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Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Research

Characterizing semen parameters and their association with reactive oxygen species in infertile men

Authors: Ashok Agarwal, Rakesh K Sharma, Reecha Sharma, Mourad Assidi, Adel M Abuzenadah, Saad Alshahrani, Damayanthi Durairajanayagam, Edmund Sabanegh

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

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Abstract

Background

A routine semen analysis is a first step in the laboratory evaluation of the infertile male. In addition, other tests such as measurement of reactive oxygen species can provide additional information regarding the etiology of male infertility. The objective of this study was to investigate the association of semen parameters with reactive oxygen species (ROS) in two groups: healthy donors of unproven and proven fertility and infertile men. In addition, we sought to establish an ROS cutoff value in seminal plasma at which a patient may be predicted to be infertile.

Methods

Seminal ejaculates from 318 infertile patients and 56 donors, including those with proven fertility were examined for semen parameters and ROS levels. Correlations were determined between traditional semen parameters and levels of ROS among the study participants. ROS levels were measured using chemiluminescence assay. Receiver operating characteristic curves were obtained to calculate a cutoff value for these tests.

Results

Proven Donors (n = 28) and Proven Donors within the past 2 years (n = 16) showed significantly better semen parameters than All Patients group (n = 318). Significantly lower ROS levels were seen in the two Proven Donor groups compared with All Patients. The cutoff value of ROS in Proven Donors was determined to be 91.9 RLU/s with a specificity of 68.8% and a sensitivity of 93.8%.

