Fetal growth restriction in cows is associated with intrauterine diselementosis
- Authors: Safonov V.A.1, Ermilova T.S.1, Chernitskiy A.E.2
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Affiliations:
- Vernadsky Institute of Geochemistry and Analytical Chemistry of the Russian Academy of Sciences
- Ural Federal Agrarian Scientific Research Center, Ural Branch of the Russian Academy of Sciences
- Issue: Vol 17, No 3 (2025)
- Pages: 208-232
- Section: Biochemistry, Genetics and Molecular Biology
- Published: 31.08.2025
- URL: https://journal-vniispk.ru/2658-6649/article/view/316251
- DOI: https://doi.org/10.12731/2658-6649-2025-17-3-1177
- EDN: https://elibrary.ru/GIKGAX
- ID: 316251
Cite item
Full Text
Abstract
Fetal growth restriction (FGR) is prevalent in highly productive dairy herds and presents a considerable challenge for animal husbandry. One contributing factor to FGR is the deficiency of essential trace elements and impaired placental transport functions in pregnant cows. In this study, we performed a comparative analysis of 12 trace elements and their ratios in the hair of newborn calves with a history of FGR (Group I, n = 18) and those born to cows with a normal pregnancy (Group II, n = 24). FGR was diagnosed based on ultrasound examinations of the pregnant cows performed at 38–45, 60–65, and 110–115 days of gestation using an Easi-Scan-3 scanner with a 4.5–8.5 MHz linear sensor (BCF Technology Ltd., Great Britain) following a previously established and published protocol. Hair samples from the calves were collected from the tail switch immediately before their first colostrum feeding. The concentrations of arsenic, cadmium, cobalt, copper, iron, mercury, manganese, molybdenum, nickel, lead, selenium, and zinc in the hair were analyzed using inductively coupled plasma mass spectrometry (Nexion 300D, Perkin Elmer, USA). To evaluate intrauterine diselementosis based on the trace element levels in the hair, various ratios were calculated: arsenic/selenium, mercury/selenium, lead/selenium, lead/zinc, cadmium/selenium, nickel/zinc, and iron/copper. Calves in Group I had significantly higher levels of cadmium in their hair (increased by 66.7%, P < 0.05) and mercury (increased by 15.0 times, P < 0.05) along with lower levels of copper (decreased by 30.7%, P < 0.05), selenium (decreased by 28.8%, P < 0.05), and zinc (decreased by 26.4%, P < 0.05) compared to calves in Group II. The concentrations of other trace elements in the hair did not differ significantly between the groups. These findings indicate that fetal development in calves during the last trimester of pregnancy occurs under conditions of an imbalance of essential and toxic trace elements. The mercury/selenium ratio in the hair of Group I calves was increased by 45.3 times (P < 0.05) compared to Group II calves, while the lead/selenium ratio was 2.81 times higher (P < 0.05), the cadmium/selenium ratio was 6.63 times higher (P < 0.05), the nickel/zinc ratio was 2.91 times higher (P < 0.05), and the iron/copper ratio was 2.64 times higher (P < 0.05). In this study, we also examined the potential causes and mechanisms underlying these imbalances.
Keywords
About the authors
Vladimir A. Safonov
Vernadsky Institute of Geochemistry and Analytical Chemistry of the Russian Academy of Sciences
Author for correspondence.
