Relationship between concentrations of macro and trace elements in serum and follicular, oviductal, and uterine fluids of the dromedary camel (Camelus dromedarius)

  • Ayman Abdel-Aziz SwelumEmail author
  • Islam M. SaadeldinEmail author
  • Sameh A. Abdelnour
  • Hani Ba-Awadh
  • Mohammed E. Abd El-Hack
  • Asmaa M. Sheiha
Regular Articles
Part of the following topical collections:
  1. Camelids


This study aimed at investigating the relationship between concentrations of macro and trace elements in blood serum, and fluids from small and large follicles (SFF and LFF, respectively), oviduct (OF), and uterus (UF) of female dromedary camels. Fluids from small (2–6 mm) and large follicles (7–20 mm), oviduct and uterus, and blood samples were collected from 19 camels. The results indicated that the concentrations of serum Mg, Fe, and Mn were significantly higher than their follicular fluid, OF, and UF concentrations. Levels of Zn, Fe, Cu, Cr, and Mn were significantly higher in SFF than in LFF. Se and Mo concentrations were higher in LFF. Co concentration was lower in serum than in reproductive tract fluids. Cr concentration was higher in UF and OF than in the serum, SFF, and LFF. High Ca concentration was observed for serum and SFF, followed by LFF. The concentration of Na was about 1.18-fold higher in SFF than in serum, OF, and LFF, and approximately 4.1-fold higher in serum than in UF. K was present in higher concentration in SFF than in serum and LFF; however, its concentration was low in UF and OF. In conclusion, this study shows the concentrations of certain elements in small and large follicular, uterine, and oviductal fluids, which may be low or high depending on their function in the development and growth of follicles. This information can support the development of new media for in vitro oocyte maturation and fertilization of female camels.


Trace minerals Follicular fluid Female camel Follicles 



We would like to thank the DSR and RSSU (Researchers Support and Services Unit) of King Saud University for their technical support.

Funding information

This study was supported by King Saud University, Deanship of Scientific Research (DSR), Research Group #RG-1438-066.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Anchordoquy, J.P., Anchordoquy, J.M., Sirini M.A., Mattioli G., Picco S.J., and Furnus C.C., 2013. Effect of different manganese concentrations during in vitro maturation of bovine oocytes on DNA integrity of cumulus cells and subsequent embryo development, Reproduction in Domestic Animal, 48(6), 905–11. doi: CrossRefGoogle Scholar
  2. Anchordoquy, J.P., Anchordoquy, J.M., Sirini, M.A, Testa J.A., Peral-García, P., and Furnus, C.C., 2015. The importance of manganese in the cytoplasmic maturation of cattle oocytes: blastocyst production improvement regardless of cumulus cells presence during in vitro maturation, Zygote, 1, 139–48.Google Scholar
  3. Bavister, B.D., 2000. Interactions between embryos and the culture milieu, Theriogenology, 53, 619–26.PubMedCrossRefGoogle Scholar
  4. Bedwal R.S. and Bahuguna A., 1994. Zinc, copper and selenium in reproduction, Experientia, 50, 626–640.PubMedCrossRefGoogle Scholar
  5. Bi, C.M., Zhang, Y.L., Liu, F.J., Zhou, T.Z., Yang, Z.J., Gao, S.Y., Wang, S.D., Chen, X.L., Zhai, X.W., Ma, X.G., Jin, L.J. and Wang S., 2013. The effect of molybdenum on the invitro development of mouse preimplantation embryos, Systems Biology in Reproductive Medicine, 59(2), 69–73.PubMedCrossRefGoogle Scholar
