Skip to main content

Advertisement

Log in

Comparative Effect of Photobiomodulation on Human Semen Samples Pre- and Post-Cryopreservation

  • Male Reproduction: Original Article
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

The primary objective of this study is to evaluate and to compare the effects of photobiomodulation (PBM) on sperm parameters both before and after cryopreservation. In this regard, 24 freshly ejaculated semen samples from normozoospermic men were included in this study. Each semen sample was randomly divided into three groups (1 ml aliquot for each group): the control group (group one) underwent conventional sperm cryopreservation (n = 24), group two underwent pre-freezing PBM exposure (810 nm, diode laser, and 0.6 J/cm2) (n = 24), and group three underwent post freezing and thawing PBM exposure (n = 24). Indicators of sperm quality, including total sperm motility (TSM), progressive sperm motility (PSM), DNA fragmentation, lipid peroxidation levels, apoptosis-like changes, and gene expression levels of protamine (PRM) 1, PRM2, and adducin 1 alpha (ADD1), were investigated in a blinded style. Due to the beneficial effect of pre-freezing PBM therapy, group 2 exhibited the highest TSM and PSM levels compared to groups 1 and 3. At the same time, DNA fragmentation and lipid peroxidation were significantly reduced in the group 2 compared to the group 1 (p = 0.024 p = 0.016, respectively). Evaluation of apoptotic/necrotic changes revealed that parameters including early apoptosis, dead, and necrotic cells decreased in the group 2 compared to the either groups 1 (p = 0. 008, p = 0. 032, p = 0. 02, respectively) or group 3 (p = 0.037, p = 0.108, p = 0.083). There were no significant differences in the expression levels of PRM1, PRM2, and ADD1 among the study groups. Based on our results, PBM therapy prior to cryopreservation, even in the normal semen samples, plays a significant protective role against cryo-damage by preserving the functional parameters of spermatozoa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

Some more information about statistical analyses were provided, so if needed, we can send as supplementary of data.

Code Availability

All analyses were carried out using SPSS software (version 22 for Windows; SPSS Inc., Chicago, IL, USA).

References

  1. Ravitsky V, Kimmins S. The forgotten men: rising rates of male infertility urgently require new approaches for its prevention, diagnosis and treatment. Biol Reprod. 2019;101(5):872–4.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sinha S. Role of Cryopreservation in Assisted Reproductive Technology (ART). Apollo Medicine. 2009;6(3):212–21.

    Article  Google Scholar 

  3. Di Santo M, Tarozzi N, Nadalini M, Borini A. Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Adv Urol. 2011;2012.

  4. Ezzati M, Shanehbandi D, Hamdi K, Rahbar S, Pashaiasl M. Influence of cryopreservation on structure and function of mammalian spermatozoa: an overview. Cell Tissue Bank. 2020;21(1):1–15.

    Article  PubMed  Google Scholar 

  5. Valcarce DG, Cartón-García F, Herráez MP, Robles V. Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development. Cryobiology. 2013;67(1):84–90.

    Article  CAS  PubMed  Google Scholar 

  6. Card CJ, Anderson EJ, Zamberlan S, Krieger KE, Kaproth M, Sartini BL. Cryopreserved bovine spermatozoal transcript profile as revealed by high-throughput ribonucleic acid sequencing. Biol Reprod. 2013;88(2):49.

    Article  PubMed  Google Scholar 

  7. Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, Guerin JF. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril. 2007;87(1):93–100.

    Article  CAS  PubMed  Google Scholar 

  8. Kopeika J, Thornhill A, Khalaf Y. The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence. Hum Reprod Update. 2015;21(2):209–27.

    Article  CAS  PubMed  Google Scholar 

  9. Kim GY. What should be done for men with sperm DNA fragmentation? Clin Exp Reprod Med. 2018;45(3):101–9.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Dai D-H, Qazi IH, Ran M-X, Liang K, Zhang Y, Zhang M, et al. Exploration of miRNA and mRNA profiles in fresh and frozen-thawed boar sperm by transcriptome and small RNA sequencing. Int J Mol Sci. 2019;20(4):802.