Email: safrus2003@mail.ru
ORCID iD: 0000-0002-5040-6178
SPIN-code: 5110-8671
Scopus Author ID: 57198771314
ResearcherId: L-7174-2016
Leading Researcher of the Laboratory of Environmental Biogeochemistry, Doctor of Biological Sciences
Russian Federation, 19, Kosygin Str., Moscow, 119991, Russian Federation
Tatiana S. Ermilova
Vernadsky Institute of Geochemistry and Analytical Chemistry of the Russian Academy of Sciences
Email: tatianaermilov@yandex.ru
ORCID iD: 0000-0002-8251-8545
SPIN-code: 6712-6866
Scopus Author ID: 57956288700
Researcher of the Laboratory of Environmental Biogeochemistry
Russian Federation, 19, Kosygin str., Moscow, 119991, Russian Federation
Anton E. Chernitskiy
Ural Federal Agrarian Scientific Research Center, Ural Branch of the Russian Academy of Sciences
Email: cherae@mail.ru
ORCID iD: 0000-0001-8953-687X
SPIN-code: 3776-3502
Scopus Author ID: 56410871400
ResearcherId: C-6746-2013
Leading Researcher of the Department of Reproductive Biology and Neonatology, Doctor of Biological Sciences
Russian Federation, 112a, Belinskogo str., Yekaterinburg, 620142, Russian Federation
References
- Butko, V. A., Lozovaya, E. G., & Mikhalev, V. I. (2020). Clinical and echographic markers for diagnosing early embryogenesis disorders in cows. Veterinary Pharmacological Bulletin, 2(11), 177-190. https://doi.org/10.17238/issn2541-8203.2020.2.177 EDN: https://elibrary.ru/pxusjv
- Vorobyev, V. I., & Vorobyev, D. V. (2014). Physiological aspects of mineral metabolism in Simmental cows bred under environmental conditions of low Se, I, and Co levels in the environment and feed of the Lower Volga region. Fundamental Research, 8-4, 864-870. EDN: https://elibrary.ru/sjmnij
- Gurkina, L. V., Naumova, I. K., & Lebedeva, M. B. (2016). Mutual action of biogenic trace elements and heavy metals in animal organisms. Agricultural Bulletin of the Upper Volga Region, 1, 32-37. EDN: https://elibrary.ru/tpzsij
- Kovalsky, V. V. (1974). Geochemical ecology. Moscow: Nauka, 300 p.
- Miroshnikov, S. A., Zavyalov, O. A., Frolov, A. N., Kharlamov, A. V., Duskaev, G. K., & Kurilkina, M. Ya. (2016). Elemental composition of wool as a model for studying interelement interactions. Beef Cattle Breeding Bulletin, 4(96), 9-14. EDN: https://elibrary.ru/xilxpt
- Safonov, V. A., Ermilova, T. S., Chernitsky, A. E., & Salimzade, E. A. O. (2024). Predicting the level of trace element nutrition in fetuses of deeply pregnant cows. Siberian Journal of Life Sciences and Agriculture, 16(3). https://doi.org/10.12731/2658-6649-2024-16-3-860 EDN: https://elibrary.ru/hxxvlk
- Skalny, A. V., & Rudakov, I. A. (2004). Bioelements in medicine. Moscow: Mir, 272 p. ISBN: 5-03-003645-8 EDN: https://elibrary.ru/wqrzft
- Abdelrahman, M.M. & Kincaid, R.L. (1993). Deposition of copper, manganese, zinc, and selenium in bovine fetal tissue at different stages of gestation. Journal of Dairy Science, 76(11), 3588-3593. https://doi.org/10.3168/jds.s0022-0302(93)77698-5
- Anas, M., Diniz, W.J.S., Menezes, A.C.B., Reynolds, L.P., Caton, J.S., Dahlen, C.R. & Ward, A.K. (2023). Maternal mineral nutrition regulates fetal genomic programming in cattle: a review. Metabolites, 13(5), 593. https://doi.org/10.3390/metabo13050593 EDN: https://elibrary.ru/cnnbmg
- Azzam, S.M., Kinder, J.E., Nielsen, M.K., Werth, L.A., Gregory, K.E., Cundiff, L.V. & Koch, R.M. (1993). Environmental effects on neonatal mortality of beef calves. Journal of Animal Science, 71(2), 282-290. https://doi.org/10.2527/1993.712282x
- Menezes, A.C.B., McCarthy, K.L., Kassetas, C.J., Baumgaertner, F., Kirsch, J.D., Dorsam, S.T., Neville, T.L., Ward, A.K., Borowicz, P.P., Reynolds, L.P., Sedivec, K.K., Forcherio, J.C., Scott, R. & Caton, J.S. (2022). Vitamin and mineral supplementation and rate of gain in beef heifers I: Effects on dam hormonal and metabolic status, fetal tissue and organ mass, and concentration of glucose and fructose in fetal fluids at d 83 of gestation. Animals, 12(14), 1757. https://doi.org/10.3390/ani12141757 EDN: https://elibrary.ru/owyxrp
- Buczinski, S.M., Fecteau, G., Lefebvre, R.C. & Smith, L.C. (2007). Fetal well-being assessment in bovine near-term gestations: Current knowledge and future perspectives arising from comparative medicine. The Canadian Veterinary Journal, 48(2), 178-183.