Conclusions

Infertile men, irrespective of their clinical diagnoses, have reduced semen parameters and elevated ROS levels compared to proven fertile men who have established a pregnancy recently or in the past. Reactive oxygen species are negatively correlated with traditional semen parameters such as concentration, motility and morphology. Measuring ROS levels in the seminal ejaculates provides clinically-relevant information to clinicians.
Appendix
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Literature
1.
go back to reference Jarow JP, Sharlip ID, Belker AM, Lipshultz LI, Sigman M, Thomas AJ, Schlegel PN, Howards SS, Nehra A, Damewood MD, Overstreet JW, Sadovsky R: Best practice policies for male infertility. Male infertility best practice policy committee of the American Urological Association Inc. J Urol. 2002, 167: 2138-2144. 10.1016/S0022-5347(05)65109-9.CrossRefPubMed Jarow JP, Sharlip ID, Belker AM, Lipshultz LI, Sigman M, Thomas AJ, Schlegel PN, Howards SS, Nehra A, Damewood MD, Overstreet JW, Sadovsky R: Best practice policies for male infertility. Male infertility best practice policy committee of the American Urological Association Inc. J Urol. 2002, 167: 2138-2144. 10.1016/S0022-5347(05)65109-9.CrossRefPubMed
2.
go back to reference Venkatesh S, Gupta NP, Kumar R, Deecaraman M, Dada R: Correlation of sperm morphology and oxidative stress in infertile men. Iran J Reprod Med. 2009, 7: 29-34. Venkatesh S, Gupta NP, Kumar R, Deecaraman M, Dada R: Correlation of sperm morphology and oxidative stress in infertile men. Iran J Reprod Med. 2009, 7: 29-34.
3.
go back to reference Hamada A, Esteves SC, Agarwal A: Unexplained male infertility: potential causes and management. Hum Androl. 2011, 1: 2-16. 10.1097/01.XHA.0000397686.82729.09.CrossRef Hamada A, Esteves SC, Agarwal A: Unexplained male infertility: potential causes and management. Hum Androl. 2011, 1: 2-16. 10.1097/01.XHA.0000397686.82729.09.CrossRef
4.
go back to reference Agarwal A, Said TM: Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU Int. 2005, 95: 503-507. 10.1111/j.1464-410X.2005.05328.x.CrossRefPubMed Agarwal A, Said TM: Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU Int. 2005, 95: 503-507. 10.1111/j.1464-410X.2005.05328.x.CrossRefPubMed
5.
go back to reference Griveau JF, Le Lannou D: Reactive oxygen species and human spermatozoa: physiology and pathology. Int J Androl. 1997, 20: 61-69. 10.1046/j.1365-2605.1997.00044.x.CrossRefPubMed Griveau JF, Le Lannou D: Reactive oxygen species and human spermatozoa: physiology and pathology. Int J Androl. 1997, 20: 61-69. 10.1046/j.1365-2605.1997.00044.x.CrossRefPubMed
6.
go back to reference Garrido N, Meseguer M, Simon C, Pellicer A, Remohi J: Pro-oxidative and anti-oxidative imbalance in human semen and its relation with male fertility. Asian J Androl. 2002, 6: 59-65. Garrido N, Meseguer M, Simon C, Pellicer A, Remohi J: Pro-oxidative and anti-oxidative imbalance in human semen and its relation with male fertility. Asian J Androl. 2002, 6: 59-65.
7.
go back to reference Gavella M, Lipovac V: NADH-dependent oxidoreductase (diaphorase) activity and isozyme pattern of sperm in infertile men. Arch Androl. 1992, 28: 135-141. 10.3109/01485019208987691.CrossRefPubMed Gavella M, Lipovac V: NADH-dependent oxidoreductase (diaphorase) activity and isozyme pattern of sperm in infertile men. Arch Androl. 1992, 28: 135-141. 10.3109/01485019208987691.CrossRefPubMed
8.
go back to reference Hamada A, Esteves SC, Nizza M, Agarwal A: Unexplained male infertility: diagnosis and management. Int Braz J Urol. 2012, 38: 576-594. 10.1590/S1677-55382012000500002.CrossRefPubMed Hamada A, Esteves SC, Nizza M, Agarwal A: Unexplained male infertility: diagnosis and management. Int Braz J Urol. 2012, 38: 576-594. 10.1590/S1677-55382012000500002.CrossRefPubMed
9.
go back to reference Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod. 1998, 59: 1037-1046. 10.1095/biolreprod59.5.1037.CrossRefPubMed Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod. 1998, 59: 1037-1046. 10.1095/biolreprod59.5.1037.CrossRefPubMed
10.
