Relationship of Seminal Oxidation-Reduction Potential with Sperm DNA Integrity and pH in Idiopathic Infertile Patients
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Measurement of Oxidation Reduction Potential
2.3. Sperm DNA Fragmentation Analysis
2.4. Sperm Chromatin Condensation Analysis
3. Results
3.1. MiOXSYS Measurements Variability
3.2. ORP, DNA Damage and DNA Condensation Relationships
4. Discussion
4.1. MiOXSYS Measurements Variability
4.2. Sperm Parameters Relationship
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- De-Kretser, D.M. Male infertility. Lancet 1997, 349, 787–790. [Google Scholar] [CrossRef]
- Hamada, A.; Esteves, S.C.; Nizza, M.; Agarwal, A. Unexplained male infertility: Diagnosis and management. Int. Braz. J. Urol. 2012, 38, 576–594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Louis, J.F.; Thoma, M.E.; Sørensen, D.N.; McLain, A.C.; King, R.B.; Sundaram, R.; Keiding, N.; Louis, G.M.B. The prevalence of couple infertility in the United States from a male perspective: Evidence from a nationally representative sample. Andrology 2013, 1, 741–748. [Google Scholar] [CrossRef] [PubMed]
- Kumar, N.; Singh, A. Trends of male factor infertility, an important cause of infertility: A review of literature. J. Hum. Reprod. Sci. 2015, 8, 191–196. [Google Scholar] [CrossRef] [PubMed]
- Lewis, S.E.M. Is sperm evaluation useful in predicting human fertility? Reproduction 2007, 134, 31–40. [Google Scholar] [CrossRef] [PubMed]
- Van Der Steeg, J.W.; Steures, P.; Eijkemans, M.J.C.; Habbema, J.D.F.; Hompes, P.G.A.; Kremer, J.A.M.; Van Der Leeuw-Harmsen, L.; Bossuyt, P.M.M.; Repping, S.; Silber, S.J.; et al. Role of semen analysis in subfertile couples. Fertil. Steril. 2011, 95, 1013–1019. [Google Scholar] [CrossRef]
- Wang, C.; Swerdloff, R.S. Limitations of semen analysis as a test of male fertility and anticipated needs from newer tests. Fertil. Steril. 2014, 102, 1502–1507. [Google Scholar] [CrossRef] [Green Version]
- Gelbaya, T.A.; Potdar, N.; Jeve, Y.B.; Nardo, L.G. Definition and epidemiology of unexplained infertility. Obstet. Gynecol. Surv. 2014, 69, 109–115. [Google Scholar] [CrossRef]
- de Lamirande, E.; Gagnon, C. Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic. Biol. Med. 1993, 14, 157–166. [Google Scholar] [CrossRef]
- Wright, C.; Milne, S.; Leeson, H. Sperm DNA damage caused by oxidative stress: Modifiable clinical, lifestyle and nutritional factors in male infertility. Reprod. BioMed. Online 2014, 28, 684–703. [Google Scholar] [CrossRef]
- Du Plessis, S.S.; Agarwal, A.; Halabi, J.; Tvrda, E. Contemporary evidence on the physiological role of reactive oxygen species in human sperm function. J. Assist. Reprod. Genet. 2015, 32, 509–520. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Roychoudhury, S.; Sharma, R.; Gupta, S.; Majzoub, A.; Sabanegh, E. Diagnostic application of oxidation-reduction potential assay for measurement of oxidative stress: Clinical utility in male factor infertility. Reprod. BioMed. Online 2017, 34, 48–57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aitken, R.J. Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol. Reprod. Dev. 2017, 84, 1039–1052. [Google Scholar] [CrossRef] [PubMed]
