Tropical Animal Health and Production

, Volume 51, Issue 7, pp 1855–1866 | Cite as

Responses of testosterone hormone concentration, semen quality, and its related pro-inflammatory cytokines in bucks following Corynebacterium pseudotuberculosis and its mycolic acid infection

  • N. M. N. Faeza
  • F. F. A. JesseEmail author
  • I. U. Hambali
  • M. N. Odhah
  • M. Umer
  • M. M. S. Wessam
  • M. L. Mohd-Azmi
  • A. H. Wahid
Regular Articles


Corynebacterium pseudotuberculosis is the causative agent of caseous lymphadenitis, a debilitating chronic disease of sheep and goats. Little is known about the buck’s reproductive pathophysiology with respect to inoculation with Corynebacterium pseudotuberculois and its immunogen mycolic acid extract. Therefore, this present study was designed to determine the concentration of testosterone hormone, pro-inflammatory cytokines, and semen quality of the experimental animals. A total of 12 bucks, divided into groups 1, 2, and 3 (Negative control group, Positive control group and Mycolic acid group respectively), were enrolled in this study. Following inoculation, all goats were observed for clinical responses and monitored for 60 days post-challenge and were then sacrificed. Blood samples were collected via the jugular once before inoculation and on a weekly basis post-challenge. Semen samples were collected 2 weeks post-challenge and prior to the sacrifice of the experimental animals. During the post inoculation period of 60 days, the concentration of testosterone hormone for group 2 was increased significantly (p < 0.05) in weeks 5, 6, and 9 but decreased in weeks 2 and 7 post inoculation. In group 3, the mean concentration of testosterone was increased significantly (p < 0.05) in weeks 5, 6, 7, and 9 post inoculation but decreased in week 2. The concentration of interleukin 6 (IL 6) in treated group 2 did not show any significant difference (p > 0.05) but increased significantly (p < 0.05) in week 2 post inoculation in group 3. For concentration of interleukin 1β (IL1β) in both treated groups 2 and 3 showed significant difference (p < 0.05) in weeks 2 and 3 post inoculation. The tumor necrosis factor-alpha (TNF-α) concentration in both treated groups 2 and 3 did not show any significant difference (p > 0.05) as compared to group 1. The concentration of interferon-γ (IFNγ) significantly increased (p < 0.05) for group 2 for weeks 2, 3, 4, and 5 where else for group 3 was not in significant difference (p > 0.05) compared to group 1. Both group 2 and group 3 showed a reduction in semen qualities as compared to group 1, but the severity was more intense in group 2 if compared to group 3. In conclusion, therefore, the present study concluded that the mycolic acid group revealed significant responses of testosterone hormone concentration, semen quality, and its related pro-inflammatory cytokines in bucks following infection but the severity lesser compared to Corynebacterium pseudotuberculosis group.


C. pseudotuberculosis Mycolic acid Pro-inflammatory cytokines Testosterone hormone Semen quality and bucks 



The authors are grateful to Mr. Yap Keng Chee, and Mr. Mohd Jefri Norsidin for their assistance. University Putra Malaysia, Faculty of Veterinary Medicine.

