The effect of electromagnetic field (EMF) exposure on synthesis and release of steroid hormones by the porcine conceptuses during the peri-implantation period
Anita Franczak A * , Ewa Monika Drzewiecka A , Wiktoria Kozlowska A , Agata Zmijewska A , Pawel Jozef Wydorski A and Anna Koziorowska BA Department of Animal Anatomy and Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1A, 10-719 Olsztyn, Poland.
B Institute of Materials Sciences, College of Natural Sciences, University of Rzeszow, Pigonia 1, 35-310 Rzeszow, Poland.
Reproduction, Fertility and Development 34(10) 722-735 https://doi.org/10.1071/RD22040
Published online: 2 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Electrical devices and power systems are the sources of EM-waves which propagate everywhere in the environment.
Aims: The study aimed to determine whether EMF induced changes in the steroidogenesis of conceptuses and whether progesterone (P4) may be a possible protectant against the effects of EMF radiation.
Methods: The entire porcine conceptuses were collected during the peri-implantation period (days 15–16 of pregnancy), divided into fragments (100 mg) and treated in vitro with EMF (50 Hz or 120 Hz, 2 or 4 h exposure), and examined to determine of CYP17A1, HSD3B1, CYP19A3, and HSD17B4 mRNA transcript and encoded protein abundance and the release of steroid hormones. Selected fragments of conceptuses were treated with P4.
Key results: In conceptuses incubated without P4, EMF at 120 Hz decreased androstenedione (A4) and testosterone (T) release after 2 h and increased oestrone (E1) release at 50 Hz and 120 Hz after 4 h exposure. In P4-treated conceptuses, EMF (50 and 120 Hz, 4 h exposure) decreased CYP19A3 mRNA transcript abundance, and increased (120 Hz, 2 h exposure) oestradiol-17β (E2) release.
Conclusions: The EMF radiation alters androgen and oestrogen synthesis and release from the conceptuses of pigs during the peri-implantation period. The P4 exerts protective effects on androgens and E1 release but it sensitises the conceptuses when comes to the mechanism of oestrogen synthesis and release during EMF radiation.
Implications: The effect of EMF radiation on the steroidogenic pathway in conceptuses may induce disturbances in their proper development and implantation.
Keywords: androgens, conceptuses, electromagnetic field, estrogens, hormone secretion, pig, reproduction, steroidogenesis.
References
Akins, EL, and Morrissette, MC (1968). Gross ovarian changes during estrous cycle of swine. American Journal of Veterinary Research 29, 1953–1957.| 5692889PubMed |
Bazer, FW, and Johnson, GA (2014). Pig blastocyst–uterine interactions. Differentiation 87, 52–65.
| Pig blastocyst–uterine interactions.Crossref | GoogleScholarGoogle Scholar | 24388881PubMed |
Bernabò, N, Tettamanti, E, Russo, V, Martelli, A, Turriani, M, Mattoli, M, and Barboni, B (2010). Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model. Theriogenology 73, 1293–1305.
| Extremely low frequency electromagnetic field exposure affects fertilization outcome in swine animal model.Crossref | GoogleScholarGoogle Scholar | 20176397PubMed |
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL, Vandesompele, J, and Wittwer, CT (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.
| The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 19246619PubMed |
Cárdenas, H, and Pope, WF (2003). Distribution and changes in amounts of the androgen receptor in the pig uterus during the estrous cycle, early pregnancy and after treatment with sex steroids. Journal of Endocrinology 177, 461–469.
| Distribution and changes in amounts of the androgen receptor in the pig uterus during the estrous cycle, early pregnancy and after treatment with sex steroids.Crossref | GoogleScholarGoogle Scholar |
Christenson, LK, Anderson, LH, Ford, SP, and Farley, DB (1994). Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2. Prostaglandins 47, 61–75.
| Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2.Crossref | GoogleScholarGoogle Scholar | 8140263PubMed |
Chu, X, Corbin, CJ, Kaminski, MA, and Conley, AJ (1999). Unique regulation of CYP17 expression in the trophectoderm of the preattachment porcine blastocyst. Endocrinology 140, 632–640.
| Unique regulation of CYP17 expression in the trophectoderm of the preattachment porcine blastocyst.Crossref | GoogleScholarGoogle Scholar | 9927287PubMed |
Ciereszko R (2009) Radioimmunoassay of steroid hormones in biological fluids. In ‘Demonstrations and methods’. (Ed. J Przala) (University of Warmia and Mazury Press: Olsztyn)
Conley, AJ, and Bird, IM (1997). The role of cytochrome P450 170α-hydroxylase and 3β-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the Δ5 and Δ4 pathways of steroidogenesis in mammals. Biology of Reproduction 56, 789–799.
| The role of cytochrome P450 170α-hydroxylase and 3β-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the Δ5 and Δ4 pathways of steroidogenesis in mammals.Crossref | GoogleScholarGoogle Scholar | 9096858PubMed |
Conley, A, Corbin, J, Smith, T, Hinshelwood, M, Liu, Z, and Simpson, E (1997). Porcine aromatases: studies on tissue-specific, functionally distinct isozymes from a single gene? The Journal of Steroid Biochemistry and Molecular Biology 61, 407–413.
| Porcine aromatases: studies on tissue-specific, functionally distinct isozymes from a single gene?Crossref | GoogleScholarGoogle Scholar | 9365218PubMed |
Dantzer, V (1985). Electron microscopy of the initial stages of placentation in the pig. Anatomy and Embryology 172, 281–293.
| Electron microscopy of the initial stages of placentation in the pig.Crossref | GoogleScholarGoogle Scholar | 4061869PubMed |
Diao, H-L, Su, R-W, Tan, H-N, Li, S-J, Lei, W, Deng, W-B, and Yang, Z-M (2008). Effects of androgen on embryo implantation in the mouse delayed-implantation model. Fertility and Sterility 90, 1376–1383.
| Effects of androgen on embryo implantation in the mouse delayed-implantation model.Crossref | GoogleScholarGoogle Scholar | 18053999PubMed |
Drzewiecka, EM, Kozlowska, W, Zmijewska, A, Wydorski, PJ, and Franczak, A (2021). Electromagnetic field (EMF) radiation alters estrogen release from the pig myometrium during the peri-implantation period. International Journal of Molecular Sciences 22, 2920.
| Electromagnetic field (EMF) radiation alters estrogen release from the pig myometrium during the peri-implantation period.Crossref | GoogleScholarGoogle Scholar | 33805726PubMed |
Fischer, HE, Bazer, FW, and Fields, MJ (1985). Steroid metabolism by endometrial and conceptus tissues during early pregnancy and pseudopregnancy in gilts. Journals of Reproduction & Fertility 75, 69–78.
| Steroid metabolism by endometrial and conceptus tissues during early pregnancy and pseudopregnancy in gilts.Crossref | GoogleScholarGoogle Scholar |
Ford, SP, Christenson, RK, and Ford, JJ (1982). Uterine blood flow and uterine arterial, venous and luminal concentrations of oestrogens on Days 11, 13 and 15 after oestrus in pregnant and non-pregnant sows. Journals of Reproduction & Fertility 64, 185–190.
| Uterine blood flow and uterine arterial, venous and luminal concentrations of oestrogens on Days 11, 13 and 15 after oestrus in pregnant and non-pregnant sows.Crossref | GoogleScholarGoogle Scholar |
Franczak, A (2008). Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs. Reproductive Biology 8, 213–228.
| Endometrial and myometrial secretion of androgens and estrone during early pregnancy and luteolysis in pigs.Crossref | GoogleScholarGoogle Scholar | 19092984PubMed |
Franczak, A, and Kotwica, G (2010). Androgens and estradiol-17β production by porcine uterine cells: in vitro study. Theriogenology 73, 232–241.