- Walczak-Jedrzejowska, R.; Wolski, J.K.; Slowikowska-Hilczer, J. The role of oxidative stress and antioxidants in male fertility. Cent. Eur. J. Urol. 2013, 66, 60–67. [Google Scholar] [CrossRef] [Green Version]
- Agarwal, A.; Bui, A.D. Oxidation-reduction potential as a new marker for oxidative stress: Correlation to male infertility. Investig. Clin. Urol. 2017, 58, 385. [Google Scholar] [CrossRef]
- Dada, R. Oxidative stress Major executioner in disease pathology role in sperm DNA damage and preventive strategies. Front. Biosci. 2017, 9, 495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Lamirande, E.; Gagnon, C. Impact of reactive oxygen species on spermatozoa: A balancing act between beneficial and detrimental effects. Hum. Reprod. 1995, 10, 15–21. [Google Scholar] [CrossRef]
- Sharma, R.K.; Pasqualotto, F.F.; Nelson, D.R.; Thomas, A.J.; 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. [Google Scholar] [CrossRef] [Green Version]
- Roychoudhury, S.; Sharma, R.; Sikka, S.; Agarwal, A. Diagnostic application of total antioxidant capacity in seminal plasma to assess oxidative stress in male factor infertility. J. Assist. Reprod. Genet. 2016, 33, 627–635. [Google Scholar] [CrossRef] [Green Version]
- Ribas-Maynou, J.; Yeste, M. Oxidative Stress in Male Infertility: Causes, Effects in Assisted Reproductive Techniques, and Protective Support of Antioxidants. Biology 2020, 9, 77. [Google Scholar] [CrossRef] [Green Version]
- Agarwal, A.; Sharma, R.; Roychoudhury, S.; Du Plessis, S.; Sabanegh, E. MiOXSYS: A novel method of measuring oxidation reduction potential in semen and seminal plasma. Fertil. Steril. 2016, 106, 566–573.e10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Henkel, R.; Sharma, R.; Tadros, N.N.; Sabanegh, E. Determination of seminal oxidation-reduction potential (ORP) as an easy and cost-effective clinical marker of male infertility. Andrologia 2018, 50, e12914. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.; Bui, A.D. Oxidation-Reduction Potential Methodology Using the MiOXSYS System. In Oxidants, Antioxidants and Impact of the Oxidative Status in Male Reproduction; Elsevier: Amsterdam, The Netherlands, 2019; pp. 217–224. ISBN 9780128125014. [Google Scholar]
- Rana, M.; Agarwal, A. Seminal Oxidation-Reduction Potential. In Male Infertility; Parekattil, S.J., Esteves, S.C., Agarwal, A., Eds.; Springer International Publishing: New York, NY, USA, 2020; pp. 377–387. ISBN 978-3-030-32299-1. [Google Scholar]
- Evenson, D.P.; Larson, K.L.; Jost, L.K. Sperm Chromatin Structure Assay: Its Clinical Use for Detecting Sperm DNA Fragmentation in Male Infertility and Comparisons With Other Techniques. J. Androl. 2002, 23, 25–43. [Google Scholar] [CrossRef]
- Zini, A.; Boman, J.M.; 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, 2663–2668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lewis, S.E.M.; Simon, L. Clinical implications of sperm DNA damage. Hum. Fertil. 2010, 13, 201–207. [Google Scholar] [CrossRef] [PubMed]
- Sharma, R.K.; Sabanegh, E.; Mahfouz, R.; Gupta, S.; Thiyagarajan, A.; Agarwal, A. TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 2010, 76, 1380–1386. [Google Scholar] [CrossRef]
- Ribas-Maynou, J.; Garcia-Peiro, A.; Abad, C.; Amengual, M.J.; Navarro, J.; Benet, J. Alkaline and neutral Comet assay profiles of sperm DNA damage in clinical groups. Hum. Reprod. 2012, 27, 652–658. [Google Scholar] [CrossRef]