- Chen, Y.H., Zhao, M., Chen, X., Zhang, Y., Wang, H., Huang, Y.Y., Wang, Z., Zhang, Z.H., Zhang, C. & Xu, D.X. (2012). Zinc supplementation during pregnancy protects against lipopolysaccharide-induced fetal growth restriction and demise through its anti-inflammatory effect. The Journal of Immunology, 183(1), 454-463. https://doi.org/10.4049/jimmunol.1103579
- Chernitskiy, A. & Safonov, V. (2019). The effects of the vitamin-mineral drug “Antimiopatik” use in cows during the dry period on postnatal growth and health of the offspring. Reproduction in Domestic Animals, 54(S3), 131-132. https://doi.org/10.1111/rda.13528 EDN: https://elibrary.ru/scexqz
- Cygan-Szczegielniak, D., Stanek, M., Giernatowska, E. & Janicki, B. (2014). Impact of breeding region and season on the content of some trace elements and heavy metals in the hair of cows. Folia Biologica, 62(3), 163-169. https://doi.org/10.3409/FB62_3.163
- Dahlen, C.R., Reynolds, L.P. & Caton, J.S. (2022). Selenium supplementation and pregnancy outcomes. Frontiers in Nutrition, 9, 1011850. https://doi.org/10.3389/fnut.2022.1011850 EDN: https://elibrary.ru/jacotg
- Eby, G.N. (2016). Principles of Environmental Geochemistry. Long Grove: Waveland Press, 514 p.
- Fitzgerald, A.M., Ryan, D.P. & Berry, D.P. (2015). Factors associated with the differential in actual gestational age and gestational age predicted from transrectal ultrasonography in pregnant dairy cows. Theriogenology, 84(3), 358-364. https://doi.org/10.1016/j.theriogenology.2015.03.023
- Georgievskii, V.I., Annenkov, B.N. & Samokhin, V.T. (1982). Mineral Nutrition of Animals. London: Butterworths, 475 p. ISBN: 0-408-10770-7 EDN: https://elibrary.ru/rtxvft
- Goff, J.P. (2018). Invited review: Mineral absorption mechanisms, mineral interactions that affect acid-base and antioxidant status, and diet considerations to improve mineral status. Journal of Dairy Science, 101(4), 2763-2813. https://doi.org/10.3168/jds.2017-13112 EDN: https://elibrary.ru/vemohd
- Greenwood, P.L. & Bell, A.W. (2019). Developmental programming and growth of livestock tissues for meat production. Veterinary Clinics of North America: Food Animal Practice, 35(2), 303-319. https://doi.org/10.1016/j.cvfa.2019.02.008
- Greenwood, P.L. & Café, L.M. (2007). Prenatal and pre-weaning growth and nutrition of cattle: long-term consequences for beef production. Animal, 1(9), 1283-1296. https://doi.org/10.1017/S175173110700050X
- Grzeszczak, K., Kwiatkowski, S. & Kosik-Bogacka, D. (2020). The role of Fe, Zn, and Cu in pregnancy. Biomolecules, 10(8), 1176. https://doi.org/10.3390/biom10081176 EDN: https://elibrary.ru/igeamy
- Harvey, K.M., Cooke, R.F., Colombo, E.A., Rett, B., de Sousa, O.A., Harvey, L.M., Russell, J.R., Pohler, K.G. & Brandão, A.P. (2021). Supplementing organic-complexed or inorganic Co, Cu, Mn, and Zn to beef cows during gestation: physiological and productive response of cows and their offspring until weaning. Journal of Animal Science, 99(5), skab095. https://doi.org/10.1093/jas/skab095 EDN: https://elibrary.ru/atclci