| Androgens and estradiol-17β production by porcine uterine cells: in vitro study.Crossref | GoogleScholarGoogle Scholar | 19880166PubMed |
Franczak, A, Wojciechowicz, B, and Kotwica, G (2013). Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle. Reproductive Biology 13, 229–237.
| Transcriptomic analysis of the porcine endometrium during early pregnancy and the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 24011194PubMed |
Franczak, A, Waszkiewicz, EM, Kozlowska, W, Zmijewska, A, and Koziorowska, A (2020). Consequences of electromagnetic field (EMF) radiation during early pregnancy - androgen synthesis and release from the myometrium of pigs in vitro. Animal Reproduction Science 218, 106465.
| Consequences of electromagnetic field (EMF) radiation during early pregnancy - androgen synthesis and release from the myometrium of pigs in vitro.Crossref | GoogleScholarGoogle Scholar | 32507253PubMed |
Geisert, RD, Renegar, RH, Thatcher, WW, Michael Roberts, R, and Bazer, FW (1982). Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions. Biology of Reproduction 27, 925–939.
| Establishment of pregnancy in the pig: I. Interrelationships between preimplantation development of the pig blastocyst and uterine endometrial secretions.Crossref | GoogleScholarGoogle Scholar | 6959653PubMed |
Geisert, RD, Zavy, MT, Moffatt, RJ, Blair, RM, and Yellin, T (1990). Embryonic steroids and the establishment of pregnancy in pigs. Journal of Reproduction and Fertility. Supplement 40, 293–305.
| 2192045PubMed |
Geisert, RD, Ross, JW, Ashworth, MD, White, FJ, Johnson, GA, and DeSilva, U (2006). Maternal recognition of pregnancy signal or endocrine disruptor: the two faces of oestrogen during establishment of pregnancy in the pig. Journal of Reproduction and Fertility. Supplement 62, 131–145.
Grandolfo, M (1993). Extremely low frequency electromagnetic fields: environmental exposure levels, epidemiological studies and risk assessment. Bioelectrochemistry and Bioenergetics 30, 239–252.
| Extremely low frequency electromagnetic fields: environmental exposure levels, epidemiological studies and risk assessment.Crossref | GoogleScholarGoogle Scholar |
Green, ML, Simmen, RC, and Simmen, FA (1995). Developmental regulation of steroidogenic enzyme gene expression in the periimplantation porcine conceptus: a paracrine role for insulin-like growth factor-I. Endocrinology 136, 3961–3970.
| Developmental regulation of steroidogenic enzyme gene expression in the periimplantation porcine conceptus: a paracrine role for insulin-like growth factor-I.Crossref | GoogleScholarGoogle Scholar | 7649105PubMed |
Hall, DPF (1986). Cytochromes P-450 and the regulation of steroid synthesis. Steroids 48, 131–196.
| Cytochromes P-450 and the regulation of steroid synthesis.Crossref | GoogleScholarGoogle Scholar |
Hu, J, Braileanu, GT, and Mirando, MA (2003). Effect of ovarian steroids on basal and oxytocin-induced prostaglandin F2α secretion from pig endometrial cells. Reproduction, Fertility and Development 15, 197–205.
| Effect of ovarian steroids on basal and oxytocin-induced prostaglandin F2α secretion from pig endometrial cells.Crossref | GoogleScholarGoogle Scholar |
Karimi, A, Ghadiri Moghaddam, F, and Valipour, M (2020). Insights in the biology of extremely low-frequency magnetic fields exposure on human health. Molecular Biology Reports 47, 5621–5633.
| Insights in the biology of extremely low-frequency magnetic fields exposure on human health.Crossref | GoogleScholarGoogle Scholar | 32515000PubMed |
Knight, JW, Bazer, FW, Thatcher, WW, Franke, DE, and Wallace, HD (1977). Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth. Journal of Animal Science 44, 620–637.
