Separate indices of homeostasis and the balance of the prooxidant–oxidant system in sheep for fetoplacental insufficiency


P.M. Skliarov, S.J. Fedorenko, S.V. Naumenko, O.V. Onyshhenko, A.M. Pasternak, K.O. Holda

Our research is aimed at solving one of the primary problems of sheep farming – receiving a viable lambs, as the level of neonatal mortality of lambs is 15% and above, which significantly reduces the profitability of the livestock industry. One of the reasons for this is the fetoplacental insufficiency, which causes the violation of antenatal development and, as a consequence, decline of the clinical condition and potential of development of newborns. Solving the problem of fetoplacental malnutrition is primarily due to issues of diagnosis and prevention, which are difficult even for humane medicine. In veterinary obstetrics this direction remains insufficiently investigated. There are only a few publications, especially for sheep, but they are devoted to the study of several other aspects of fetoplacental insufficiency. Fetoplacental malnutrition is a multifactorial pathology, but in livestock production, ecologically deficient factors and defective/unbalanced feeding are the leading ones, which negatively affect the structure and function of the fetoplacental complex in particular. In particular, the concentration of free radical oxyslides increases while simultaneously reducing the antioxidant defense of the organism. According to the results of studies of individual homeostasis and the balance of the prooxidant–antioxidant system, their differences in the sheep breed are clinically healthy, compared with the animals for fetoplacental insufficiency. The results obtained will be used by us in the further development of the method of objective diagnosis and the program of rational prevention of fetoplacental insufficiency in sheep.

Keywords: Viable lambs; Antenatal pathology; Diagnosis; Antioxidant defense; Fetoplacental complex

Agarwal, A., Aponte‒Mellado, A., Premkumar, B.J., Shaman, A., Gupta, S. (2012). The effects of oxidative stress on female reproduction: a review. Reprod. Biol. Endocrinol., 10 (1), 49. doi: 10.1186/1477‒7827‒10‒49.

Agarwal, A., Gupta, S., Sikka, S. (2006). The role of free radicals and antioxidants in reproduction. Curr. Opin. Obstet. Gynecol., 18, 325‒332. doi: 10.1097/01.gco.0000193003.58158.4e.

Ajlamazjan, J.K., Kulakov, V.I., Radzinskij, V.E., Savel’eva, G.M., red. (2013). Akusherstvo: nacional’noe rukovodstvo. GJeOTAR–Media, Moscow (in Russian).

Al‒Gubory, K.H., Bolifraud, P., Germain, G., Nicole, A., Ceballos‒Picot, I. (2004). Antioxidant enzymatic defence systems in sheep corpus luteum throughout pregnancy. Reproduction, 128 (6), 767‒774. doi: 10.1530/rep.1.00389.

Al–Gubory, K.H., Fowler, P.A., Garrel, C. (2010). The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int. J. Biochem. Cell Biol., 42 (10), 1634–1650. doi: 10.1016/j.biocel.2010.06.001.

Alonso‒Alvarez, C., Canelo, T., Romero‒Haro, A.Á. (2017). The oxidative cost of reproduction: Theoretical questions and alternative mechanisms. BioScience, 67(3), 258‒270. doi: 10.1093/biosci/biw176.

Antunović, Z., Šperanda, M., Steine,r Z. (2004). The influence of age and the reproductive status to the blood indicators of the ewes. Arch. Tierzucht Dumm., 47, 265–273. doi: 10.5194/aab–47–265–2004.

Audette, M.C., Kingdom, J.C. (2018). Screening for fetal growth restriction and placental insufficiency. Seminars in Fetal and Neonatal Medicine, 23 (20), 119‒125. doi: 10.1016/j.siny.2017.11.004.

Bardien, N., Whitehead, C.L., Tong, S., Ugoni, A., McDonal, S., Walker, S.P. (2016). Placental insufficiency in fetuses that slow in growth but are born appropriate for gestational age: a prospective longitudinal study. PloS one, 11 (1): e0142788. doi: 10.1371/journal.pone.0142788.

Basistij, O.V. (2016). Morfofunkcіonal'nі zmіni v placentі u vagіtnih pri zatrimcі rostu ploda. Health of women, 8 (114), 55–58. doi: 10.15574/HW.2016.114.55 (in Ukrainian).

