Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Effects of fetal genotype and sex on developmental response to maternal malnutrition

Laura Cogollos A , Consolacion Garcia-Contreras B , Marta Vazquez-Gomez C , Susana Astiz A , Raul Sanchez-Sanchez A , Ernesto Gomez-Fidalgo A , Cristina Ovilo B , Beatriz Isabel C and Antonio Gonzalez-Bulnes A D E
+ Author Affiliations
- Author Affiliations

A Department of Animal Reproduction, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Avda. Puerta de Hierro s/n, 28040 Madrid, Spain.

B Department of Animal Genetics, INIA, Ctra. De A Coruña Km. 7, 28040 Madrid, Spain.

C Faculty of Veterinary Sciences, UCM, Avda. Puerta de Hierro s/n, 28040 Madrid, Spain.

D Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Italy.

E Corresponding author. Email: bulnes@inia.es

Reproduction, Fertility and Development 29(6) 1155-1168 https://doi.org/10.1071/RD15385
Submitted: 27 September 2015  Accepted: 15 March 2016   Published: 17 May 2016

Abstract

The present study aimed to determine whether developmental patterns, adiposity level and fatty-acid composition of fetuses exposed to maternal malnutrition are driven by their sex or their genotype, or both, as these may modulate the adaptive response to the intrauterine environment independently of the maternal genotype. We used a single maternal genotype (purebred Iberian (IB) sows), which was inseminated with heterospermic semen (obtained by mixing semen from Iberian and Large White (LW) boars), to obtain four different subsets of fetuses (male and female, purebred (IB × IB) and crossbred (IB × LW)) in Iberian purebred sows. Analysis of fetal phenotypes indicated a better adaptive response of the female offspring, which was modulated by their genotype. When faced with prenatal undernutrition, females prioritised the growth of vital organs (brain, liver, lungs, kidneys and intestine) at the expense of bone and muscle. Moreover, the analysis of fat composition showed a higher availability of essential fatty acids in the female sex than in their male counterparts and also in the Iberian genotype than in crossbred fetuses. These results are of high translational value for understanding ethnic differences in prenatal programming of postnatal health and disease status, and show evidence that prenatal development and metabolic traits are primarily determined by fetal sex and strongly modulated by fetal genotype.

Additional keywords: developmental programming, ethnicity, fatty acids.


References

Adkisson, H. D., Risener, F., Zarrinkar, P., Walla, M., Christie, W., and Wuthier, R. (1991). Unique fatty-acid composition of normal cartilage: discovery of high levels of n-9 eicosatrienoic acid and low levels of n-6 polyunsaturated fatty acids. FASEB J. 5, 344–353.
| 1:CAS:528:DyaK3MXhvVals7k%3D&md5=a4643ba5b1c9ba2e6a73210fae89f99eCAS | 2001795PubMed |

Aiken, C. E., and Ozanne, S. E. (2013). Sex differences in developmental programming models. Reproduction 145, R1–R13.
Sex differences in developmental programming models.CrossRef | 1:CAS:528:DC%2BC3sXhslGisLg%3D&md5=480ae7f94cdd64ec75ab4b52307b25c5CAS | 23081892PubMed |

Attie, A. D., Krauss, R. M., Gray-Keller, M. P., Brownlie, A., Miyazaki, M., Kastelein, J. J., Lusis, A. J., Stalenhoef, A. F., Stoehr, J. P., Hayden, M. R., and Ntambi, J. M. (2002). Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia. J. Lipid Res. 43, 1899–1907.
Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia.CrossRef | 1:CAS:528:DC%2BD38Xos1yht7g%3D&md5=0da4f3a4b457a83310f18f86ac5c1df2CAS | 12401889PubMed |

Ayuso, M., Fernández, A., Núñez, Y., Benítez, R., Isabel, B., Barragán, C., Fernández, A. I., Rey, A. I., Medrano, J. F., Cánovas, Á., González-Bulnes, A., López-Bote, C., and Ovilo, C. (2015). Comparative analysis of muscle transcriptome between pig genotypes identifies genes and regulatory mechanisms associated to growth, fatness and metabolism. PLoS ONE 10, e0145162.
Comparative analysis of muscle transcriptome between pig genotypes identifies genes and regulatory mechanisms associated to growth, fatness and metabolism.CrossRef | 26695515PubMed |

