Impotentia generandi in male dromedary camels: heavy metal and trace element profiles and their relations to clinical findings and semen quality

  • Ahmed AliEmail author
  • Derar R. Derar
  • Essam M. Abdel-Elmoniem
  • Tariq I. Almundarij
Regular Articles


The aim of this study was to investigate the profiles of cadmium (Cd), lead (Pb), selenium (Se), zinc (Zn), copper (Cu), molybdenum (Mo), iron (Fe), and manganese (Mn) in serum of dromedary camels with impotentia generandi and their associations with the clinical findings and semen analysis data. Sixteen male dromedary camels with impotentia generandi (IG group) and 5 fertile camels (FERT group) were used. The external and internal genital organs were examined using visual inspection, palpation, and ultrasonography. Semen was collected by electroejaculation and examined for volume, count, motility, viability, and abnormality. Blood was collected from all camels and serum was harvested. All serum samples were digested by concentrated acids and analyzed for heavy metals and trace elements by flame emission atomic absorption spectrophotometer. Results showed that the mean heavy metal and trace element concentrations in serum were in the following descending order Fe > Zn > Cu > Cd > Mo > Se > Mn > Pb. Cd was higher in IG than in FERT males (P = 0.02). Se was greater in FERT than in IG groups (P = 0.003). Zn was higher in in FERT than in IG groups (P = 0.001). There were positive correlations between Zn and sperm count (r = 0.59, P = 0.005) and sperm motility (r = 0.57, P = 0.005) and a tendency for negative correlation between Zn and sperm abnormalities (r = − 0.44, P = 0.05). In conclusion, Cd might be implicated as a cause of infertility in male camels. Deficiencies of Se and Zn may also have adverse impacts on male camel reproduction.


Male infertility Dromedary camel Trace elements Heavy metals 


Compliance with ethical standards

This study was approved by the Animal Care and Welfare Committee, Deanship of Scientific Research, Qassim University, Kingdom of Saudi Arabia.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdalla O.M., Wasfi I.A., Gadir F.A., 1988. The Arabian race camel normal parameters. I. Haemogram, enzymes and minerals. Comp. Bioch. Physiol., 90A, 237–239. CrossRefGoogle Scholar
  2. Ahsan, U., Kamran, Z., Raza, I., Ahmad, S., Babar, W., Riaz, M.H., Iqbal, Z., 2014. Role of selenium in male reproduction - a review, Animal Reproduction Science, 146, 55–62.CrossRefGoogle Scholar
  3. Akinloye, O., Arowojolu, A.O., Shittu, O.B., Abbiyesuku, F.M., Adejuwon, C.A., Osotimehin, B., 2006. Serum and seminal plasma hormonal profiles of infertile Nigerian male, African journal of medicine and medical sciences, 35, 468–73.Google Scholar
  4. Alaee, S., Monsefi, M., 2013. Effect of cadmium on oxidative stress of testes in adult male mice, Iranian Journal of Reproductive Medicine, 11, 39–44.Google Scholar
  5. Ali, I., Damdimopoulou, P., Stenius, U., Adamsson, A., Mäkelä, S. I., Åkesson, A., Berglund, M., Håkansson, H., Halldin, K., 2012. Cadmium-induced effects on cellular signaling pathways in the liver of transgenic estrogen reporter mice, Toxicological Sciences, 127, 66–75.CrossRefGoogle Scholar
  6. Ali, A., Derar, R., Al-Sobayil, F., Mehana, S., Al-Hawas, A., 2014. Impotentia generandi in male dromedary camels: clinical findings, semen characteristics, and testicular histopathology, Theriogenology, 82, 890–6.CrossRefGoogle Scholar
  7. Ali, A., Derar, D., Al-Sobyil, F.A., Zeitoun, M.M., Hassanein, K.M.A., Al-Howas, A., 2016. Phimosis in male dromedary camels: Clinical findings and changes in the hemogram, nitric oxide metabolites, and testosterone concentrations. Theriogenology, 85(9):1576–1581.Google Scholar