Bekmukhambetov, Y., Mamyrbayev, A., Dzharkenov, T., Kravtsova, N., Utesheva, Z., Tusupkaliev, A., Ryzhkova, S., Darzhanova, K., Bekzhanova, M. (2016). Metabolic and immunologic aspects of fetoplacental insufficiency. Am. J. Reprod. Immunol., 76 (4), 299‒306. doi: 10.1111/aji.12544.

Burkitova, A.M., Prokhorova, V.S., Bolotskikh, V.M. (2017). Aktual'nye diagnosticheskie i klinicheskie problemy pri perenoshennoj beremennosti v sovremennom akusherstve. Zhurnal akusherstva i zhenskih boleznej, 66 (2), 93–103. doi: 10.17816/JOWD66293–103.

Burton, G.J., Jauniaux, E. (2011). Oxidative stress. Best Practice & Research Clinical Obstetrics & Gynaecology, 25 (3), 287–299.

Camacho, L.E., Chen, X., Hay, W.W. Jr., Limesand, S.W. (2017). Enhanced insulin secretion and insulin sensitivity in young lambs with placental insufficiency‒induced intrauterine growth restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 313 (2), 101‒109. doi: 10.1152/ajpregu.00068.2017.

Costa, V.M., Carvalho, F., Bastos, M.L., Carvalho, R.A., Carvalho, M., Remião, F. (2011). Contribution of catecholamine reactive intermediates and oxidative stress to the pathologic features of heart diseases. Curr. Med. Chem., 18 (15), 2272–2314. doi: 10.2174/092986711795656081.

Crempien, C. (2001). Control de la mortalidad neonatal de corderos. In Cursos Avances en Producción Ovina. Serie Actas INIA N◦ 10; INIA: Santiago, Chile, 51–67.

Diner, N.M., Uzlova, T.V., Kirsanov, M.S. (2016). Hronicheskaja placentarnaja nedostatochnost': voprosy diagnostiki i akusherskoj taktiki. Vestnik uralskoi meditsinskoi akademicheskoi nauki, 3, 5–13. doi: 10.22138/2500‒0918‒2016‒15‒3‒5‒13 (in Russian).

Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev., 82 (1), 47–95. doi: 10.1152/physrev.00018.2001.

Durmuș, İ., Evcİmen, M., Salİm, M.N., Küçükkurt, İ., İnce, S., Eryavuz, A. (2017). Determination of changes in some biochemical parameters and oxidant–antioxidant balance after food intake in sheep. Kocatepe Veterinary Journal, 10 (1), 1–6. doi: 10.5578/kvj.46508.

Duttaroy, A.K. (2014). Transport of fatty acids across the human placenta: a review. Prog Lipid Res., 48 (1), 52–61. doi: 10.1016/j.plipres.2008.11.001.

Dwyer, C.M., Morgan, C.A. (2006). Maintenance of body temperature in the neonatal lamb: effects of breed, birth weight, and litter size. J Anim Sci, 84,1093‒1101. doi: 10.2527/2006.8451093x.

Erisir, M., Benzer, F., Kandemir, F.M. (2009). Changes in the rate of lipid peroxidation in plasma and selected blood antioxidants before and during pregnancy in ewes. Acta Vet. Brno, 78, 237‒242. doi: 10.2754/avb200978020237.

Forman, H.J., Davies, K.J.A., Ursini, F. (2014). How do nutritional antioxidants really work: Nucleophilic tone and para‒hormesis versus free radical scavenging in vivo. Free Radical Biology and Medicine, 66, 24‒35. doi: 10.1016/j.freeradbiomed.2013.05.045.

Foyer, C.H., Noctor, G. (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant. Cell. 17 (7), 1866–1875. doi:

Fthenakis, G.C., Arsenos, G., Brozos, C., Fragkou, I.A., Giadinis, N.D., Giannenas, I., Mavrogiann, V.S., Papadopoulos, E., Valasi, I. (2012). Health management of ewes during pregnancy. Anim. Reprod. Sci., 130 (3–4), 198–212. doi: 10.1016/j.anireprosci.2012.01.016.

