DOI QR코드

DOI QR Code

Testicular Cell Indices and Peripheral Blood Testosterone Concentrations in Relation to Age and Semen Quality in Crossbred (Holstein Friesian×Tharparkar) Bulls

  • Rajak, S.K. (Theriogenology Lab., National Dairy Research Institute) ;
  • Kumaresan, A. (Theriogenology Lab., National Dairy Research Institute) ;
  • Gaurav, M.K. (Livestock Research Centre, National Dairy Research Institute) ;
  • Layek, S.S. (Theriogenology Lab., National Dairy Research Institute) ;
  • Mohanty, T.K. (Livestock Research Centre, National Dairy Research Institute) ;
  • Aslam, M.K. Muhammad (Theriogenology Lab., National Dairy Research Institute) ;
  • Tripathi, U.K. (Theriogenology Lab., National Dairy Research Institute) ;
  • Prasad, Shiv (Livestock Research Centre, National Dairy Research Institute) ;
  • De, S. (Animal Biotechnology Centre, National Dairy Research Institute)
  • Received : 2014.02.24
  • Accepted : 2014.05.19
  • Published : 2014.11.01

Abstract

Present study analyzed the changes in peripheral blood testosterone concentrations and testicular cytogram in relation to age and semen quality in crossbred males. Three different age groups of crossbred males viz. bull calves (6 months, n = 5), young bulls (15 months, n = 5) and adult bulls (4 to 6 years, n = 8) were utilized for the study. Testicular fine needle aspiration cytology technique was used to quantify testicular cytology and their indices. Peripheral blood testosterone concentrations were measured using enzyme-linked immunosorbent assay method. Semen samples collected from adult bulls were microscopically evaluated for quality parameters. Mean peripheral blood testosterone concentrations in bull calves, young bulls and adult bulls were $2.28{\pm}0.09ng/mL$, $1.42{\pm}0.22ng/mL$ and $5.66{\pm}1.08ng/mL$ respectively, and that in adult bulls were significantly different (p<0.01) from young bulls and bull calves. There was no significant difference between the proportion of different testicular cells in bull calves and young bulls. Between young and adult bulls, significant differences (p<0.01) were observed in the proportion of spermatocytes, spermatozoa, and sperm: Sertoli cell ratio. The proportions of Sertoli cells showed a significant difference (p<0.01) between the three age groups. The number of primary spermatocytes had a positive correlation with peripheral blood testosterone concentrations in bull calves (r = 0.719, p<0.01). Number of Sertoli cells per 100 germ cells was negatively correlated with blood testosterone concentration in young bulls (r = -0.713, p<0.01). Among different semen parameters in adult bulls, ejaculate volume (r = 0.790, p<0.05) had positive relationship, and sperm motility had significant negative correlation (r = -0.711, p<0.05) with testosterone concentrations. The number of Sertoli cells and Sertoli cell index had a positive correlation with various semen quality parameters (p<0.001). Results of the present study conclude that number of Sertoli cells and Sertoli cell index are good indicators of semen quality, but peripheral blood testosterone concentrations may not have a direct relationship with various seminal attributes in crossbred bulls.