  8. Ali, A., Derar, D.R., Zeitoun, M.M., Al-Sobayil, F., 2018. Impotentia generandi in male dromedary camels: FSH, LH and testosterone profiles and their association with clinical findings and semen analysis data, Theriogenology, 120, 98–104.CrossRefGoogle Scholar
  9. Antoniou, V., Zantopoulos, N. and Tsoukali-Papadopoulou, H., 1995. Selected heavy metal concentrations in goat liver and kidney, Veterinary and Human Toxicology, 37, 20–2.Google Scholar
  10. Athamna, O.M., Bengoumi, M., Faye, B., 2012. Selenium and copper status of camels in Al-Jouf area (Saudi Arabia), Tropical Animal Health Production, 44, 551–556.CrossRefGoogle Scholar
  11. Bengoumi, M., Essamadi, A.K., Tressol, J.C., Faye, B. 1998. Comparative study of copper and zinc metabolism in cattle and camel. Biol Trace Elem Res, 63, 81–94.CrossRefGoogle Scholar
  12. Bertelsmann, H., Keppler, S., Höltershinken, M., Bollwein, H., Behne, D., Alber, D., Bukalis, G., Kyriakopoulos, A., Sieme, H., 2010. Selenium in blood, semen, seminal plasma and spermatozoa of stallions and its relationship to sperm quality, Journal of Reproduction and Fertility, 22, 886–891.CrossRefGoogle Scholar
  13. Boitani, C., Puglisi, R., 2008. Selenium, a key element in spermatogenesis and male fertility, Advances in Experimental Medicine and Biology, 636, 65–73.CrossRefGoogle Scholar
  14. Bonde, J.P., 2010. Male reproductive organs are at risk from environmental hazards Asian Journal of Andrology, 12, 152–6.CrossRefGoogle Scholar
  15. Chung, N.P., Cheng, C.Y., 2001. Is Cadmium Chloride- Induced Inter-Sertoli Tight Junction Permeability Barrier Disruption a Suitable in Vitro Model to Study the Events of Junction Disassembly during Spermatogenesis in the Rat Testis? Endocrinology, 142, 1878–1888.CrossRefGoogle Scholar
  16. Derar R., Hussein H.A., Ali A. 2012. Reference values for the genitalia of male dromedary before and after puberty using caliper and ultrasonography in subtropics. Theriogenology, 77, 459–465.CrossRefGoogle Scholar
  17. Derar, D., Ali, A., Tharwat, M., Al-Sobayil, F., Zeitoun, M.M., 2017. Erectile dysfunction in male dromedary camels: Clinical findings and changes in the nitric oxide metabolite, cardiac troponin I and testosterone concentrations, Theriogenology, 89, 201–205.CrossRefGoogle Scholar
  18. El-Demerdash, F.M., Yousef, M.I., Kedwany, F.S., Baghdadi, H.H., 2004. Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and beta-carotene. Food Chem Toxicol, 42(10):1563–1571.Google Scholar
  19. El Khouly, A.A., Abbas, T.A., Moustafa, T., 2001. Myocardial dystrophy in camel calves in the United Arab Emirates (field cases), Emirates Journal of Agricultural Sciences, 13, 11–17.Google Scholar
  20. Fallah, A., Mohammad-Hasani, A., Colagar, A.H., 2018. Zinc is an Essential Element for Male Fertility: A Review of Zn Roles in Men’s Health, Germination, Sperm Quality, and Fertilization, Journal of Reproduction and Infertility, 9, 69–81.Google Scholar
  21. Faye, B., Bengoumi, M., 1994. Trace-elements status in camels. A review. Biol Trace Elem Res., 41, 1–11. Review.CrossRefGoogle Scholar
  22. Faye, B., Bengoumi, M., 1997. Comparative trace-element status in camel and cow. J. Camel Pract. Res., 4, 213–215.Google Scholar
  23. Faye, B., Bengoumi, M., 2018. Camel clinical biochemistry and hematology. Chapter 7: trace elements. Springer Publ., Switzerland.Google Scholar
  24. Faye, B., Grillet, C., 1984. La carence en cuivre chez les ruminants domestiques de la region d’Awash (Ethiopie), Revue d’Elevage et de Médecine Vétérinaire des, Pays Tropicaux, 37, 42–60.Google Scholar
