Decreased melatonin levels and increased levels of advanced oxidation protein products in the seminal plasma are related to male infertility
Ewa Maria Kratz A E , Agnieszka Piwowar B , Michal Zeman C , Katarína Stebelová C and Theresia Thalhammer DA Department of Chemistry and Immunochemistry, Faculty of Medicine, Wrocław Medical University, O. Bujwida 44A, 50-345 Wrocław, Poland.
B Department of Toxicology, Faculty of Pharmacy, Wrocław Medical University, Borowska 211, 50-556 Wrocław, Poland.
C Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, Mlynska dolina B2, 84215 Bratislava, Slovak Republic.
D Institute of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Waehringer Guertel 18-20 Vienna, Austria.
E Corresponding author. Email: ewa.kratz@umed.wroc.pl
Reproduction, Fertility and Development 28(4) 507-515 https://doi.org/10.1071/RD14165
Submitted: 19 May 2014 Accepted: 23 July 2014 Published: 12 September 2014
Abstract
Melatonin, an indolamine secreted by the pineal gland, is known as a powerful free-radical scavenger and wide-spectrum antioxidant. Therefore, the aim of this study was to correlate markers of oxidative protein damage (advanced oxidation protein products, AOPPs) and the total antioxidant capacity (TAC) with melatonin levels in the seminal plasma of men with azoospermia (n = 37), theratozoospermia (n = 29) and fertile controls (normozoospermia, n = 37). Melatonin concentration was measured by radioimmunoassay. The levels of AOPP as well as TAC efficiency (determined by the ferric reducing antioxidant power, FRAP) were estimated by spectrophotometric methods. The concentration of melatonin and AOPP significantly differed in azoospermic (P < 0.0001) and theratozoospermic (P < 0.0001) patients versus fertile men, and correlated negatively (r = –0.33, P = 0.0016). The TAC levels were significantly higher in azoospermia than in theratozoospermia (P = 0.0022) and the control group (P = 0.00016). In azoospermia, the AOPP concentration was also significantly higher than that observed in theratozoospermia (P = 0.00029). Decreased levels of melatonin together with elevated AOPP altered the oxidative–antioxidative balance in the ejaculate, thereby reducing fertility. Therefore, melatonin and AOPP levels may serve as additional diagnostic markers of semen quality and male reproductive potential.
Additional keywords: azoospermia, male fertility, oxidative stress, theratozoospermia, total antioxidant capacity.
References
Acuña-Castroviejo, D., Escames, G., Venegas, C., Díaz-Casado, M. E., Lima-Cabello, E., López, L. C., Rosales-Corral, S., Tan, D. X., and Reiter, R. J. (2014). Extrapineal melatonin: sources, regulation and potential functions. Cell. Mol. Life Sci. , .| Extrapineal melatonin: sources, regulation and potential functions.Crossref | GoogleScholarGoogle Scholar | 24554058PubMed |
Agarwal, A., and Allamaneni, S. S. (2011). Free radicals and male reproduction. J. Indian Med. Assoc. 109, 184–187.
| 22010591PubMed |
Agarwal, A., Nallella, K. P., Allamaneni, S. S., and Said, T. M. (2004). Role of antioxidants in treatment of male infertility: an overview of the literature. Reprod. Biomed. Online 8, 616–627.
| Role of antioxidants in treatment of male infertility: an overview of the literature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlCrtLg%3D&md5=1a72dd1b5a62126019102723a59dcd2bCAS | 15169573PubMed |
Agarwal, A., Makker, K., and Sharma, R. (2008). Clinical relevance of oxidative stress in male factor infertility: an update. Am. J. Reprod. Immunol. 59, 2–11.
| Clinical relevance of oxidative stress in male factor infertility: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1Wjsbc%3D&md5=88b22c162d5aca71669bdeea43bc31ffCAS | 18154591PubMed |
Aitken, R. J., and Curry, B. J. (2011). Redox regulation of human sperm function: from the physiological control of sperm capacitation to the aetiology of infertility and DNA damage in the germ line. Antioxid. Redox Signal. 14, 367–381.