go back to reference Alvarez JG, Sharma RK, Ollero M, Saleh RA, Lopez MC, Thomas AJ, Agarwal A: Increased DNA damage in sperm from leukocytospermic semen samples as determined by the sperm chromatin structure assay. Fertil Steril. 2002, 78: 319-329. 10.1016/S0015-0282(02)03201-6.CrossRefPubMed Alvarez JG, Sharma RK, Ollero M, Saleh RA, Lopez MC, Thomas AJ, Agarwal A: Increased DNA damage in sperm from leukocytospermic semen samples as determined by the sperm chromatin structure assay. Fertil Steril. 2002, 78: 319-329. 10.1016/S0015-0282(02)03201-6.CrossRefPubMed
11.
go back to reference Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Alvarez JG: Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod. 2001, 16: 1912-1921. 10.1093/humrep/16.9.1912.CrossRefPubMed Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Alvarez JG: Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod. 2001, 16: 1912-1921. 10.1093/humrep/16.9.1912.CrossRefPubMed
12.
go back to reference Saleh RA, Agarwal A, Kandirali E, Sharma RK, Thomas AJ, Nada EA, Alvarez JG: Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertil Steril. 2002, 78: 1215-1224. 10.1016/S0015-0282(02)04237-1.CrossRefPubMed Saleh RA, Agarwal A, Kandirali E, Sharma RK, Thomas AJ, Nada EA, Alvarez JG: Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertil Steril. 2002, 78: 1215-1224. 10.1016/S0015-0282(02)04237-1.CrossRefPubMed
13.
go back to reference Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003, 79: 829-843. 10.1016/S0015-0282(02)04948-8.CrossRefPubMed Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003, 79: 829-843. 10.1016/S0015-0282(02)04948-8.CrossRefPubMed
14.
go back to reference Aitken RJ, Harkiss D, Buckingham D: Relationship between iron-catalysed lipid peroxidation potential and human sperm function. J Reprod Fertil. 1993, 98: 257-265. 10.1530/jrf.0.0980257.CrossRefPubMed Aitken RJ, Harkiss D, Buckingham D: Relationship between iron-catalysed lipid peroxidation potential and human sperm function. J Reprod Fertil. 1993, 98: 257-265. 10.1530/jrf.0.0980257.CrossRefPubMed
15.
go back to reference Aitken RJ, Harkiss D, Buckingham DW: Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev. 1993, 35: 302-315. 10.1002/mrd.1080350313.CrossRefPubMed Aitken RJ, Harkiss D, Buckingham DW: Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev. 1993, 35: 302-315. 10.1002/mrd.1080350313.CrossRefPubMed
16.
go back to reference Aitken RJ, Irvine DS, Wu FC: Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991, 164: 542-551. 10.1016/S0002-9378(11)80017-7.CrossRefPubMed Aitken RJ, Irvine DS, Wu FC: Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991, 164: 542-551. 10.1016/S0002-9378(11)80017-7.CrossRefPubMed
17.
go back to reference Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ, Agarwal A: Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril. 2000, 73: 459-464. 10.1016/S0015-0282(99)00567-1.CrossRefPubMed Pasqualotto FF, Sharma RK, Nelson DR, Thomas AJ, Agarwal A: Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril. 2000, 73: 459-464. 10.1016/S0015-0282(99)00567-1.CrossRefPubMed
18.
go back to reference Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A: The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod. 1999, 14: 2801-2807. 10.1093/humrep/14.11.2801.CrossRefPubMed Sharma RK, Pasqualotto FF, Nelson DR, Thomas AJ, Agarwal A: The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility. Hum Reprod. 1999, 14: 2801-2807. 10.1093/humrep/14.11.2801.CrossRefPubMed
19.
go back to reference Agarwal A, Saleh RA: Role of oxidants in male infertility: rationale, significance, and treatment. Urol Clin North Am. 2002, 29: 817-827. 10.1016/S0094-0143(02)00081-2.CrossRefPubMed Agarwal A, Saleh RA: Role of oxidants in male infertility: rationale, significance, and treatment. Urol Clin North Am. 2002, 29: 817-827. 10.1016/S0094-0143(02)00081-2.CrossRefPubMed
20.
go back to reference Padron OF, Brackett NL, Sharma RK, Lynne CM, Thomas AJ, Agarwal A: Seminal reactive oxygen species and sperm motility and morphology in men with spinal cord injury. Fertil Steril. 1997, 67: 1115-1120. 10.1016/S0015-0282(97)81448-3.CrossRefPubMed Padron OF, Brackett NL, Sharma RK, Lynne CM, Thomas AJ, Agarwal A: Seminal reactive oxygen species and sperm motility and morphology in men with spinal cord injury. Fertil Steril. 1997, 67: 1115-1120. 10.1016/S0015-0282(97)81448-3.CrossRefPubMed
