DOI QR코드

DOI QR Code

The effects of oral antioxidants on the semen of men with idiopathic oligoasthenoteratozoospermia

  • Alahmar, Ahmed T (Department of Pharmacology and Toxicology, College of Pharmacy, University of Babylon)
  • 투고 : 2018.03.02
  • 심사 : 2018.04.16
  • 발행 : 2018.06.30

초록

It has been estimated that approximately 15% of reproductive-age couples suffer from infertility. Male factors contribute to almost half of infertility cases, and in many patients the underlying cause of oligoasthenoteratozoospermia is unknown. Accumulating evidence suggests that oxidative stress plays a role as a contributing factor to male infertility, and reactive oxygen species have been shown to impair sperm function and motility and to damage sperm membrane and DNA. Therefore, this review explored the evidence provided by studies published from 2002 to 2017 on the impact of oral antioxidants (vitamin C, vitamin E, L-carnitine, coenzyme Q10, zinc, selenium, and pentoxifylline) on seminal fluid parameters in men with idiopathic oligoasthenoteratozoospermia. Most of the studies were randomized controlled studies that investigated the effect of single or combined antioxidants and reported improvements in at least one semen parameter. The most noteworthy effect that was found was that the use of multiple antioxidants increased sperm motility and concentration. Nonetheless, there is a lack of agreement on the dose, the duration of treatment, and whether individual or combined oral antioxidants should be used. Therefore, the current review provides evidence supporting the use of oral antioxidants in the treatment of infertile men with idiopathic oligoasthenoteratozoospermia.

키워드

참고문헌

  1. Sharlip ID, Jarow JP, Belker AM, Lipshultz LI, Sigman M, Thomas AJ, et al. Best practice policies for male infertility. Fertil Steril 2002;77:873-82. https://doi.org/10.1016/S0015-0282(02)03105-9
  2. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 2007; 22:1506-12. https://doi.org/10.1093/humrep/dem046
  3. Cooper TG, Noonan E, von Eckardstein S, Auger J, Baker HW, Behre HM, et al. World Health Organization reference values for human semen characteristics. Hum Reprod Update 2010;16:231-45. https://doi.org/10.1093/humupd/dmp048
  4. Ghanbarzadeh S, Garjani A, Ziaee M, Khorrami A. CoQ10 and Lcarnitine attenuate the effect of high LDL and oxidized LDL on spermatogenesis in male rats. Drug Res (Stuttg) 2014;64:510-5.
  5. Zhao J, Dong X, Hu X, Long Z, Wang L, Liu Q, et al. Zinc levels in seminal plasma and their correlation with male infertility: a systematic review and meta-analysis. Sci Rep 2016;6:22386. https://doi.org/10.1038/srep22386
  6. Dorostghoal M, Kazeminejad SR, Shahbazian N, Pourmehdi M, Jabbari A. Oxidative stress status and sperm DNA fragmentation in fertile and infertile men. Andrologia 2017;49:e12762. https://doi.org/10.1111/and.12762
  7. Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014;32:1-17. https://doi.org/10.5534/wjmh.2014.32.1.1
  8. Oluwakemi O, Olufeyisipe A. DNA fragmentation and oxidative stress compromise sperm motility and survival in late pregnancy exposure to omega-9 fatty acid in rats. Iran J Basic Med Sci 2016;19:511-20.