| Redox regulation of human sperm function: from the physiological control of sperm capacitation to the aetiology of infertility and DNA damage in the germ line.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1SjsA%3D%3D&md5=7ffd1cf6888f94c83883b4893ad2d90bCAS | 20522002PubMed |
Aitken, R. J., Ryan, A. L., Curry, B. J., and Baker, M. A. (2003). Multiple forms of redox activity in populations of human spermatozoa. Mol. Hum. Reprod. 9, 645–661.
| Multiple forms of redox activity in populations of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVeruro%3D&md5=e88bb7453821df3af224b38f80a15218CAS | 14561808PubMed |
Awad, H., Halawa, F., Mostafa, T., and Atta, H. (2006). Melatonin hormone profile in infertile males. Int. J. Androl. 29, 409–413.
| Melatonin hormone profile in infertile males.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVSrurs%3D&md5=24d7d1f17efc63d11fceba4d897cc637CAS | 16371109PubMed |
Bauer, M. E., Muller, G. C., Correa, B. L., Vianna, P., Turner, J. E., and Bosch, J. A. (2013). Psychoneuroendocrine interventions aimed at attenuating immunosenescence: a review. Biogerontology 14, 9–20.
| Psychoneuroendocrine interventions aimed at attenuating immunosenescence: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1yqtrw%3D&md5=44e7181c9608e22a82925dbcf64a9f6cCAS | 23283592PubMed |
Benedetti, S., Tagliamonte, M. C., Catalani, S., Primiterra, M., Canestrari, F., De Stefani, S., Palini, S., and Bulletti, C. (2012). Differences in blood and semen oxidative status in fertile and infertile men, and their relationship with sperm quality. Reprod. Biomed. Online 25, 300–306.
| Differences in blood and semen oxidative status in fertile and infertile men, and their relationship with sperm quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhtlait73K&md5=09688b92a5e4023ae1a67bcece45282eCAS | 22818093PubMed |
Benzie, I. F., and Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal. Biochem. 239, 70–76.
| The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFCmt7Y%3D&md5=4f019817699ee1db77deac1151f47faaCAS | 8660627PubMed |
Cooper, T. G., Noonan, E., Von Eckardstein, S., Auger, J., Baker, H. W., Behre, H. M., Haugen, T. B., Kruger, T., Wang, C., Mbizvo, M. T., and Vogelsong, K. M. (2010). World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 16, 231–245.
| World Health Organization reference values for human semen characteristics.Crossref | GoogleScholarGoogle Scholar | 19934213PubMed |
Cruz, M. H., Leal, C. L., Cruz, J. F., Tan, D. X., and Reiter, R. J. (2014). Role of melatonin in production and preservation of gametes and embryos: a brief review. Anim. Reprod. Sci. 145, 150–160.
| Role of melatonin in production and preservation of gametes and embryos: a brief review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFCksb8%3D&md5=196eef7ad164e8b858ec9385a656586fCAS | 24559971PubMed |
Espino, J., Bejarano, I., Ortiz, A., Lozano, G. M., García, J. F., Pariente, J. A., and Rodríguez, A. B. (2010). Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa. Fertil. Steril. 94, 1915–1917.
| Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1SrtLzO&md5=2d26c9c28b53f3a1622c1ca319bf040dCAS | 20152967PubMed |
Espino, J., Ortiz, Á., Bejarano, I., Lozano, G. M., Monllor, F., García, J. F., Rodríguez, A. B., and Pariente, J. A. (2011). Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways. Fertil. Steril. 95, 2290–2296.
| Melatonin protects human spermatozoa from apoptosis via melatonin receptor- and extracellular signal-regulated kinase-mediated pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsFWns7g%3D&md5=5a7c7001299cd074e992e2b080a03b9bCAS | 21497337PubMed |
Frączek, M., and Kurpisz, M. (2007). Inflammatory mediators exert toxic effects of oxidative stress on human spermatozoa. J. Androl. 28, 325–333.