  6. Brison, D.R. and Leese, H.J., 1993. Role of chloride transport in the development of the rat blastocyst, Biology of Reproduction. 48, 692–702.PubMedCrossRefGoogle Scholar
  7. Casslen B., and Nilsson B., 1984. Human uterine fluid, examined in undiluted samples for osmolarity and the concentrations of inorganic ions, albumin, glucose, and urea, American Journal of Obstetric and Gynecology, 150, 877–81.CrossRefGoogle Scholar
  8. Chang, S.C.S., Jones, J.D., and Ellefson R.D., 1976. The porcine ovarian follicle: I. Selected chemical analysis of follicular fluid at different developmental stages, Biology of Reproduction, 15, 321–328.PubMedGoogle Scholar
  9. Choi, S.K., Park, K.D, Kim, D.A, Lee, D.W., and Kim, Y.J., 2013. Preparation of camel milk liposome and its anti-aging effects, Journal of Society of Cosmetic Scientists of Korea, 40(2), 155–161.CrossRefGoogle Scholar
  10. Corrah, L., 1996. Trace mineral requirement of grazing cattle, Animal Feed Science and Technology, 59, 61–70.CrossRefGoogle Scholar
  11. El-Redwan, R.M. and Tabll A., 2007. Camel lactoferrin markedly inhibits hepatitis C virus genotype 4 infection of human peripheral blood leukocytes, Journal of Immunoassay and Immunochemistry, 28(3), 267–277.CrossRefGoogle Scholar
  12. Gerard, N., Loiseau, S., Duchamp, G., and Seguin, F., 2002. Analysis of the variations of follicular fluid composition during follicular growth and maturation in the mare using proton nuclear magnetic resonance (1H NMR), Reproduction, 124, 241–248.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Geshi, M., Takenouchi, N., Yamauchi, N. and Nagai T., 2000. Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells, Biology of Reproduction, 63, 1730–1734.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Ghoneim, I.M., Waheed, M.M., El-Bahr, S.M., Alhaider A.K., and Al-Eknah, M.M., 2013. Comparison of some biochemical and hormonal constituents of overs follicles and preovulatory follicles in camels (Camelus dromedarius), Theriogenology, 79, 647–652.PubMedCrossRefPubMedCentralGoogle Scholar
  15. Greger, J.L., 1998. Dietary standards for manganese: overlap between nutritional and toxicological studies, Journal of Nutrition, 128, 368S–371S.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Grippo, A.A., Henault, M.A., Anderson, S.H., and Killian, G.J., 1992. Cation concentrations in fluid from the oviduct ampulla and isthmus of cows during the estrous cycle, Journal of Dairy Science., 75, 58–65.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Habib, H.M., Ibrahim, W.H., Schneider-Stock, R., and Hassan, H.M. (2013). Camel milk lactoferrin reduces the proliferation of colorectal cancer cells and exerts antioxidant and DNA damage inhibitory activities, Food Chemistry, 141(1), 148–152PubMedCrossRefPubMedCentralGoogle Scholar
  18. Hamdi, M., Lopera-Vasque, R., Maillo, V., Sanchez-Calabuig M.J., Nunez, C., Gutierrez-Adan A., and Rizos D., 2018. Bovine oviductal and uterine fluid support in vitro embryo development. Reproduction, Fertility and Development, CrossRefGoogle Scholar
  19. Hobbs, J.G., and Kaye, P.L., 1986. Glycine and Na+ transport in preimplantation mouse embryos, Journal of Reproduction and Fertility, 77, 61–6.PubMedCrossRefGoogle Scholar
  20. Hugentobler, S.A., Morris, D.G., and Kane M.T., 2004. In situ oviduct and uterine pH in cattle, Theriogenology, 61, 1419–27.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hugentobler, S.A., Morris, D.G., Sreenan, J.M., and Diskin, M.G., 2007. Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine, Theriogenology, 68, 538–548.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Hurley, L., 1981. Teratogenic aspects of manganese, zinc and copper nutrition, Physiological Reviews, 61, 249–295PubMedCrossRefPubMedCentralGoogle Scholar
