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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Restricted feed intake in lactating primiparous sows. II. Effects on subsequent litter sex ratio and embryonic gene expression

G. Oliver A C , S. Novak A , J. L. Patterson A , J. A. Pasternak A , F. Paradis A , M. Norrby B , K. Oxtoby A , M. K. Dyck A , W. T. Dixon A and G. R. Foxcroft A
+ Author Affiliations
- Author Affiliations

A Swine Reproduction-Development Program, Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, T6G 2P5, Canada.

B Swedish Univesity of Agricultural Sciences, Department of Anatomy, Physiology and Biochemistry PO Box 7011, S-750 07, Uppsala, Sweden.

C Corresponding author. Email: goliver@ualberta.ca

Reproduction, Fertility and Development 23(7) 899-911 https://doi.org/10.1071/RD11013
Submitted: 8 January 2011  Accepted: 8 April 2011   Published: 26 August 2011

Abstract

Expression of panels of candidate genes controlling myogenesis, angiogenesis and gender-specific imprinting of development were analysed in embryonic, placental and endometrial tissues recovered at Day 30 of gestation from a subset of primiparous sows that were either feed restricted (Restrict; n = 17) or fed to appetite (Control; n = 15) during the last week of the previous lactation. Embryos were also sex typed to investigate gender bias in response to treatments. Average embryonic weight was lower in the subset of Restrict compared with Control litters (1.38 ± 0.07 vs 1.59 ± 0.08 g, respectively) and the male : female sex ratio was higher (P < 0.05) in embryos (litters) recovered from Restrict sows. Treatment affected (P ≤ 0.05) the expression of embryonic and placental genes involved in insulin-like growth factor (IGF) 2 signalling, including IGF2, INSR and IGF2R. Embryonic expression of ESR1 was also affected by treatment (P < 0.03) and sex × treatment interactions were observed for the expression of embryonic ESR1 (P < 0.05) and placental ANGPT2 (P < 0.03). At the molecular level, these results support the suggestion that changes in placental function are not the primary mechanism mediating detrimental effects of previous sow catabolism on early embryonic development in the feed-restricted lactational sow model. However, perturbations in the IGF2 system are implicated as mediators of these effects.

Additional keywords: catabolism, epigenetics.


References

Belkacemi, L., Nelson, D. M., Desai, M., and Ross, M. G. (2010). Maternal undernutrition influences placental fetal development. Biol. Reprod. 83, 325–331.
Maternal undernutrition influences placental fetal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrsrrO&md5=147b337e5820c8ca742dd9eb80388c7fCAS | 20445129PubMed |

Bèrard, J., and Bee, G. (2010). Effects of dietary l-arginine supplementation to gilts during early gestation on feotal survival, growth and myofiber formation. Animal 4, 1680–1687.
Effects of dietary l-arginine supplementation to gilts during early gestation on feotal survival, growth and myofiber formation.Crossref | GoogleScholarGoogle Scholar | 22445121PubMed |

Buckingham, M., Bajard, L., Chang, T., Daubas, P., Hadchouel, J., Meilhac, S., Montarras, D., Rocancourt, D., and Relaix, F. (2003). The formation of skeletal muscle: from somite to limb. J. Anat. 202, 59–68.
The formation of skeletal muscle: from somite to limb.Crossref | GoogleScholarGoogle Scholar | 12587921PubMed |

Clowes, E. J., Aherne, F. X., and Foxcroft, G. R. (1994). Effect of delayed breeding on the endocrinology and fecundity of sows. J. Anim. Sci. 72, 283–291.
| 1:CAS:528:DyaK2cXhsFCgsbc%3D&md5=885dc4abdb1f5b2973ca8aeaf85af1bcCAS | 8157512PubMed |

Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., and Fowden, A. L. (2010). Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J. Physiol. 588, 527–538.
Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvV2js7o%3D&md5=6f058a9616d83f3c21c182ce8b4fca8dCAS | 19948659PubMed |

Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., and Reik, W. (2002). Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417, 945–948.
Placental-specific IGF-II is a major modulator of placental and fetal growth.Crossref | GoogleScholarGoogle Scholar | 12087403PubMed |