  9. Agarwal A, Roychoudhury S, Bjugstad KB, Cho CL. Oxidation-reduction potential of semen: what is its role in the treatment of male infertility? Ther Adv Urol 2016;8:302-18. https://doi.org/10.1177/1756287216652779
  10. Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction 2001;122:497-506. https://doi.org/10.1530/rep.0.1220497
  11. Cocuzza M, Sikka SC, Athayde KS, Agarwal A. Clinical relevance of oxidative stress and sperm chromatin damage in male infertility: an evidence based analysis. Int Braz J Urol 2007;33:603-21. https://doi.org/10.1590/S1677-55382007000500002
  12. Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 2003;79:829-43. https://doi.org/10.1016/S0015-0282(02)04948-8
  13. Gharagozloo P, Gutierrez-Adan A, Champroux A, Noblanc A, Kocer A, Calle A, et al. A novel antioxidant formulation designed to treat male infertility associated with oxidative stress: promising preclinical evidence from animal models. Hum Reprod 2016;31:252-62. https://doi.org/10.1093/humrep/dev302
  14. 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
  15. Ozmen B, Koutlaki N, Youssry M, Diedrich K, Al-Hasani S. DNA damage of human spermatozoa in assisted reproduction: origins, diagnosis, impacts and safety. Reprod Biomed Online 2007;14:384-95. https://doi.org/10.1016/S1472-6483(10)60883-8
  16. Lewis SE, Simon L. Clinical implications of sperm DNA damage. Hum Fertil (Camb) 2010;13:201-7. https://doi.org/10.3109/14647273.2010.528823
  17. Tarozzi N, Bizzaro D, Flamigni C, Borini A. Clinical relevance of sperm DNA damage in assisted reproduction. Reprod Biomed Online 2007;14:746-57. https://doi.org/10.1016/S1472-6483(10)60678-5
  18. Zini A, San Gabriel M, Baazeem A. Antioxidants and sperm DNA damage: a clinical perspective. J Assist Reprod Genet 2009;26:427-32. https://doi.org/10.1007/s10815-009-9343-5
  19. Zini A, Al-Hathal N. Antioxidant therapy in male infertility: fact or fiction? Asian J Androl 2011;13:374-81. https://doi.org/10.1038/aja.2010.182
  20. Adewoyin M, Ibrahim M, Roszaman R, Isa ML, Alewi NA, Rafa AA, et al. Male infertility: the effect of natural antioxidants and phytocompounds on seminal oxidative stress. Diseases 2017;5:E9. https://doi.org/10.3390/diseases5010009
  21. Imamovic Kumalic S, Pinter B. Review of clinical trials on effects of oral antioxidants on basic semen and other parameters in idiopathic oligoasthenoteratozoospermia. Biomed Res Int 2014;2014:426951.
  22. Akmal M, Qadri JQ, Al-Waili NS, Thangal S, Haq A, Saloom KY. Improvement in human semen quality after oral supplementation of vitamin C. J Med Food 2006;9:440-2. https://doi.org/10.1089/jmf.2006.9.440
  23. Eslamian G, Amirjannati N, Rashidkhani B, Sadeghi MR, Hekmatdoost A. Nutrient patterns and asthenozoospermia: a case-control study. Andrologia 2017;49:e12624. https://doi.org/10.1111/and.12624
  24. Cyrus A, Kabir A, Goodarzi D, Moghimi M. The effect of adjuvant vitamin C after varicocele surgery on sperm quality and quantity in infertile men: a double blind placebo controlled clinical trial. Int Braz J Urol 2015;41:230-8. https://doi.org/10.1590/S1677-5538.IBJU.2015.02.07
  25. Kobori Y, Ota S, Sato R, Yagi H, Soh S, Arai G, et al. Antioxidant cosupplementation therapy with vitamin C, vitamin E, and coenzyme Q10 in patients with oligoasthenozoospermia. Arch Ital Urol Androl 2014;86:1-4. https://doi.org/10.4081/aiua.2014.1.1
  26. Das UB, Mallick M, Debnath JM, Ghosh D. Protective effect of ascorbic acid on cyclophosphamide- induced testicular gametogenic and androgenic disorders in male rats. Asian J Androl 2002;4:201-7.
  27. Vahidinia A, Rahbar AR, Shakoori Mahmoodabadi MM. Effect of astaxanthin, vitamin E, and vitamin C in combination with calorie restriction on sperm quality and quantity in male rats. J Diet Suppl 2017;14:252-63. https://doi.org/10.1080/19390211.2016.1211783
  28. Shabanian S, Farahbod F, Rafieian M, Ganji F, Adib A. The effects of vitamin C on sperm quality parameters in laboratory rats following long-term exposure to cyclophosphamide. J Adv Pharm Technol Res 2017;8:73-9.