Galan, H.L., Hussey, M.J., Barbera, A., Ferrazzi, E., Chung, M., Hobbins, J.C., Battaglia, F.C. (1999). Relationship of fetal growth to duration of heat stress in an ovine model of placental insufficiency. Am. J. Obstet. Gynecol., 180, 1278–1282. doi: 10.1016/S0002‒9378(99)70629‒0.

Galenko–Jaroshevskij, P.A., Chekman, I.S., Gorchakova, N.A. (2001). Ocherki farmakologii sredstv metabolicheskoj terapii. Medicina, Moskva (in Russian).

Gimerh, F.I. (1967). K opredeleniju glutationa krovi. Laboratornoe delo, 9, 564 (in Russian).

Gubskij, J.I., Belenichev, I.F., Levickij, E.L. (2005). Toksikologicheskie posledstvija okislitel'noj modifikacii belka. Sovremennye problemy toksikologii, 2, 4–20 (in Russian).

Gür, S., Türk, G., Demirci, E., Yüce, A., Sönmez, M., Özer, S., Aksu, E.H. (2011). Effect of pregnancy and foetal number on diameter of corpus luteum, maternal progesterone concentration and oxidant/antioxidant balance in ewes. Reprod. Domest. Anim., 46, 289‒295. doi: 10.1111/j.1439‒0531.2010.01660.x.

Gutyj, B., Stybel, V., Darmohray, L., Lavryshyn, Y., Turko, I., Hachak, Y., Shcherbatyy, A., Bushueva, I., Parchenko, V.V., Kaplaushenko, A., Krushelnytska, O. (2017). Prooxidant‒antioxidant balance in the organism of bulls (young cattle) after using cadmium load. Ukrainian Journal of Ecology, 7 (4), 589‒596. doi: 10.15421/2017_165.

Halliwell, B., Gutteridge, J.M. (2015). Free radicals in biology and medicine. Oxford University Press, USA. doi: 10.1093/acprof:oso/9780198717478.001.0001.

Husain, M., Bourret, T.J., McCollister, B.D., Jones–Carson, J., Laughlin, J., Vázquez–Torres, A. (2008) Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. J. Biol. Chem., 283 (12), 7682–7689. doi: 10.1074/jbc.M708845200.

Hussein, A.N. (2017). The effect of zinc and copper deficiency on hematological parameters, oxidative stress and antioxidants levels in the sheep. Basrah Journal of Veterinary Research, 16 (2), 344–355.

Kandiel, M.M.M., El–Khaiat, H.M., Mahmoud, K.G.M. (2016). Changes in some hematobiochemical and hormonal profile in Barki sheep with various reproductive statuses. Small Ruminant Research, 136, 87–95. doi: 10.1016/j.smallrumres.2016.01.011.

Koroljuk, M.A., Levanova, A.I., Majorova, I.T., Tokarev, V.E. (1988). Metod opredelenija aktivnosti katalazy. Laboratornoe delo, 1, 16–19 (in Russian).

Krichkovskaja, L.V., Donchenko, G.V., Chernyshov, S.I., Nikitchenko, J.V., Zhukov, V.I. (2001). Prirodnye antioksidanty (biotehnologicheskie, biologicheskie i medicinskie aspekty). Model' Vselennoj, Har'kov (in Russian).

Lee, M.T., Lin, W.C., Yu, B., Lee, T.T. (2017). Antioxidant capacity of phytochemicals and their potential effects on oxidative status in animals ‒ A review. Asian‒Australasian journal of animal sciences, 30 (3), 299‒308. doi: 10.5713/ajas.16.0438.

Lees, C., Marlow, N., Arabin, B., Bilardo, C.M., Brezinka, C., Derks, J.B., Duvekot, J., Frusca, T., Diemert, A., Ferrazzi, E., Ganzevoort, W., Hecher, K., Martinelli, P., Ostermayer, E., Papageorghiou, A.T., Schlembach, D., Schneider, K.T., Thilaganathan, B., Todros, T., van Wassenaer‒Leemhuis, A., Valcamonico, A., Visser, G.H., Wolf, H. (2013). Perinatal morbidity and mortality in early‒onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE). Ultrasound Obstet. Gynecol., 42 (4), 400‒408. doi: 10.1002/uog.13190.

