Static magnetic field can ameliorate detrimental effects of cryopreservation on human spermatozoa

Campo magnético estático puede mejorar los efectos perjudiciales de la criopreservación en espermatozoides humanos

This study aims to improve the freezing-thawing process of human sperm using a static magnetic field. The study included 25 normozoospermic human samples. After an initial evaluation of sperm parameters, samples were prepared by the direct swim-up method. Before freezing, sperm motility, viability, morphology, acrosome reaction and DNA fragmentation rate were assessed. The samples were divided into 4 groups: 0, 1, 5 and 10 mT, and each group was frozen by the rapid freezing method. After thawing, the parameters were re-evaluated and compared between groups. Sperm motility decreased significantly during cryopreservation in all groups. The static magnetic field did not protect against decreased progressive motility after freezing, but the total sperm motility was significantly higher in the 10 mT group compared to the other groups. Sperm viability was higher in the 10 mT group than in the other groups. There was no significant difference in the rate of normal sperm morphology after freezing. The rate of spermatozoa with intact acrosome decreased after freeze-thawing, and the static magnetic field did not protect against the acrosome reaction. The rate of DNA integrity was significantly higher in the 10 mT group compared to the other groups. A static magnetic field with an intensity of 10 mT improved sperm viability and DNA integrity compared to other groups. However, it did not provide significant protection against decreased sperm motility or acrosome reaction.

Resumen

Este estudio tiene como objetivo mejorar el proceso de congelación-descongelación de los espermatozoides humanos mediante un campo magnético estático. El estudio incluyó 25 muestras humanas normozoospérmicas. Tras una evaluación inicial de los parámetros espermáticos, las muestras se prepararon mediante el método de natación directa. Antes de la congelación, se evaluaron la motilidad, la viabilidad, la morfología, la reacción acrosómica y la tasa de fragmentación del DNA de los espermatozoides. Las muestras se dividieron en 4 grupos: 0, 1, 5 y 10 mT, y cada grupo se congeló mediante el método de congelación rápida. Tras la descongelación, los parámetros se reevaluaron y se compararon entre los grupos. La motilidad de los espermatozoides disminuyó significativamente durante la criopreservación en todos los grupos. El campo magnético estático no protegió contra la disminución progresiva de la motilidad después de la congelación, pero la motilidad total de los espermatozoides fue significativamente mayor en el grupo de 10 mT en comparación con los demás grupos. La viabilidad de los espermatozoides fue mayor en el grupo de 10 mT que en los demás grupos. No hubo diferencias significativas en la tasa de morfología normal de los espermatozoides después de la congelación. La tasa de espermatozoides con acrosoma intacto disminuyó después de la congelación-descongelación, y el campo magnético estático no protegió contra la reacción acrosómica. La tasa de integridad del DNA fue significativamente mayor en el grupo de 10 mT en comparación con los otros grupos. Un campo magnético estático con una intensidad de 10 mT mejoró la viabilidad de los espermatozoides y la integridad del DNA en comparación con otros grupos. Sin embargo, no proporcionó una protección significativa contra la disminución de la motilidad de los espermatozoides o la reacción acrosómica.

Rapid freezing; Sperm cells; Cryoinjury; DNA integrity; Acrosome reaction

Palabras Clave

Congelación rápida; Espermatozoides; Criolesión; Integridad del DNA; Reacción acrosómica

[1] Chen L, Dong Z, Chen X. Fertility preservation in pediatric healthcare: a review. Frontiers in Endocrinology. 2023; 14: 141147898.

[2] Bahmyari R, Zare M, Sharma R, Agarwal A, Halvaei I. The efficacy of antioxidants in sperm parameters and production of reactive oxygen species levels during the freeze‐thaw process: a systematic review and meta‐analysis. Andrologia. 2020; 52: e13514.

[3] Banihani SA, Alawneh RF. Human semen samples with high antioxidant reservoir may exhibit lower post-cryopreservation recovery of sperm motility. Biomolecules. 2019; 9: 111.

[4] Hezavehei M, Sharafi M, Kouchesfahani HM, Henkel R, Agarwal A, Esmaeili V, et al. Sperm cryopreservation: a review on current molecular cryobiology and advanced approaches. Reproductive BioMedicine Online. 2018; 37: 327–339.

[5] Alipour M, Hajipour-Verdom B, Javan M, Abdolmaleki P. Static and electromagnetic fields differently affect proliferation and cell death through acid enhancement of ROS generation in mesenchymal stem cells. Radiation Research. 2022; 198: 384–395.

[6] Yan Z, Sun T, Tan W, Wang Z, Yan J, Miao J, et al. Magnetic field boosts the transmembrane transport efficiency of magnesium ions from PLLA bone scaffold. Small. 2023; 19: e1301426.

[7] Wu H, Li C, Masood M, Zhang Z, González-Almela E, Castells-Garcia A, et al. Static magnetic fields regulate T-type calcium ion channels and mediate mesenchymal stem cells proliferation. Cells. 2022; 11: 2460.

[8] Albuquerque WWC, Costa RMPB, Fernandes TDSE, Porto ALF. Evidences of the static magnetic field influence on cellular systems. Progress in Biophysics and Molecular Biology. 2016; 121: 16–28.

[9] Lin C, Chang W, Lee S, Feng S, Lin C, Fan K, et al. Influence of a static magnetic field on the slow freezing of human erythrocytes. International Journal of Radiation Biology. 2013; 89: 51–56.

[10] Lin CY, Wei PL, Chang WJ, Huang YK, Feng SW, Lin CT, et al. Slow freezing coupled static magnetic field exposure enhances cryopreservative efficiency—a study on human erythrocytes. PLOS ONE. 2013; 8: e58988.

