprod Med 2016;43:199-206. https://doi.org/10.5653/cerm.2016.43.4.199
  21. Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, Francois Guerin J. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril 2007;87:93-100. https://doi.org/10.1016/j.fertnstert.2006.05.057
  22. Speyer BE, Pizzey AR, Ranieri M, Joshi R, Delhanty JD, Serhal P. Fall in implantation rates following ICSI with sperm with high DNA fragmentation. Hum Reprod 2010;25:1609-18. https://doi.org/10.1093/humrep/deq116
  23. Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, Giwercman A. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod 2004;19:1401-8. https://doi.org/10.1093/humrep/deh280
  24. Boe-Hansen GB, Fedder J, Ersboll AK, Christensen P. The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Hum Reprod 2006;21:1576-82. https://doi.org/10.1093/humrep/del019
  25. Trisini AT, Singh NP, Duty SM, Hauser R. Relationship between human semen parameters and deoxyribonucleic acid damage assessed by the neutral comet assay. Fertil Steril 2004;82:1623-32. https://doi.org/10.1016/j.fertnstert.2004.05.087
  26. Zini A, Meriano J, Kader K, Jarvi K, Laskin CA, Cadesky K. Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod 2005;20:3476-80. https://doi.org/10.1093/humrep/dei266
  27. Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 2007;22:174-9. https://doi.org/10.1093/humrep/del326
  28. Zhao J, Zhang Q, Wang Y, Li Y. Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis. Fertil Steril 2014;102:998-1005.e8. https://doi.org/10.1016/j.fertnstert.2014.06.033
  29. Anifandis G, Bounartzi T, Messini CI, Dafopoulos K, Markandona R, Sotiriou S, et al. Sperm DNA fragmentation measured by Halosperm does not impact on embryo quality and ongoing pregnancy rates in IVF/ICSI treatments. Andrologia 2015;47:295-302. https://doi.org/10.1111/and.12259
  30. Simon L, Brunborg G, Stevenson M, Lutton D, McManus J, Lewis SE. Clinical significance of sperm DNA damage in assisted reproduction outcome. Hum Reprod 2010;25:1594-608. https://doi.org/10.1093/humrep/deq103
  31. Zhang Z, Zhu L, Jiang H, Chen H, Chen Y, Dai Y. Sperm DNA fragmentation index and pregnancy outcome after IVF or ICSI: a meta-analysis. J Assist Reprod Genet 2015;32:17-26. https://doi.org/10.1007/s10815-014-0374-1
  32. Evenson DP, Wixon R. Data analysis of two in vivo fertility studies using sperm chromatin structure assay-derived DNA fragmentation index vs. pregnancy outcome. Fertil Steril 2008;90:1229-31. https://doi.org/10.1016/j.fertnstert.2007.10.066
  33. Manochantr S, Chiamchanya C, Sobhon P. Relationship between chromatin condensation, DNA integrity and quality of ejaculated spermatozoa from infertile men. Andrologia 2012;44:187-99.
  34. Brahem S, Mehdi M, Elghezal H, Saad A. Semen processing by density gradient centrifugation is useful in selecting sperm with higher double-strand DNA integrity. Andrologia 2011;43:196-202. https://doi.org/10.1111/j.1439-0272.2010.01050.x
  35. Sivanarayana T, Krishna CR, Prakash GJ, Krishna KM, Madan K, Rani BS, et al. CASA derived human sperm abnormalities: correlation with chromatin packing and DNA fragmentation. J Assist Reprod Genet 2012;29:1327-34. https://doi.org/10.1007/s10815-012-9885-9
  36. Varghese AC, Bragais FM, Mukhopadhyay D, Kundu S, Pal M, Bhattacharyya AK, et al. Human sperm DNA integrity in normal and abnormal semen samples and its correlation with sperm characteristics. Andrologia 2009;41:207-15. https://doi.org/10.1111/j.1439-0272.2009.00917.x
  37. Chan PJ, Corselli JU, Patton WC, Jacobson JD, Chan SR, King A. A simple comet assay for archived sperm correlates DNA fragmentation to reduced hyperactivation and penetration of zona-free hamster oocytes. Fertil Steril 2001;75:186-92. https://doi.org/10.1016/S0015-0282(00)01655-1
  38. Boushaba S, Belaaloui G. Sperm DNA fragmentation and standard semen parameters in algerian infertile male partners. World J Mens Health 2015;33:1-7. https://doi.org/10.5534/wjmh.2015.33.1.1
  39. Virant-Klun I, Tomazevic T, Meden-Vrtovec H. Sperm singlestranded DNA, detected by acridine orange staining, reduces fertilization and quality of ICSI-derived embryos. J Assist Reprod Genet 2002;19:319-28. https://doi.org/10.1023/A:1016006509036