  25. Foresta, C., Garolla, A., Cosci, I., Menegazzo, M., Ferigo, M., Gandin, V., De Toni, L., 2014. Role of zinc trafficking in male fertility: from germ to sperm, Human Reproduction, 29, 1134–45.Google Scholar
  26. Foresta, C., Garolla, A., Cosci, I., Menegazzo, M., Ferigo, M., Gandin, V., De Toni, L., 2014. Role of zinc trafficking in male fertility: from germ to sperm, Human Reproduction, 29, 1134–45.Google Scholar
  27. Fowler, B.A. 2009. Monitoring of human populations for early markers of cadmium toxicity: a review. Toxicol Appl Pharm., 238, 294–300.CrossRefGoogle Scholar
  28. Hidiroglou, M., 1979. Trace element deficiencies and fertility in ruminants: a review, Journal of Dairy Science, 62, 1195–206.CrossRefGoogle Scholar
  29. Jurewicz, J., Hanke, W., Radwan, M., Bonde, J.P., 2009. Environmental factors and semen quality. International Journal of Occupational Medicine and environmental Health, 22, 305–29.Google Scholar
  30. Meeker, J.D., Rossano, M.G., Protas, B., Diamond, M.P., Puscheck, E., Daly, D., Paneth, N., Wirth, J.J., 2008. Cadmium, lead, and other metals in relation to semen quality: human evidence for molybdenum as a male reproductive toxicant, Environmental Health Perspectives, 116, 1473–1479.CrossRefGoogle Scholar
  31. Moffat, A.C.; Jackson, J.V., Moss, M.S., Widdop, B., 1986. Metals and Anions. In: Clarke, S Isolation And Identification Of Drugs, 2nd Ed., The Pharmaceutical Press, London.Google Scholar
  32. Monsefi, M., Alaee, S., Moradshahi, A., Rohani, L., 2010. Cadmium induced infertility in male mice, Environmental Toxicology, 25, 94–102.Google Scholar
  33. Morrow, H., 2010. “Cadmium and Cadmium Alloys”. Kirk-Othmer Encyclopedia of Chemical Technology. John Wiley and Sons. 1–36.Google Scholar
  34. Moslemi, M.K., Tavanbakhsh, S., 2011. Selenium-vitamin E supplementation in infertile men: effects on semen parameters and pregnancy rate, International Journal of General Medicine, 23, 99–104.CrossRefGoogle Scholar
  35. Mustafa A.B., Sayied A.A., Atti K.A.A., 2012. Trace minerals profile in wild pasture and in the blood serum of camel in Butana region., Res. Opin. Anim. Vet. Sci., 2, 329–333. Google Scholar
  36. Pflieger-Bruss, S., Schuppe, H.C., Schill, W.B., 2004. The male reproductive system and its susceptibility to endocrine disrupting chemicals, Andrologia, 36, 337–45.CrossRefGoogle Scholar
  37. Pizent, A., Tariba, B., Živković, T. 2012. Reproductive toxicity of metals in men. Arhiv za Higijenu Rada i Toksikologiju, 63, 35–46.CrossRefGoogle Scholar
  38. Prasad, A.S., 2003. "Zinc deficiency: Has been known of for 40 years but ignored by global health organisations", British Medical Journal, 326, 409–410.CrossRefGoogle Scholar
  39. Rutagwenda, T., Lechner-Doll, M., Kaske, M., Engelhardt, W. V., Schultka, W., Schwartz, H. J.,1989. Adaptation strategies of camels on a thornbush savannah pasture, comparison with other domestic animals. Options Méditerranéennes, Série Séminaires n°2, C.I.H.E.A.M., 69–73.Google Scholar
  40. Sağlam, H.S., Altundağ, H., Atik, Y.T., Dündar, M.S., Adsan, Ö, 2015. Trace elements levels in the serum, urine, and semen of patients with infertility, Turkish Journal of Medical Science, 45, 443–448.CrossRefGoogle Scholar
  41. Sakhaee, E., Emadi, L., Abshenas, J., Kheirandish, R., Azari, O., Amiri, E., 2012. Evaluation of epididymal sperm quality following experimentally induced copper poisoning in male rats, Andrologia, 44, 110–116.CrossRefGoogle Scholar
  42. Sghiri, A., Driancourt, M.A., 1999. Seasonal effects on fertility and ovarian follicular growth and maturation in camels (Camelus dromedarius), Animal Reproduction Science, 55, 223–237.CrossRefGoogle Scholar