| Conceptus development in intact and unilaterally hysterectomized-ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids and fetal growth.Crossref | GoogleScholarGoogle Scholar | 853021PubMed |
Ko, Y, Choi, I, Green, ML, Simmen, FA, and Simmen, RCM (1994). Transient expression of the cytochrome P450 aromatase gene in elongating porcine blastocysts is correlated with uterine insulin-like growth factor levels during peri-implantation development. Molecular Reproduction and Development 37, 1–11.
| Transient expression of the cytochrome P450 aromatase gene in elongating porcine blastocysts is correlated with uterine insulin-like growth factor levels during peri-implantation development.Crossref | GoogleScholarGoogle Scholar | 8129925PubMed |
Kowalski, AA, Vale-Cruz, DS, Simmen, FA, and Simmen, RCM (2004). Uterine androgen receptors: roles in estrogen-mediated gene expression and DNA synthesis. Biology of Reproduction 70, 1349–1357.
| Uterine androgen receptors: roles in estrogen-mediated gene expression and DNA synthesis.Crossref | GoogleScholarGoogle Scholar | 14711790PubMed |
Koziorowska, A, Pasiud, E, Fila, M, and Romerowicz-Misielak, M (2016). The impact of electromagnetic field at a frequency of 50 Hz and a magnetic induction of 2.5 mT on viability of pineal cells in vitro. Journal of Biological Regulators and Homeostatic Agents 30, 1067–1072.
| 28078855PubMed |
Koziorowska, A, Waszkiewicz, EM, Romerowicz-Misielak, M, Zglejc-Waszak, K, and Franczak, A (2018). Extremely low-frequency electromagnetic field (EMF) generates alterations in the synthesis and secretion of oestradiol-17β (E2) in uterine tissues: an in vitro study. Theriogenology 110, 86–95.
| Extremely low-frequency electromagnetic field (EMF) generates alterations in the synthesis and secretion of oestradiol-17β (E2) in uterine tissues: an in vitro study.Crossref | GoogleScholarGoogle Scholar | 29353145PubMed |
Kozlowska, W, Drzewiecka, EM, Zmijewska, A, Koziorowska, A, and Franczak, A (2021). Effects of electromagnetic field (EMF) radiation on androgen synthesis and release from the pig endometrium during the fetal peri-implantation period. Animal Reproduction Science 226, 106694.
| Effects of electromagnetic field (EMF) radiation on androgen synthesis and release from the pig endometrium during the fetal peri-implantation period.Crossref | GoogleScholarGoogle Scholar | 33486154PubMed |
Kuster, N, and Schönborn, F (2000). Recommended minimal requirements and development guidelines for exposure setups of bio-experiments addressing the health risk concern of wireless communications. Bioelectromagnetics 21, 508–514.
| Recommended minimal requirements and development guidelines for exposure setups of bio-experiments addressing the health risk concern of wireless communications.Crossref | GoogleScholarGoogle Scholar | 11015115PubMed |
Lacy-hulbert, A, Metcalfe, JC, and Hesketh, R (1998). Biological responses to electromagnetic fields 1. The FASEB Journal 12, 395–420.
| Biological responses to electromagnetic fields 1.Crossref | GoogleScholarGoogle Scholar | 9535213PubMed |
Livak, KJ, and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |
Mansuori, E, Alihemmati, A, and Mesbahi, A (2020). An overview on the effects of power frequency electromagnetic field exposure on the female reproduction system, pregnancy outcome and fetal development. Journal of Medicinal and Chemical Sciences 3, 60–70.
| An overview on the effects of power frequency electromagnetic field exposure on the female reproduction system, pregnancy outcome and fetal development.Crossref | GoogleScholarGoogle Scholar |
Martyniak, M, Franczak, A, and Kotwica, G (2018). Synthesis of steroid hormones in the porcine oviduct during early pregnancy. Reproductive Biology 18, 143–150.