Barbero, A., Astiz, S., Lopez-Bote, C. J., Perez-Solana, M. L., Ayuso, M., Garcia-Real, I., and Gonzalez-Bulnes, A. (2013). Maternal malnutrition and offspring sex determine juvenile obesity and metabolic disorders in a swine model of leptin resistance. PLoS One 8, e78424.
Maternal malnutrition and offspring sex determine juvenile obesity and metabolic disorders in a swine model of leptin resistance.CrossRef | 1:CAS:528:DC%2BC3sXhslWgsb3L&md5=21b0885ea8ef7ba31e5f5f245029f20eCAS | 24205230PubMed |

Barea, R., Isabel, B., Nieto, R., Lopez-Bote, C., and Aguilera, J. F. (2013). Evolution of the fatty-acid profile of subcutaneous back-fat adipose tissue in growing Iberian and Landrace × Large White pigs. Animal 7, 688–698.
Evolution of the fatty-acid profile of subcutaneous back-fat adipose tissue in growing Iberian and Landrace × Large White pigs.CrossRef | 1:CAS:528:DC%2BC3sXjt1Wks70%3D&md5=cbfcbb7fcdd4263557031b08708510c0CAS | 23031353PubMed |

Bee, G. (2004). Effect of early gestation feeding, birth weight and gender of progeny on muscle fibre characteristics of pigs at slaughter. J. Anim. Sci. 82, 826–836.
| 1:CAS:528:DC%2BD2cXhvVCku7g%3D&md5=57ad21a9bcd5b8b0b819c88613173e4cCAS | 15032440PubMed |

Biezenski, J. J. (1975). Fetal lipid metabolism. Obstet. Gynecol. Annu. 4, 39–70.
| 1:CAS:528:DyaE2sXmvVyhug%3D%3D&md5=1ef046979008cedc9488e1a85b63122fCAS | 1095993PubMed |

Briana, D. D., and Malamitsi-Puchner, A. (2013). Small-for-gestational-age birth weight: impact on lung structure and function. Paediatr. Respir. Rev. 14, 256–262.
Small-for-gestational-age birth weight: impact on lung structure and function.CrossRef | 23249620PubMed |

British Society of Animal Science (2003) ‘Nutrient Requirement Standards for Pigs’. (British Society of Animal Science: Penicuik, UK.)

Caron-Jobin, M., Mauvoisin, D., Michaud, A., Veilleux, A., Noel, S., Fortier, M. P., Julien, P., Tchernof, A., and Mounier, C. (2012). Stearic acid content of abdominal adipose tissues in obese women. Nutr. Diabetes 2, e23.
Stearic acid content of abdominal adipose tissues in obese women.CrossRef | 1:STN:280:DC%2BC3s7js1Gmtw%3D%3D&md5=22bb08d306fbbdc7183e266c1960aadbCAS | 23154679PubMed |

Charneca, R., Nunes, J., and Le Dividich, J. (2010). Body composition and blood parameters of newborn piglets from Alentejano and conventional (Large White × Landrace) genotype. Span. J. Agric. Res. 8, 317–325.
Body composition and blood parameters of newborn piglets from Alentejano and conventional (Large White × Landrace) genotype.CrossRef |

Clifton, V. L., and Murphy, V. E. (2004). Maternal asthma as a model for examining fetal sex-specific effects on maternal physiology and placental mechanisms that regulate human fetal growth. Placenta 25, S45–S52.
Maternal asthma as a model for examining fetal sex-specific effects on maternal physiology and placental mechanisms that regulate human fetal growth.CrossRef | 1:CAS:528:DC%2BD2cXitFKmur8%3D&md5=b9662e459d8626f9674c63ece49927b3CAS | 15033307PubMed |

