Lasers in Medical Science

, Volume 31, Issue 4, pp 695–704 | Cite as

Low-level laser therapy to recovery testicular degeneration in rams: effects on seminal characteristics, scrotal temperature, plasma testosterone concentration, and testes histopathology

  • Maíra Bianchi Rodrigues Alves
  • Rubens Paes de Arruda
  • Leonardo Batissaco
  • Shirley Andrea Florez-Rodriguez
  • Bruna Marcele Martins de Oliveira
  • Mariana Andrade Torres
  • Gisele Mouro Ravagnani
  • Renata Lançoni
  • Tamie Guibu de Almeida
  • Vanessa Martins Storillo
  • Vinicius Silva Vellone
  • Celso Rodrigues Franci
  • Helder Esteves Thomé
  • Carolina Luz Canella
  • André Furugen Cesar De Andrade
  • Eneiva Carla Carvalho Celeghini
Original Article

Abstract

The aim of this study was to investigate the efficiency of low-level laser therapy (LLLT) to recovery testicular degeneration in rams. In the first study, rams were induced to testicular degeneration by scrotal insulation, and then, they were treated using LLLT at 28 J/cm2 (INS28) or 56 J/cm2 (INS56) energy densities. Sperm kinetics, morphology, and membranes integrity as well as proportion of lumen area in seminiferous tubule were assessed. In the second study, rams were submitted or not to scrotal insulation and treated or not by the best protocol of LLLT defined by experiment 1 (INS28). In this study were evaluated sperm kinetics, morphology, membranes integrity, ROS production, and DNA integrity. Testosterone serum concentration and proportion of lumen area in seminiferous tubule were also analyzed. Insulation was effective in promoting sperm injuries in both experiments. Biostimulatory effect was observed in experiment 1: INS28 presented smaller proportion of lumen area (P = 0.0001) and less degeneration degree (P = 0.0002). However, in experiment 2, there was no difference between the groups (P = 0.17). In addition, LLLT did not improve sperm quality, and there was a decreasing for total and progressive motility (P = 0.02) and integrity of sperm membranes (P = 0.01) in LLLT-treated groups. Moreover, testosterone concentration was not improved by LLLT (P = 0.37). Stimulation of aerobic phosphorylation by LLLT may have led to a deregulated increase in ROS leading to sperm damages. Thus, LLLT at energy of 28 J/cm2 (808 nm of wavelength and 30 mW of power output) can induce sperm damages and increase the quantity of cells in seminiferous tubule in rams.