[11] Tablado L, Pérez-Sánchez F, Núñez J, Núñez M, Soler C. Effects of exposure to static magnetic fields on the morphology and morphometry of mouse epididymal sperm. Bioelectromagnetics. 1998; 19: 377–383.

[12] Emura R, Ashida N, Higashi T, Takeuchi T. Orientation of bull sperms in static magnetic fields. Bioelectromagnetics. 2001; 22: 60–65.

[13] Formicki K, Szulc J, Korzelecka‐Orkisz A, Tański A, Kurzydłowski J, Grzonka J, et al. The effect of a magnetic field on trout (Salmo trutta Linnaeus, 1758) sperm motility parameters and fertilisation rate. Journal of Applied Ichthyology. 2015; 31: 136–146.

[14] Formicki K, Szulc J, Taňski A, Korzelecka-Orkisz A, Witkowski A, Kwiatkowski P. The effect of static magnetic field on Danube huchen, Hucho hucho (L.) sperm motility parameters. Archives of Polish Fisheries. 2013; 21: 189–197.

[15] Kazemein Jasemi VS, Samadi F, Eimani H, Hasani S, Fathi R, Shahverdi A, et al. Function of vitrified mouse ovaries tissue under static magnetic field after autotransplantation. Veterinary Research Forum. 2017; 8: 243–249.

[16] Jasmi VK, Samadi F, Eimani H, Hasani S, Fathi R, Shahverdi A. Follicle development in grafted mouse ovaries after vitrification processes under static magnetic field. CryoLetters. 2017; 38: 166–177.

[17] Kazemein Jasemi VS, Samadi F, Eimani H, Hasani S, Fathi R, Shahverdi A. Comparison of allotransplantation of fresh and vitrified mouse ovaries to the testicular tissue under influence of the static magnetic field. Cell Journal. 2017; 19: 492–505.

[18] WHO. WHO laboratory manual for the examination and processing of human semen. 5th edn. Geneva, Switzerland: World Health Organization. 2010.

[19] Hajipour Verdom B, Abdolmaleki P, Behmanesh M. The static magnetic field remotely boosts the efficiency of doxorubicin through modulating ROS behaviors. Scientific Reports. 2018; 8: 990.

[20] Talbot P, Chacon RS. A triple‐stain technique for evaluating normal acrosome reactions of human sperm. Journal of Experimental Zoology. 1981; 215: 201–208.

[21] Feyzmanesh S, Halvaei I, Baheiraei N. Alginate effects on human sperm parameters during freezing and thawing: a prospective study. Cell Journal. 2022; 24: 417–423.

[22] Baniasadi F, Hajiaghalou S, Shahverdi A, Pirhajati V, Fathi R. Static magnetic field halves cryoinjuries of vitrified mouse COCs, improves their functions and modulates pluripotency of derived blastocysts. Theriogenology. 2021; 163: 31–42.

[23] Toledo EJL, Ramalho TC, Magriotis ZM. Influence of magnetic field on physical-chemical properties of the liquid water: insights from experimental and theoretical models. Journal of Molecular Structure. 2008; 888: 409–415.

[24] Dini L, Abbro L. Bioeffects of moderate-intensity static magnetic fields on cell cultures. Micron. 2005; 36: 195–217.

[25] Wowk B. Electric and magnetic fields in cryopreservation. Cryobiology. 2012; 64: 301–303.

[26] Ghafelebashi M.S MP, Shahverdi A.H, Doranian D, Sabaghian, M MS. Effect of static magnetic field on male sperm parameters. Modares Journal of Biotechnology. 2020; 11: 279–285.

[27] Barnes FS, Greenebaum B. Biological and medical aspects of electromagnetic fields. 3rd edn. CRC press: Boca Raton. 2007.

[28] Rosen AD. Mechanism of action of moderate-intensity static magnetic fields on biological systems. Cell Biochemistry and Biophysics. 2003; 39: 163–173.

[29] Kirschvink J. Magnetite-based magnetoreception. Current Opinion in Neurobiology. 2001; 11: 462–467.

[30] Blesbois E, Grasseau I, Seigneurin F. Membrane fluidity and the ability of domestic bird spermatozoa to survive cryopreservation. Reproduction. 2005; 129: 371–378.

[31] Lo Y, Pan Y, Lin C, Chang W, Huang H. Static magnetic field increases survival rate of thawed RBCs frozen in DMSO-free solution. Journal of Medical and Biological Engineering. 2017; 37: 157–161.

[32] Khodarahmi I, Mobasheri H, Firouzi M. The effect of 2.1 T static magnetic field on astrocyte viability and morphology. Magnetic Resonance Imaging. 2010; 28: 903–909.

[33] Wójcik-Piotrowicz K, Kaszuba-Zwoińska J, Rokita E, Thor P. Cell viability modulation through changes of Ca2+-dependent signalling pathways. Progress in Biophysics and Molecular Biology. 2016; 121: 45–53.

[34] Ghodbane S, Lahbib A, Sakly M, Abdelmelek H. Bioeffects of static magnetic fields: oxidative stress, genotoxic effects, and cancer studies. BioMed Research International. 2013; 2013: 602987.

[35] Teodori L, Giovanetti A, Albertini MC, Rocchi M, Perniconi B, Valente MG, et al. Static magnetic fields modulate X-ray-induced DNA damage in human glioblastoma primary cells. Journal of Radiation Research. 2014; 55: 218–227.

[36] Miyakoshi J. Effects of static magnetic fields at the cellular level. Progress in Biophysics and Molecular Biology. 2005; 87: 213–223.