- Hicks, Z.M. & Yates, D.T. (2021). Going up inflame: Reviewing the underexplored role of inflammatory programming in stress-induced intrauterine growth restricted livestock. Frontiers in Animal Science, 2, 761421. https://doi.org/10.3389/fanim.2021.761421 EDN: https://elibrary.ru/tgiodw
- Hracsko, Z., Orvos, H., Novak, Z., Pal, A. & Varga, I.S. (2008). Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Report, 13(1), 11-16. https://doi.org/10.1179/135100008X259097
- Issah, I., Duah, M.S., Arko-Mensah, J., Bawua, S.A., Agyekum, T.P. & Fobil, J.N. (2024). Exposure to metal mixtures and adverse pregnancy and birth outcomes: A systematic review. Science of the Total Environment, 908, 168380. https://doi.org/10.1016/j.scitotenv.2023.168380
- Joksimović-Todorović, M., Davidović, V. & Bojanić-Rašović, M. (2016). The effects of some microelements supplementation: Selenium, zinc and copper into dairy cows feeds on their health and reproductive performances. Biotechnology in Animal Husbandry, 32(2), 101-110. https://doi.org/10.2298/BAH1602101J
- Kalaeva, E., Kalaev, V., Chernitskiy, A., Alhamed, M. & Safonov, V. (2020). Incidence risk of bronchopneumonia in newborn calves associated with intrauterine diselementosis. Veterinary World, 13(5), 987-995. https://doi.org/10.14202/vetworld.2020.987-995 EDN: https://elibrary.ru/vnsrtq
- Lewicka, I., Kocyłowski, R., Grzesiak, M., Gaj, Z., Oszukowski, P. & Suliburska, J. (2017). Selected trace elements concentrations in pregnancy and their possible role - Literature review. Ginekologia Polska, 88(9), 509-514. https://doi.org/10.5603/gp.a2017.0093
- Lonergan, P., Forde, N. & Spencer, T. (2016). Role of progesterone in embryo development in cattle. Reproduction, Fertility and Development, 28(1-2), 66-74. https://doi.org/10.1071/rd15326
- Mao, W.H., Albrecht, E., Teuscher, F., Yang, Q., Zhao, R.Q. & Wegner, J. (2008). Growth-and breed-related changes of fetal development in cattle. Asian-Australasian Journal of Animal Sciences, 21(5), 640-647. https://doi.org/10.5713/ajas.2008.70293
- Marques, R.S., Cooke, R.F., Rodrigues, M.C., Cappellozza, B.I., Mills, R.R., Larson, C.K., Moriel, P. & Bohnert, D.W. (2016). Effects of organic or inorganic cobalt, copper, manganese, and zinc supplementation to late-gestating beef cows on productive and physiological responses of the offspring. Journal of Animal Science, 94(3), 1215-1226. https://doi.org/10.2527/jas.2015-0036
- McCarthy, K.L., Menezes, A.C., Kassetas, C.J., Baumgaertner, F., Kirsch, J.D., Dorsam, S.T., Neville, T.L., Ward, A.K., Borowicz, P.P., Reynolds, L.P., Sedivec, K.K., Forcherio, J.C., Scott, R., Caton, J.S. & Dahlen, C.R. (2022). Vitamin and mineral supplementation and rate of gain in beef heifers II: effects on concentration of trace minerals in maternal liver and fetal liver, muscle, allantoic, and amniotic fluids at day 83 of gestation. Animals, 12(15), 1925. https://doi.org/10.3390/ani12151925 EDN: https://elibrary.ru/jwjlpc
- McKeating, D.R., Fisher, J.J. & Perkins, A.V. (2019). Elemental metabolomics and pregnancy outcomes. Nutrients, 11(1), 73. https://doi.org/10.3390/nu11010073 EDN: https://elibrary.ru/chgslm
- Mehdi, Y. & Dufrasne, I. (2016). Selenium in cattle: a review. Molecules, 21(4), 545. https://doi.org/10.3390/molecules21040545 EDN: https://elibrary.ru/wuigrb
