Effect of Lepidium meyenii (maca) on testicular function of mice with chemically and physically induced subfertility

Andrologia

Volumn 48, Issue 8, 2016, Pages 927-934

  Valdivia Cuya, M ^a   Yarasca De La Vega, K ^a   Levano Sanchez G ^a   Vasquez Cavero J ^a   Temoche Garcia H ^a   Torres Torres, L ^a   Cruz Ornetta, V ^a  

^a UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS   (Peru)

Author keywords

chemical subfertility (ketoconazole); Lepidium meyenii; physical subfertility (ELF MF); sperm count; sperm motility

Indexed keywords

CYTOCHROME P450; DNA; KETOCONAZOLE; LEPIDIUM MEYENII EXTRACT;

ANDROGEN SYNTHESIS; ANIMAL EXPERIMENT; ARTICLE; CHEMICALLY INDUCED DISORDER; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG EFFICACY; LEPIDIUM; LEPIDIUM MEYENII; MALE; MALE INFERTILITY; MEDICINAL PLANT; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; SPERMATOZOON; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; SUBFERTILITY; TESTIS FUNCTION;

EID: 84988978865     PISSN: 03034569     EISSN: 14390272     Source Type: Journal    
DOI: 10.1111/and.12682     Document Type: Article

References (59)