Keywords

References

  1. Campbell, R. G., J. C. Hancock, and L. Rothschild. 1953. Counting live and dead bull spermatozoa. J. Exp. Biol. 30:44-49.
  2. Chapwanya, A., J. Callanan, H. Larkin, L. Keenan, and L. Vaughan. 2008. Breeding soundness evaluation by semen analysis, testicular fine needle aspiration cytology and transscrotal ultrasonography. Irish Vet. J. 61:315-318.
  3. Chase, C. C., P. J. Chenoweth, R. E. Larsen, T. A. Olson, A. C. Hammond, M. A. Menchaca, and R. D. Randel. 1997. Growth and reproductive development from weaning through 20 months of age among breeds of bulls in subtropical Florida. Theriogenology 47:723-745. https://doi.org/10.1016/S0093-691X(97)00030-7
  4. Foresta, C. and A. Varotto. 1992. Assessment of testicular cytology by fine needle aspiration as a diagnostic parameter in the evaluation of the oligospermic subject. Fertil. Steril. 58:1028-1033.
  5. Franca, L. R. and L. D. Russell. 1998. The testis of domestic animals. In: Male Reproduction: A Multidisciplinary Overview (Eds. F. Martinez-Garcia and J. Regadera). Churchill Livingstone, Madrid, Spain. pp. 197-219.
  6. Gholami, H., A. Towhidi, Z. Shahneh, and E. Dirandeh. 2010. The relationship of plasma leptin concentration and puberty in Holstein bull calves (Bos taurus). J. Anim. Physiol. Anim. Nutr. (Berl.) 94:797-802. https://doi.org/10.1111/j.1439-0396.2009.00970.x
  7. Goeritz, F., M. Quest, A. Wagener, M. Fassbender, A. Broich, Hildebrandt, T. B. Hildebrandt, R. R. Hofmann, and S. Blottner. 2003. Seasonal timing of sperm production in roe deer: interrelationship among changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology 59:1487-1502. https://doi.org/10.1016/S0093-691X(02)01201-3
  8. Gulia, S., M. Sarkar, V. Kumar, H. H. Meyer, and B. S. Prakash. 2010. Divergent development of testosterone secretion in male zebu (Bos indicus) and crossbred cattle (Bos indicus${\times}$Bos taurus) and buffaloes (Bubalus bubalis) during growth. Trop. Anim. Health Prod. 42:1143-1148. https://doi.org/10.1007/s11250-010-9538-x
  9. Hafez, E. S. E. 2000. Reproduction in Farm Animals, 7th Edition. Lippincott Williams and Wilkins: pp. 293-397.
  10. Hentrich., A., M. Wolter, C. Szardening-Kirchner, G. H. Luers, M. Bergmann, S. Kliesch, and L. Konrad. 2011. Reduced numbers of Sertoli, germ, and spermatogonial stem cells in impaired spermatogenesis. Mod. Pathol. 24:1380-1389. https://doi.org/10.1038/modpathol.2011.97
  11. Hinton, B. T., M. A. Palladino, D. Rudolph, Z. J. Lan, and J. C. Labus. 1996. The role of epididymis in the protection of spermatozoa. Curr. Top. Dev. 33:61-102. https://doi.org/10.1016/S0070-2153(08)60337-3
  12. Javed, M. T., A. Khan, and M. Ali. 2000. Influnce of season on seminal plasma testosterone and oesterogen in healthy and abnormal buffalo bulls and their relationship with other semen parameters. Vet. Arhiv. 70:141-149.
  13. Jeyendran, R. S., H. H. Vander-Ven, P. M. Perez, B. G. Crabo, and L. J. D. Zaneveld. 1984. Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J. Reprod. Fertil. 70:219-228. https://doi.org/10.1530/jrf.0.0700219
  14. Johnson, L. 1991. Spermatogenesis. In: Reproduction in Domestic Animals (Ed. P. T. Cupps). Fourth ed. Academic Press Inc., San Diego, CA, USA. pp. 173-219.
  15. Johnston, H., P. J. Baker, M. Abel, H. M. Charlton, G. Jackson, L. Fleming, T. R. Kumar, and P. J. O'Shaughnessy. 2004. Regulation of Sertoli cell number and activity by folliclestimulating hormone and androgen during postnatal development in the mouse. Endocrinology 145:318-329. https://doi.org/10.1210/en.2003-1055
  16. Khatun, M., S. Kaur, Kanchan, and C. S. Mukhopadhyay. 2103. Subfertility problems leading to disposal of breeding bulls. Asian Australas. J. Anim. Sci. 26:303-308. https://doi.org/10.5713/ajas.2012.12413