  29. European Commission. Commission directive 2008/100/EC of 28 October 2008 amending council directive 90/496/EEC on nutrition labelling for foodstuffs as regards recommended daily allowance, energy conversion factors and definitions. Official J Eur Union 2008;L285/9.
  30. Greco E, Iacobelli M, Rienzi L, Ubaldi F, Ferrero S, Tesarik J. Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment. J Androl 2005;26:349-53. https://doi.org/10.2164/jandrol.04146
  31. Moslemi MK, Tavanbakhsh S. Selenium-vitamin E supplementation in infertile men: effects on semen parameters and pregnancy rate. Int J Gen Med 2011;4:99-104.
  32. Greco E, Romano S, Iacobelli M, Ferrero S, Baroni E, Minasi MG, et al. ICSI in cases of sperm DNA damage: beneficial effect of oral antioxidant treatment. Hum Reprod 2005;20:2590-4. https://doi.org/10.1093/humrep/dei091
  33. ElSheikh MG, Hosny MB, Elshenoufy A, Elghamrawi H, Fayad A, Abdelrahman S. Combination of vitamin E and clomiphene citrate in treating patients with idiopathic oligoasthenozoospermia: a prospective, randomized trial. Andrology 2015;3:864-7. https://doi.org/10.1111/andr.12086
  34. Gvozdjakova A, Kucharska J, Dubravicky J, Mojto V, Singh RB. Coenzyme Q10, ${\alpha}$-tocopherol, and oxidative stress could be important metabolic biomarkers of male infertility. Dis Markers 2015;2015:827941.
  35. Arduini A, Bonomini M, Savica V, Amato A, Zammit V. Carnitine in metabolic disease: potential for pharmacological intervention. Pharmacol Ther 2008;120:149-56. https://doi.org/10.1016/j.pharmthera.2008.08.008
  36. Enomoto A, Wempe MF, Tsuchida H, Shin HJ, Cha SH, Anzai N, et al. Molecular identification of a novel carnitine transporter specific to human testis: insights into the mechanism of carnitine recognition. J Biol Chem 2002;277:36262-71. https://doi.org/10.1074/jbc.M203883200
  37. Moslemi Mehni N, Ketabchi AA, Hosseini E. Combination effect of Pentoxifylline and L-carnitine on idiopathic oligoasthenoteratozoospermia. Iran J Reprod Med 2014;12:817-24.
  38. Haseen Ahmed SD, Ahsan S, Iqbal T, Ahmed Burney SI. Relationship of seminal free L-Carnitine with functional spermatozoal characteristics: results from an observational study conducted in a tertiary care hospital of Karachi, Pakistan. J Pak Med Assoc 2017;67:280-4.
  39. Ahmed SD, Karira KA, Jagdesh, Ahsan S. Role of L-carnitine in male infertility. J Pak Med Assoc 2011;61:732-6.
  40. Lenzi A, Sgro P, Salacone P, Paoli D, Gilio B, Lombardo F, et al. A placebo-controlled double-blind randomized trial of the use of combined l-carnitine and l-acetyl-carnitine treatment in men with asthenozoospermia. Fertil Steril 2004;81:1578-84. https://doi.org/10.1016/j.fertnstert.2003.10.034
  41. Garolla A, Maiorino M, Roverato A, Roveri A, Ursini F, Foresta C. Oral carnitine supplementation increases sperm motility in asthenozoospermic men with normal sperm phospholipid hydroperoxide glutathione peroxidase levels. Fertil Steril 2005;83:355-61. https://doi.org/10.1016/j.fertnstert.2004.10.010
  42. Balercia G, Regoli F, Armeni T, Koverech A, Mantero F, Boscaro M. Placebo-controlled double-blind randomized trial on the use of L-carnitine, L-acetylcarnitine, or combined L-carnitine and L-acetylcarnitine in men with idiopathic asthenozoospermia. Fertil Steril 2005;84:662-71. https://doi.org/10.1016/j.fertnstert.2005.03.064
  43. Wang YX, Yang SW, Qu CB, Huo HX, Li W, Li JD, et al. L-carnitine: safe and effective for asthenozoospermia. Zhonghua Nan Ke Xue 2010;16:420-2.