Costello, P. M., Rowlerson, A., Astaman, N. A., Anthony, F. E., Sayer, A. A., Cooper, C., Hanson, M. A., and Green, L. R. (2008). Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development. J. Physiol. 586, 2371–2379.
Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlartbs%3D&md5=be94659d756f038d469b8d0325189f3cCAS | 18339691PubMed |

Dwyer, C. M., and Stickland, N. C. (1992). Does the anatomical location of a muscle affect the influence of undernutrition on muscle fibre number? J. Anat. 181, 373–376.
| 1295876PubMed |

Dwyer, C. M., Stickland, N. C., and Fletcher, J. M. (1994). The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. J. Anim. Sci. 72, 911–917.
| 1:STN:280:DyaK2c3osVahsA%3D%3D&md5=287192f5f04aa546976e61e2c14df92bCAS | 8014156PubMed |

Dwyer, C. M., Madgwick, A. J., Ward, S. S., and Stickland, N. C. (1995). Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig. Reprod. Fertil. Dev. 7, 1285–1292.
Effect of maternal undernutrition in early gestation on the development of fetal myofibres in the guinea-pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK283kvFegtg%3D%3D&md5=5ef862deea449184ad877b053d762f2fCAS | 8848601PubMed |

Elsas, L. J., Endo, F., Strumlauf, E., Elders, J., and Priest, J. H. (1985). Leprechaunism: an inherited defect in a high-affinity insulin receptor. Am. J. Hum. Genet. 37, 73–88.
| 1:CAS:528:DyaL2MXhs1CktbY%3D&md5=7c2bfe82c18342d91e08fe98b95a1053CAS | 3883764PubMed |

Foxcroft, G., Bee, G., Dixon, W., Hahn, M., Harding, J., Patterson, J., Putman, T., Sarmento, S., Smit, M., Tse, W.-Y., and Town, S. (2007). Consequences of selection for litter size on piglet development. In: ‘Paradigms of Pig Science’. (Eds J. Wiseman, M. A. Varley, S. McOrist and B. Kemp.) pp. 207–229. (Nottingham University Press: Nottingham.)

Foxcroft, G. R., Dixon, W. T., Dyck, M. K., Novak, S., Harding, J. C. S., and Almeida, F. C. R. L. (2009). Prenatal programming of postnatal development in the pig. In: ‘Control of Pig Reproduction VIII’. (Eds H. Rodriguez-Martinez, J. L. Vallet and A. J. Ziecik.) pp. 213–231. (Nottingham University Press: Nottingham.) Soc. Reprod. Fertil. Suppl. Vol. 66, pp. 213–231.

John, R. M. (2010). Engineering mouse models to investigate the function of imprinting. Brief Funct. Genomics 9, 294–303.
Engineering mouse models to investigate the function of imprinting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFKgsro%3D&md5=e80b0337b4c782d408178f8e6c19905bCAS | 20675686PubMed |

Joshi, R. L., Lamothe, B., Cordonnier, N., Mesbah, K., Monthioux, E., Jami, J., and Bucchini, D. (1996). Targeted disruption of the insulin receptor gene in the mouse results in neonatal lethality. EMBO J. 15, 1542–1547.
| 1:CAS:528:DyaK28XisVOmtL0%3D&md5=a74571dae21bb02b21cc4f95869ff3ffCAS | 8612577PubMed |

Killian, J. K., Nolan, C. M., Wylie, A. A., Vu, T. H., Hoffman, A. R., and Jirtle, R. L. (2001). Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary. Hum. Mol. Genet. 10, 1721–1728.
Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntFCitL0%3D&md5=ba4c98bd56751678bfb0d01032ea8007CAS | 11532981PubMed |

Kim, I., Kim, J. H., Ryu, Y. S., Liu, M., and Koh, G. Y. (2000). Tumor necrosis factor-alpha upregulates angiopoietin-2 in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 269, 361–365.
Tumor necrosis factor-alpha upregulates angiopoietin-2 in human umbilical vein endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsFKiurk%3D&md5=9e8647c91ea31f9eea4391b9da13c3cbCAS | 10708557PubMed |

Krook, A., Brueton, L., and O'Rahilly, S. (1993). Homozygous nonsense mutation in the insulin receptor gene in infant with leprechaunism. Lancet 342, 277–278.
Homozygous nonsense mutation in the insulin receptor gene in infant with leprechaunism.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3szitlKksQ%3D%3D&md5=8bad4339560ed1c5928328017e1f338fCAS | 8101305PubMed |