- Mikhalev, V., Shabunin, S., Safonov, V. & Chernitskiy, A. (2018). Metabolic status of newborn calves with intrauterine growth retardation. Reproduction in Domestic Animals, 53(S2), 168-168. https://doi.org/10.1111/rda.13272 EDN: https://elibrary.ru/uyvpyt
- Miroshnikov, S.A., Zavyalov, O.A., Frolov, A.N., Bolodurina, I.P., Kalashnikov, V.V., Grabeklis, A.R., Tinkov, A.A. & Skalny, A.V. (2017). The reference intervals of hair trace element content in Hereford cows and heifers (Bos taurus). Biological Trace Element Research, 180(1), 56-62. https://doi.org/10.1007/s12011-017-0991-5 EDN: https://elibrary.ru/xnceki
- Miroshnikov, S., Zavyalov, O., Frolov, A., Sleptsov, I., Sirazetdinov, F. & Poberukhin, M. The content of toxic elements in hair of dairy cows as an indicator of productivity and elemental status of animals. Environmental Science and Pollution Research, 26(18), 18554-18564. https://doi.org/10.1007/s11356-019-05163-5 EDN: https://elibrary.ru/itdenp
- Mion, B., Madureira, G., Spricigo, J.F.W., King, K., Van Winters, B., LaMarre, J., LeBlanc, S.J., Steele, M.A. & Ribeiro, E.S. (2023). Effects of source of supplementary trace minerals in pre- and postpartum diets on reproductive biology and performance in dairy cows. Journal of Dairy Science, 106(7), 5074-5095. https://doi.org/10.3168/jds.2022-22784 EDN: https://elibrary.ru/irlmkn
- Neve, J. (1992). Clinical implications of trace elements in endocrinology. Biological Trace Element Research, 32(1), 173-185. https://doi.org/10.1007/BF02784602 EDN: https://elibrary.ru/rxzwum
- Nezhdanov, A., Shabunin, S., Mikhalev, V., Klimov, N. & Chernitskiy, A. (2014). Endocrine and metabolic mechanisms of embryo and fetal intrauterine growth retardation in dairy cows. Turkish Journal of Veterinary and Animal Sciences, 38(6), 675-680. https://doi.org/10.3906/vet-1405-12 EDN: https://elibrary.ru/ssgdbn
- Nezhdanov, A.G., Mikhalev, V.I., Chusova, G.G., Papin, N.E., Chernitskiy, A.E. & Lozovaya, E.G. (2016). Metabolic status of the cows under intrauterine growth retardation of embryo and fetus. Agricultural Biology, 51(2), 230-237. https://doi.org/10.15389/agrobiology.2016.2.230eng EDN: https://elibrary.ru/vvhkih
- Ojeda, M.L., Nogales, F., Romero-Herrera, I. & Carreras, O. (2021). Fetal programming is deeply related to maternal selenium status and oxidative balance; experimental offspring health repercussions. Nutrients, 13(6), 2085. https://doi.org/10.3390/nu13062085 EDN: https://elibrary.ru/htkrwl
- Omur, A., Kirbas, A., Aksu, E., Kandemir, F., Dorman, E., Kaynar, O. & Ucar, O. (2016). Effects of antioxidant vitamins (A, D, E) and trace elements (Cu, Mn, Se, Zn) on some metabolic and reproductive profiles in dairy cows during transition period. Polish Journal of Veterinary Sciences, 19(4), 697-706. https://doi.org/10.1515/pjvs-2016-0088 EDN: https://elibrary.ru/yxuqqp
- Patra, R.C., Swarup, D., Sharma, M.C. & Naresh, R. (2006). Trace mineral profile in blood and hair from cattle environmentally exposed to lead and cadmium around different industrial units. Journal of Veterinary Medicine. A, Physiology, Pathology, Clinical Medicine, 53(10), 511-517. https://doi.org/10.1111/j.1439-0442.2006.00868.x