Cuffe, J. S., Dickinson, H., Simmons, D. G., and Moritz, K. M. (2011). Sex-specific changes in placental growth and MAPK following short-term maternal dexamethasone exposure in the mouse. Placenta 32, 981–989.
Sex-specific changes in placental growth and MAPK following short-term maternal dexamethasone exposure in the mouse.CrossRef | 1:CAS:528:DC%2BC3MXhsFGjt7bM&md5=cecd9021059bd8ee512d9ebef1e9043bCAS | 21974799PubMed |

Cuffe, J. S., O’Sullivan, L., Simmons, D. G., Anderson, S. T., and Moritz, K. M. (2012). Maternal corticosterone exposure in the mouse has sex-specific effects on placental growth and mRNA expression. Endocrinology 153, 5500–5511.
Maternal corticosterone exposure in the mouse has sex-specific effects on placental growth and mRNA expression.CrossRef | 1:CAS:528:DC%2BC38Xhs1OnsLfE&md5=4fd8a912f02362a2aacfe8c3fad19be5CAS | 22919064PubMed |

Dawkins, M. J. (1966). Biochemical aspects of developing function in newborn mammalian liver. Br. Med. Bull. 22, 27–33.
| 1:CAS:528:DyaF28XksF2htLw%3D&md5=a0bde4667083a26a0efc586ee0abf02bCAS | 5321811PubMed |

D’Inca, R., Kloareg, M., Gras-Le Guen, C., and Le Huerou-Luron, I. (2010). Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile and bacterial colonisation in neonatal pigs. J. Nutr. 140, 925–931.
Intrauterine growth restriction modifies the developmental pattern of intestinal structure, transcriptomic profile and bacterial colonisation in neonatal pigs.CrossRef | 1:CAS:528:DC%2BC3cXlsVWrsLY%3D&md5=3fa10dc8a718d5c29c38bbd7c6d5782aCAS | 20335628PubMed |

Fain, J., and Scow, R. (1966). Fatty-acid synthesis in vivo in maternal and fetal tissues in rat. Am. J. Physiol. 210, 19–25.
| 1:CAS:528:DyaF28XlsVaktg%3D%3D&md5=285741ee9c6e1d89207b1242ea8b2db3CAS |

Fall, C. H. (2013). Fetal malnutrition and long-term outcomes. Nestle Nutr. Inst. Workshop Ser. 74, 11–25.
Fetal malnutrition and long-term outcomes.CrossRef | 23887100PubMed |

Gentili, S., Morrison, J. L., and McMillen, I. C. (2009). Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2 and HSDL1 mRNA in the sheep fetus in late gestation. Biol. Reprod. 80, 1121–1127.
Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2 and HSDL1 mRNA in the sheep fetus in late gestation.CrossRef | 1:CAS:528:DC%2BD1MXmtlGms70%3D&md5=a2a2b082b60432a373e4346dec9829bcCAS | 19208549PubMed |

Giussani, D. A. (2011). The vulnerable developing brain. Proc. Natl. Acad. Sci. USA 108, 2641–2642.
The vulnerable developing brain.CrossRef | 1:CAS:528:DC%2BC3MXisVeks70%3D&md5=5cdb6cf07d1167b34e97f5336afa09e8CAS | 21297035PubMed |

Gonzalez-Bulnes, A., Ovilo, C., Lopez-Bote, C. J., Astiz, S., Ayuso, M., Perez-Solana, M. L., Sanchez-Sanchez, R., and Torres-Rovira, L. (2012). Gender-specific early postnatal catch-up growth after intrauterine growth retardation by food restriction in swine with obesity/leptin resistance. Reproduction 144, 269–278.
Gender-specific early postnatal catch-up growth after intrauterine growth retardation by food restriction in swine with obesity/leptin resistance.CrossRef | 1:CAS:528:DC%2BC38Xht1Kksr%2FM&md5=d05a842756dc40e2c43d967f9c872b9bCAS | 22692087PubMed |

Gonzalez-Bulnes, A., Astiz, S., Ovilo, C., Lopez-Bote, C. J., Sanchez-Sanchez, R., Perez-Solana, M. L., Torres-Rovira, L., Ayuso, M., and Gonzalez, J. (2014). Early-postnatal changes in adiposity and lipid profile by transgenerational developmental programming in swine with obesity/leptin resistance. J. Endocrinol. 223, M17–M29.
Early-postnatal changes in adiposity and lipid profile by transgenerational developmental programming in swine with obesity/leptin resistance.CrossRef | 25107535PubMed |