| Synthesis of steroid hormones in the porcine oviduct during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 29472137PubMed |
Meyer, AE, Pfeiffer, CA, Brooks, KE, Spate, LD, Benne, JA, Cecil, R, Samuel, MS, Murphy, CN, Behura, S, McLean, MK, Ciernia, LA, Smith, MF, Whitworth, KM, Wells, KD, Spencer, TE, Prather, RS, and Geisert, RD (2019). New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig. Biology of Reproduction 101, 148–161.
| New perspective on conceptus estrogens in maternal recognition and pregnancy establishment in the pig.Crossref | GoogleScholarGoogle Scholar | 31066888PubMed |
Miller, WL, and Auchus, RJ (2011). The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocrine Reviews 32, 81–151.
| The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders.Crossref | GoogleScholarGoogle Scholar | 21051590PubMed |
Oestrup, O, Hall, V, Petkov, SG, Wolf, XA, Hyldig, S, and Hyttel, P (2009). From zygote to implantation: Morphological and molecular dynamics during embryo development in the pig. Reproduction in Domestic Animals 44, 39–49.
| From zygote to implantation: Morphological and molecular dynamics during embryo development in the pig.Crossref | GoogleScholarGoogle Scholar | 19660079PubMed |
Okatan, DÖ, Kaya, H, Aliyazıcıoğlu, Y, Demir, S, Çolakoğlu, S, and Odacı, E (2018). Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat. International Journal of Radiation Biology 94, 186–198.
| Continuous 900-megahertz electromagnetic field applied in middle and late-adolescence causes qualitative and quantitative changes in the ovarian morphology, tissue and blood biochemistry of the rat.Crossref | GoogleScholarGoogle Scholar | 29268055PubMed |
Payne, AH, and Hales, DB (2004). Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Reviews 25, 947–970.
| Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones.Crossref | GoogleScholarGoogle Scholar | 15583024PubMed |
Portelli, LA, Falldorf, K, Thuróczy, G, and Cuppen, J (2018). Retrospective estimation of the electric and magnetic field exposure conditions in in vitro experimental reports reveal considerable potential for uncertainty. Bioelectromagnetics 39, 231–243.
| Retrospective estimation of the electric and magnetic field exposure conditions in in vitro experimental reports reveal considerable potential for uncertainty.Crossref | GoogleScholarGoogle Scholar | 29171034PubMed |
Ryan, DP, Yaakub, H, Harrington, D, and Lynch, PB (1994). Follicular development during early pregnancy and the estrous cycle of the sow. Theriogenology 42, 623–632.
| Follicular development during early pregnancy and the estrous cycle of the sow.Crossref | GoogleScholarGoogle Scholar | 16727568PubMed |
Simpson, ER, and Davis, SR (2001). Minireview: Aromatase and the regulation of estrogen biosynthesis—some new perspectives. Endocrinology 142, 4589–4594.
| Minireview: Aromatase and the regulation of estrogen biosynthesis—some new perspectives.Crossref | GoogleScholarGoogle Scholar | 11606422PubMed |
Simpson, ER, Clyne, C, Speed, C, Rubin, G, and Bulun, S (2001). Tissue-specific estrogen biosynthesis and metabolism. Annals of the New York Academy of Sciences 949, 58–67.
| Tissue-specific estrogen biosynthesis and metabolism.Crossref | GoogleScholarGoogle Scholar | 11795380PubMed |
Solek, P, Majchrowicz, L, Bloniarz, D, Krotoszynska, E, and Koziorowski, M (2017). Pulsed or continuous electromagnetic field induce p53/p21-mediated apoptotic signaling pathway in mouse spermatogenic cells in vitro and thus may affect male fertility. Toxicology 382, 84–92.
| Pulsed or continuous electromagnetic field induce p53/p21-mediated apoptotic signaling pathway in mouse spermatogenic cells in vitro and thus may affect male fertility.Crossref | GoogleScholarGoogle Scholar | 28323003PubMed |
Szafrańska, B, Ziecik, A, and Okrasa, S (2002). Primary antisera against selected steroids or proteins and secondary antisera against gamma-globulins--an available tool for studies of reproductive processes. Reproductive Biology 2, 187–204.