Levchenko, V.І., Golovaha, V.І., Kondrahіn, І.P., Rublenko, M.V., Sahnjuk, V.V., Cvіlіhovs'kij, M.І., Apuhovs'ka, L.І., Bezuh, V.M., Vovkotrub, N.V., Kіbkalo, D.V., Moskalenko, V.P., Rozumnjuk, A.V., Slіvіns'ka, L.G., Tishkіvs'kij, M.J., Chub, O.V. (2010). Metody laboratornoi' klinichnoi' diagnostyky hvorob tvaryn. Agrarna osvіta, Kyiv (in Ukrainian).

Li, Y., Li, H., Sha, Q., Hai, R., Wang, Y., Son, Y., Gao, F. (2018). Effects of maternal undernutrition on the growth, development and antioxidant status of ovine placentome subtypes during late pregnancy. Theriogenology, 110, 96‒102. doi: 10.1016/j.theriogenology.2018.01.002.

Liang, L.P., Jarrett, S.G., Patel, M. (2008). Chelation of mitochondrial iron prevents seizure–induced mitochondrial dysfunction and neuronal injury. J. Neurosci., 28 (45), 11550–11556. doi: 10.1523/JNEUROSCI.3016–08.2008.

Limesand, S.W., Rozance, P.J., Smith, D., Hay, W.W. Jr. (2007). Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction. Am. J. Physiol. Endocrinol. Metab., 293 (6), 1716‒1725. doi: 10.1152/ajpendo.00459.2007.

Liu, X., Claus, P., Wu, M., Verhamme, P., Pokreisz, P., Vandenwijngaert, S., Dubois, C., Vanhaecke, J., Verbeken, E., Bogaert, J., Janssens, S. (2013). Placental growth factor increases regional myocardial blood flow and contractile function in chronic myocardial ischemia. Am. J. Physiol. Heart. Circ. Physiol., 304 (6), 885–894. doi: 10.1152/ajpheart.00587.2012.

Longo, L.D. (2018). Some aspects of the physiology of the placenta. The Rise of Fetal and Neonatal Physiology, 153–194. doi: 10.1007/978–1–4939–7483–2_8.

Lu, J., Wang, Z., Cao, J., Chen, Y., Dong, Y. (2018). A novel and compact review on the role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology, 16 (1), 80. doi: 10.1186/s12958–018–0391–5.

Lü, J.M., Lin, P.H., Yao, Q., Chen, C. (2010). Chemical and molecular mechanisms of antioxidants: experimental approaches and model systems. Journal of cellular and molecular medicine, 14 (4), 840–860. doi: org/10.1111/j.1582–4934.2009.00897.x.

Lykkesfeldt, J., Svendsen, O. (2007). Oxidants and antioxidants in disease: Oxidative stress in farm animals. Vet. J., 173, 502–511. doi: 10.1016/j.tvjl.2006.06.005.

Makatsariya, A.D., Bitsadze, V.O., Khizroeva, D.K,, Khamani, I.V. (2016). Placental insufficiency in complicated pregnancy and possibility of treatment with dipyridamole. Akusherstvo, ginekologiya i reproduktsiya, 4, 72–82 (in Russian). doi: 10.17749/2313–7347.2016.10.4.072–082.

Marseglia, L., D’Angelo, G., Manti, S., Arrigo, T., Barberi, I., Reiter, R.J., Gitto, E. (2014). Oxidative stress‒mediated aging during the fetal and perinatal periods. Oxidative medicine and cellular longevity. doi: 10.1155/2014/358375.

Mirończuk‒Chodakowska, I., Witkowska, A.M., Zujko, M.E. (2018). Endogenous non‒enzymatic antioxidants in the human body. Advances in Medical Sciences, 63 (1), 68‒78. doi: 10.1016/j.advms.2017.05.005.

Mohebbi‒Fani, M., Mirzaci, A., Nazifi, S., Shabbooie, Z. (2012). Changes of vitamins A, E, and C and lipid peroxidation status of breeding and pregnant sheep during dry seasons on medium‒to‒low quality forages. Trop. Anim. Health Prod., 44, 259‒265. doi: 10.1007/s11250‒011‒0012‒1.