1. Aitken, R., Buckingham, D., West, K., Wu, F., Zikopoulos, K., & Richardson, D. (1992). Differential contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patientes and fertile donors. Journal of Reproduction and Fertility, 94, 451–462.
2. Akdag, M. Z., Dasdag, S., Uzunlar, A. K., Ulukaya, E., Oral, A. Y., Çelik, N., & Akşen, F. (2013). Can safe and long-term exposure to extremely low frequency (50 Hz) magnetic fields affect apoptosis, reproduction, and oxidative stress? International Journal of Radiation Biology, 89, 1053–1060.
3. Al-Akhras, M. A., Elbetieha, A., Hasan, M. K., Al-Omari, I., Darmani, H., & Albiss, B. (2001). Effects of extremely low frequency magnetic field on fertility of adult male and female rats. Bioelectromagnetics, 22, 340–344.
4. Amaral, A., Lourenço, B., Marques, M., & Ramalho-Santos, J. (2013). Mitochondria functionality and sperm quality. Reproduction, 146, 163–174.
5. Awoniyi, C. A., Reece, M. S., Hurst, B. S., Faber, K. A., Chandrashekar, V., & Schlaff, W. D. (1993). Maintenance of sexual function with testosterone in the gonadotropin-releasing hormone-immunized hypogonadotropic infertile male rat. Biology of Reproduction, 49, 1170–1176.
6. Balick, M. J., & Lee, R. (2002). Maca: From traditional food crop to energy and libido stimulant. Alternative Therapies in Health and Medicine, 8, 96–98.
7. Barassi, N., Benavides, F., & Ceccarelli, A. (1996). Ética en el uso de animales de experimentación. Medicina, 56(5), 1.
8. Berg, D., Büchel, K. H., Plempel, M., & Regel, E. (1986). Antimycotic sterol biosynthesis inhibitors. Trends in Pharmacological Sciences, 7, 233–238.
9. Bernabò, N., Tettamanti, E., Pistilli, M. G., Nardinocchi, D., Berardinelli, P., Mattioli, M., & Barboni, B. (2007). Effects of 50Hz extremely low frequency magnetic field on the morphology and function of boar spermatozoa capacitated in vitro. Theriogenology, 67, 801–815.
10. Bogani, P., Simonini, F., Iriti, M., Rossoni, M., Faoro, F., Poletti, A., & Visioli, F. (2006). Lepidium meyenii (Maca) does not exert direct androgenic activities. Journal of Ethnopharmacology, 104, 415–417.
11. de Bruyn, L., & de Jager, L. (2010). Effect of long-term exposure to a randomly varied 50 Hz power frequency magnetic field on the fertility of the mouse. Electromagnetic Biology and Medicine, 29, 52–61.
12. Bustos-Obregón, E., Yucra, S., & Gonzales, G. F. (2005). Lepidium meyenii (Maca) reduces spermatogenic damage induced by a single dose of malathion in mice. Asian Journal of Andrology, 7, 71–76.
13. Cruz, V., Nuñez, T., Varela, A., Ayala, A., Tafur, J., Luna, L., & Quispe, R. (2012). Diseño e implementación de un sistema de exposición a campos magnéticos de baja frecuencia para ratones de prueba en estudios biológicos. Electronica–UNMSM, 30, 3–8.
14. De Kretser, D. M. (1997). Male infertility. Lancet, 349, 787–790.
15. De Kretser, D. M., & Baker, H. W. (1999). Infertility in men: Recent advances and continuing controversies. Journal of Clinical Endocrinology and Metabolism, 84, 3443–3450.
16. De la Cruz, R. W., & Arroyo, A. J. (2012). Efecto del extracto etanólico de maca (Lepidium meyenii Walp) sobre los niveles de testosterona y el conteo de espermatozoides de ratones machos. Revista Médica Panacea, 2, 2–6.
17. De Vita, R., Cavallo, D., Raganella, L., Eleuteri, P., Grollino, M. G., & Calugi, A. (1995). Effects of 50 Hz magnetic fields on mouse spermatogenesis monitored by flow cytometric analysis. Bioelectromagnetics, 16, 330–334.
18. Duan, W., Liu, C., Wu, H., Chen, C., Zhang, T., Gao, P., Luo, X., Yu, Z., & Zhou, Z. (2014). Effects of exposure to extremely low frequency magnetic fields on spermatogenesis in adult rats. Bioelectromagnetics, 35(1), 58–69.
19. Gonzales, G. F., Cordova, A., Gonzales, C., Chung, A., Vega, K., & Villena, A. (2001). Lepidium meyenii (Maca) improved semen parameters in adult men. Asian Journal of Andrology, 3, 301–304.
20. Gonzales, G. F., Miranda, S., Nieto, J., Fernández, G., Yucra, S., Rubio, J., Yi, P., & Gasco, M. (2005). Red maca (Lepidium meyenii) reduced prostate size in rats. Reproductive Biology and Endocrinology, 3(1), 1–16.