  40. Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res 2005;322:33-41. https://doi.org/10.1007/s00441-005-1097-5
  41. Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, et al. Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod 2006;21:2876-81. https://doi.org/10.1093/humrep/del251
  42. Lin MH, Kuo-Kuang Lee R, Li SH, Lu CH, Sun FJ, Hwu YM. Sperm chromatin structure assay parameters are not related to fertilization rates, embryo quality, and pregnancy rates in in vitro fertilization and intracytoplasmic sperm injection, but might be related to spontaneous abortion rates. Fertil Steril 2008;90:352-9. https://doi.org/10.1016/j.fertnstert.2007.06.018
  43. Avendano C, Franchi A, Duran H, Oehninger S. DNA fragmentation of normal spermatozoa negatively impacts embryo quality and intracytoplasmic sperm injection outcome. Fertil Steril 2010;94:549-57. https://doi.org/10.1016/j.fertnstert.2009.02.050
  44. Enciso M, Pieczenik G, Cohen J, Wells D. Development of a novel synthetic oligopeptide for the detection of DNA damage in human spermatozoa. Hum Reprod 2012;27:2254-66. https://doi.org/10.1093/humrep/des201
  45. Frydman N, Prisant N, Hesters L, Frydman R, Tachdjian G, Cohen-Bacrie P, et al. Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertil Steril 2008;89:92-7. https://doi.org/10.1016/j.fertnstert.2007.02.022
  46. Zini A, Boman JM, Belzile E, Ciampi A. Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod 2008;23:2663-8. https://doi.org/10.1093/humrep/den321
  47. Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S, et al. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod 2012;27:2908-17. https://doi.org/10.1093/humrep/des261
  48. Zidi-Jrah I, Hajlaoui A, Mougou-Zerelli S, Kammoun M, Meniaoui I, Sallem A, et al. Relationship between sperm aneuploidy, sperm DNA integrity, chromatin packaging, traditional semen parameters, and recurrent pregnancy loss. Fertil Steril 2016;105:58-64. https://doi.org/10.1016/j.fertnstert.2015.09.041
  49. Caglar GS, Koster F, Schopper B, Asimakopoulos B, Nehls B, Nikolettos N, et al. Semen DNA fragmentation index, evaluated with both TUNEL and Comet assay, and the ICSI outcome. In Vivo 2007;21:1075-80.
  50. Nicopoullos JD, Gilling-Smith C, Almeida PA, Homa S, Norman-Taylor JQ, Ramsay JW. Sperm DNA fragmentation in subfertile men: the effect on the outcome of intracytoplasmic sperm injection and correlation with sperm variables. BJU Int 2008;101:1553-60. https://doi.org/10.1111/j.1464-410X.2008.07518.x
  51. Dar S, Grover SA, Moskovtsev SI, Swanson S, Baratz A, Librach CL. In vitro fertilization-intracytoplasmic sperm injection outcome in patients with a markedly high DNA fragmentation index (>50%). Fertil Steril 2013;100:75-80. https://doi.org/10.1016/j.fertnstert.2013.03.011
  52. Collins JA, Barnhart KT, Schlegel PN. Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertil Steril 2008;89:823-31. https://doi.org/10.1016/j.fertnstert.2007.04.055
  53. Practice Committee of the American Society for Reproductive Medicine. The clinical utility of sperm DNA integrity testing. Fertil Steril 2006;86(5 Suppl 1):S35-7.
  54. Evenson D, Jost L. Sperm chromatin structure assay is useful for fertility assessment. Methods Cell Sci 2000;22:169-89. https://doi.org/10.1023/A:1009844109023
  55. Avendano C, Franchi A, Taylor S, Morshedi M, Bocca S, Oehninger S. Fragmentation of DNA in morphologically normal human spermatozoa. Fertil Steril 2009;91:1077-84. https://doi.org/10.1016/j.fertnstert.2008.01.015
  56. Tamburrino L, Marchiani S, Montoya M, Elia Marino F, Natali I, Cambi M, et al. Mechanisms and clinical correlates of sperm DNA damage. Asian J Androl 2012;14:24-31. https://doi.org/10.1038/aja.2011.59
  57. Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, et al. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004;81:965-72. https://doi.org/10.1016/j.fertnstert.2003.09.044
  58. Hazout A, Dumont-Hassan M, Junca AM, Cohen Bacrie P, Tesarik J. High-magnification ICSI overcomes paternal effect resistant to conventional ICSI. Reprod Biomed Online 2006;12:19-25.