  23. Hussein, H.A., and Staufenbiel, R., 2012. Variations in copper concentration and ceruloplasmin activity of dairy cows in relation to lactation stages with regard to ceruloplasmin to copper ratios, Biological trace element research, 146(1), 47–52PubMedCrossRefPubMedCentralGoogle Scholar
  24. Iwata, H., Hashimoto, S., Ohota, M., Kimura, K., Shibano, K., and Miyake, M., 2004. Effects of follicle size and electrolytes and glucose in maturation medium on nuclear maturation and developmental competence of bovine oocytes, Reproduction. 127, 159–164.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Jeon, Y., Yoon, J.D., Cai, L., Hwang S.U., Kim, E., Zheng, Z., Lee, E., Kim, D.Y., and Hyun, S.H., 2014. Supplementation of zinc on oocyte in vitro maturation improves preimplatation embryonic development in pigs, Theriogenology, 82(6), 866–874.PubMedCrossRefPubMedCentralGoogle Scholar
  26. Jordan, E.R., Chapman, T.E., Holtan, D.W., and Swanson, L.V., 1983. Relationship of dietary crude protein to composition of uterine secretions and blood in high-producing postpartum dairy cows, Journal of Dairy Science, 66, 1854–62PubMedCrossRefPubMedCentralGoogle Scholar
  27. Junior, A.R.P., Tilburg, M.E., Lobo, M.D.P., Monterio-Moeriro, A.C.O., Melo, C.H.S., Souza-Fabjan, J.M.G., Araugo, A.A., Melo, L.M., Teixeria, D.I.A., Moura, A.A. and Freitas, V.J.F., 2018. Proteomic analysis of follicular fluid from tropically adapted goats. Animal Reproduction Journal, 188, 35–44. doi: Scholar
  28. Kanwar, J.R., Roy, K., Patel, Y., Zhou, S.F., Singh, M.R., Singh, D., Nasir, M., Sehgal, R., Sehgal, A., Singh, R.S., et al., 2015. Multifunctional iron bound lactoferrin and nanomedicinal approaches to enhance its bioactive functions, Molecules 20(6), 9703–9731.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Kenny, D.A., Humpherson, P., Leese, H.J., Mooris, D., Tomos, A., Diskin, M.G., et al., 2002. Effect of elevated systemic concentrations of ammonia and urea on the metabolite and ionic composition of oviductal fluid in cattle, Biology of Reproduction, 66, 1797–804.PubMedCrossRefPubMedCentralGoogle Scholar
  30. Kolesarova, A., Capcarova, M., Medvedova, M., Sirotkin, A.V., Kovacik, J., 2011. In vitro assessment of iron effect on porcine ovarian granulosa cells: secretory activity, markers of proliferation and apoptosis, Physiological Research, 60, 503–510PubMedGoogle Scholar
  31. Kumar, S., Pandey, A.K., Razzaque, W.A.A, Dwived, D.K., 2011. Importance of micro minerals in reproductive performance of livestock, Veterinary World, 4(5), 230–233CrossRefGoogle Scholar
  32. Lapointe, S., and Sirard, M.A., 1996. Importance of calcium for the binding of oviductal fluid proteins to the membranes of bovine spermatozoa, Molecular Reproduction and Development, 44, 234–40.PubMedCrossRefGoogle Scholar
  33. Leroy, J.L., Vanholder, T., Delanghe, J.R., Opsomer, G., Vansoom, A., Bols, P.E.,and de Kruif, A., 2004. Metabolite and ionic composition of follicular fluid from different sized follicles and their relationship to serum concentrations in dairy cows, Animal Reproduction Science, 80, 201–211.PubMedCrossRefGoogle Scholar
  34. Leung, P.C.K., and Steele, G.L., 1992. Intracellular signaling in the gonads, Endocrine Reviews, 13, 476–497.PubMedGoogle Scholar
  35. Lieu, P.T., Heiskala, M., Peterson, P.A., and Yang, Y., 2001. The roles of iron in health and disease. Molecular Aspects of Medicine, 22, 1–87.PubMedCrossRefGoogle Scholar