Funding information

The work received funding from FRGS grant (5524796) from KPT, Malaysia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Adza-Rina, M. N., Zamri-Saad, M., Shahirudin, S., Normah, M. Y., and Niecorrita, W. (2013).Efficacy of a commercially available vaccine against caseous lymphadenitis in goats. Proceedings of the 25 th Annual General Meeting and Veterinary Association Malaysia Congress, Malaysia, 50.Google Scholar
  2. Alessandro, SG., Filipe, B.C., Rebeca, B.P., Nubia, S., Dayana, R., Andrey P.L., Marcos, B.H., Anderson, M., Vasco, A., and Aurora, M.G.G. (2011). Caseous ymphadenitis: epidemiology, diagnosis, and control. The IIOAB journal.2(2). 33–43Google Scholar
  3. Arsenault J., Girard, C., Dubreuil, P., Daignault, D., Galarneau, J. R., Boisclair, J., Simard, C., and Bélanger D. (2003).Prevalence of and carcass condemnation from maedi-visna, paratuberculosis and caseous lymphadenitis in culled sheep from Quebac, Canada.Preventive Veterinary Medicine, 59: 67–81.CrossRefPubMedGoogle Scholar
  4. Azenabor, A., Ekun, A.O., and Akinloye, O. (2015). Impact of Inflammation on Male Reproductive Tract.Journal of Reproduction and Infertility.16(3):123–129.PubMedGoogle Scholar
  5. Baird, G. J., and Fontaine, M. C. (2007).Corynebacterium pseudotuberculosis and its role in ovine caseous lymphadenitis. Journal of Comparative Pathology, 137: 179-210.CrossRefPubMedGoogle Scholar
  6. Brogden, K. A., & Engen, R. L. (1990). Alterations in the phospholipid composition and morphology of ovine erythrocytes after intravenous inoculation of Corynebacterium pseudotuberculosis. American Journal of Veterinary Research, 51(6), 874–877.PubMedGoogle Scholar
  7. Brown, C., Olander, H., Biberstein, E., & Morse, S. (1986). Use of a toxoid vaccine to protect goats against intradermal challenge exposure to Corynebacterium pseudotuberculosis. American journal of veterinary research, 47(5), 1116–1119.PubMedGoogle Scholar
  8. Buxton, A., & Fraser, G. (1977). Corynebacterium. Edinburgh: Blackwell Scientific Publications.Google Scholar
  9. Coffin, D. L. (1953). Manual of Veterinary Medicine, 3rdedn. Ithaca, New York: Comstock Publishing Associates.Google Scholar
  10. Collett, M. G., Bath, G. F., and Cameron C. M. (1994).Corynebacetrium pseudotuberculosis infections. In J. Coetzer, G. R. Thomson & R. C. Tustin (Eds.), Infectious diseases of livestock with special reference to Southern Africa (2nded.) (pp. 1387-1395). Cape Town: Oxford University PressGoogle Scholar
  11. Daffe, M., & Etienne, G. (1999). The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tubercle and lung disease, 79(3), 153–169.CrossRefPubMedGoogle Scholar
  12. Damien, P., de Sousa-D'Auria, C., Houssin, C., Grimaldi, C., Chami, M., Daffé, M., & Guilhot, C. (2004). A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proceedings of the National Academy of Sciences, 101(1), 314–319.CrossRefGoogle Scholar
  13. Dorella, F. A., Pacheco, L. G. C., Oliveira, S. C., Miyoshi, A., and Azevedo, V. (2006). Corynebacterium pseudotuberculosis: microbiology, biochemical properties, pathogenesis and molecular studies of virulence. Veterinary Research, 37: 201–218.CrossRefPubMedGoogle Scholar
  14. Goldberger, A. C., Lipsky, B. A., and Plorde, J. J. (1981). Suppurative granulomatous lymphadenitis caused by Corynebacteriumovis (pseudotuberculosis). American Journal of Clinical Pathology, 76: 486–490.CrossRefPubMedGoogle Scholar
  15. Hafez, B., Hafez, E. (2000). Reproduction in Farm Animals. Wiley, USA (Lippincott Williams & Wilkins Eds).Google Scholar
  16. Hancock, J. L. (1959). Morphological Characteristics of Spermatozoa and Fertility. Int. J. Fert. 4:347-359.Google Scholar