Keywords

Biostimulation Sperm Spermatozoa Proliferation Male Infertility 

References

  1. 1.
    Hansen PJ (2009) Effects of heat stress on mammalian reproduction. Philos Trans R Soc Lond B Biol Sci 364:3341–3350. doi:10.1098/rstb.2009.0131 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Setchell BP (1998) The parkes lecture. Heat and the testis. J Reprod Fertil 114:179–194CrossRefPubMedGoogle Scholar
  3. 3.
    Paul C, Teng S, Saunders PTK (2009) A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 919:913–919. doi:10.1095/biolreprod.108.071779 CrossRefGoogle Scholar
  4. 4.
    Paul C, Murray AA, Spears N, Saunders PTK (2008) A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136:73–84. doi:10.1530/REP-08-0036 CrossRefPubMedGoogle Scholar
  5. 5.
    Pérez-Crespo M, Pintado B, Gutiérrez-Adán A (2008) Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol Reprod Dev 75:40–47. doi:10.1002/mrd CrossRefPubMedGoogle Scholar
  6. 6.
    Bicudo SD, Siqueira JB, Meira C (2007) Patologias do sistema reprodutor de touros. Biológico 69:43–48Google Scholar
  7. 7.
    Arruda RP, Silva DF, Alonso MA, Andrade AFC, Nascimento J, Gallego AM et al (2010) Nutraceuticals in reproduction of bulls and stallions. Rev Bras Zootec 39:393–400. doi:10.1590/S1516-35982010001300043 CrossRefGoogle Scholar
  8. 8.
    Navratil L, Kymplova J (2002) Contraindications in noninvasive laser therapy: truth and fiction. J Clin Laser Med Surg 20:341–343CrossRefPubMedGoogle Scholar
  9. 9.
    Barboza CAG, Ginani F, Soares DM, Henriques ÁCG, Freitas RDA (2014) Low-level laser irradiation induces in vitro proliferation of mesenchymal stem cells. Einstein (São Paulo) 12:75–81. doi:10.1590/S1679-45082014AO2824 CrossRefGoogle Scholar
  10. 10.
    Ginani F, Soares DM, Barreto MPEV, Barboza CAG (2015) Effect of low-level laser therapy on mesenchymal stem cell proliferation: a systematic review. Lasers Med Sci. doi:10.1007/s10103-015-1730-9 Google Scholar
  11. 11.
    Soleimani M, Abbasnia E, Fathi M, Sahraei H, Fathi Y, Kaka G (2012) The effects of low-level laser irradiation on differentiation and proliferation of human bone marrow mesenchymal stem cells into neurons and osteoblasts—an in vitro study. Lasers Med Sci 27:423–430. doi:10.1007/s10103-011-0930-1 CrossRefPubMedGoogle Scholar
  12. 12.
    Taha MF, Valojerdi MR (2004) Quantitative and qualitative changes of the seminiferous epithelium induced by Ga. Al. As. (830 nm) laser radiation. Lasers Surg Med 34:352–359. doi:10.1002/lsm.20027 CrossRefPubMedGoogle Scholar
  13. 13.
    Hasan P, Rijadi SA, Purnomo S, Kainama H (1989) The possible application of low reactive level laser therapy in the treatment of male infertility. Laser Ther 1:49–59CrossRefGoogle Scholar
  14. 14.
    Karu T (1987) Photobiological fundamentals of low-power laser therapy. IEEE J Quantum Electron 23:1703–1717. doi:10.1109/JQE.1987.1073236 CrossRefGoogle Scholar
  15. 15.
    Karu T (2003) Cellular mechanisms of low power laser therapy: new questions. Lasers Med Dent 3:79–100Google Scholar
  16. 16.
    Basile RC, Albernaz RM, Pereira MC, Araújo R, Ferraz GC, Queiroz-Neto A (2010) Guia prático de exames termográficos em equinos. Rev Bras Med Equina 6:24–28Google Scholar
  17. 17.
    Bavister D, Lorraine M (1983) Development of preimplantation in a defined embryos of the golden culture medium. Biol Trace Elem Res 28:235–247Google Scholar
  18. 18.
    Blom E (1973) The ultrastructure of some characteristic sperm defects and a proposal for a new classification of the bull spermiogram. Nord Vet Med 25:383–391PubMedGoogle Scholar
  19. 19.
    Celeghini ECC, Nascimento J, Raphael CF, Andrade AFC, Arruda RP (2010) Simultaneous assessment of plasmatic, acrosomal, and mitochondrial membranes in ram sperm by fluorescent probes. Arq Bras Med Vet e Zootec 62:536–543. doi:10.1590/S0102-09352010000300006 CrossRefGoogle Scholar
  20. 20.
    Alves MBR, Andrade AFC, Arruda RP, Batissaco L, Florez-Rodriguez SA, Lançoni R et al (2015) An efficient technique to detect sperm reactive oxygen species: the Cell Rox Deep Red® fluorescent probe. Biochem Physiol Open Access 4:1–5. doi:10.4172/2168-9652.1000157 Google Scholar
  21. 21.
    Brito LFC, Silva AEDF, Barbosa RT, Unanian MM, Kastelic JP (2003) Effects of scrotal insulation on sperm production, semen quality, and testicular echotexture in Bos indicus and Bos indicus × Bos taurus bulls. Anim Reprod Sci 79:1–15. doi:10.1016/S0378-4320(03)00082-4 CrossRefPubMedGoogle Scholar
  22. 22.
    Fernandes CE, Dode MAN, Pereira D, Silva AEDF (2008) Effects of scrotal insulation in Nellore bulls (Bos taurus indicus) on seminal quality and its relationship with in vitro fertilizing ability. Theriogenology 70:1560–1568. doi:10.1016/j.theriogenology.2008.07.005 CrossRefPubMedGoogle Scholar
  23. 23.
    Arman C, Quintana Casares PI, Sanchez-Partida LG, Setchell BP (2006) Ram sperm motility after intermittent scrotal insulation evaluated by manual and computer-assisted methods. Asian J Androl 8:411–418. doi:10.1111/j.1745-7262.2006.00145.x CrossRefPubMedGoogle Scholar
  24. 24.
    Kastelic JP, Cook RB, Coulter GH, Saacke RG (1996) Insulating the scrotal neck affects semen quality and scrotal/testicular temperatures in the bull. Theriogenology 45:935–942CrossRefPubMedGoogle Scholar
  25. 25.
    Mester E, Szende B, Gärtner P (1968) The effect of laser beams on the growth of hair in mice. Radiobiol Radiother 9:621–626Google Scholar
  26. 26.
    Gnyawali SC, Chen Y, Wu F, Bartels KE, Wicksted JP, Liu H, Sen CK, Chen WR (2008) Temperature measurement on tissue surface during laser irradiation. Eng Comput 46:159–168. doi:10.1007/s11517-007-0251-5 Google Scholar
  27. 27.
    Farivar S, Malekshahabi T, Shiari R (2014) Biological effects of low level laser therapy. J Lasers Med Sci 5:58–62PubMedPubMedCentralGoogle Scholar
  28. 28.
    Karu TI (1988) Molecular mechanism of the therapeutic effect of low-intensity laser irradiation. Lasers Life Sci 2:53–74Google Scholar