Hansen, A. E., Wiese, H. F., Adam, D. J., Boelsche, A. N., Haggard, M. E., Davis, H., Newsom, W. T., and Pesut, L. (1964). Influence of diet on blood serum lipids in pregnant women and newborn infants. Am. J. Clin. Nutr. 15, 11–19.
| 1:CAS:528:DyaF2cXksFKntbk%3D&md5=8a463e5cb4f191feda963c5742ac3159CAS | 14192741PubMed |

Haugen, G., Hanson, M., Kiserud, T., Crozier, S., Inskip, H., and Godfrey, K. M. (2005). Fetal liver-sparing cardiovascular adaptations linked to mother’s slimness and diet. Circ. Res. 96, 12–14.
Fetal liver-sparing cardiovascular adaptations linked to mother’s slimness and diet.CrossRef | 1:CAS:528:DC%2BD2MXjt1Gr&md5=9e31a335c3abece0c9edad4d223d0abdCAS | 15576647PubMed |

Herrera, E. (2002). Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine 19, 43–55.
Lipid metabolism in pregnancy and its consequences in the fetus and newborn.CrossRef | 1:CAS:528:DC%2BD3sXhtFKitbk%3D&md5=535f01a730fa18425992eb8d085d5b10CAS | 12583601PubMed |

Hulver, M. W., Berggren, J. R., Carper, M. J., Miyazaki, M., Ntambi, J. M., Hoffman, E. P., Thyfault, J. P., Stevens, R., Dohm, G. L., Houmard, J. A., and Muoio, D. M. (2005). Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty-acid partitioning in obese humans. Cell Metab. 2, 251–261.
Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty-acid partitioning in obese humans.CrossRef | 1:CAS:528:DC%2BD2MXhtFGktrjP&md5=bee486ff7f5d0097d79f238de9aba3d3CAS | 16213227PubMed |

Johnston, P. V., Johnson, O. C., and Kummerow, F. A. (1957). Non-transfer of trans fatty acids from mother to young. Proc. Soc. Exp. Biol. Med. 96, 760–762.
Non-transfer of trans fatty acids from mother to young.CrossRef | 1:CAS:528:DyaG1cXks1WgtQ%3D%3D&md5=5fd3d4b11d6ed7294b5dc24d8d4795d3CAS | 13505852PubMed |

Leat, W. M. F. (1962). Studies on pig diets containing different amounts of linoleic acid. Br. J. Nutr. 16, 559–569.
Studies on pig diets containing different amounts of linoleic acid.CrossRef | 1:CAS:528:DyaF3sXktFOitbk%3D&md5=34a111fb9907e3cf47bcd3c347033596CAS |

Leskanich, C. O., and Noble, R. C. (1999). The comparative roles of polyunsaturated fatty acids in pig neonatal development. Br. J. Nutr. 81, 87–106.
| 1:CAS:528:DyaK1MXhvFahtL4%3D&md5=ca3b5f754b568e0744a9589ba97defedCAS | 10450326PubMed |

Lopez-Bote, C. J., Rey, A. I., Isabel, B., and Sanz, R. (1997). Effect of feeding diets high in monounsaturated fatty acids and alpha-tocopheryl acetate to rabbits on resulting carcass fatty-acid profile and lipid oxidation. J. Anim. Sci. 64, 177–186.
Effect of feeding diets high in monounsaturated fatty acids and alpha-tocopheryl acetate to rabbits on resulting carcass fatty-acid profile and lipid oxidation.CrossRef | 1:CAS:528:DyaK2sXktlOksLk%3D&md5=65935ab2f8ace8bc9a7ceba2d4881411CAS |

Marmer, W. N., and Maxwell, R. J. (1981). Dry column method for the quantitative extraction and simultaneous class separation of lipids from muscle tissue. Lipids 16, 365–371.
Dry column method for the quantitative extraction and simultaneous class separation of lipids from muscle tissue.CrossRef | 1:CAS:528:DyaL3MXkt1Slsrc%3D&md5=068f3de487d64cc4ebd50b6773fa204dCAS | 7253844PubMed |