Lopez, M. F., Dikkes, P., Zurakowski, D., and Villa-Komaroff, L. (1996). Insulin-like growth factor II affects the appearance and glycogen content of glycogen cells in the murine placenta. Endocrinology 137, 2100–2108.
Insulin-like growth factor II affects the appearance and glycogen content of glycogen cells in the murine placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XisFCqsbc%3D&md5=028a341eaaf586348bcdfbfa842fd062CAS | 8612553PubMed |

Lunney, L. H. (1998). Compensatory placental growth after restricted maternal nutrition in early pregnancy. Placenta 19, 105–111.
Compensatory placental growth after restricted maternal nutrition in early pregnancy.Crossref | GoogleScholarGoogle Scholar |

MacLaughlin, S. M., Walker, S. K., Kleemann, D. O., Tosh, D. N., and McMillen, I. C. (2010). Periconceptional undernutrition and being a twin each alter kidney development in the sheep fetus during early gestation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R692–R699.
Periconceptional undernutrition and being a twin each alter kidney development in the sheep fetus during early gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFGntro%3D&md5=92e009242fd29fd2ee4c8c931c955336CAS | 20053964PubMed |

Milkiewicz, M., Ispanovic, E., Doyle, J. L., and Haas, T. L. (2006). Regulators of angiogenesis and strategies for their therapeutic manipulation. Int. J. Biochem. Cell Biol. 38, 333–357.
Regulators of angiogenesis and strategies for their therapeutic manipulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCrtr3M&md5=ca53453728c6293342f42534744dde44CAS | 16309946PubMed |

Monk, D., Arnaud, P., Apostolidou, S., Hills, F. A., Kelsey, G., Stanier, P., Feil, R., and Moore, G. E. (2006). Limited evolutionary conservation of imprinting in the human placenta. Proc. Natl Acad. Sci. USA 103, 6623–6628.
Limited evolutionary conservation of imprinting in the human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVKrt7Y%3D&md5=0e1a2f8e9e86aa464ffbf8e925a11477CAS | 16614068PubMed |

Nezer, C., Moreau, L., Brouwers, B., Coppieters, W., Detilleux, J., Hanset, R., Karim, L., Kvasz, A., Leroy, P., and Georges, M. (1999). An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nat. Genet. 21, 155–156.
An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVCltg%3D%3D&md5=4dfb3c9aa7496615956f9753dfd2c56eCAS | 9988262PubMed |

Ong, K., Kratzsch, J., Kiess, W., Costello, M., Scott, C., and Dunger, D. (2000). Size at birth and cord blood levels of insulin, insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-1 (IGFBP-1), IGFBP-3, and the soluble IGF-II/mannose-6-phosphate receptor in term human infants. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. J. Clin. Endocrinol. Metab. 85, 4266–4269.
Size at birth and cord blood levels of insulin, insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-1 (IGFBP-1), IGFBP-3, and the soluble IGF-II/mannose-6-phosphate receptor in term human infants. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlWmsrg%3D&md5=6a4ac293c5cbb4af529a3742f63b757bCAS | 11095465PubMed |

Patterson, J., Wellen, A., Hahn, M., Pasternak, A., Lowe, J., DeHass, S., Kraus, D., Williams, N., and Foxcroft, G. (2008). Responses to delayed estrus after weaning in sows using oral progestagen treatment. J. Anim. Sci. 86, 1996–2004.
Responses to delayed estrus after weaning in sows using oral progestagen treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt12hsbY%3D&md5=89b143ac7f2c56a2ea55fc23f49c74e3CAS | 18407977PubMed |

Patterson, J. L., Smit, M. N., Novak, S., Wellen, A. P., and Foxcroft, G. R. (2011). Restricted feed intake in lactating primiparous sows. I. Effects on sow metabolic state and subsequent reproductive performance. Reprod. Fertil. Dev 23, 889–898.
Restricted feed intake in lactating primiparous sows. I. Effects on sow metabolic state and subsequent reproductive performance.Crossref | GoogleScholarGoogle Scholar | 21871208PubMed |

Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=3cfd2ff99dae9a87dc2a76cece195022CAS | 11328886PubMed |