21.
go back to reference Sharma RK, Agarwal A: Role of reactive oxygen species in male infertility. Urology. 1996, 48: 835-850. 10.1016/S0090-4295(96)00313-5.CrossRefPubMed Sharma RK, Agarwal A: Role of reactive oxygen species in male infertility. Urology. 1996, 48: 835-850. 10.1016/S0090-4295(96)00313-5.CrossRefPubMed
22.
go back to reference Shekarriz M, Sharma RK, Thomas AJ, Agarwal A: Positive myeloperoxidase staining (Endtz test) as an indicator of excessive reactive oxygen species formation in semen. J Assist Reprod Genet. 1995, 12: 70-74. 10.1007/BF02211372.CrossRefPubMed Shekarriz M, Sharma RK, Thomas AJ, Agarwal A: Positive myeloperoxidase staining (Endtz test) as an indicator of excessive reactive oxygen species formation in semen. J Assist Reprod Genet. 1995, 12: 70-74. 10.1007/BF02211372.CrossRefPubMed
23.
go back to reference Kobayashi H, Gil-Guzman E, Mahran AM, Sharma R, Nelson DR, Thomas AJ, Agarwa A: Quality control of reactive oxygen species measurement by luminol-dependent chemiluminescence assay. J Androl. 2001, 22: 568-574.PubMed Kobayashi H, Gil-Guzman E, Mahran AM, Sharma R, Nelson DR, Thomas AJ, Agarwa A: Quality control of reactive oxygen species measurement by luminol-dependent chemiluminescence assay. J Androl. 2001, 22: 568-574.PubMed
24.
go back to reference Shekarriz M, Thomas AJ, Agarwal A: Incidence and level of seminal reactive oxygen species in normal men. Urology. 1995, 45: 103-107. 10.1016/S0090-4295(95)97088-6.CrossRefPubMed Shekarriz M, Thomas AJ, Agarwal A: Incidence and level of seminal reactive oxygen species in normal men. Urology. 1995, 45: 103-107. 10.1016/S0090-4295(95)97088-6.CrossRefPubMed
25.
go back to reference Agarwal A, Allamaneni SS, Said TM: Chemiluminescence technique for measuring reactive oxygen species. Reprod Biomed Online. 2004, 9: 466-468. 10.1016/S1472-6483(10)61284-9.CrossRefPubMed Agarwal A, Allamaneni SS, Said TM: Chemiluminescence technique for measuring reactive oxygen species. Reprod Biomed Online. 2004, 9: 466-468. 10.1016/S1472-6483(10)61284-9.CrossRefPubMed
26.
go back to reference Agarwal A, Gupta S, Sikka S: The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol. 2006, 18: 325-332. 10.1097/01.gco.0000193003.58158.4e.CrossRefPubMed Agarwal A, Gupta S, Sikka S: The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol. 2006, 18: 325-332. 10.1097/01.gco.0000193003.58158.4e.CrossRefPubMed
27.
go back to reference Athayde KS, Cocuzza M, Agarwal A, Krajcir N, Lucon AM, Srougi M, Hallak J: Development of normal reference values for seminal reactive oxygen species and their correlation with leukocytes and semen parameters in a fertile population. J Androl. 2007, 28: 613-620. 10.2164/jandrol.106.001966.CrossRefPubMed Athayde KS, Cocuzza M, Agarwal A, Krajcir N, Lucon AM, Srougi M, Hallak J: Development of normal reference values for seminal reactive oxygen species and their correlation with leukocytes and semen parameters in a fertile population. J Androl. 2007, 28: 613-620. 10.2164/jandrol.106.001966.CrossRefPubMed
28.
go back to reference Aziz N, Saleh RA, Sharma RK, Lewis-Jones I, Esfandiari N, Thomas AJ, Agarwal A: Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil Steril. 2004, 81: 349-354. 10.1016/j.fertnstert.2003.06.026.CrossRefPubMed Aziz N, Saleh RA, Sharma RK, Lewis-Jones I, Esfandiari N, Thomas AJ, Agarwal A: Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil Steril. 2004, 81: 349-354. 10.1016/j.fertnstert.2003.06.026.CrossRefPubMed
29.
go back to reference World Health Organization: WHO laboratory manual for the examination and processing of human semen. 2010, Geneva: World Health Organization, 5 World Health Organization: WHO laboratory manual for the examination and processing of human semen. 2010, Geneva: World Health Organization, 5
30.
go back to reference Kashou AH, Sharma R, Agarwal A: Assessment of oxidative stress in sperm and semen. Methods Mol Biol. 2013, 927: 351-361. 10.1007/978-1-62703-038-0_30.CrossRefPubMed Kashou AH, Sharma R, Agarwal A: Assessment of oxidative stress in sperm and semen. Methods Mol Biol. 2013, 927: 351-361. 10.1007/978-1-62703-038-0_30.CrossRefPubMed