  59. Lewis SE, John Aitken R, Conner SJ, Iuliis GD, Evenson DP, Henkel R, et al. The impact of sperm DNA damage in assisted conception and beyond: recent advances in diagnosis and treatment. Reprod Biomed Online 2013;27:325-37. https://doi.org/10.1016/j.rbmo.2013.06.014
  60. Maettner R, Sterzik K, Isachenko V, Strehler E, Rahimi G, Alabart JL, et al. Quality of human spermatozoa: relationship between high-magnification sperm morphology and DNA integrity. Andrologia 2014;46:547-55. https://doi.org/10.1111/and.12114
  61. Osman A, Alsomait H, Seshadri S, El-Toukhy T, Khalaf Y. The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis. Reprod Biomed Online 2015;30:120-7. https://doi.org/10.1016/j.rbmo.2014.10.018
  62. Jiang H, He RB, Wang CL, Zhu J. The relationship of sperm DNA fragmentation index with the outcomes of in-vitro fertilisationembryo transfer and intracytoplasmic sperm injection. J Obstet Gynaecol 2011;31:636-9. https://doi.org/10.3109/01443615.2011.590910
  63. Larson-Cook KL, Brannian JD, Hansen KA, Kasperson KM, Aamold ET, Evenson DP. Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertil Steril 2003;80:895-902. https://doi.org/10.1016/S0015-0282(03)01116-6
  64. Benchaib M, Braun V, Lornage J, Hadj S, Salle B, Lejeune H, et al. Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Hum Reprod 2003;18:1023-8. https://doi.org/10.1093/humrep/deg228
  65. Virro MR, Larson-Cook KL, Evenson DP. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril 2004;81:1289-95. https://doi.org/10.1016/j.fertnstert.2003.09.063
  66. Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D. Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil Steril 2004;82:378-83. https://doi.org/10.1016/j.fertnstert.2003.12.039
  67. Wdowiak A, Bakalczuk S, Bakalczuk G. The effect of sperm DNA fragmentation on the dynamics of the embryonic development in intracytoplasmatic sperm injection. Reprod Biol 2015;15:94-100. https://doi.org/10.1016/j.repbio.2015.03.003
  68. Host E, Lindenberg S, Smidt-Jensen S. The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstet Gynecol Scand 2000;79:559-63. https://doi.org/10.1080/j.1600-0412.2000.079007559.x
  69. Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, Sakkas D. Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Hum Reprod 2001;16:2160-5. https://doi.org/10.1093/humrep/16.10.2160
  70. Check JH, Graziano V, Cohen R, Krotec J, Check ML. Effect of an abnormal sperm chromatin structural assay (SCSA) on pregnancy outcome following (IVF) with ICSI in previous IVF failures. Arch Androl 2005;51:121-4. https://doi.org/10.1080/014850190518125
  71. Oleszczuk K, Giwercman A, Bungum M. Sperm chromatin structure assay in prediction of in vitro fertilization outcome. Andrology 2016;4:290-6. https://doi.org/10.1111/andr.12153
  72. Evenson D, Wixon R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online 2006;12:466-72. https://doi.org/10.1016/S1472-6483(10)62000-7
  73. Henkel R, Kierspel E, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, et al. DNA fragmentation of spermatozoa and assisted reproduction technology. Reprod Biomed Online 2003;7:477-84. https://doi.org/10.1016/S1472-6483(10)61893-7
  74. Van Dyk Q, Lanzendorf S, Kolm P, Hodgen GD, Mahony MC. Incidence of aneuploid spermatozoa from subfertile men: selected with motility versus hemizona-bound. Hum Reprod 2000;15:1529-36. https://doi.org/10.1093/humrep/15.7.1529
  75. Kumar D, Upadhya D, Uppangala S, Salian SR, Kalthur G, Adiga SK. Nuclear DNA fragmentation negatively affects zona binding competence of Y bearing mouse spermatozoa. J Assist Reprod Genet 2013;30:1611-5. https://doi.org/10.1007/s10815-013-0123-x
  76. Moskovtsev SI, Willis J, White J, Mullen JB. Sperm DNA damage: correlation to severity of semen abnormalities. Urology 2009;74:789-93. https://doi.org/10.1016/j.urology.2009.05.043
  77. Khadem N, Poorhoseyni A, Jalali M, Akbary A, Heydari ST. Sperm DNA fragmentation in couples with unexplained recurrent spontaneous abortions. Andrologia 2014;46:126-30. https://doi.org/10.1111/and.12056

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