Pomp, D., Good, B. A., Geisert, R. D., Corbin, C. J., and Conley, A. J. (1995). Sex identification in mammals with polymerase chain reaction and its use to examine sex effects on diameter of day-10 or -11 pig embryos. J. Anim. Sci. 73, 1408–1415.
| 1:CAS:528:DyaK2MXlsFSjur4%3D&md5=00e09f61e1dbf780e65088227174a9d8CAS | 7665371PubMed |

Quigley, S. P., Kleemann, D. O., Kakar, M. A., Owens, J. A., Nattrass, G. S., Maddocks, S., and Walker, S. K. (2005). Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Anim. Reprod. Sci. 87, 241–251.
Myogenesis in sheep is altered by maternal feed intake during the peri-conception period.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MzhvFyrsA%3D%3D&md5=8efbd86754d1ccd0a4858ffed81be805CAS | 15911174PubMed |

Rehfeldt, C., and Kuhn, G. (2006). Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J. Anim. Sci. 84, E113–E123.
| 16582082PubMed |

Reik, W., Davies, K., Dean, W., Kelsey, G., and Constancia, M. (2001). Imprinted genes and the coordination of fetal and postnatal growth in mammals. Novartis Found. Symp. 237, 19–35.
Imprinted genes and the coordination of fetal and postnatal growth in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslaru7o%3D&md5=2ba5f7d33a0c68baf2b108ac9706e5e8CAS | 11444044PubMed |

Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., Tycko, B., and Sibley, C. (2003). Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J. Physiol. 547, 35–44.
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFSktro%3D&md5=9fa102735fbb1aff57e82d4ec9001722CAS | 12562908PubMed |

Reynolds, L. P., and Redmer, D. A. (2001). Angiogenesis in the placenta. Biol. Reprod. 64, 1033–1040.
Angiogenesis in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1artbk%3D&md5=2e7718efc3b5e4a1ef1c663967251c13CAS | 11259247PubMed |

Reynolds, L. P., Borowicz, P. P., Caton, J. S., Vonnahme, K. A., Luther, J. S., Buchanan, D. S., Hafez, S. A., Grazul-Bilska, A. T., and Redmer, D. A. (2010a). Uteroplacental vascular development and placental function: an update. Int. J. Dev. Biol. 54, 355–366.
Uteroplacental vascular development and placental function: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltVajtbY%3D&md5=5099df1b2ecd23a37977c3f30486d33eCAS | 19924632PubMed |

Reynolds, L. P., Borowicz, P. P., Caton, J. S., Vonnahme, K. A., Luther, J. S., Hammer, C. J., Maddock Carlin, K. R., Grazul-Bilska, A. T., and Redmer, D. A. (2010b). Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J. Anim. Sci. 88, E61–E72.
Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3psl2ksw%3D%3D&md5=6ede368e94572553f85c5b2ade9d5cb7CAS | 20023136PubMed |

Rothschild, M., Jacobson, C., Vaske, D., Tuggle, C., Wang, L., Short, T., Eckardt, G., Sasaki, S., Vincent, A., McLaren, D., Southwood, O., van der Steen, H., Mileham, A., and Plastow, G. (1996). The estrogen receptor locus is associated with a major gene influencing litter size in pigs. Proc. Natl Acad. Sci. USA 93, 201–205.
The estrogen receptor locus is associated with a major gene influencing litter size in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjslyiuw%3D%3D&md5=3270a9d02767347bcf3beae3c54ea502CAS | 8552604PubMed |

Sferruzzi-Perri, A. N., Owens, J. A., Standen, P., and Roberts, C. T. (2008). Maternal insulin-like growth factor-II promotes placental functional development via the Type 2 IGF receptor in the guinea pig. Placenta 29, 347–355.
Maternal insulin-like growth factor-II promotes placental functional development via the Type 2 IGF receptor in the guinea pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1Sqsbg%3D&md5=44a19b06e91ab576808f35f548c2f1abCAS | 18339421PubMed |

Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., Sato, T. N., and Yancopoulos, G. D. (1996). Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171–1180.
Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXit1GhtQ%3D%3D&md5=dc7a3d3cef15b33b4d8bd2d0232aaf62CAS | 8980224PubMed |