Martin, S. S., Qasim, A., and Reilly, M. P. (2008). Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J. Am. Coll. Cardiol. 52, 1201–1210.
Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease.CrossRef | 1:CAS:528:DC%2BD1cXhtF2rtr%2FL&md5=e5d6986453125f5348d11705569e50c4CAS | 18926322PubMed |

Menon, N. K., Moore, C., and Dhopeshwarkar, G. A. (1981). Effect of essential fatty acid deficiency on maternal, placental and fetal rat tissues. J. Nutr. 111, 1602–1610.
| 1:CAS:528:DyaL3MXlvVGqs74%3D&md5=66dcdff2a460a281ce881aa2ac342900CAS | 7277037PubMed |

Mizuta, E., Kokubo, Y., Yamanaka, I., Miyamoto, Y., Okayama, A., Yoshimasa, Y., Tomoike, H., Morisaki, H., and Morisaki, T. (2008). Leptin gene and leptin receptor gene polymorphisms are associated with sweet preference and obesity. Hypertens. Res. 31, 1069–1077.
Leptin gene and leptin receptor gene polymorphisms are associated with sweet preference and obesity.CrossRef | 1:CAS:528:DC%2BD1cXhtFaqsbbE&md5=57db12de9835077fbf3576302432b1c4CAS | 18716353PubMed |

Moore, C. E., and Dhopeshwarkar, G. A. (1980). Placental transport of trans fatty acids in the rat. Lipids 15, 1023–1028.
Placental transport of trans fatty acids in the rat.CrossRef | 1:CAS:528:DyaL3MXotFWksA%3D%3D&md5=ac160279f55d9f2dc13a77793ee2d6f5CAS | 7219071PubMed |

Moritz, K. M., Cuffe, J. S., Wilson, L. B., Dickinson, H., Wlodek, M. E., Simmons, D. G., and Denton, K. M. (2010). Review. Sex-specific programming: a critical role for the renal renin–angiotensin system. Placenta 31, S40–S46.
Review. Sex-specific programming: a critical role for the renal renin–angiotensin system.CrossRef | 20116093PubMed |

Moya, F. (2014). Pre-term nutrition and the lung. World Rev. Nutr. Diet. 110, 239–252.
Pre-term nutrition and the lung.CrossRef | 24751634PubMed |

Myers, M. G., Cowley, M. A., and Munzberg, H. (2008). Mechanisms of leptin action and leptin resistance. Annu. Rev. Physiol. 70, 537–556.
Mechanisms of leptin action and leptin resistance.CrossRef | 1:CAS:528:DC%2BD1cXkt1eqt7k%3D&md5=4e354b8bfb60aa23f89075d57815cd15CAS | 17937601PubMed |

Olivares, A., Rey, A. I., Daza, A., and Lopez-Bote, C. J. (2009). High dietary vitamin A interferes with tissue alpha-tocopherol concentrations in fattening pigs: a study that examines administration and withdrawal times. Animal 3, 1264–1270.
High dietary vitamin A interferes with tissue alpha-tocopherol concentrations in fattening pigs: a study that examines administration and withdrawal times.CrossRef | 1:CAS:528:DC%2BD1MXhtFeqtLrO&md5=12dbd500f99b32baed90ed064b58d115CAS | 22444902PubMed |

Óvilo, C., Fernández, A., Noguera, J. L., Barragán, C., Letón, R., Rodríguez, C., Mercadé, A., Alves, E., Folch, J. M., Varona, L., and Toro, M. (2005). Fine mapping of porcine chromosome 6 QTL and LEPR effects on body composition in multiple generations of an Iberian by Landrace intercross. Genet. Res. 85, 57–67.
Fine mapping of porcine chromosome 6 QTL and LEPR effects on body composition in multiple generations of an Iberian by Landrace intercross.CrossRef | 16089036PubMed |