- Ribas-Maynou, J.; García-Peiró, A.; Fernandez-Encinas, A.; Amengual, M.J.; Prada, E.; Cortés, P.; Navarro, J.; Benet, J. Double Stranded Sperm DNA Breaks, Measured by Comet Assay, Are Associated with Unexplained Recurrent Miscarriage in Couples without a Female Factor. PLoS ONE 2012, 7, e44679. [Google Scholar] [CrossRef] [Green Version]
- Ribas-Maynou, J.; Benet, J. Single and double strand sperm DNA damage: Different reproductive effects on male fertility. Genes 2019, 10, 105. [Google Scholar] [CrossRef] [Green Version]
- Ribas-Maynou, J.; García-Peiró, A.; Fernández-Encinas, A.; Abad, C.; Amengual, M.J.; Prada, E.; Navarro, J.; Benet, J. Comprehensive analysis of sperm DNA fragmentation by five different assays: TUNEL assay, SCSA, SCD test and alkaline and neutral Comet assay. Andrology 2013, 1, 715–722. [Google Scholar] [CrossRef]
- Javed, A.; Talkad, M.S.; Ramaiah, M.K. Evaluation of sperm DNA fragmentation using multiple methods: A comparison of their predictive power for male infertility. Clin. Exp. Reprod. Med. 2019, 46, 14–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Homa, S.T.; Vassiliou, A.M.; Stone, J.; Killeen, A.P.; Dawkins, A.; Xie, J.; Gould, F.; Ramsay, J.W.A. A comparison between two assays for measuring seminal oxidative stress and their relationship with sperm DNA fragmentation and semen parameters. Genes 2019, 10, 236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Iuliis, G.N.; Thomson, L.K.; Mitchell, L.A.; Finnie, J.M.; Koppers, A.J.; Hedges, A.; Nixon, B.; Aitken, R.J. DNA Damage in Human Spermatozoa Is Highly Correlated with the Efficiency of Chromatin Remodeling and the Formation of 8-Hydroxy-2′-Deoxyguanosine, a Marker of Oxidative Stress1. Biol. Reprod. 2009, 81, 517–524. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- García-Peiró, A.; Oliver-Bonet, M.; Navarro, J.; Abad, C.; Guitart, M.; Amengual, M.J.; Gosálvez, J.; Benet, J. Dynamics of sperm DNA fragmentation in patients carrying structurally rearranged chromosomes. Int. J. Androl. 2011, 34, 546–553. [Google Scholar] [CrossRef]
- Oliva, R.; Castillo, J. Proteomics and the genetics of sperm chromatin condensation. Asian J. Androl. 2011, 13, 24–30. [Google Scholar] [CrossRef] [Green Version]
- Mozdarani, H.; Nili, H.A.; Aleyasin, A. Correlation of sperm DNA damage with protamine deficiency in Iranian subfertile men. Reprod. BioMed. Online 2009, 18, 479–485. [Google Scholar] [CrossRef]
- Atshan, M.; Kakavand, K.; Hosseini, S.H.; Gilani, M.A.S.; Meybodi, A.M.; Sabbaghian, M. Evaluation of sperm DNA fragmentation and chromatin structure in infertile men with immotile short-tail sperm defect. Andrologia 2020, 52, e13445. [Google Scholar] [CrossRef]
- Ozkosem, B.; Feinstein, S.I.; Fisher, A.B.; O’Flaherty, C. Absence of Peroxiredoxin 6 Amplifies the Effect of Oxidant Stress on Mobility and SCSA/CMA3 Defined Chromatin Quality and Impairs Fertilizing Ability of Mouse Spermatozoa. Biol. Reprod. 2016, 94, 68. [Google Scholar] [CrossRef] [Green Version]
- Oumaima, A.; Tesnim, A.; Zohra, H.; Amira, S.; Ines, Z.; Sana, C.; Intissar, G.; Lobna, E.; Ali, J.; Meriem, M. Investigation on the origin of sperm morphological defects: Oxidative attacks, chromatin immaturity, and DNA fragmentation. Environ. Sci. Pollut. Res. 2018, 25, 13775–13786. [Google Scholar] [CrossRef]