  44. Ahmadvand H, Tavafi M, Khosrowbeygi A. Amelioration of altered antioxidant enzymes activity and glomerulosclerosis by coenzyme Q10 in alloxan-induced diabetic rats. J Diabetes Complications 2012;26:476-82. https://doi.org/10.1016/j.jdiacomp.2012.06.004
  45. Lee BJ, Huang YC, Chen SJ, Lin PT. Coenzyme Q10 supplementation reduces oxidative stress and increases antioxidant enzyme activity in patients with coronary artery disease. Nutrition 2012; 28:250-5. https://doi.org/10.1016/j.nut.2011.06.004
  46. Ognjanovic BI, Markovic SD, Pavlovic SZ, Zikic RV, Stajn AS, Saicic ZS. Combined effects of coenzyme Q(10) and vitamin E in cadmium induced alterations of antioxidant defense system in the rat heart. Environ Toxicol Pharmacol 2006;22:219-24. https://doi.org/10.1016/j.etap.2006.03.008
  47. Safarinejad MR. Efficacy of coenzyme Q10 on semen parameters, sperm function and reproductive hormones in infertile men. J Urol 2009;182:237-48. https://doi.org/10.1016/j.juro.2009.02.121
  48. Safarinejad MR, Safarinejad S, Shafiei N, Safarinejad S. Effects of the reduced form of coenzyme Q10 (ubiquinol) on semen parameters in men with idiopathic infertility: a double-blind, placebo controlled, randomized study. J Urol 2012;188:526-31. https://doi.org/10.1016/j.juro.2012.03.131
  49. Safarinejad MR. The effect of coenzyme Q10 supplementation on partner pregnancy rate in infertile men with idiopathic oligoasthenoteratozoospermia: an open-label prospective study. Int Urol Nephrol 2012;44:689-700. https://doi.org/10.1007/s11255-011-0081-0
  50. Nadjarzadeh A, Shidfar F, Amirjannati N, Vafa MR, Motevalian SA, Gohari MR, et al. Effect of Coenzyme Q10 supplementation on antioxidant enzymes activity and oxidative stress of seminal plasma: a double-blind randomised clinical trial. Andrologia 2014;46:177-83. https://doi.org/10.1111/and.12062
  51. Nadjarzadeh A, Sadeghi MR, Amirjannati N, Vafa MR, Motevalian SA, Gohari MR, et al. Coenzyme Q10 improves seminal oxidative defense but does not affect on semen parameters in idiopathic oligoasthenoteratozoospermia: a randomized double-blind, placebo controlled trial. J Endocrinol Invest 2011;34:e224-8.
  52. Thakur AS, Littarru GP, Funahashi I, Painkara US, Dange NS, Chauhan P. Effect of ubiquinol therapy on sperm parameters and serum testosterone levels in oligoasthenozoospermic infertile men. J Clin Diagn Res 2015;9:BC01-3.