| Inflammatory mediators exert toxic effects of oxidative stress on human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 17079739PubMed |
Fujinoki, M. (2008). Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 136, 533–541.
| Melatonin-enhanced hyperactivation of hamster sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVCjtrnK&md5=af6d6c59e651f7e69851e35568d17b7fCAS | 18715981PubMed |
Galano, A., Tan, D. X., and Reiter, R. J. (2011). Melatonin as a natural ally against oxidative stress: a physicochemical examination. J. Pineal Res. 51, 1–16.
| Melatonin as a natural ally against oxidative stress: a physicochemical examination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpslKqsro%3D&md5=a62779380a8b24bdb67e2c0d7f1937e2CAS | 21752095PubMed |
Galano, A., Tan, D. X., and Reiter, R. J. (2013). On the free-radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J. Pineal Res. 54, 245–257.
| On the free-radical scavenging activities of melatonin’s metabolites, AFMK and AMK.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkslSks7g%3D&md5=3b11899d0ceb762138e741284bafa2deCAS | 22998574PubMed |
Gharagozloo, P., and Aitken, R. J. (2011). The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum. Reprod. 26, 1628–1640.
| The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy.Crossref | GoogleScholarGoogle Scholar | 21546386PubMed |
Hardeland, R. (2005). Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine 27, 119–130.
| Antioxidative protection by melatonin: multiplicity of mechanisms from radical detoxification to radical avoidance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFansLnM&md5=03c12039c53bf7e7076e52d8b87b6047CAS | 16217125PubMed |
Hardeland, R. (2013). Melatonin and the theories of ageing: a critical appraisal of melatonin’s role in anti-ageing mechanisms. J. Pineal Res. 55, 325–356.
| 1:CAS:528:DC%2BC3sXhs1SlsrjN&md5=60d49187e3e792fadaed41ee6b341a4fCAS | 24112071PubMed |
Hsieh, Y. Y., Sun, Y. L., Chang, C. C., Lee, Y. S., Tsai, H. D., and Lin, C. S. (2002). Superoxide dismutase activities of spermatozoa and seminal plasma are not correlated with male infertility. J. Clin. Lab. Anal. 16, 127–131.
| Superoxide dismutase activities of spermatozoa and seminal plasma are not correlated with male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslSksb0%3D&md5=db36a886e24328dbdd35e8158a70cecdCAS | 11968048PubMed |
Ji, Y. L., Wang, H., Meng, C., Zhao, X. F., Zhang, C., Zhang, Y., Zhao, M., Chen, Y. H., Meng, X. H., and Xu, D. X. (2012). Melatonin alleviates cadmium-induced cellular stress and germ-cell apoptosis in testes. J. Pineal Res. 52, 71–79.
| Melatonin alleviates cadmium-induced cellular stress and germ-cell apoptosis in testes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12nsLnP&md5=38b0395d1356bd20f1d4b8c102d3b1acCAS | 21793897PubMed |
Lee, R., Margaritis, M., Channon, K. M., and Antoniades, C. (2012). Evaluating oxidative stress in human cardiovascular disease: methodological aspects and considerations. Curr. Med. Chem. 19, 2504–2520.
| Evaluating oxidative stress in human cardiovascular disease: methodological aspects and considerations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XoslShs7c%3D&md5=2f0a1842bbc7d8965311f1ee35de7df6CAS | 22489713PubMed |
Makker, K., Agarwal, A., and Sharma, R. (2009). Oxidative stress and male infertility. Indian J. Med. Res. 129, 357–367.
| 1:CAS:528:DC%2BD1MXovFSntr0%3D&md5=e74f6b5bd6fd649b61f8a5fd8532a35bCAS | 19535829PubMed |
Mora-Esteves, C., and Shin, D. (2013). Nutrient supplementation: improving male fertility four-fold. Semin. Reprod. Med. 31, 293–300.