Óvilo, C., Fernández, A., Fernández, A. I., Folch, J. M., Varona, L., Benítez, R., Nuñez, Y., Rodríguez, C., and Silió, L. (2010). Hypothalamic expression of porcine leptin receptor (LEPR), neuropeptide Y (NPY) and cocaine- and amphetamine-regulated transcript (CART) genes is influenced by LEPR genotype. Mamm. Genome 21, 583–591.
Hypothalamic expression of porcine leptin receptor (LEPR), neuropeptide Y (NPY) and cocaine- and amphetamine-regulated transcript (CART) genes is influenced by LEPR genotype.CrossRef | 21128076PubMed |

Óvilo, C., Benítez, R., Fernández, A., Núñez, Y., Ayuso, M., Fernández, A. I., Rodríguez, C., Isabel, B., Rey, A. I., López-Bote, C., and Silió, L. (2014). Longissimus dorsi transcriptome analysis of purebred and crossbred Iberian pigs differing in muscle characteristics. BMC Genomics 15, 413.
Longissimus dorsi transcriptome analysis of purebred and crossbred Iberian pigs differing in muscle characteristics.CrossRef | 24885501PubMed |

Paillard, F., Catheline, D., Duff, F. L., Bouriel, M., Deugnier, Y., Pouchard, M., Daubert, J. C., and Legrand, P. (2008). Plasma palmitoleic acid, a product of stearoyl-coA desaturase activity, is an independent marker of triglyceridemia and abdominal adiposity. Nutr. Metab. Cardiovasc. Dis. 18, 436–440.
Plasma palmitoleic acid, a product of stearoyl-coA desaturase activity, is an independent marker of triglyceridemia and abdominal adiposity.CrossRef | 1:CAS:528:DC%2BD1cXhtVWmtrvP&md5=02ea2318aa10770b2a90cd94b40f94b2CAS | 18068341PubMed |

Paixão, A. D., and Alexander, B. T. (2013). How is the kidney impacted by the perinatal maternal environment to develop hypertension? Biol. Reprod. 89, 144.
How is the kidney impacted by the perinatal maternal environment to develop hypertension?CrossRef | 24227755PubMed |

Peeling, A. N., and Smart, J. L. (1994). Review of literature showing that undernutrition affects the growth rate of all processes in the brain to the same extent. Metab. Brain Dis. 9, 33–42.
Review of literature showing that undernutrition affects the growth rate of all processes in the brain to the same extent.CrossRef | 1:CAS:528:DyaK2cXlslyguro%3D&md5=ed8301291516ef2d1272a1330175655aCAS | 8058029PubMed |

Père, M. C. (2003). Materno–fetal exchanges and utilisation of nutrients by the fetus: comparison between species. Reprod. Nutr. Dev. 43, 1–15.
Materno–fetal exchanges and utilisation of nutrients by the fetus: comparison between species.CrossRef | 12785446PubMed |

Perry, B. D. (2002). Childhood experience and the expression of genetic potential: what childhood neglect tells us about nature and nurture. Brain Mind 3, 79–100.
Childhood experience and the expression of genetic potential: what childhood neglect tells us about nature and nurture.CrossRef |

Pike, K., Jane Pillow, J., and Lucas, J. S. (2012). Long-term respiratory consequences of intrauterine growth restriction. Semin. Fetal Neonatal Med. 17, 92–98.
Long-term respiratory consequences of intrauterine growth restriction.CrossRef | 22277109PubMed |

Poudyal, H., and Brown, L. (2011). Stearoyl-CoA desaturase: a vital checkpoint in the development and progression of obesity. Endocrine, Metabolic & Immune Disorders-Drug Targets 11, 217–231.
Stearoyl-CoA desaturase: a vital checkpoint in the development and progression of obesity.CrossRef | 1:CAS:528:DC%2BC3MXhtVOksLnJ&md5=3724dc094d2bd4f6ed3d9120b08f9ef7CAS |

Quiniou, N., Dagorn, J., and Gaudré, D. (2002). Variation of piglets’ birth weight and consequences on subsequent performance. Livest. Prod. Sci. 78, 63–70.
Variation of piglets’ birth weight and consequences on subsequent performance.CrossRef |

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 |

Ritz, E., Amann, K., Koleganova, N., and Benz, K. (2011). Prenatal programming effects on blood pressure and renal function. Nat. Rev. Nephrol. 7, 137–144.
Prenatal programming effects on blood pressure and renal function.CrossRef | 21283139PubMed |