  17. Kumar, N., R. P. Verma, L. P. Singh, V. P. Varshney, and R. S. Dass. 2006. Effect of different concentrations and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone concentration in crossbred cattle (Bos indicus${\times}$Bos taurus) bulls. Reprod. Nutr. Dev. 46:663-675. https://doi.org/10.1051/rnd:2006041
  18. Leal, M. C., S. C. Becker-Silva, H. Chiarini-Garcia, and L. R. Franca. 2004. Sertoli cell efficiency and daily sperm production in goats (Capra hircus). Anim. Reprod. 1:122-128.
  19. Leme, D. P. and F. O. Papa. 2000. Cytologic identification and quantification of testicular cell types using fine needle aspiration in horses. Equine Vet. J. 32:444-446.
  20. Leme, D. P. and F. O. Papa. 2010. How to perform and interpret testicular fine needle aspiration in stallion. J. Equine Vet. Sci. 30:590-596. https://doi.org/10.1016/j.jevs.2010.09.003
  21. Mathur, A. K., S. Tyagi, and S. P. Singh. 2002. Frieswal bull - an experience of HF with Sahiwal. J. Livest. Poult. Prod. 18:21-23.
  22. McLachlau, R. I., N. G. Wreford, L. O'Donnell, D. M. de Kretser and D. M. Robertson. 1996. The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J. Endocrinol. 148:1-9. https://doi.org/10.1677/joe.0.1480001
  23. Mukhopadhyay, C. S., A. K. Gupta, B. R. Yadav, K. Khate, V. S. Raina, T. K. Mohanty, and P. P. Dey. 2010. Subfertility in males: an important cause of bull disposal in bovines. Asian Australas. J. Anim. Sci. 23:450-455. https://doi.org/10.5713/ajas.2010.90298
  24. Post, T. B. and B. M. Bindon. 1983. Plasma luteinizing hormone and testosterone concentrations in different breeds of young beef bulls in the tropics. Aust. J. Biol. Sci. 36:545-550.
  25. Rajak, S. K., U. K. Tripathi, N. M. Attupuram, P. Boro, S. S. Layek, M. K. M. Aslam, A. Kumaresan, T. K. Mohanty, L. Sreela, and M. A. Prakash. 2014. Relationship of blood and seminal plasma testosterone concentrations with semen quality in crossbred bulls. Indian J. Dairy Sci. 67:162-167.
  26. Rajak, S. K., A. Kumaresan, M. K. Gaurav, M. K. M. Aslam, T. K. Mohanty, S. Prasad, A. K. Chakravarty, and V. Venkatasubramanian. 2013. Testicular biometry and semen quality is not altered by the process of fine needle aspiration in crossbred bulls. Indian J. Anim. Sci. 83:732-735.
  27. Rawlings, N. C., H. D. Hafs, and L. V. Swanson. 1972. Testicular and blood plasma androgens in Holstein bulls from birth through puberty. J. Anim. Sci. 34:435-440.
  28. Robaire, B. and R. S. Viger. 1995. Regulation of epdidymal epithelial cell function. Biol. Reprod. 52:226-236. https://doi.org/10.1095/biolreprod52.2.226
  29. Russell, L. D. and R. N. Peterson. 1984. Determination of the elongate spermatid-Sertoli cell ratio in various mammals. J. Reprod. Fertil. 70:635-641. https://doi.org/10.1530/jrf.0.0700635
  30. Salisbury, G. W., N. L. VanDenmark, and J. R. Lodge. 1985. Physiology of Reproduction and Artificial Insemination of cattle. 2nd edition. CBS Publ. Dist., New Delhi, India.
  31. Santos, M., R. Marcos, and M. Canictti. 2010. Cytologic study of normal canine testis. Theriogenology 73:208-214. https://doi.org/10.1016/j.theriogenology.2009.07.030
  32. Santos, M. D., C. A. A. Torres, J. R. M. Ruas, J. D. Guimaraes, and J. M. S. Filho. 2004. Reproductive potential of Nelore bulls submitted to different bull:cow proportion. Arq. Bras. Med. Vet. Zootec. 56:497-503.
  33. Santra, A., N. Agrwal, D. N. Kamara, and N. N. Pathak. 1999. Effect of level of concentrate supplement on blood biochemical changes and testosterone level in crossbred (Bos indicus${\times}$Bos Taurus) calves. Asian Australas. J. Anim. Sci. 12:881-885. https://doi.org/10.5713/ajas.1999.881
  34. Schallenberger, E., P. Hartl, D. Schams, W. Lorrmann, and R. Hahn. 1991. Hormone profiles and fertility in bulls. Tierzuchter 43:402-403.
  35. Scott, H. M., G. R. Hutchison, I. K. Mahood, N. Hallmark, M. Welsh, K. DeGendt, G. Verhoeven, P. J. O'Shaughnessy, and R. M. Sharpe. 2007. Role of androgens in fetal testis development and dysgenesis. Endocrinology 148:2027-2036. https://doi.org/10.1210/en.2006-1622