- Aitken, R.J.; De Iuliis, G.N. On the possible origins of DNA damage in human spermatozoa. Mol. Hum. Reprod. 2010, 16, 3–13. [Google Scholar] [CrossRef] [Green Version]
- World Health Organization, Department of Reproductive Health and Research. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th ed.; World Health Organization: Geneva, Switzerland, 2010; ISBN 9789241547789. [Google Scholar]
- Rijnders, S.; Bolscher, J.G.M.; McDonnell, J.; Vermeiden, J.P.W. Filling Time of a Lamellar Capillary-Filling Semen Analysis Chamber Is a Rapid, Precise, and Accurate Method to Assess Viscosity of Seminal Plasma. J. Androl. 2007, 28, 461–465. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Selvam, M.P.; Arafa, M.; Okada, H.; Homa, S.; Killeen, A.; Balaban, B.; Saleh, R.; Armagan, A.; Roychoudhury, S.; et al. Multi-center evaluation of oxidation-reduction potential by the MiOXSYS in males with abnormal semen. Asian J. Androl. 2019, 21, 565–569. [Google Scholar] [CrossRef] [PubMed]
- García-Peiró, A.; Ribas-Maynou, J.; Oliver-Bonet, M.; Navarro, J.; Checa, M.A.; Nikolaou, A.; Amengual, M.J.; Abad, C.; Benet, J. Multiple Determinations of Sperm DNA Fragmentation Show That Varicocelectomy Is Not Indicated for Infertile Patients with Subclinical Varicocele. BioMed Res. Int. 2014. [Google Scholar] [CrossRef]
- Casanovas, A.; Ribas-Maynou, J.; Lara-Cerrillo, S.; Jimenez-Macedo, A.R.; Hortal, O.; Benet, J.; Carrera, J.; García-Peiró, A. Double-stranded sperm DNA damage is a cause of delay in embryo development and can impair implantation rates. Fertil. Steril. 2019, 111, 699–707. [Google Scholar] [CrossRef] [PubMed]
- Martins, A.D.; Agarwal, A. Oxidation reduction potential: A new biomarker of Male infertility. Panminerva Med. 2019, 61, 108–117. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Arafa, M.; Chandrakumar, R.; Majzoub, A.; Al Said, S.; Elbardisi, H. A multicenter study to evaluate oxidative stress by oxidation-reduction potential, a reliable and reproducible method. Andrology 2017, 5, 939–945. [Google Scholar] [CrossRef]
- Agarwal, A.; Sharma, R.; Henkel, R.; Roychoudhury, S.; Sikka, S.C.; du Plessis, S.; Sarda, Y.B.; Speyer, C.; Nouh, M.; Douglas, C.; et al. Cumene hydroperoxide induced changes in oxidation–reduction potential in fresh and frozen seminal ejaculates. Andrologia 2018, 50. [Google Scholar] [CrossRef]
- Shackelford, C.D.; Malusis, M.A.; Majeski, M.J.; Stern, R.T. Electrical conductivity breakthrough curves. J. Geotech. Geoenviron. Eng. 1999, 125, 260–270. [Google Scholar] [CrossRef]
- Leveling, T. The Relationship between pH and Conductivity in a Lithium Contaminated, De-Ionized Water System; FERMILAB-PBAR-NOTE-674; Fermilab: Batavia, IL, USA, 2002; pp. 1–11. [Google Scholar]
- Ouhadi, V.; Goodarzi, A. Factors impacting the electro conductivity variatons of clayey soils. Iran. J. Sci. Technol. Trans. B Eng. 2007, 31, 109–121. [Google Scholar]
- Arafa, M.; Agarwal, A.; Al Said, S.; Majzoub, A.; Sharma, R.; Bjugstad, K.B.; Al Rumaihi, K.; Elbardisi, H. Semen quality and infertility status can be identified through measures of oxidation-reduction potential. Andrologia 2018, 50. [Google Scholar] [CrossRef]