Copyright information

© Springer-Verlag London 2016

Authors and Affiliations

  • Maíra Bianchi Rodrigues Alves
    • 1
  • Rubens Paes de Arruda
    • 2
  • Leonardo Batissaco
    • 1
  • Shirley Andrea Florez-Rodriguez
    • 1
  • Bruna Marcele Martins de Oliveira
    • 1
  • Mariana Andrade Torres
    • 3
  • Gisele Mouro Ravagnani
    • 3
  • Renata Lançoni
    • 2
  • Tamie Guibu de Almeida
    • 1
  • Vanessa Martins Storillo
    • 1
  • Vinicius Silva Vellone
    • 1
  • Celso Rodrigues Franci
    • 4
  • Helder Esteves Thomé
    • 1
  • Carolina Luz Canella
    • 1
  • André Furugen Cesar De Andrade
    • 3
  • Eneiva Carla Carvalho Celeghini
    • 1
  1. 1.Laboratory of Teaching and Research in Pathology of Reproduction, Center of Biotechnology in Animal Reproduction, Department of Animal Reproduction, School of Veterinary Medicine and Animal ScienceUniversity of Sao Paulo (USP)PirassunungaBrazil
  2. 2.Laboratory of Semen Biotechnology and Andrology, Center of Biotechnology in Animal Reproduction, Department of Animal Reproduction, School of Veterinary Medicine and Animal ScienceUniversity of Sao Paulo (USP)PirassunungaBrazil
  3. 3.Laboratory of Andrology and Embryo Technology, Department of Animal Reproduction, School of Veterinary Medicine and Animal ScienceUniversity of Sao Paulo (USP)PirassunungaBrazil
  4. 4.Laboratory of Neuroendocrinology and Reproduction, Department of Physiology – Faculty of MedicineUniversity of Sao Paulo (USP)Ribeirao PretoBrazil

Personalised recommendations