| Nutrient supplementation: improving male fertility four-fold.Crossref | GoogleScholarGoogle Scholar | 23775385PubMed |
Ortiz, A., Espino, J., Bejarano, I., Lozano, G. M., Monllor, F., García, J. F., Pariente, J. A., and Rodríguez, A. B. (2011). High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure to melatonin improves aspects of sperm motility. J. Pineal Res. 50, 132–139.
| 1:CAS:528:DC%2BC3MXivF2ksrg%3D&md5=97d24a247507d8c72601bf919d3d869eCAS | 20964711PubMed |
Pahune, P. P., Choudhari, A. R., and Muley, P. A. (2013). The total antioxidant power of semen and its correlation with the fertility potential of human male subjects. J. Clin. Diagn. Res. 7, 991–995.
| The total antioxidant power of semen and its correlation with the fertility potential of human male subjects.Crossref | GoogleScholarGoogle Scholar | 23905087PubMed |
Pasqualotto, F. F., Sharma, R. K., Potts, J. M., Nelson, D. R., Thomas, A. J., and Agarwal, A. (2000). Seminal oxidative stress in patients with chronic prostatitis. Urology 55, 881–885.
| Seminal oxidative stress in patients with chronic prostatitis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czgtFSmuw%3D%3D&md5=2b781d7e6f26a3370e55cc516cf77657CAS | 10840100PubMed |
Pieri, C., Marra, M., Moroni, F., Recchioni, R., and Marcheselli, F. (1994). Melatonin: a peroxyl radical scavenger more effective than vitamin E. Life Sci. 55, PL271–PL276.
| Melatonin: a peroxyl radical scavenger more effective than vitamin E.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1amu7c%3D&md5=cd9f778a6c6ebed5661015df627193a3CAS | 7934611PubMed |
Poeggeler, B., Saarela, S., Reiter, R. J., Tan, D. X., Chen, L. D., and Manchester, L. C. (1994). Melatonin – a highly potent endogenous radical scavenger and electron donor: new aspects of the oxidation chemistry of this indole accessed in vitro. Ann. N. Y. Acad. Sci. 738, 419–420.
| Melatonin – a highly potent endogenous radical scavenger and electron donor: new aspects of the oxidation chemistry of this indole accessed in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvV2ksLg%3D&md5=d464e9e0b12b83e1fef765fd796e0f78CAS | 7832450PubMed |
Pohanka, M. (2011). Alzheimer’s disease and related neurodegenerative disorders: implication and counteracting of melatonin. J. Appl. Biomed. 9, 185–196.
| Alzheimer’s disease and related neurodegenerative disorders: implication and counteracting of melatonin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Sgurg%3D&md5=673a15ace5034f007a0a87bd63a23d9cCAS |
Reiter, R. J., Tan, D. X., Manchester, L. C., Paredes, S. D., Mayo, J. C., and Sainz, R. M. (2009). Melatonin and reproduction revisited. Biol. Reprod. 81, 445–456.
| Melatonin and reproduction revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu77F&md5=b950b5d39d6c70db00559b470eefe68dCAS | 19439728PubMed |
Reiter, R. J., Manchester, L. C., and Tan, D. X. (2010). Neurotoxins: free-radical mechanisms and melatonin protection. Curr. Neuropharmacol. 8, 194–210.
| Neurotoxins: free-radical mechanisms and melatonin protection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2mtrvI&md5=66e4821e842683784f9306a37acb133aCAS | 21358970PubMed |
Reiter, R. J., Rosales-Corral, S. A., Manchester, L. C., and Tan, D. X. (2013). Peripheral reproductive organ health and melatonin: ready for prime time. Int. J. Mol. Sci. 14, 7231–7272.
| Peripheral reproductive organ health and melatonin: ready for prime time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtFWktrw%3D&md5=ddddc800c3b23399582699cb71409527CAS | 23549263PubMed |
Rossi, S. P., Windschuettl, S., Matzkin, M. E., Terradas, C., Ponzio, R., Puigdomenech, E., Levalle, O., Calandra, R. S., Mayerhofer, A., and Frungieri, M. B. (2014). Melatonin in testes of infertile men: evidence for anti-proliferative and anti-oxidant effects on local macrophage and mast cell populations. Andrology 2, 436–449.