  43. Shalini, S., Bansal, M.P., 2005. Role of selenium in regulation of spermatogenesis: involvement of activator protein 1, Biofactors, 23, 151–62.CrossRefGoogle Scholar
  44. Shalini, S., Bansal, M.P., 2006. Role of selenium in spermatogenesis: differential expression of cjun and cfos in tubular cells of mice testis, Molecular and Cellular Biochemistry., 292, 27–38.CrossRefGoogle Scholar
  45. Shalini, S., Bansal, M.P., 2007. Alterations in selenium status influences reproductive potential of male mice by modulation of transcription factor NF-kappaB, Biometals, 20, 49–59.CrossRefGoogle Scholar
  46. Shinohara, A., Watanabe, H., 1996. Role of essential trace elements on sexual function and its disorder, Nihon Rinsho, 54, 155–61.Google Scholar
  47. Skidmore, J.A., Morton, K.M., Billah, M., 2013. Artificial insemination in dromedary camels, Animal Reproduction Science, 136, 178–86.CrossRefGoogle Scholar
  48. Sun, J., Yu, G.,, Zhang, Y., Liu, X., Du, C, Wang, L., Li, Z., Wang, C., 2017. Heavy Metal Level in Human Semen with Different Fertility: a Meta-Analysis. Biology of Trace Element research, 176, 27–36.CrossRefGoogle Scholar
  49. Tam, P., Liu, W., 1985. Gonadal development and fertility of mice treated prenatally with cadmium during the early organogenesis stages, Teratology, 32, 453–462.CrossRefGoogle Scholar
  50. Thompson, J., Bannigan, J., 2008. Cadmium: toxic effects on the reproductive system and the embryo, Reproductive Toxicology, 25, 304–315.CrossRefGoogle Scholar
  51. Tremellen, K., 2008. Oxidative stress and male infertility: A clinical perspective, Human Reproduction Update, 14, 243–258.CrossRefGoogle Scholar
  52. Tvrda, E., Peer, R., Sikka, S.C., Agarwal, A., 2015. Iron and copper in male reproduction: a double-edged sword, Journal of Assisted Reproduction and Genetics, 32, 3–16.CrossRefGoogle Scholar
  53. Wani, N.A., Billah, M., Skidmore, J.A., 2008. Studies on liquefaction and storage of ejaculated dromedary camel (Camelus dromedarius) semen, Animal Reproduction Science, 109, 309–318.CrossRefGoogle Scholar
  54. Wdowiak, A., Bakalczuk, G., Bakalczuk, S., 2015. Evaluation of effect of selected trace elements on dynamics of sperm DNA fragmentation. Postȩpy higieny i medycyny doświadczalnej (Online), 31;69, 1405–10.Google Scholar
  55. Wernery U., Abraham A.A., Jyothi T., Abubakar Ali Y., George R.M., 2009. Mineral and vitamin contents in the blood of racing dromedaries in the United Arab Emirates. J. Camel Pract. Res., 16, 39–40. Google Scholar
  56. Wong, C., Mruk, D.D., Lui, W., Cheng, C.Y., 2004. Regulation of blood-testis barrier dynamics: an in vivo study, Journal of Cell Science, 117, 783–798.CrossRefGoogle Scholar
  57. Xu, B., Chia, S.E., Tsakok, M., Ong, C.N., 1993. Trace elements in blood and seminal plasma and their relationship to sperm quality, Reproductive Toxicology, 7, 613–618.CrossRefGoogle Scholar
  58. Zhao, J., Dong, X., Hu, X., Long, Z., Wang, L., Liu, Q., Sun, B., Wang, Q., Wu, Q., Li, L. (2016) Zinc levels in seminal plasma and their correlation with male infertility: A systematic review and meta-analysis, Scientific Reports 2, 6:22386.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Ahmed Ali
    • 1
    • 2
    Email author
  • Derar R. Derar
    • 1
    • 2
  • Essam M. Abdel-Elmoniem
    • 3
  • Tariq I. Almundarij
    • 1
  1. 1.Department of Veterinary Medicine, College of Agriculture and Veterinary MedicineBuraydahSaudi Arabia
  2. 2.Department of Theriogenology, Faculty of Veterinary MedicineAssiut UniversityAssiutEgypt
  3. 3.Department of Soil, College of Agriculture and Veterinary MedicineBuraydahSaudi Arabia

Personalised recommendations