Roden, M., Price, T. B., Perseghin, G., Petersen, K. F., Rothman, D. L., Cline, G. W., and Shulman, G. I. (1996). Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 97, 2859–2865.
Mechanism of free fatty acid-induced insulin resistance in humans.CrossRef | 1:CAS:528:DyaK28XjvVWksLw%3D&md5=8f63a0fdc9f05c94de55a185a63a7b41CAS | 8675698PubMed |

Rudolph, A. M. (1984). The fetal circulation and its response to stress. J. Dev. Physiol. 6, 11–19.
| 1:STN:280:DyaL2c7mtlaltg%3D%3D&md5=e6c12f1a172979bf5c137951765d55a7CAS | 6707438PubMed |

Ruiz, J., Antequera, T., Andres, A., Petron, M., and Muriel, E. (2004). Improvement of a solid-phase extraction method for analysis of lipid fractions in muscle foods. Anal. Chim. Acta 520, 201–205.
Improvement of a solid-phase extraction method for analysis of lipid fractions in muscle foods.CrossRef | 1:CAS:528:DC%2BD2cXms1yksb8%3D&md5=e7e3da9d46f3502cabf19a27e1a8239aCAS |

Segura, J., and Lopez-Bote, C. J. (2014). A laboratory-efficient method for intramuscular fat analysis. Food Chem. 145, 821–825.
A laboratory-efficient method for intramuscular fat analysis.CrossRef | 1:CAS:528:DC%2BC3sXhs1Witb7J&md5=168627d8338a3cb2bc552b80aa4086ecCAS | 24128551PubMed |

Shelley, H. J. (1961). Glycogen reserves and their changes at birth and in anoxia. Br. Med. Bull. 17, 137–143.

Stark, M. J., Dierkx, L., Clifton, V. L., and Wright, I. M. (2006). Alterations in the maternal peripheral microvascular response in pregnancies complicated by pre-eclampsia and the impact of fetal sex. J. Soc. Gynecol. Investig. 13, 573–578.
Alterations in the maternal peripheral microvascular response in pregnancies complicated by pre-eclampsia and the impact of fetal sex.CrossRef | 17055308PubMed |

Torres-Rovira, L., Astiz, S., Caro, A., Lopez-Bote, C., Ovilo, C., Pallares, P., Perez-Solana, M. L., Sanchez-Sanchez, R., and Gonzalez-Bulnes, A. (2012). Diet-induced swine model with obesity/leptin resistance for the study of metabolic syndrome and Type 2 diabetes. Scientific World Journal 2012, 510149.
Diet-induced swine model with obesity/leptin resistance for the study of metabolic syndrome and Type 2 diabetes.CrossRef | 1:STN:280:DC%2BC38nmt1Sisg%3D%3D&md5=0852a68a70e3287b35052386aa8ebb50CAS | 22629144PubMed |

Torres-Rovira, L., Tarrade, A., Astiz, S., Mourier, E., Perez-Solana, M., de la Cruz, P., Gomez-Fidalgo, E., Sanchez-Sanchez, R., Chavatte-Palmer, P., and Gonzalez-Bulnes, A. (2013). Sex and breed-dependent organ development and metabolic responses in fetuses from lean and obese/leptin resistant swine. PLoS One 8, e66728.
Sex and breed-dependent organ development and metabolic responses in fetuses from lean and obese/leptin resistant swine.CrossRef | 1:CAS:528:DC%2BC3sXht1ejurbN&md5=b998aaacb2fe0b8e3167c62136075639CAS | 23935823PubMed |

Yu, V. Y., and Upadhyay, A. (2004). Neonatal management of the growth-restricted infant. Semin. Fetal Neonatal Med. 9, 403–409.
Neonatal management of the growth-restricted infant.CrossRef | 15691776PubMed |

Zana-Taïeb, E., Aubelle, M. S., El Ayoubi, M., Lopez, E., and Jarreau, P. H. (2013). Intrauterine growth retardation and lung development. Arch. Pediatr. 20, 1053–1058.
| 23886868PubMed |



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