| Melatonin in testes of infertile men: evidence for anti-proliferative and anti-oxidant effects on local macrophage and mast cell populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvF2ks7g%3D&md5=cdda4dc6e33787447bc87d669ae88a00CAS | 24659586PubMed |
Saalu, L. C. (2010). The incriminating role of reactive oxygen species in idiopathic male infertility: an evidence-based evaluation. Pak. J. Biol. Sci. 13, 413–422.
| The incriminating role of reactive oxygen species in idiopathic male infertility: an evidence-based evaluation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OlsrrP&md5=111a44f697c5f8abbd92d6907ddf6d04CAS | 20973394PubMed |
Saleh, R. A., Agarwal, A., Sharma, R. K., Nelson, D. R., and Thomas, A. J. (2002). Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study. Fertil. Steril. 78, 491–499.
| Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study.Crossref | GoogleScholarGoogle Scholar | 12215323PubMed |
Sanocka, D., Miesel, R., Jedrzejczak, P., and Kurpisz, M. K. (1996). Oxidative stress and male infertility. J. Androl. 17, 449–454.
| 1:STN:280:DyaK2s%2FksVKgug%3D%3D&md5=0ad8dbb591e513d44db6a246f3e8e5c5CAS | 8889709PubMed |
Sanocka, D., Miesel, R., Jedrzejczak, P., Chełmonska-Soyta, A. C., and Kurpisz, M. (1997). Effect of reactive oxygen species and the activity of antioxidant systems on human semen; association with male infertility. Int. J. Androl. 20, 255–264.
| Effect of reactive oxygen species and the activity of antioxidant systems on human semen; association with male infertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvmtlSjsw%3D%3D&md5=a0bc8e0b623036dea1a7ea7e62d42b3eCAS | 16130269PubMed |
Sarabia, L., Maurer, I., and Bustos-Obregón, E. (2009). Melatonin prevents damage elicited by the organophosphorous pesticide diazinon on the mouse testis. Ecotoxicol. Environ. Saf. 72, 938–942.
| Melatonin prevents damage elicited by the organophosphorous pesticide diazinon on the mouse testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Chtrw%3D&md5=9b20ecf0d32b5b5810aca3c95d4d3907CAS | 18565581PubMed |
Semercioz, A., Onur, R., Ogras, S., and Orhan, I. (2003). Effects of melatonin on testicular tissue nitric oxide level and antioxidant enzyme activities in experimentally induced left varicocele. Neuroendocrinol. Lett. 24, 86–90.
| 1:CAS:528:DC%2BD3sXktVOrtLg%3D&md5=b7fcb45aecda861cf311a54ce0c02e35CAS | 12743540PubMed |
Sharma, R., Agarwal, A., Mohanty, G., Du Plessis, S. S., Gopalan, B., Willard, B., Yadav, S. P., and Sabanegh, E. (2013). Proteomic analysis of seminal fluid from men exhibiting oxidative stress. Reprod. Biol. Endocrinol. 11, 85.
| Proteomic analysis of seminal fluid from men exhibiting oxidative stress.Crossref | GoogleScholarGoogle Scholar | 24004880PubMed |
Showell, M. G., Brown, J., Yazdani, A., Stankiewicz, M. T., and Hart, R. J. (2011). Antioxidants for male subfertility. Cochrane Database Syst. Rev. 1, CD007411.
| 21249690PubMed |
Siciliano, L., Tarantino, P., Longobardi, F., Rago, V., De Stefano, C., and Carpino, A. (2001). Impaired seminal antioxidant capacity in human semen with hyperviscosity or oligoasthenozoospermia. J. Androl. 22, 798–803.
| 1:CAS:528:DC%2BD3MXnt1Sqsbk%3D&md5=49ca365c6c01f124b7185c224eea1088CAS | 11545292PubMed |
Stebelová, K., Herichová, I., and Zeman, M. (2007). Diabetes induces changes in melatonin concentrations in peripheral tissues of rat. Neuroendocrinol. Lett. 28, 159–165.