Monson, T., Wright, T., Galan, H.L., Reynolds, P.R., Arroyo, J.A. (2017). Caspase dependent and independent mechanisms of apoptosis across gestation in a sheep model of placental insufficiency and intrauterine growth restriction. Apoptosis, 22, 710–718. doi: 10.1007/s10495‒017‒1343‒9.

Murashko, A.V., Ishenko, A.I., Magomedova, S.M., Didikin, S.S., Zinovyeva, L.V., Pavlova, L.A., Kozin, S.V., Drapkina, J.S. (2016). Experimental Treatment of Placental Insufficiency in Animal Model (by IGF‒1). American Journal of Clinical Medicine Research, 4 (2), 34‒37. doi: 10.12691/ajcmr‒4‒2‒4.

Murphy, M.P. (2014). Antioxidants as therapies: can we improve on nature? Free Radical Biology and Medicine, 66, 20‒23. doi: 10.1016/j.freeradbiomed.2013.04.010.

Mutinati, M., Piccinno, M., Roncetti, M., Campanile, D., Rizzo, A., Sciorsci, R.L. (2013). Oxidative stress during pregnancy in the sheep. Review article. Reprod. Domest. Anim., 48, 353–357. doi: 10.1111/rda.12141.

Nawito, M.F., El Hameed, A.R.A., Sosa, A.S.A., Mahmoud, K.G.M. (2016). Impact of pregnancy and nutrition on oxidant/antioxidant balance in sheep and goats reared in South Sinai, Egypt. Veterinary world, 9 (8), 801. doi: 10.14202/vetworld.2016.801‒805.

Omidi, A., Vakili, S., Nazifi, S., Parker, M.O. (2017). Acute‒phase proteins, oxidative stress, and antioxidant defense in crib‒biting horses. Journal of Veterinary Behavior, 20, 31‒36. doi: 10.1016/j.jveb.2016.06.005.

Ordiyants, I.M., Mekhdieva, U.T., Savicheva, A.M. (2018). Modern approaches to the diagnosis of placental insufficiency according to cardiotocography. Research'n Practical Medicine Journal, 5 (3), 96‒101. doi: 10.17709/2409‒2231‒2018‒5‒3‒9 (in Russian).

Pahomova, Z.E., Komilova, M.S. (2016). Ocenka disfunkcii jendotelija fetoplacentarnogo kompleksa pri prezhdevre–mennoj otslojke normal'no raspolozhennoj placenty. Vestnik sovremennoj klinicheskoj mediciny, 9 (1), 51–57. doi:10.20969/vskm.2016.9(1).51–57 (in Russian).

Papa, G.R., Magnarelli, G., Rovedatti, M.G. (2018). Susceptibility of placental mitochondria to oxidative stress. Birth defects research, 110 (16), 1228‒1232. doi: 10.1002/bdr2.1377.

Perfil’ev, V.Y., Zverev, Y.F., Zharikov, A.Y., Bryukhanov, V.M. (2017). The role of free radical oxidation in the development of experimental urate nephropathy. Bulletin of experimental biology and medicine, 163 (1), 28‒30. doi: 10.1007/s10517‒017‒3730‒1.

Perrone, S., Santacroce, A., Picardi, A., Buonocore, G. (2016). Fetal programming and early identification of newborns at high risk of free radical‒mediated diseases. World journal of clinical pediatrics, 5 (2), 172‒181. doi: 10.5409/wjcp.v5.i2.172.

Perrone, S., Tataranno, M.L., Negro, S., Longini, M., Toti, M.S., Alagna, M.G., Proietti, F., Bazzini, F., Toti, P., Buonocore, G. (2016). Placental histological examination and the relationship with oxidative stress in preterm infants. Placenta, 46, 72–78.

Perrone, S., Tataranno, M.L., Santacroce, A., Bracciali, C., Riccitelli, M., Alagna, M.G., Longini, M., Belvisi, E., Bazzini, F., Buonocore, G. (2016). Fetal programming, maternal nutrition, and oxidative stress hypothesis. Journal of Pediatric Biochemistry, 6 (02), 96‒102. doi: 10.1055/s‒0036‒1593811.

Pisoschi, A.M., Pop, A. (2015). The role of antioxidants in the chemistry of oxidative stress: A review. European Journal of Medicinal Chemistry, 97, 55‒74. doi: 10.1016/j.ejmech.2015.04.040.