  36. Massányi, P., Trandžík, J., Nad, P., Koréneková, B., Skalická, M., Toman, R., Lukáč, N., Strapák, P., Halo M., and Turčan J., 2003. Concentration of copper, iron, zinc, cadmium, lead, and nickel in boar semen and relation to the spermatozoa quality. Journal of Environmental Science and Health, Part A: Toxic/ Hazardous Substances and Environmental Engineering, 38(11), 2643–2651.CrossRefGoogle Scholar
  37. Ménézo, Y., Lichtblau, I., and Elder, K., 2013. New insights into human pre-implantation metabolism in vivo and in vitro. Journal of Assisted Reproduction and Genetics 30, 293–303.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Ménézo, Y., Guérin, P., and Elde K., 2015. The oviduct: a neglected organ due for re-assessment in IVF. Mini Review. Reproductive BioMedicine Online (2015).Google Scholar
  39. Mistry, H.D., Pipkin, F.B., Redman, C.W.G., and Poston, L., 2012. Selenium in reproductive health. American Journal of Obstetrics and Gynecology, 206, 21–30.PubMedCrossRefGoogle Scholar
  40. Mitchell, L.M., Robinson, J.J., Watt, R.G., McEvoy, T.G., Ashworth, C.J., Rooke, J.A., and Dwyer, C.M., 2007. Effects of cobalt/vitamin B12 status in ewes on ovum development and lamb viability at birth. Reproduction, Fertility and Development, 19, 553–562.CrossRefGoogle Scholar
  41. Murugan, M.A., Gangadharan, B., and Mathur, P.P., 2002. Antioxidative effect of fullerenol on goat epididymal spermatozoa. Asian Journal of Andrology., 4, 149–152.PubMedGoogle Scholar
  42. Nandi, S., Girish Kumar, V., Manjunatha, B.M., Ramesh, H.S., Gupta, P.S., .2008. Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells. Theriogenology, 69(2), 186–96.PubMedCrossRefGoogle Scholar
  43. Pechova, A., and Pavlata L. (2007). Chromium as an essential nutrient: a review. Veterinarni Medicina, 52(1), 1–18. CrossRefGoogle Scholar
  44. Phillipo, M., Humphries, W.R., Atkinson, T., Henderson, G.D., and Gaythwaite, P.H., 1987. The effect of molybdenum and iron on copper status, puberty, fertility and oestrus cycles in cattle. The Journal of Agricultural Science, 109, 326–336.Google Scholar
  45. Pillai, V.V., Weber, D.M., Phinney, B.S., and Selvaraj, V., 2017. Profiling of proteins secreted in the bovine oviduct reveals diverse functions of this luminal microenvironment. PLoS ONE, 12(11), e0188105.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Qu, A.F., Ying, X., Guo, W., Guo, Q., Chen, G., Liu, Y., and Ding, Z., 2007. The role of Zn-a glycoprotein in sperm motility is mediated by changes in cyclic AMP. Reproduction, 134, 569–576.PubMedCrossRefGoogle Scholar
  47. Ramos, G.B., Sia, A.J., Callejas, N.A.N., Revilla, C.J.P., Alfonso, N., and Sia, S.G., 2013. Pregestational and gestational maternal selenium – supplement: influence on ethanol – induced dysmorphogenesis in murine postimplantation embryos. Asian journal of experimental biological sciences, 4, 361–368.Google Scholar
  48. Russell, S.T., Russell, T.P., Zimmerman, B.A., and Domin, M.J., 2004. Induction of lipolysis in vitro and loss of body fat in vivo by zinc-alpha2-glycoprotein, Biochimica et Biophysica Acta, 1636, 59–68.PubMedCrossRefGoogle Scholar
  49. Saadeldin, I.M., Swelum, A., Alzahrani F.A., and Alowaimer, A. N., 2018. The current perspectives of dromedary camel stem cells research. Review Article, International Journal of Veterinary Science and Medicine, 6, S27–S30.PubMedGoogle Scholar