    Article  CAS  PubMed Central  Google Scholar 

  11. Jodar M, Selvaraju S, Sendler E, Diamond MP, Krawetz SA, Network RM. The presence, role and clinical use of spermatozoal RNAs. Hum Reprod Update. 2013;19(6):604–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Amidi F, Pazhohan A, ShabaniNashtaei M, Khodarahmian M, Nekoonam S. The role of antioxidants in sperm freezing: a review. Cell Tissue Bank. 2016;17(4):745–56.

    Article  CAS  PubMed  Google Scholar 

  13. Bucak MN, Ateşşahin A, Varişli O, Yüce A, Tekin N, Akçay A. The influence of trehalose, taurine, cysteamine and hyaluronan on ram semen Microscopic and oxidative stress parameters after freeze-thawing process. Theriogenology. 2007;67(5):1060–7.

    Article  CAS  PubMed  Google Scholar 

  14. Fabozzi G, Starita MF, Rega E, Alteri A, Colicchia A, Piscitelli C, et al. Evaluation of the efficiency of two different freezing media and two different protocols to preserve human spermatozoa from cryoinjury. Int J Reprod Med. 2016;2016.

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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. Reprod Biomed Online. 2018;37(3):327–39.

    Article  CAS  PubMed  Google Scholar 

  16. Hanna R, Agas D, Benedicenti S, Ferrando S, Laus F, Cuteri V, et al. A comparative study between the effectiveness of 980 nm photobiomodulation delivered by hand-piece with Gaussian vs. flat-top profiles on osteoblasts maturation. Front Endocrinol. 2019;10:92.

    Article  Google Scholar 

  17. Zupin L, Pascolo L, Luppi S, Ottaviani G, Crovella S, Ricci G. Photobiomodulation therapy for male infertility. Lasers Med Sci. 2020;35(8):1671–80.

    Article  PubMed  Google Scholar 

  18. Gabel CP, Carroll J, Harrison K. Sperm motility is enhanced by low level laser and light emitting diode photobiomodulation with a dose-dependent response and differential effects in fresh and frozen samples. Laser Ther. 2018;27(2):131–6.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Preece D, Chow KW, Gomez-Godinez V, Gustafson K, Esener S, Ravida N, et al. Red light improves spermatozoa motility and does not induce oxidative DNA damage. Sci Rep. 2017;7:46480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Safian F, Novin MG, Nazarian H, Mofarahe ZS, Abdollahifar M-A, Jajarmi V, et al. Photobiomodulation preconditioned human semen protects sperm cells against detrimental effects of cryopreservation. Cryobiology. 2020;98:239–44.

    Article  PubMed  Google Scholar 

  21. Lu J-C, Huang Y-F, Lü N-Q. WHO Laboratory Manual for the Examination and Processing of Human Semen: its applicability to andrology laboratories in China. Zhonghua Nan Ke Xue. 2010;16(10):867–71.

  22. Dong L, Zhang X, Yang F, Li J, Yu X, Li Y. Effect of oral alpha-lipoic acid (ALA) on the treatment of male infertility: A protocol for systematic review and meta-analysis. Medicine. 2019;98(51).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nabi A, Khalili M, Halvaei I, Roodbari F. Prolonged incubation of processed human spermatozoa will increase DNA fragmentation. Andrologia. 2014;46(4):374–9.

    Article  CAS  PubMed  Google Scholar 

  24. Tavalaee M, Deemeh M, Arbabian M, Nasr-Esfahani M. Density gradient centrifugation before or after magnetic-activated cell sorting: which technique is more useful for clinical sperm selection? J Assist Reprod Genet. 2012;29(1):31–8.

    Article  CAS  PubMed  Google Scholar 

  25. Ostermeier GC, Goodrich RJ, Diamond MP, Dix DJ, Krawetz SA. Toward using stable spermatozoal RNAs for prognostic assessment of male factor fertility. Fertil Steril. 2005;83(6):1687–94.

    Article  PubMed  Google Scholar 

  26. Zeng C, He L, Peng W, Ding L, Tang K, Fang D, et al. Selection of optimal reference genes for quantitative RT-PCR studies of boar spermatozoa cryopreservation. Cryobiology. 2014;68(1):113–21.