Redline, R.W. (2015). The clinical implications of placental diagnoses. Semin. Perinatol., 39 (1), 2–8. doi: 10.1053/j.semperi.2014.10.002.

Rios, T.S., Sánchez‒Torres Esqueda, M.T., Cruz, A.D., Cordero Mora, J.L., Guinzberg Perrusquía, R., Rabanales Morales, J.L., Figueroa Velasco, J.L., Hernández Bautista, J. (2017). Oxidative state of ewes with different number of parity during gestation and lactation. Pesq. Vet. Bras., 37 (12), 1405‒1410, doi: 10.1590/S0100‒736X2017001200008.

Romanenko, T.G. (2017). Placentarna disfunkcіja jak prediktor nevinoshuvannja vagіtnostі. Reproduktivna endokrinologіja, 1, 77‒82. doi:‒4117.2017.33.8‒77‒82 (in Ukrainian).

Roos, S., Kanai, Y., Prasad, P.D., Powell, T.L., Jansson, T. (2009). Regulation of placental amino acid transporter activity by mammalian target of rapamycin. Am. J. Physiol. Cell. Physiol., 296 (1), 142–150. doi: 10.1152/ajpcell.00330.2008.

Rozance, P.J., Anderson, M., Martinez, M., Fahy, A., Macko, A.R., Kailey, J., Seedorf, G.J., Abman, S.H., Hay, W.W. Jr., Limesand, S.W. (2015). Placental insufficiency decreases pancreatic vascularity and disrupts hepatocyte growth factor signaling in the pancreatic islet endothelial cell in fetal sheep. Diabetes, 64 (2), 555‒564. doi: 10.2337/db14‒0462. 

Rozance, P.J., Zastoupil, L., Wesolowski, S.R., Goldstrohm, D.A., Strahan, B., Cree‐Green, M., Sheffield‐Moore, M., Meschia, G., Hay, W.W. Jr., Wilkening, R.B., Brown, L.D. (2017). Skeletal muscle protein accretion rates and hindlimb growth are reduced in late gestation intrauterine growth‐restricted fetal sheep. The Journal of Physiology, 596 (1), 67‒82. doi: 10.1113/JP275230.

Sales, F., Peralta, O.A., Narbona, E., McCoard, S., De los Reyes, M., González–Bulnes, A., Parraguez, V.H. (2018). Hypoxia and oxidative stress are associated with reduced fetal growth in twin and undernourished sheep pregnancies. Animals, 8 (11), 217. doi: 10.3390/ani8110217.

Schoots, M.H., Gordijn, S.J., Scherjon, S.A., van Goor, H., Hillebrands, J.–L. (2018). Oxidative stress in placental pathology. Placenta, 69, 153–161. doi: 10.1016/j.placenta.2018.03.003.

Sebire, N.J. (2017). Implications of placental pathology for disease mechanisms; methods, issues and future approaches. Placenta, 52, 122‒126. doi: 10.1016/j.placenta.2016.05.006.

Sehgal, A., Dahlstrom, J.E., Chan, Y., Allison, B.J., Miller, S.L., Polglase, G.R. (2018). Placental histopathology in preterm fetal growth restriction. Journal of Paediatrics and Child Health. doi: 10.1111/jpc.14251.

Serviddio, G., Bellanti, F., Vendemiale, G. (2013). Free radical biology for medicine: learning from nonalcoholic fatty liver disease. Free Radic. Biol. Med., 65, 952–968. doi: 10.1016/j.freeradbiomed.2013.08.174.

Sidorova, I.S., Makarov, I.O. (2005).  Kliniko–diagnosticheskie aspekty fetoplacentarnoj nedostatochnosti. MIA, Moskva (in Russian).

Silva, L.C.G., Regazzi, F.M., Lúcio, C.F., Veiga, G.A.L., Angrimani, D.S.R., Fernandes, C.B., Vannucchi, C.I. (2018). Redox, acid‒base and clinical analysis of preterm and term neonatal lambs. Anim. Reprod., 15 (1), 51‒55. doi: 10.21451/1984‒3143‒2017‒AR0054.