- Majzoub, A.; Arafa, M.; El Ansari, W.; Mahdi, M.; Agarwal, A.; Al-Said, S.; Elbardisi, H. Correlation of oxidation reduction potential and total motile sperm count: Its utility in the evaluation of male fertility potential. Asian J. Androl. 2020, 22, 317–322. [Google Scholar] [CrossRef] [PubMed]
- Aitken, R.J.; De Iuliis, G.N.; McLachlan, R.I. Biological and clinical significance of DNA damage in the male germ line. Int. J. Androl. 2009, 32, 46–56. [Google Scholar] [CrossRef] [PubMed]
- Sakkas, D.; Alvarez, J.G. Sperm DNA fragmentation: Mechanisms of origin, impact on reproductive outcome, and analysis. Fertil. Steril. 2010, 93, 1027–1036. [Google Scholar] [CrossRef] [PubMed]
- Gawecka, J.E.; Boaz, S.; Kasperson, K.; Nguyen, H.; Evenson, D.P.; Ward, W.S. Luminal fluid of epididymis and vas deferens contributes to sperm chromatin fragmentation. Hum. Reprod. 2015, 30, 2725–2736. [Google Scholar] [CrossRef] [Green Version]
- Xie, P.; Keating, D.; Parrella, A.; Cheung, S.; Rosenwaks, Z.; Goldstein, M.; Palermo, G.D. Sperm Genomic Integrity by TUNEL Varies throughout the Male Genital Tract. J. Urol. 2020, 203, 802–808. [Google Scholar] [CrossRef]
- Mayorga-Torres, B.J.M.; Camargo, M.; Cadavid, P.; du Plessis, S.S.; Maya, W.D.C. Are oxidative stress markers associated with unexplained male infertility? Andrologia 2017, 49, e12659. [Google Scholar] [CrossRef]
- Elbardisi, H.; Finelli, R.; Agarwal, A.; Majzoub, A.; Henkel, R.; Arafa, M. Predictive value of oxidative stress testing in semen for sperm DNA fragmentation assessed by sperm chromatin dispersion test. Andrology 2020, 8, 610–617. [Google Scholar] [CrossRef]
- Tanaka, T.; Kobori, Y.; Terai, K.; Inoue, Y.; Osaka, A.; Yoshikawa, N.; Shimomura, Y.; Suzuki, K.; Minami, T.; Iwahata, T.; et al. Seminal oxidation–reduction potential and sperm DNA fragmentation index increase among infertile men with varicocele. Hum. Fertil. 2020. [Google Scholar] [CrossRef]
- Majzoub, A.; Arafa, M.; Mahdi, M.; Agarwal, A.; Al Said, S.; Al-Emadi, I.; El Ansari, W.; Alattar, A.; Al Rumaihi, K.; Elbardisi, H. Oxidation-reduction potential and sperm DNA fragmentation, and their associations with sperm morphological anomalies amongst fertile and infertile men. Arab J. Urol. 2018, 16, 87–95. [Google Scholar] [CrossRef] [Green Version]
- Tvrdá, E.; Arroyo, F.; Gosálvez, J. Dynamic assessment of human sperm DNA damage I: The effect of seminal plasma-sperm co-incubation after ejaculation. Int. Urol. Nephrol. 2018, 50, 1381–1388. [Google Scholar] [CrossRef]
- Gosálvez, J.; Cortés-Gutierez, E.; López-Fernández, C.; Fernández, J.L.; Caballero, P.; Nuñez, R. Sperm deoxyribonucleic acid fragmentation dynamics in fertile donors. Fertil. Steril. 2009, 92, 170–173. [Google Scholar] [CrossRef] [PubMed]
Measures | Mean ± Standard Deviation | 95% Confidence Interval |
sORP1 (n = 37) | 57.01 ± 27.32 | 47.90–66.12 |
sORP2 (n = 32) * | 55.71 ± 25.84 | 46.39–65.02 |
Statistical test | Statistical value | p-value |
Pearson correlation (sORP1 vs sORP2) | r = 0.853 | <0.001 |
Paired samples T-student (sORP1 vs sORP2) | t = 2.306 | 0.028 |
Semen Parameters | Mean ± Std. Deviation | 95% Confidence Interval |
---|---|---|
nsORP-C (mV/106 sperm/mL) | 3.02 ± 9.50 | −0.35–6.39 |