- Plemyashov, K. & Korochkina, E. (2022). Monitoring of vitamin-mineral metabolism’ indicators in cows of different period of lactation. FASEB Journal, 36(S1), R3113. https://doi.org/10.1096/fasebj.2022.36.S1.R3113 EDN: https://elibrary.ru/vhdzqa
- Reynolds, L.P., Borowicz, P.P., Caton, J.S., Crouse, M.S., Dahlen, C.R. & Ward, A.K. (2019). Developmental programming of fetal growth and development. Veterinary Clinics of North America: Food Animal Practice, 35(2), 229-247. https://doi.org/10.1016/j.cvfa.2019.02.006
- Safonov, V. & Chernitskiy, A. (2022). Trace elements deficiency in dairy cows in the biogeochemical province of the Republic of Belarus and biological effects of its correction. In: New Prospects in Environmental Geosciences and Hydrogeosciences [H. Chenchouni, H. I. Chaminé, M. F. Khan, et al. (Eds.)]. CAJG 2019. Advances in Science, Technology & Innovation. Cham: Springer, pp. 185-187. https://doi.org/10.1007/978-3-030-72543-3_41 EDN: https://elibrary.ru/oaaagpd
- Safonov, V., Salimzade, E., Ermilova, T. & Chernitskiy, A. (2022). Retrospective diagnosis of intrauterine diselementosis in newborn calves. BIO Web of Conferences, 52, 00033. https://doi.org/10.1051/bioconf/20225200033 EDN: https://elibrary.ru/wpdjbv
- Safonov, V.A. (2018). Biological role of selenium and correction effects of its content in the organism of animals. Geochemistry International, 56(10), 1046-1050. https://doi.org/10.1134/s0016702918100105 EDN: https://elibrary.ru/yswlbb
- Safonov, V.A., Mikhalev, V.I. & Chernitskiy, A.E. (2018). Antioxidant status and functional condition of respiratory system of newborn calves with intrauterine growth retardation. Agricultural Biology, 53(4), 831-841. https://doi.org/10.15389/agrobiology.2018.4.831eng EDN: https://elibrary.ru/uzbltk
- Shabunin, S., Nezhdanov, A., Mikhalev, V., Lozovaya, E. & Chernitskiy, A. (2017). Diselementosis as a risk factor of embryo loss in lactating cows. Turkish Journal of Veterinary and Animal Sciences, 41(4), 453-459. https://doi.org/10.3906/vet-1609-76 EDN: https://elibrary.ru/zcymlp
- Suttle, N.F. (2022). Mineral Nutrition of Livestock. 5th ed. Boston: CABI, 600 p. https://doi.org/10.1079/9781789240924.0000
- Van Eetvelde, M., Kamal, M.M., Hostens, M., Vandaele, L., Fiems, L.O. & Opsomer, G. (2016). Evidence for placental compensation in cattle. Animal, 10(8), 1342-1350. https://doi.org/10.1017/S1751731116000318
- Van Emon, M., Sanford, C. & McCoski, S. (2020). Impacts of bovine trace mineral supplementation on maternal and offspring production and health. Animals, 10(12), 2404. https://doi.org/10.3390/ani10122404 EDN: https://elibrary.ru/ylxmrs
- Vorobyov, V., Vorobyov, D., Polkovnichenko, A. & Safonov, V. (2018). The physiological status of acclimatized Simmental cattle of the Austrian selection in the biogeochemical conditions of the Lower Volga Region. American Journal of Agriculture and Forestry, 6(6), 198-207. https://doi.org/10.11648/j.ajaf.20180606.17
- Wu, G., Bazer, F.W., Wallace, J.M. & Spencer, T.E. (2006). Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science, 84(9), 2316-2337. https://doi.org/10.2527/jas.2006-156
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