Simioni, C., Zauli, G., Martelli, A.M., Vitale, M., Sacchetti, G., Gonelli, A., Neri, L.M. (2018). Oxidative stress: role of physical exercise and antioxidant nutraceuticals in adulthood and aging. Oncotarget, 9 (24), 17181–17198. doi:10.18632/oncotarget.24729.

Sirota, T.V. (1999). Novyj podhod v issledovanii processa autookislenija adrenalina i ispol'zovanie ego dlja izmerenija aktivnosti superoksiddismutazy. Voprosy medicinskoj himii, 45 (3), 263–271 (in Russian).

Skljarov, P.N. (2013). Antenatal'naja patologija u ovec i koz: diagnostika i profilaktika. Dal'nevostochnyj agrarnyj vestnik, 1 (25), 36‒40. doi: 10.24411/1999‒6837‒2014‒00025 (in Ukrainian).

Stein, P.K., Kleiger, R.E. (1999). Insights from the study of heart rate variability. Ann. Rev. Med., 50, 249‒261. doi: 10.1146/

Talukder, S., Kerrisk, K.L., Gabai, G., Celi, P. (2017). Role of oxidant–antioxidant balance in reproduction of domestic animals. Animal Production Science, 57 (8), 1588‒1597. doi: 10.1071/AN15619.

Tezikov, J.V., Lipatov, I.S., Frolova, N.A., Kutuzova, O.A., Prihod'ko, A.V. (2016). Methodology of preventing major obstetrical syndromes. Gynecology, Obstetrics and Perinatology, 15 (2), 20‒30. doi: 10.20953/1726‒1678‒2016‒2‒20‒30 (in Russian).

Van der Linden, D.S., Sciascia, Q., Sales, F., McCoard, S.A. (2013). Placental nutrient transport is affected by pregnancy rank in sheep. Journal of Animal Science, 91 (2), 644–653. doi:10.2527/jas.2012–5629.

Vasylieva, N. (2017). Economic aspects of food security in Ukrainian meat and milk clusters.  Agris On–line Papers in Economics and Informatics, 9 (3), 81–92. doi: 10.7160/aol.2017.090308

Veropotvelyan, N.P., Veropotvelyan, P.N., Tsehmistrenko, I.S., Bondarenko, A.A., Usenko, T.V. (2016). Morphological classification of lesions of the placenta. Health of women, 8 (114), 63–71. doi: 10.15574/HW.2016.114.63.

Voevodin, S.M., Shemanaeva, T.V., Shhegolev, A.I. (2017). Placentarnaja nedostatochnost' i ugroza preryvanija beremennosti: sovremennyj vzgljad na problemu. Ginekologija, 19 (4), 50–52. doi: 10.26442/2079‒5696_19.4.50‒52 (in Russian).

Wang, S., He, G., Chen, M., Zuo, T., Xu, W., Liu, X. (2017). The role of antioxidant enzymes in the ovaries. Oxidative medicine and cellular longevity, 2017. doi: 10.1155/2017/4371714.

Wesolowski, S.R., Hay, W.W. Jr. (2016). Role of placental insufficiency and intrauterine growth restriction on the activation of fetal hepatic glucose production. Mol. Cell. Endocrinol., 5 (435), 61–68. doi: 10.1016/j.mce.2015.12.016.

Yuksel, S., Yigit, A. (2015). Malondialdehyde and nitric oxide levels and catalase, superoxide dismutase, and glutathione peroxidase levels in maternal blood during different trimesters of pregnancy and in the cord blood of newborns. Turk. J. Med. Sci., 45, 454–459. doi:10.3906/sag–1311–72.

Zanardo, V., Franzoi, M., Vedovato, S., Trevisanuto, D., Suppiej, A., Chiarelli, S (2008). Placental lesions and abnormal neurocognitive function at school age in extremely low‒birth weight infants. Pediatr. Dev. Pathol., 11 (2), 164. doi: 10.2350/07‒08‒0327.

Zhang, S., Regnault, T.R., Barker, P.L., Botting, K.J., McMillen, I.C., McMillan, C.M., Roberts, C.T., Morrison, J.L. (2015). Placental adaptations in growth restriction. Nutrients, 7 (1), 360‒389. doi: 10.3390/nu7010360.

Share this article