31.
go back to reference Desai N, Sharma R, Makker K, Sabanegh E, Agarwal A: Physiologic and pathologic levels of reactive oxygen species in neat semen of infertile men. Fertil Steril. 2009, 92: 1626-1631. 10.1016/j.fertnstert.2008.08.109.CrossRefPubMed Desai N, Sharma R, Makker K, Sabanegh E, Agarwal A: Physiologic and pathologic levels of reactive oxygen species in neat semen of infertile men. Fertil Steril. 2009, 92: 1626-1631. 10.1016/j.fertnstert.2008.08.109.CrossRefPubMed
32.
go back to reference Said TM, Agarwal A, Sharma RK, Mascha E, Sikka SC, Thomas AJ: Human sperm superoxide anion generation and correlation with semen quality in patients with male infertility. Fertil Steril. 2004, 82: 871-877. 10.1016/j.fertnstert.2004.02.132.CrossRefPubMed Said TM, Agarwal A, Sharma RK, Mascha E, Sikka SC, Thomas AJ: Human sperm superoxide anion generation and correlation with semen quality in patients with male infertility. Fertil Steril. 2004, 82: 871-877. 10.1016/j.fertnstert.2004.02.132.CrossRefPubMed
33.
go back to reference Whittington K, Harrison SC, Williams KM, Day JL, McLaughlin EA, Hull MG, Ford WC: Reactive oxygen species (ROS) production and the outcome of diagnostic tests of sperm function. Int J Androl. 1999, 22: 236-242. 10.1046/j.1365-2605.1999.00174.x.CrossRefPubMed Whittington K, Harrison SC, Williams KM, Day JL, McLaughlin EA, Hull MG, Ford WC: Reactive oxygen species (ROS) production and the outcome of diagnostic tests of sperm function. Int J Androl. 1999, 22: 236-242. 10.1046/j.1365-2605.1999.00174.x.CrossRefPubMed
34.
go back to reference Aitken RJ, Ryan AL, Baker MA, McLaughlin EA: Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic Biol Med. 2004, 36: 994-1010. 10.1016/j.freeradbiomed.2004.01.017.CrossRefPubMed Aitken RJ, Ryan AL, Baker MA, McLaughlin EA: Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic Biol Med. 2004, 36: 994-1010. 10.1016/j.freeradbiomed.2004.01.017.CrossRefPubMed
35.
go back to reference Baker MA, Aitken RJ: The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol. 2004, 216: 47-54. 10.1016/j.mce.2003.10.068.CrossRefPubMed Baker MA, Aitken RJ: The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol. 2004, 216: 47-54. 10.1016/j.mce.2003.10.068.CrossRefPubMed
36.
go back to reference Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, Thomas AJ: Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril. 2003, 79: 1597-1605.CrossRefPubMed Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, Thomas AJ: Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril. 2003, 79: 1597-1605.CrossRefPubMed
37.
go back to reference Sukcharoen N, Keith J, Irvine DS, Aitken RJ: Prediction of the in-vitro fertilization (IVF) potential of human spermatozoa using sperm function tests: the effect of the delay between testing and IVF. Hum Reprod. 1996, 11: 1030-1034. 10.1093/oxfordjournals.humrep.a019291.CrossRefPubMed Sukcharoen N, Keith J, Irvine DS, Aitken RJ: Prediction of the in-vitro fertilization (IVF) potential of human spermatozoa using sperm function tests: the effect of the delay between testing and IVF. Hum Reprod. 1996, 11: 1030-1034. 10.1093/oxfordjournals.humrep.a019291.CrossRefPubMed
38.
go back to reference Yeung CH, De Geyter C, De Geyter M, Nieschlag E: Production of reactive oxygen species by and hydrogen peroxide scavenging activity of spermatozoa in an IVF program. J Assist Reprod Genet. 1996, 13: 495-500. 10.1007/BF02066531.CrossRefPubMed Yeung CH, De Geyter C, De Geyter M, Nieschlag E: Production of reactive oxygen species by and hydrogen peroxide scavenging activity of spermatozoa in an IVF program. J Assist Reprod Genet. 1996, 13: 495-500. 10.1007/BF02066531.CrossRefPubMed
39.
go back to reference Jarow JS, Sigman M, Kolettis PN, Lipshultz LR, McClure RD, Nangia AK, Naughton CK, Prins G, Sandlow JI, Schlegel PN: The optimal evaluation of the infertile male: AUA Best Practice Statement. Edited by: American Urological Association, Education and Research Inc. 2010, 1-38. Jarow JS, Sigman M, Kolettis PN, Lipshultz LR, McClure RD, Nangia AK, Naughton CK, Prins G, Sandlow JI, Schlegel PN: The optimal evaluation of the infertile male: AUA Best Practice Statement. Edited by: American Urological Association, Education and Research Inc. 2010, 1-38.