  53. Lafuente R, Gonzalez-Comadran M, Sola I, Lopez G, Brassesco M, Carreras R, et al. Coenzyme Q10 and male infertility: a metaanalysis. J Assist Reprod Genet 2013;30:1147-56. https://doi.org/10.1007/s10815-013-0047-5
  54. Olayemi FO. A review on some causes of male infertility. Afr J Biotechnol 2010;9:2834-42.
  55. Khan MS, Zaman S, Sajjad M, Shoaib M, Gilani G. Assessment of the level of trace element zinc in seminal plasma of males and evaluation of its role in male infertility. Int J Appl Basic Med Res 2011;1:93-6. https://doi.org/10.4103/2229-516X.91152
  56. Favier AE. The role of zinc in reproduction: hormonal mechanisms. Biol Trace Elem Res 1992;32:363-82. https://doi.org/10.1007/BF02784623
  57. Freedman LP. Anatomy of the steroid receptor zinc finger region. Endocr Rev 1992;13:129-45. https://doi.org/10.1210/edrv-13-2-129
  58. Kothari RP, Chaudhari AR. Zinc levels in seminal fluid in infertile males and its relation with serum free testosterone. J Clin Diagn Res 2016;10:CC05-8.
  59. Hadwan MH, Almashhedy LA, Alsalman AR. Study of the effects of oral zinc supplementation on peroxynitrite levels, arginase activity and NO synthase activity in seminal plasma of Iraqi asthenospermic patients. Reprod Biol Endocrinol 2014;12:1. https://doi.org/10.1186/1477-7827-12-1
  60. Hadwan MH, Almashhedy LA, Alsalman AR. Oral zinc supplementation restores high molecular weight seminal zinc binding protein to normal value in Iraqi infertile men. BMC Urol 2012;12:32. https://doi.org/10.1186/1471-2490-12-32
  61. Raigani M, Yaghmaei B, Amirjannti N, Lakpour N, Akhondi MM, Zeraati H, et al. The micronutrient supplements, zinc sulphate and folic acid, did not ameliorate sperm functional parameters in oligoasthenoteratozoospermic men. Andrologia 2014;46:956-62. https://doi.org/10.1111/and.12180
  62. Flohe L. Selenium in mammalian spermiogenesis. Biol Chem 2007;388:987-95.
  63. Safarinejad MR, Safarinejad S. Efficacy of selenium and/or Nacetyl-cysteine for improving semen parameters in infertile men: a double-blind, placebo controlled, randomized study. J Urol 2009;181:741-51.
  64. Keskes-Ammar L, Feki-Chakroun N, Rebai T, Sahnoun Z, Ghozzi H, Hammami S, et al. Sperm oxidative stress and the effect of an oral vitamin E and selenium supplement on semen quality in infertile men. Arch Androl 2003;49:83-94. https://doi.org/10.1080/01485010390129269
  65. Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, et al. Selenium-enriched probiotics improves murine male fertility compromised by high fat diet. Biol Trace Elem Res 2012;147:251-60. https://doi.org/10.1007/s12011-011-9308-2
  66. Ghasemzadeh A, Karkon-Shayan F, Yousefzadeh S, Naghavi-Behzad M, Hamdi K. Study of pentoxifylline effects on motility and viability of spermatozoa from infertile asthenozoospermic males. Niger Med J 2016;57:324-8. https://doi.org/10.4103/0300-1652.193857
  67. Amer M, Metawae B, Hosny H, Raef A. Beneficial effect of adding pentoxifylline to processed semen samples on ICSI outcome in infertile males with mild and moderate asthenozoospermia: a randomized controlled prospective crossover study. Iran J Reprod Med 2013;11:939-44.