nsORP-V (mV/cps) | 9.84 ± 6.33 | 7.66–12.02 |
nsORP-P (mV/U pH) | 7.05 ± 3.52 | 5.86–8.24 |
TUNEL (%) | 42.23 ± 14.98 | 37.37–47.09 |
Alkaline comet (%) | 34.33 ± 15.07 | 29.64–39.03 |
OTM alkaline comet | 0.82 ± 0.23 | 0.75–0.90 |
Neutral comet (%) | 66.17 ± 15.63 | 61.3–71.04 |
OTM neutral comet | 0.62 ± 0.16 | 0.57–0.68 |
CMA3 (%) | 38.06 ± 16.51 | 32.78–43.34 |
Viscosity (cps) | 9.13 ± 13.34 | 4.80–13.45 |
pH | 8.13 ± 0.39 | 8.01–8.26 |
Sperm concentration (106 sperm/mL) | 68.14 ± 57.49 | 48.97–87.30 |
Total motility (%) | 58.85 ± 16.50 | 53.35–64.35 |
Progressive motility (%) | 46.69 ± 19.03 | 40.35–53.04 |
Normal morphology (%) | 11.36 ± 12.74 | 6.42–16.30 |
Seminal volume (mL) | 3.00 ± 1.46 | 2.53–3.46 |
Semen Parameters | nsORP-C | nsORP-V | nsORP-P |
---|---|---|---|
TUNEL (%) | ρ = 0.160 | ρ = 0.173 | ρ = 0.213 |
Alkaline comet (%) | ρ = 0.125 | r = −0.005 | r = 0.061 |
OTM alkaline comet | ρ = −0.039 | r = −0.252 | r = 0.125 |
Neutral comet (%) | ρ = −0.249 | r = 0.036 | r = −0.054 |
OTM neutral comet | ρ = 0.129 | ρ = 0.338 | ρ = −0.028 |
CMA3 (%) | ρ = −0.394 * | ρ = −0.545 ** | ρ = −0.337* |
Viscosity (cps) | ρ = −0.009 r2 = 0.138 * | — | ρ = −0.416 * |
pH | ρ = −0.002 | ρ = −0.347 * | — |
Sperm concentration (106 sperm/mL) | — | ρ = 0.089 | ρ = 0.081 |
Total motility (%) | ρ = −0.198 | r = −0.477 ** | r = −0.355 * |
Progressive motility (%) | ρ = 0.125 | r = −0.485 ** | r = −0.445 * |
Normal morphology (%) | ρ = −0.138 | ρ = −0.005 | ρ = 0.163 |
Seminal volume (mL) | ρ = 0.452 ** | r = −0.058 | r = 0.342 * |
Semen Parameters | TUNEL | Alkaline Comet | OTM Alkaline | Neutral Comet | OTM Neutral | CMA3 |
---|---|---|---|---|---|---|
CMA3 (%) | 0.338 * | 0.346 * | −0.043 | −0.043 | −0.230 | — |
Viscosity (cps) | −0.125 | 0.321 * | 0.390 * | −0.083 | −0.463 ** | 0.202 |
pH | 0.166 | −0.165 | −0.229 | 0.004 | −0.018 | 0.395 ** |
Sperm concentration (106 sperm/mL) | −0.048 | −0.214 | −0.106 | 0.210 | −0.197 | 0.242 |
Total motility (%) | −0.037 | −0.363 * | −0.372 * | 0.022 | −0.016 | −0.024 |
Progressive motility (%) | −0.384 * | −0.417 ** | −0.349 * | −0.059 | −0.175 | −0.391 * |
Normal morphology (%) | 0.010 | 0.080 | 0.215 | −0.161 | −0.228 | 0.099 |
Seminal volume (mL) | −0.006 | −0.147 | 0.108 | −0.300 | −0.230 | −0.363* |
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Garcia-Segura, S.; Ribas-Maynou, J.; Lara-Cerrillo, S.; Garcia-Peiró, A.; Castel, A.B.; Benet, J.; Oliver-Bonet, M. Relationship of Seminal Oxidation-Reduction Potential with Sperm DNA Integrity and pH in Idiopathic Infertile Patients. Biology 2020, 9, 262. https://doi.org/10.3390/biology9090262
Garcia-Segura S, Ribas-Maynou J, Lara-Cerrillo S, Garcia-Peiró A, Castel AB, Benet J, Oliver-Bonet M. Relationship of Seminal Oxidation-Reduction Potential with Sperm DNA Integrity and pH in Idiopathic Infertile Patients. Biology. 2020; 9(9):262. https://doi.org/10.3390/biology9090262
Chicago/Turabian StyleGarcia-Segura, Sergio, Jordi Ribas-Maynou, Sandra Lara-Cerrillo, Agustín Garcia-Peiró, Ana Belén Castel, Jordi Benet, and Maria Oliver-Bonet. 2020. "Relationship of Seminal Oxidation-Reduction Potential with Sperm DNA Integrity and pH in Idiopathic Infertile Patients" Biology 9, no. 9: 262. https://doi.org/10.3390/biology9090262