40.
go back to reference Menkveld R, Wong WY, Lombard CJ, Wetzels AM, Thomas CM, Merkus HM, Steegers-Theunissen RP: Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort towards standardization of in-vivo thresholds. Hum Reprod. 2001, 16: 1165-1171. 10.1093/humrep/16.6.1165.CrossRefPubMed Menkveld R, Wong WY, Lombard CJ, Wetzels AM, Thomas CM, Merkus HM, Steegers-Theunissen RP: Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort towards standardization of in-vivo thresholds. Hum Reprod. 2001, 16: 1165-1171. 10.1093/humrep/16.6.1165.CrossRefPubMed
41.
go back to reference 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: 603-621. 10.1590/S1677-55382007000500002.CrossRefPubMed 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: 603-621. 10.1590/S1677-55382007000500002.CrossRefPubMed
42.
go back to reference Zorn B, Vidmar G, Meden-Vrtovec H: 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. 2003, 26: 279-285. 10.1046/j.1365-2605.2003.00424.x.CrossRefPubMed Zorn B, Vidmar G, Meden-Vrtovec H: 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. 2003, 26: 279-285. 10.1046/j.1365-2605.2003.00424.x.CrossRefPubMed
43.
go back to reference Agarwal A, Allamaneni SS, Nallella KP, George AT, Mascha E: Correlation of reactive oxygen species levels with the fertilization rate after in vitro fertilization: a qualified meta-analysis. Fertil Steril. 2005, 84: 228-231. 10.1016/j.fertnstert.2004.12.057.CrossRefPubMed Agarwal A, Allamaneni SS, Nallella KP, George AT, Mascha E: Correlation of reactive oxygen species levels with the fertilization rate after in vitro fertilization: a qualified meta-analysis. Fertil Steril. 2005, 84: 228-231. 10.1016/j.fertnstert.2004.12.057.CrossRefPubMed
44.
go back to reference Hammadeh ME, Radwan M, Al-Hasani S, Micu R, Rosenbaum P, Lorenz M, Schmidt W: Comparison of reactive oxygen species concentration in seminal plasma and semen parameters in partners of pregnant and non-pregnant patients after IVF/ICSI. Reprod Biomed Online. 2006, 13: 696-706. 10.1016/S1472-6483(10)60661-X.CrossRefPubMed Hammadeh ME, Radwan M, Al-Hasani S, Micu R, Rosenbaum P, Lorenz M, Schmidt W: Comparison of reactive oxygen species concentration in seminal plasma and semen parameters in partners of pregnant and non-pregnant patients after IVF/ICSI. Reprod Biomed Online. 2006, 13: 696-706. 10.1016/S1472-6483(10)60661-X.CrossRefPubMed
45.
go back to reference Agarwal A, Sekhon LH: The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb). 2010, 13: 217-225. 10.3109/14647273.2010.532279.CrossRef Agarwal A, Sekhon LH: The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb). 2010, 13: 217-225. 10.3109/14647273.2010.532279.CrossRef
46.
go back to reference Banihani S, Sharma R, Bayachou M, Sabanegh E, Agarwal A: Human sperm DNA oxidation, motility and viability in the presence of L-carnitine during in vitro incubation and centrifugation. Andrologia. 2012, 44: 505-512.CrossRefPubMed Banihani S, Sharma R, Bayachou M, Sabanegh E, Agarwal A: Human sperm DNA oxidation, motility and viability in the presence of L-carnitine during in vitro incubation and centrifugation. Andrologia. 2012, 44: 505-512.CrossRefPubMed
47.
go back to reference Comhaire FH, El Garem Y, Mahmoud A, Eertmans F, Schoonjans F: Combined conventional/antioxidant “Astaxanthin” treatment for male infertility: a double blind, randomized trial. Asian J Androl. 2005, 7: 257-262. 10.1111/j.1745-7262.2005.00047.x.CrossRefPubMed Comhaire FH, El Garem Y, Mahmoud A, Eertmans F, Schoonjans F: Combined conventional/antioxidant “Astaxanthin” treatment for male infertility: a double blind, randomized trial. Asian J Androl. 2005, 7: 257-262. 10.1111/j.1745-7262.2005.00047.x.CrossRefPubMed
Metadata
Title
Characterizing semen parameters and their association with reactive oxygen species in infertile men
Authors
Ashok Agarwal
Rakesh K Sharma
Reecha Sharma
Mourad Assidi
Adel M Abuzenadah
Saad Alshahrani
Damayanthi Durairajanayagam
Edmund Sabanegh
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-33

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