  50. Salleh, N., Baines, D.L., Naftalin, R.J., and Milligan, S.R., 2005. The hormonal control of uterine fluid secretion and adsorption. The Journal of Membrane Biology, 206, 17–28.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Shori, A.B., 2015. Camel milk as a potential therapy for controlling diabetes and its complications: a review of in vivo studies. Journal of Food and Drug Analysis, 23(4), 609–618.PubMedCrossRefPubMedCentralGoogle Scholar
  52. Sreenan, J.M., and Morris, D.G., 2007. Amino acids in oviduct and uterine fluid and blood plasma during the estrous cycle in the bovine. Molecular Reproduction and Development, 74, 445–454. doi: Scholar
  53. Stock, C.E., and Fraser, L.R., 1989. Divalent cations, capacitation and the acrosome reaction in human spermatozoa. Journal of Reproduction and Fertility, 87, 463–78.PubMedCrossRefPubMedCentralGoogle Scholar
  54. Swelum, A.A. and Alowaimer, A.N., 2015. The efficacy of controlled internal drug release (CIDR) in synchronizing the follicular wave in dromedary camels (Camelus dromedarius) during the breeding season. Theriogenology, 84, 1542–1548.PubMedCrossRefPubMedCentralGoogle Scholar
  55. Swelum, A.A., Saadeldin, I., Moumen, A., Ba-Awadh, H. and Alowaimer, A.N., 2018. Efficient follicular wave synchronization using a progesterone-releasing intravaginal device (PRIDΔ) in Camelus dromedaries. Theriogenology 118, 203–211.PubMedCrossRefPubMedCentralGoogle Scholar
  56. Tareq, K.M., Akter, Q.S., Khandoker, M.A., and Tsujii, H., 2012. Selenium and vitamin E improve the in vitro maturation, fertilization and culture to blastocyst of porcine oocytes. Journal of Reproduction and Development 58(6), 621–8.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Tibary, A., and Anouassi, A., 1997. Reproductive physiology in the female camelidae. In: Theriogenology in camelidae: anatomy, physiology, pathology and artificial breeding. IAVH II. Rabat, Morocco. 169-241.Google Scholar
  58. Tuormaa, T. E., 2000. Chromium selenium copper and other trace minerals in health and reproduction. Journal of Molecular Medicine, 15, 145–157.Google Scholar
  59. Ufer, C., Wang, C.C., 2011. The roles of glutathione peroxidases during embryo development. Frontiers in Molecular Neuroscience, 4, 1–14.Google Scholar
  60. Ur-Rahman, Z., Bukhari, S.A., Ahmad, N., Akhtar, N., Ijaz, A., Yousaf, M.S. and Ha, I.U., 2008. Dynamics of follicular fluid in one-humped camel (Camelus dromedarius). Reproduction in Domestic Animal, 43, 664–671.CrossRefGoogle Scholar
  61. Vito, L., Vincenzo, T., Marco, D., Mohamed, H., Mabrouk, M.S., Giovanni, M.L., and Cataldo, D., 2009. A survey of chemical and nutritional characteristics of halophytes plants used by camels in Southern Tunisia. Tropical Animal Health and Production 41, 209–215.CrossRefGoogle Scholar
  62. Whitaker, M., 2006. Calcium at fertilization and in early development. Physiological Reviews. 86(1), 25–88.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Zhang, Y.L., Liu, F.J., Chen, X.L., Zhang, Z.Q., Shu, R.Z.,Yu, X.L., Zhai, X.W., Jin, L.J., Ma, X.G., Qi, Q., and Liu, Z.J,. 2013. Dual effects of molybdenum on mouse oocyte quality and ovarian oxidative stress. Systems Biology in Reproductive Medicine, 59(6), 312–318.PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Animal Production, College of Food and Agricultural SciencesKing Saud UniversityRiyradhKingdom of Saudi Arabia
  2. 2.Department of Theriogenology, Faculty of Veterinary MedicineZagazig UniversityZagazigEgypt
  3. 3.Physiology Department, Faculty of veterinary MedicineZagazig UniversityZagazigEgypt
  4. 4.Animal Production Department, Faculty of AgricultureZagazig UniversityZagazigEgypt
  5. 5.Poultry Department, Faculty of AgricultureZagazig UniversityZagazigEgypt

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