  17. Jeanine, L.B., Laurel, M.H., Alan, M.H., John, A.F., and Mildred, S.C. (1996).Reproductive effects of chronic administration of murine interferon-gamma. Elsevier, Reproductive Toxicology, 10(5): 379–391Google Scholar
  18. Jesse, F., Azlan, C., Saharee, A., Murugaiyah, M., Noordin, M., Jasni, S., Ragavan, K., Hassan, M., Haron, A., & Siti, K. (2008). Control of Caseous Lymphadenitis (CLA) in goat at UPM Farm. Proceedings of the 20th Veterinary Association Malaysia (VAM’08).Google Scholar
  19. Jesse, F. F. A., Osman, A. Y., Adamu, L., Azri, N. A., Haron, A. W., Saad, M. Z., Omar, A. R., and Sharee, A. A. (2013a). Caseous lymphadenitis in a goat. South Asian Journal of Life Sciences, 1(1): 19–20.Google Scholar
  20. Jesse, F., Randolf, P., Saharee, A., Wahid, A., Zamri-Saad, M., Jasni, S., Omar, A., Adamu, L., & Abdinasir, Y. (2013b). Clinico-pathological response of mice following oral route infection of C.pseudotuberculosis.Google Scholar
  21. Jesse, F. F. A., Adamu, L., Abdinasir, Y. O., Ahmad Fauzan, M., Abd Wahid, H., and Abdul Aziz, S. (2013c). Polymerase chain reaction of C. pseudotuberculosis in the brain of mice following oral inoculation. International Journal of Animal and Veterinary Advance (5): 29-33.Google Scholar
  22. Jesse, F. F. A., Latif, N.-A. A., Chung, E. L. T., Adamu, L., Sarah, S. A., Zamri-Saad, M., Haron, A. W., & Mohd, M. A. (2016a). Cytokines (IL 1β and IL 6) Responses in Non-Pregnant Does Infected with Corynebacteriumpseudotuberculosis Following Intradermal Route of Infection in Chronic State. International Journal of Livestock Research, 6(6), 1–8.CrossRefGoogle Scholar
  23. Jesse, F.F.A., Bitrus, A.A., Abba, Y., Chung, E.L.T., Sadiq, M.A., Hambali, I.U., Perera, H., Haron, A.W., Lila, M.A.M., Saharee, A.A., Norsidin, M.J., Harith, A. (2016b). Strategic management of a clinical case of recurrent caseaous lyphadenitis in a goat farm. Res J Vet Pract 4(3): 42.46.Google Scholar
  24. Jesse, F. F. A., Odhah, M. N., Mohd, M. A A., Zamri-Saad, M., Haron, A. W., Umar, H., and Zaid K.M. (2017).Pro-Inflammatory Cytokine (IL-1β and IL-6) Response in Goats Challenged with Corynebacterium pseudotuberculosis and its Immunogen Mycolic Acids. American Journal of Animal and Veterinary Sciences. 12(1), 26–31.CrossRefGoogle Scholar
  25. Komala, T. S., Ramlan, M., Yeoh N. N., Surayani, A. R., and SharifahHamidah, S. M. A. (2008).Survey of caseous lymphadenitis in small ruminant farms from two districts in perak, Malaysia-Kinta and Hilir Perak.Tropical Biomedicine, 25(3): 196–201.PubMedGoogle Scholar
  26. Maegawa, M., Kamada, M., Irahara, M., Yamamoto, S., Yoshikawa, S., and Kasai, Y. (2002). A repertoire of cytokines in human seminal plasma. Journal of Reproduction Immunology, 54(1–2): 33–42.CrossRefGoogle Scholar
  27. McFarland, J. (1907). The nephelometer: an instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. Journal of the American Medical Association, 49(14), 1176–1178.CrossRefGoogle Scholar
  28. McNeil, M., Daffe, M., & Brennan, P. (1991). Location of the mycolyl ester substituents in the cell walls of mycobacteria. Journal of Biological Chemistry, 266(20), 13217–13223.PubMedGoogle Scholar
  29. Mouihate, A., X. Chen, and Q. J. Pittman. (1998). Interleukin-1b fever in rats: gender difference and estrous cycle influence. Journal of American Phisiological Society. 275 (Regulatory Integrative Comp. Physiol. 44): R1450–R1454.Google Scholar
  30. Othman, A. M., Jesse, F. F. A., Adamu, L., Abba, Y., Adza-Rina, M. N., Saharee, A. A., Wahid, A. H., and Zamri-Saad, M. (2014). Changes in serum progesterone and estrogen concentrations in non-pregnant Boer does following experimental infection with Corynebacterium pseudotuberculosis. Journal of Veterinary Advances, 4(5): 524–528.Google Scholar