21. Gonzales, G. F., Cordova, A., Vega, K., Chung, A., Villena, A., Góñez, C., & Castillo, S. (2002). Effect of Lepidium meyenii (MACA) on sexual desire and its absent relationship with serum testosterone levels in adult healthy men. Andrologia, 34, 367–372.
22. Gonzales, G., Gasco, M., Cordova, A., Chung, A., Rubio, J., & Villegas, L. (2004). Effect of Lepidium meyenii (Maca) on spermatogenesis in male rats acutely exposed to high altitude (4340 m). Journal of Endocrinology, 180, 87–95.
23. Gonzales, G. F., Miranda, S., Nieto, J., Fernández, G., Yucra, S., Rubio, J., … & Gasco, M. (2005). Red maca (Lepidium meyenii) reduced prostate size in rats. Reproductive Biology and Endocrinology, 3, 5. DOI: 10.1186/1477-7827-3-5
24. Gonzales, G. F., Nieto, J., Rubio, J., & Gasco, M. (2006). Effect of Black maca (Lepidium meyenii) on one spermatogenic cycle in rats. Andrologia, 38, 166–172.
25. Gye, M. C., & Park, C. J. (2012). Effect of electromagnetic field exposure on the reproductive system. Clinical and Experimental Reproductive Medicine, 39, 1–9.
26. Heckman, W. R., Kane, B. R., Pakyz, R. E., & Cosentino, M. J. (1992). The effect of ketoconazole on endocrine and reproductive parameters in male mice and rats. Journal of Andrology, 13, 191–198.
27. Heredia-Rojas, J. A., Caballero-Hernandez, D. E., Rodriguez-de la Fuente, A. O., Ramos-Alfano, G., & Rodriguez-Flores, L. E. (2004). Lack of alterations on meiotic chromosomes and morphological characteristics of male germ cells in mice exposed to a 60 Hz and 2.0 mT magnetic field. Bioelectromagnetics, 25, 63–68.
28. Hull, M. G., Glazener, C. M., Kelly, N. J., Conway, D. I., Foster, P. A., Hinton, R. A., … Desai, K. M. (1985). Population study of causes, treatment, and outcome of infertility. British Medical Journal, 291, 1693–1697.
29. ICNIRP - International Commission on Non-Ionizing Radiation Protection. (2003). Exposure to static and low frequency electromagnetic fields, biological effects and health consequences (0–100 kHz). Bernhardt JH et al., eds. (pp. 500). Oberschleissheim: International Commission on Non-ionizing Radiation Protection.
30. ICNIRP (2010). Guidelines for limiting exposure to time-varying electric and magnetic fields (1 Hz–100 KHz). Health Physics, 99, 818–836.
31. IEEE (1992) Standards Coordinating Committee 28, on Non-Ionizing Radiation Hazards. 3 kHz to 300 GHz. IEEE.
32. IEEE (2002). Standard for safety levels with respect to human exposure to electromagnetic fields, 0–3 kHz. New York: IEEE.
33. Iorio, R., Scrimaglio, R., Rantucci, E., Monache, S. D., Di Gaetano, A., Finetti, N., … Colonna, R. (2007). A preliminary study of oscillating electromagnetic field effects on human spermatozoon motility. Bioelectromagnetics, 28(1), 72–75.
34. Iorio, R., Scrimaglio, R., Rantucci, E., Monache, S. D., Di Gaetano, A., Finetti, N., … & Colonna, R. (2007). A preliminary study of oscillating electromagnetic field effects on human spermatozoon motility. Bioelectromagnetics, 28, 72–75.
35. Joshi, S. C., Jain, G. C., & Lata, M. (1993). Effects of ketoconazole (an imidazole antifugal agent) on the fertility and reproductive function of male mice. Acta Europaea Fertilitatis, 25(1), 55–58.
36. Kaya, M., Boleken, M. E., Zeyrek, F., Ozardali, I., Kanmaz, T., Erel, O., & Yücesan, S. (2006). Oxidative and antioxidative status in the testes of rats with acute epididymitis. Urologia Internationalis, 76, 353–358.
37. Kim, H. S., Park, B. J., Jang, H. J., Ipper, N. S., Kim, S. H., Kim, Y. J., … Kim, Y. W. (2014). Continuous exposure to 60 Hz magnetic fields induces duration-and dose-dependent apoptosis of testicular germ cells. Bioelectromagnetics, 35, 100–107.
38. Kowalczuk, C. I., Robbins, L., Thomas, J. M., & Saunders, R. D. (1995). Dominant lethal studies in male mice after exposure to a 50 Hz magnetic field. Mutation Research, 328, 229–237.
39. Lee, J. S., Ahn, S. S., Jung, K. C., Kim, Y. W., & Lee, S. K. (2004). Effects of 60 Hz electromagnetic field exposure on testicular germ cell apoptosis in mice. Asian Journal of Andrology, 6, 29–34.
40. Leifke, E., & Nieschlag, E. (1995). Male infertility treatment in the light of evidence-based medicine. Andrologia, 28, 23–30.