  68. Nabi A, Khalili MA, Fesahat F, Talebi A, Ghasemi-Esmailabad S. Pentoxifylline increase sperm motility in devitrified spermatozoa from asthenozoospermic patient without damage chromatin and DNA integrity. Cryobiology 2017;76:59-64. https://doi.org/10.1016/j.cryobiol.2017.04.008
  69. Safarinejad MR. Effect of pentoxifylline on semen parameters, reproductive hormones, and seminal plasma antioxidant capacity in men with idiopathic infertility: a randomized double-blind placebo-controlled study. Int Urol Nephrol 2011;43:315-28. https://doi.org/10.1007/s11255-010-9826-4
  70. Oliva A, Dotta A, Multigner L. Pentoxifylline and antioxidants improve sperm quality in male patients with varicocele. Fertil Steril 2009;91(4 Suppl):1536-9. https://doi.org/10.1016/j.fertnstert.2008.09.024
  71. Wirleitner B, Vanderzwalmen P, Stecher A, Spitzer D, Schuff M, Schwerda D, et al. Dietary supplementation of antioxidants improves semen quality of IVF patients in terms of motility, sperm count, and nuclear vacuolization. Int J Vitam Nutr Res 2012;82:391-8. https://doi.org/10.1024/0300-9831/a000136
  72. Alahmar AT. Effect of vitamin C, vitamin E, zinc, selenium, and coenzyme Q10 in infertile men with idiopathic oligoasthenozoospermia. Int J Infertil Fetal Med 2017;8:45-9. https://doi.org/10.5005/jp-journals-10016-1147
  73. 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
  74. Piomboni P, Gambera L, Serafini F, Campanella G, Morgante G, De Leo V. Sperm quality improvement after natural anti-oxidant treatment of asthenoteratospermic men with leukocytospermia. Asian J Androl 2008;10:201-6. https://doi.org/10.1111/j.1745-7262.2008.00356.x
  75. Gopinath P, Kalra B, Saxena A, Malik S, Kochhar K, Kalra S, et al. Fixed dose combination therapy of antioxidants in treatment of idiopathic oligoasthenozoospermia: results of a randomized, double-blind, placebo-controlled clinical trial. Int J Infertil Fetal Med 2013;4:6-13. https://doi.org/10.5005/jp-journals-10016-1053
  76. Tremellen K, Miari G, Froiland D, Thompson J. A randomised control trial examining the effect of an antioxidant (Menevit) on pregnancy outcome during IVF-ICSI treatment. Aust N Z J Obstet Gynaecol 2007;47:216-21. https://doi.org/10.1111/j.1479-828X.2007.00723.x
  77. Busetto GM, Koverech A, Messano M, Antonini G, De Berardinis E, Gentile V. Prospective open-label study on the efficacy and tolerability of a combination of nutritional supplements in primary infertile patients with idiopathic astenoteratozoospermia. Arch Ital Urol Androl 2012;84:137-40.
  78. Ghanem H, Shaeer O, El-Segini A. Combination clomiphene citrate and antioxidant therapy for idiopathic male infertility: a randomized controlled trial. Fertil Steril 2010;93:2232-5. https://doi.org/10.1016/j.fertnstert.2009.01.117
  79. Comhaire FH, Christophe AB, Zalata AA, Dhooge WS, Mahmoud AM, Depuydt CE. The effects of combined conventional treatment, oral antioxidants and essential fatty acids on sperm biology in subfertile men. Prostaglandins Leukot Essent Fatty Acids 2000;63:159-65. https://doi.org/10.1054/plef.2000.0174
  80. Akpinar E, Bashan I, Bozdemir N, Saatci E. Which is the best anthropometric technique to identify obesity: body mass index, waist circumference or waist-hip ratio? Coll Antropol 2007;31: 387-93.
  81. Mayorga-Torres BJM, Camargo M, Cadavid AP, du Plessis SS, Cardona Maya WD. Are oxidative stress markers associated with unexplained male infertility? Andrologia 2017;49:e12659. https://doi.org/10.1111/and.12659
  82. Hosen MB, Islam MR, Begum F, Kabir Y, Howlader MZ. Oxidative stress induced sperm DNA damage, a possible reason for male infertility. Iran J Reprod Med 2015;13:525-32.
  83. Tremellen K. Oxidative stress and male infertility: a clinical perspective. Hum Reprod Update 2008;14:243-58. https://doi.org/10.1093/humupd/dmn004
  84. Crha I, Hruba D, Ventruba P, Fiala J, Totusek J, Visnova H. Ascorbic acid and infertility treatment. Cent Eur J Public Health 2003;11:63-7.