  36. Scott, H. M., G. R. Hutchison, M. S. Jobling, C. McKinnell, A. J. Drake, and R. M. Sharpe. 2008. Relationship between androgen action in the 'male programming window', fetal Sertoli cell number and adult testis size in the rat. Endocrinology 149:5280-5287. https://doi.org/10.1210/en.2008-0413
  37. Sekasiddhi, P. and S. Buban. 1997. Hormone profiles in low libido bulls. J. Thai Vet. Med. Asso. 48:43-49.
  38. Sharpe, R. M. 2010. Environmental/lifestyle effects on spermatogenesis. Phil. Trans. R. Soc. B 365:1697-1712. https://doi.org/10.1098/rstb.2009.0206
  39. Sharpe, R. M., C. McKinnell, C. Kivlin, and J. S. Fisher. 2003. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125:769-784. https://doi.org/10.1530/rep.0.1250769
  40. Singh, A. 2005. Crossbreeding of cattle for increasing milk poduction in India: A Review. Indian. J. Anim. Sci. 75:383-390.
  41. Souza, L. W. O., A. F. C. Andrade, E. C. C. Celeghini, J. A. Negrao, and R. P. de-Arruda. 2011. Correlation between sperm characteristics and testosterone in bovine seminal plasma by direct radio immunoassay. R. Bras. Zootec. 40: 2721-2724.
  42. Sudheer, S. and C. J. Xavier. 2000. Disposal pattern of breeding bulls in Kerala. Ind. J. Anim. Reprod. 21:72-73.
  43. Suresh, R., R. Medhamurthy, and N. R. Moudgal. 1995. Comparative studies on the effects of specific immunoneutralisation of endogenous FSH or LH on testicular germ cell transformation in the adult bonnet monkey (Macaca radiata). Am. J. Reprod. Immunol. 34:35-43. https://doi.org/10.1111/j.1600-0897.1995.tb00917.x
  44. Tuli, R. H., I. S. Lohan, R. L. Goyal, and S. P. Singal. 1991. Testosterone and progesterone hormones in buffalo bull seminal plasma and their correlations with seminal characteristics. Indian J. Dairy Sci. 44:587-589.
  45. Vijetha, B. T., S. S. Layek, A. Kumaresan, T. K. Mohanty, A. K. Gupta, A. K. Chakravarty, A. Manimaran, and Shiv Prasad. 2014. Effects of pedigree and exotic genetic inheritance on semen production traits of dairy bulls. Asian Pac. J. Reprod. 3:13-17. https://doi.org/10.1016/S2305-0500(13)60178-5
  46. Watson, P. F. 1975. Use of Giemsa stain to detect changes in acrosome of frozen ram spermatozoa. Vet. Rec. 97:12-15. https://doi.org/10.1136/vr.97.1.12
  47. Wolfe, F. 1996. Biochemical and endocrinological parameters as indicators of the freezability of the semen of bulls of different ages. Thesis, Tierarztliche Hochschule, Hannover.
  48. Yang, Y. and C. Han. 2010. GDNF stimulates the proliferation of cultured mouse immature Sertoli cells via its receptor subunit NCAM and ERK1/2 signalling pathway. BMC Cell Biol. 11:78. https://doi.org/10.1186/1471-2121-11-78

Cited by

  1. Beyond Testis Size: Links between Spermatogenesis and Sperm Traits in a Seasonal Breeding Mammal vol.10, pp.10, 2015, https://doi.org/10.1371/journal.pone.0139240
  2. Morphometric evaluation of seminiferous tubule and proportionate numerical analysis of Sertoli and spermatogenic cells indicate differences between crossbred and purebred bulls vol.8, pp.5, 2015, https://doi.org/10.14202/vetworld.2015.645-650
  3. Influence of season and climatic variables on testicular cytology, semen quality and melatonin concentrations in crossbred bucks reared under subtropical climate vol.62, pp.9, 2018, https://doi.org/10.1007/s00484-018-1571-x
  4. Seasonal changes in semen quality and correlation with plasma hormone profiles in Karan Fries bulls vol.47, pp.6, 2016, https://doi.org/10.1080/09291016.2016.1213361
  5. Seasonal variations in hormones and enzymes of seminal plasma and its relationship with semen quality in crossbred cattle bulls vol.51, pp.4, 2020, https://doi.org/10.1080/09291016.2018.1548873
  6. The impact of regular sperm donation on bulls’ seminal plasma hormonal profile and phantom response vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-90630-8