| 14666157PubMed |
Tarleton, BJ, Wiley, AA, and Bartol, FF (1999). Endometrial development and adenogenesis in the neonatal pig: Effects of estradiol valerate and the antiestrogen ICI 182,780. Biology of Reproduction 61, 253–263.
| Endometrial development and adenogenesis in the neonatal pig: Effects of estradiol valerate and the antiestrogen ICI 182,780.Crossref | GoogleScholarGoogle Scholar | 10377057PubMed |
Turkman S, Taweel A (2020) Business process model driven approach for automatic use case model generation. In ‘Business modeling and software design. BMSD 2020. Vol. 391’. (Ed. B Shishkov) (Springer: Cham)
| Crossref |
Vallet, JL, and Christenson, RK (1996). The effect of estrone and estradiol treatment on endometrial total protein, uteroferrin, and retinol-binding protein secretion during midpregnancy or midpseudopregnancy in swine. Journal of Animal Science 74, 2765–2772.
| The effect of estrone and estradiol treatment on endometrial total protein, uteroferrin, and retinol-binding protein secretion during midpregnancy or midpseudopregnancy in swine.Crossref | GoogleScholarGoogle Scholar | 8923192PubMed |
Waclawik, A, Jabbour, HN, Blitek, A, and Ziecik, AJ (2009). Estradiol-17β, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology 150, 3823–3832.
| Estradiol-17β, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium.Crossref | GoogleScholarGoogle Scholar | 19359378PubMed |
Waszkiewicz, EM, Zmijewska, A, Kozlowska, W, and Franczak, A (2020). Effects of LH and FSH on androgen and oestrogen release in the myometrium of pigs during the oestrous cycle and early pregnancy. Reproduction, Fertility and Development 32, 1200–1211.
| Effects of LH and FSH on androgen and oestrogen release in the myometrium of pigs during the oestrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar |
Wojciechowicz, B, Kotwica, G, Kolakowska, J, and Franczak, A (2013). The activity and localization of 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase and release of androstenedione and progesterone by uterine tissues during early pregnancy and the estrous cycle in pigs. Journal of Reproduction and Development 59, 49–58.
| The activity and localization of 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase and release of androstenedione and progesterone by uterine tissues during early pregnancy and the estrous cycle in pigs.Crossref | GoogleScholarGoogle Scholar |
Wojciechowicz, B, Kotwica, G, Zglejc, K, Waszkiewicz, E, and Franczak, A (2017). Expression of 17β-hydroxysteroid dehydrogenase and the effects of LH, FSH and prolactin on oestrone and 17β-oestradiol secretion in the endometrium of pigs during early pregnancy and the oestrous cycle. Reproduction, Fertility and Development 29, 975–984.
| Expression of 17β-hydroxysteroid dehydrogenase and the effects of LH, FSH and prolactin on oestrone and 17β-oestradiol secretion in the endometrium of pigs during early pregnancy and the oestrous cycle.Crossref | GoogleScholarGoogle Scholar |
Ziecik, AJ (2002). Old, new and the newest concepts of inhibition of luteolysis during early pregnancy in pig. Domestic Animal Endocrinology 23, 265–275.
| Old, new and the newest concepts of inhibition of luteolysis during early pregnancy in pig.Crossref | GoogleScholarGoogle Scholar | 12142243PubMed |
Ziecik, AJ, Waclawik, A, Kaczmarek, MM, Blitek, A, Moza Jalali, B, and Andronowska, A (2011). Mechanisms for the establishment of pregnancy in the pig. Reproduction in Domestic Animals 46, 31–41.
| Mechanisms for the establishment of pregnancy in the pig.Crossref | GoogleScholarGoogle Scholar | 21854459PubMed |