    Article  CAS  PubMed  Google Scholar 

  27. Hatef B, Taromchi A, Nejatbakhsh R, Farrokhi A, Shokri S. Supplementation of freezing media with stromal cell-derived factor-1α preserves human sperm from cryodamage. Cryobiology. 2017;79:37–42.

    Article  CAS  PubMed  Google Scholar 

  28. Topraggaleh T, Shahverdi A, Rastegarnia A, Ebrahimi B, Shafiepour V, Sharbatoghli M, et al. Effect of cysteine and glutamine added to extender on post-thaw sperm functional parameters of buffalo bull. Andrologia. 2014;46(7):777–83.

    Article  CAS  PubMed  Google Scholar 

  29. 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. Reprod Biomed Online. 2018;37(3):327–39.

    Article  CAS  PubMed  Google Scholar 

  30. Valcarce D, Cartón-García F, Herráez M, Robles V. Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development. Cryobiology. 2013;67(1):84–90.

    Article  CAS  PubMed  Google Scholar 

  31. García-Herrero S, Garrido N, Martínez-Conejero JA, Remohí J, Pellicer A, Meseguer M. Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI. Reprod Biomed Online. 2011;22(1):25–36.

    Article  PubMed  Google Scholar 

  32. Ortiz-Rodriguez JM, Ortega-Ferrusola C, Gil MC, Martín-Cano FE, Gaitskell-Phillips G, Rodríguez-Martínez H, et al. Transcriptome analysis reveals that fertilization with cryopreserved sperm downregulates genes relevant for early embryo development in the horse. PloS one. 2019;14(6):e0213420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rahiminia T, Hosseini A, Anvari M, Ghasemi-Esmailabad S, Talebi AR. Modern human sperm freezing: effect on DNA, chromatin and acrosome integrity. Taiwan J Obstet Gynecol. 2017;56(4):472–6.

    Article  PubMed  Google Scholar 

  34. Fernandes GH, de Carvalho Pde T, Serra AJ, Crespilho AM, Peron JP, Rossato C, et al. The effect of low-level laser irradiation on sperm motility, and integrity of the plasma membrane and acrosome in cryopreserved bovine sperm. PLoS One. 2015;10(3):e0121487.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Karu TI. Lasers in infertility treatment: irradiation of oocytes and spermatozoa. Photomed Laser Surg. 2012;30(5):239–41.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lubart R, Friedmann H, Sinyakov M, Cohen N, Breitbart H. Changes in calcium transport in mammalian sperm mitochondria and plasma membranes caused by 780 nm irradiation. Lasers Surg Med. 1997;21(5):493–9.

    Article  CAS  PubMed  Google Scholar 

  37. Valcarce DG, Cartón-García F, Riesco MF, Herráez MP, Robles V. Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development. Andrology. 2013;1(5):723–30.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank staffs of Andrology Laboratories of Assisted Reproduction Unit at Tleghani Hospital,Tehran, Iran, for their nice collaboration.

Funding

The present article was financially supported by Menʼs Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences,Tehran, Iran (grant no: 21180).

Author information

Authors and Affiliations

Authors

Contributions

Dr Safian, Dr Ghaffari and Dr. Bayat wrote the proposal and manuscript. Dr Safian performed the methods. Dr Jajarmi, Dr Abdollahifar, Dr Nazarian, Dr Shams Mofarahe, and Dr Chien added some comments. Dr Kazemi and Dr Raee grammatically edited the paper. Dr Safian analyzed statistically the data. Dr Ghaffari did help in some methods.

Corresponding author

Correspondence to Marefat Ghaffari Novin.

Ethics declarations

Ethical Approval and Consent to participate

It was mentioned in materials and methods.

Consent for Publication

It was not applicable.

Conflicts of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 35 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Safian, F., Bayat, M., Jajarmi, V. et al. Comparative Effect of Photobiomodulation on Human Semen Samples Pre- and Post-Cryopreservation. Reprod. Sci. 29, 1463–1470 (2022). https://doi.org/10.1007/s43032-021-00805-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43032-021-00805-x

Keywords

Navigation