41. Loo, D. T. (2011). In situ detection of apoptosis by the TUNEL assay: An overview of techniques. Methods in Molecular Biology, 682, 3–13.
42. Lundsberg, L. S., Bracken, M. B., & Belanger, K. (1995). Occupationally related magnetic field exposure and male subfertility. Fertility and Sterility, 63, 384–391.
43. Melnikovova, I., Fait, T., Kolarova, M., Fernandez, E. C., & Milella, L. (2015). Effect of Lepidium meyenii Walp. on semen parameters and serum hormone levels in healthy adult men: A double-blind, randomized, placebo-controlled pilot study. Evidence-Based Complementary and Alternative Medicine: eCAM, Article ID 324369.
44. Mundy, A. J., Ryder, T. A., & Edmonds, D. K. (1995). Asthenozoospermia and the human sperm mid-piece. Human Reproduction, 10, 116–119.
45. Olfert, E. D., Cross, B. M., & McWilliam, A. A. (Eds.) (1993). Guide to the care and use of experimental animals, Vol. 1 (2) (pp. 298). Ottawa, ON: Canadian Council on Animal Care.
46. Pelliccione, F., Micillo, A., Cordeschi, G., D'Angeli, A., Necozione, S., Gandini, L., … Francavilla, S. (2011). Altered ultrastructure of mitocondrial membranes is strongly associated with unexplained asthenozoospermia. Fertility and Sterility, 95, 641–646.
47. Qi, G., Zuo, X., Zhou, L., Aoki, E., Okamula, A., Watanebe, M., … Shimamoto, F. (2015). Effects of extremely low-frequency electromagnetic fields (ELF-EMF) exposure on B6C3F1 mice. Environmental Health and Preventive Medicine, 20, 287–293.
48. Quispe, J., Valle-Campos, A., Ulloa, G., Rodriguez, L., Granados, E., Limaymanta, O., … Valdivia, M. (2015) In vitro effect of extremely low frequency magnetic field on the sperm motility of Alpacas: A preliminary study (Abstract). The Annual Meeting of Bioelectromagnetics Society European Bioelectromagnetics Association-BioEM, pp. 199–203.
49. Roychoudhury, S., Jedlicka, J., Parkanyi, V., Rafay, J., Ondruska, L., Massanyi, P., & Bulla, J. (2009). Influence of a 50 hz extra low frequency electromagnetic field on spermatozoa motility and fertilization rates in rabbits. Journal of Environmental Science and Health Part A, 44(10), 1041–1047.
50. Ruiz-Pesini, E., Diez, C., Lapena, A., Perez-Martos, A., Montoya, J., Alvarez, E., … Lopez-Perez, M. (1998). Correlation of sperm motility with mitocondrial enzymatic activities. Clinical Chemistry, 44, 1616–1620.
51. Ryan, B. M., Symanski, R. R., Pomeranz, L. E., Johnson, T. R., Gauger, J. R., & McCormick, D. L. (1999). Multigeneration reproductive toxicity assessment of 60-Hz magnetic fields using a continuous breeding protocol in rats. Teratology, 59, 156–162.
52. Saadeldin, I. M., Fadel, A. M., Hamada, M. M. Z., & El-Badry, A. A. (2011). Effects of exposure to 50 Hz, 1 Gauss magnetic field on reproductive traits in male albino rats. Acta Veterinaria Brno, 80, 107–111.
53. Saki, G., Rahim, F., & Dahaz, S. (2010). Effect of supplementation of zinc on count, motility and in vitro fertilization capacity of spermatozoa of magnetic field exposed rats. Journal of Biological Sciences, 10, 174–177.
54. Shin, J. H., Moon, H. J., Kim, T. S., Kang, I. H., Ki, H. Y., Choi, K. S., & Han, S. Y. (2006). Repeated 28-day oral toxicity study of vinclozolin in rats based on the draft protocol for the “Enhanced OECD Test Guideline No. 407” to detect endocrine effects. Archives of Toxicology, 80, 547–554.
55. Stewart, I. (1998). Epidemiology and etiology of male infertility. Human Reproduction, 13, 33–44.
56. Wolf, F. I., Torsello, A., Tedesco, B., Fasanella, S., Boninsegna, A., D'Ascenzo, M, &Cittadini,A. (2005). 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: Possible involvement of a redox mechanism. Biochimica et Biophysica Acta, 1743, 120–129.
57. World Health Organization (2007). Environmental Health Criteria 238. Extremely low frequency (ELF) fields. Geneva: World Health Organization.
58. World Health Organization (2010). Laboratory manual for the examination and processing of human semen, 5th ed. Cambridge: Cambridge University.
59. Zheng, B. L., He, K., Khim, C. H., Rogers, L., Shao, Y., Huang, Z. Y., … Zheng, Q. Y. (2000). Effect of a lipidic extract from Lepidium meyenii on sexual behavior in mice and rats. Urology, 55, 598–602.