  85. Sheweita SA, Tilmisany AM, Al-Sawaf H. Mechanisms of male infertility: role of antioxidants. Curr Drug Metab 2005;6:495-501. https://doi.org/10.2174/138920005774330594
  86. Jacob RA. The integrated antioxidant system. Nutr Res 1995;15:755-66. https://doi.org/10.1016/0271-5317(95)00041-G
  87. Singh A, Jahan N, Radhakrishnan G, Banerjee BD. To evaluate the efficacy of combination antioxidant therapy on oxidative stress parameters in seminal plasma in the male infertility. J Clin Diagn Res 2016;10:QC14-7.
  88. Safarinejad MR, Shafiei N, Safarinejad S. A prospective doubleblind randomized placebo-controlled study of the effect of saffron (Crocus sativus Linn.) on semen parameters and seminal plasma antioxidant capacity in infertile men with idiopathic oligoasthenoteratozoospermia. Phytother Res 2011;25:508-16. https://doi.org/10.1002/ptr.3294
  89. Janevic T, Kahn LG, Landsbergis P, Cirillo PM, Cohn BA, Liu X, et al. Effects of work and life stress on semen quality. Fertil Steril 2014; 102:530-8. https://doi.org/10.1016/j.fertnstert.2014.04.021

피인용 문헌

  1. The use of antioxidant therapy as preconceptional care in men vol.24, pp.4, 2018, https://doi.org/10.17116/repro20182404189
  2. Role of Oxidative Stress in Male Infertility: An Updated Review vol.12, pp.1, 2019, https://doi.org/10.4103/jhrs.jhrs_150_18
  3. Dietary Antioxidant Intake in Relation to Semen Quality Parameters in Infertile Men: a Cross-Sectional Study vol.8, pp.3, 2018, https://doi.org/10.7762/cnr.2019.8.3.229
  4. The impact of two doses of coenzyme Q10 on semen parameters and antioxidant status in men with idiopathic oligoasthenoteratozoospermia vol.46, pp.3, 2018, https://doi.org/10.5653/cerm.2019.00136
  5. Protective Effects of Antioxidant Supplements on Sperm Parameters, Sperm DNA Damage and Level of Seminal ROS in RPL Patients: A Clinical Trial Study vol.21, pp.11, 2018, https://doi.org/10.5812/ircmj.94197
  6. The role of oxidative stress and hypoxia in renal disease vol.38, pp.4, 2018, https://doi.org/10.23876/j.krcp.19.063
  7. Effect of Zinc Supplementation on Urate Pathway Enzymes in Spermatozoa and Seminal Plasma of Iraqi Asthenozoospermic Patients: A Randomized Controlled Trial vol.13, pp.4, 2020, https://doi.org/10.22074/ijfs.2020.5760
  8. Combination therapy with antioxidants improves total motile sperm counts: A Preliminary Study vol.19, pp.1, 2018, https://doi.org/10.1002/rmb2.12308
  9. Protective effect of vitamin E on sperm parameters in rats infected with Candida albicans vol.52, pp.7, 2018, https://doi.org/10.1111/and.13593
  10. Potential Pathogenic Bacteria in Seminal Microbiota of Patients with Different Types of Dysspermatism vol.10, pp.None, 2018, https://doi.org/10.1038/s41598-020-63787-x
  11. Impact of oxidative stress on semen parameters in normozoospermic infertile men: a case-control study vol.26, pp.1, 2018, https://doi.org/10.1186/s12301-020-00061-6
  12. Sperm oxidative stress: clinical significance and management vol.2021, pp.3, 2018, https://doi.org/10.21518/2079-701x-2021-3-19-27
  13. Coenzyme Q10, oxidative stress markers, and sperm DNA damage in men with idiopathic oligoasthenoteratospermia vol.48, pp.2, 2018, https://doi.org/10.5653/cerm.2020.04084
  14. Coenzyme Q10, oxidative stress, and male infertility: A review vol.48, pp.2, 2021, https://doi.org/10.5653/cerm.2020.04175