Tayade, C., Fang, Y., and Croy, B. A. (2007). A review of gene expression in porcine endometrial lymphocytes, endothelium and trophoblast during pregnancy success and failure. J. Reprod. Dev. 53, 455–463.
A review of gene expression in porcine endometrial lymphocytes, endothelium and trophoblast during pregnancy success and failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosVyls74%3D&md5=607a48541ffbd7452d3db1b85cfa03ebCAS | 17617733PubMed |

Taylor, S. I., Cama, A., Kadowaki, H., Kadowaki, T., and Accili, D. (1990). Mutations of the human insulin receptor gene. Trends Endocrinol. Metab. 1, 134–139.
Mutations of the human insulin receptor gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xitlarsbk%3D&md5=e0cebaf260713cb26baa2dee13082cf5CAS | 18411106PubMed |

Town, S. C., Putman, C. T., Turchinsky, N. J., Dixon, W. T., and Foxcroft, G. R. (2004). Number of conceptuses in utero affects porcine fetal muscle development. Reproduction 128, 443–454.
Number of conceptuses in utero affects porcine fetal muscle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlGjsLs%3D&md5=a75fda122d48057a06ca120cc0d1e837CAS | 15454639PubMed |

Tse, W. Y., Town, S. C., Murdoch, G. K., Novak, S., Dyck, M. K., Putman, C. T., Foxcroft, G. R., and Dixon, W. T. (2008). Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation. Reprod. Fertil. Dev. 20, 497–504.
Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFagsrw%3D&md5=9728afa7df50db42ddc9ea44f648a65dCAS | 18462612PubMed |

van Rens, B. T., and van der Lende, T. (2002). Piglet and placental traits at term in relation to the estrogen receptor genotype in gilts. Theriogenology 57, 1651–1667.
Piglet and placental traits at term in relation to the estrogen receptor genotype in gilts.Crossref | GoogleScholarGoogle Scholar | 12035976PubMed |

Vinsky, M. D., Novak, S., Dixon, W. T., Dyck, M. K., and Foxcroft, G. R. (2006). Nutritional restriction in lactating primiparous sows selectively affects female embryo survival and overall litter development. Reprod. Fertil. Dev. 18, 347–355.
Nutritional restriction in lactating primiparous sows selectively affects female embryo survival and overall litter development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD287ms1Slug%3D%3D&md5=ea395c1f4337a51163b1354cb6863fe4CAS | 16554010PubMed |

Vinsky, M. D., Murdoch, G. K., Dixon, W. T., Dyck, M. K., and Foxcroft, G. R. (2007). Altered epigenetic variance in surviving litters from nutritionally restricted lactating primiparous sows. Reprod. Fertil. Dev. 19, 430–435.
Altered epigenetic variance in surviving litters from nutritionally restricted lactating primiparous sows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFKnsL0%3D&md5=ed4fef954de01426c21054c8158fc2dcCAS | 17394790PubMed |

Vonnahme, K. A., and Ford, S. P. (2004). Placental vascular endothelial growth factor receptor system mRNA expression in pigs selected for placental efficiency. J. Physiol. 554, 194–201.
Placental vascular endothelial growth factor receptor system mRNA expression in pigs selected for placental efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvVCguw%3D%3D&md5=a9b8b7a97ee14c9d4acfa0a21a106d77CAS | 14678501PubMed |

Wu, G., Bazer, F. W., Wallace, J. M., and Spencer, T. E. (2006). Board-invited review. Intrauterine growth retardation: implications for the animal sciences. J. Anim. Sci. 84, 2316–2337.
Board-invited review. Intrauterine growth retardation: implications for the animal sciences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFGktLs%3D&md5=ffcda68a2f8946e672593f7e72d5c2eaCAS | 16908634PubMed |

Zak, L. J., Cosgrove, J. R., Aherne, F. X., and Foxcroft, G. R. (1997a). Pattern of feed intake and associated metabolic and endocrine changes differentially affect postweaning fertility in primiparous lactating sows. J. Anim. Sci. 75, 208–216.
| 1:CAS:528:DyaK2sXhtVGkur0%3D&md5=03232cb4c47603f0d45bf20610a1c625CAS | 9027568PubMed |

Zak, L. J., Xu, X., Hardin, R. T., and Foxcroft, G. R. (1997b). Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. J. Reprod. Fertil. 110, 99–106.
Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVans74%3D&md5=bef6a9ab81a404a85a2abd88f60987b4CAS | 9227363PubMed |