  31. Paton, M.W., (2010). The epidemiology and control of Caseous lymphadenitis in Australian sheep flocks. PhD Thesis, Murdoch University.Google Scholar
  32. Pépin, M., Seow, H. F., Corner, L., Rothel, J. S., Hodgson, A. L., and Wood, P. R. (1997). Cytokine gene expression in sheep following experimental infection with various strains of Corynebacterium pseudotuberculosis differing in virulence. Veterinary Research, 28(2): 149–163.PubMedGoogle Scholar
  33. Portevin, D., de Sousa-D’Auria, C., Houssin, C., Grimaldi, C., Chami, M., Daffe´ , M., and Guilhot, C. (2004). A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in Mycobacteria and related organisms. Proc. Natl. Acad. Sci. USA, 101:314–319.Google Scholar
  34. Radostits, O. M., Gay, C. C., Blood, D. C., and Hinchcliff, K. W. (2000). Caseous lymphadenitis in sheep and goats. In W. B. Saunders (Ed.), Veterinary Medicine: A Textbook of the Diseases of Cattle, Sheep, Pigs, Goats and Horses (9thed.). London.Google Scholar
  35. Rekwot, P. I., Oyedipe, E. O., Dawuda, P. M., & Sekoni, V. O. (1997). Age and hourly related changes of serum testosterone and spermiogram of prepubertal bulls fed two levels of nutrition. Veternary Journal, 153(3), 341–347.Google Scholar
  36. Shamsuddin, M., Amiri, Y., & Bhuiyan, M. (2000). Characteristics of buck semen with regard to ejaculate numbers, collecion intervals, diluents and preservation periods. Reproduction in Domestic Animals, 35(2), 53–57.CrossRefGoogle Scholar
  37. Stoops, S. G., Renshaw, H. W. and Thilsted, J. P. (1984). Ovine caseouslymhadenitis: disease prevalence, lesion distribution, and thoracic manifestations in a population of mature culled sheep from western United States. American Journal of Veterinary Research, 45: 557–561.PubMedGoogle Scholar
  38. Zaid, K.M., Zurin, A.M., Jesse, F.F A., Saharee, A.A., Jasni, S., Rosnina, Y., and Wahid, A.H. (2016). Relationship between the Corynebacterium pseudotuberculosis,phospholipase D inoculation and the fertility characteristics of crossbred Boer bucks. Livestock Science, 191, 12–21CrossRefGoogle Scholar
  39. Zemjanis, R. . (1970). Diagnostic and therapeutic technique in animal reproduction Baltimore: Williams and Wilkins Company.Google Scholar
  40. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffe´, M. (2008). Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190:5672–5680.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • N. M. N. Faeza
    • 1
    • 2
  • F. F. A. Jesse
    • 1
    • 3
    • 4
    Email author
  • I. U. Hambali
    • 1
    • 5
  • M. N. Odhah
    • 1
  • M. Umer
    • 6
  • M. M. S. Wessam
    • 7
  • M. L. Mohd-Azmi
    • 8
  • A. H. Wahid
    • 1
  1. 1.Department of Veterinary Clinical Studies, Faculty of Veterinary MedicineUniversiti Putra MalaysiaSerdangMalaysia
  2. 2.Makmal BioSerasiBangiMalaysia
  3. 3.Institute of Tropical Agriculture and Food Security (ITAFoS)Universiti Putra MalaysiaSerdangMalaysia
  4. 4.University Community Transformation Centre (UCTC)Universiti Putra Malaysia (UPM)SerdangMalaysia
  5. 5.Department of Veterinary Public health and Preventive MedicineUniversity of MaiduguriMaiduguriNigeria
  6. 6.Lasbela University of Agriculture Water and Marine Sciences Uthal PakistanUthalPakistan
  7. 7.Department of Internal and Preventive MedicineUniversity of BasraBasra StateIraq
  8. 8.Department of Veterinary Pathology and Microbiology, Faculty of Veterinary MedicineUniversiti Putra MalaysiaSerdangMalaysia

Personalised recommendations