| 17435669PubMed |
Stefulj, J., Hörtner, M., Ghosh, M., Schauenstein, K., Rinner, I., Wölfler, A., Semmler, J., and Liebmann, P. M. (2001). Gene expression of the key enzymes of melatonin synthesis in extrapineal tissues of the rat. J. Pineal Res. 30, 243–247.
| Gene expression of the key enzymes of melatonin synthesis in extrapineal tissues of the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtlSjsrk%3D&md5=2f109daa48d1496c76614e6d752033d6CAS | 11339514PubMed |
Tijmes, M., Pedraza, R., and Valladares, L. (1996). Melatonin in the rat testis: evidence for local synthesis. Steroids 61, 65–68.
| Melatonin in the rat testis: evidence for local synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVGgsrk%3D&md5=8015c4f2b4fdaf01dfcfa1593a37a073CAS | 8750434PubMed |
Tkaczuk-Włach, J., Kankofer, M., and Jakiel, G. (2002). Activity of superoxide dismutase and glutathione peroxidase in human semen in normozoospermia and spermatopathy. Ann. Univ. Mariae Curie Sklodowska Med. 57, 369–375.
| 12898864PubMed |
Vician, M., Zeman, M., Herichová, I., Juráni, M., Blazícek, P., and Matis, P. (1999). Melatonin content in plasma and large intestine of patients with colorectal carcinoma before and after surgery. J. Pineal Res. 27, 164–169.
| Melatonin content in plasma and large intestine of patients with colorectal carcinoma before and after surgery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslars7c%3D&md5=1098e5440741a1d8d4aa55c1b136778cCAS | 10535766PubMed |
Wang, X., Sharma, R. K., Sikka, S. C., Thomas, A. J., Falcone, T., and Agarwal, A. (2003). Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility. Fertil. Steril. 80, 531–535.
| Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility.Crossref | GoogleScholarGoogle Scholar | 12969693PubMed |
WHO (2010) ‘WHO laboratory manual for the examination and processing of human semen 5th edn.’ (WHO Press, World Health Organization: Geneva.)
Witko-Sarsat, V., Friedlander, M., Capeillère-Blandin, C., Nguyen-Khoa, T., Nguyen, A. T., Zingraff, J., Jungers, P., and Descamps-Latscha, B. (1996). Advanced oxidation protein products as a novel marker of oxidative stress in uraemia. Kidney Int. 49, 1304–1313.
| Advanced oxidation protein products as a novel marker of oxidative stress in uraemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xkslagsbs%3D&md5=008209c308861992fab224d08bcd2d1dCAS | 8731095PubMed |
Zegers-Hochschild, F., Adamson, G. D., De Mouzon, J., Ishihara, O., Mansour, R., Nygren, K., Sullivan, E., and Vanderpoel, S. (2009). International Committee for Monitoring Assisted Reproductive Technology; World Health Organization. International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil. Steril. 92, 1520–1524.
| International Committee for Monitoring Assisted Reproductive Technology; World Health Organization. International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology, 2009.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MjivFKqtA%3D%3D&md5=1ee1fa7518aec1ceb02449867f1dc2c1CAS | 19828144PubMed |
Zhang, K., Lv, Z., Jia, X., and Huang, D. (2012). Melatonin prevents testicular damage in hyperlipidaemic mice. Andrologia 44, 230–236.
| Melatonin prevents testicular damage in hyperlipidaemic mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGgurzP&md5=af0fff0d6ffde885f0e1f6f44113172bCAS | 22260292PubMed |
Zini, A., Garrels, K., and Phang, D. (2000). Antioxidant activity in the semen of fertile and infertile men. Urology 55, 922–926.
| Antioxidant activity in the semen of fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czgtFSluw%3D%3D&md5=6b93b95f1940432e5bfd5345ed142328CAS | 10840110PubMed |