Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Off to the right start: how pregnancy and early life can determine future animal health and production

K. L. Gatford A B D , C. T. Roberts A B , K. L. Kind A C and P. I. Hynd C
+ Author Affiliations
- Author Affiliations

A Robinson Research Institute University of Adelaide, SA 5005, Australia.

B Adelaide Medical School, University of Adelaide, SA 5005, Australia.

C School of Animal and Veterinary Sciences, University of Adelaide, Roseworthy, SA 5371, Australia.

D Corresponding author. Email: kathy.gatford@adelaide.edu.au

Animal Production Science 58(3) 459-475 https://doi.org/10.1071/AN17014
Submitted: 10 January 2017  Accepted: 23 August 2017   Published: 5 January 2018

Abstract

Animal producers are well aware that a low-birthweight animal is more likely to die in the first few days of life, and, if it survives, it is likely to perform poorly. We are now coming to appreciate that early life events can permanently change an animal’s developmental trajectory, also often referred to as developmental programming. This is an area of current interest in biomedicine, where the concept is known as the ‘developmental origins of health and disease’ (DOHaD). Current gaps in understanding include many of the underlying mechanisms, and whether and how we might intervene and restore the potential for healthy and productive development. This review introduces the biomedical perspective of developmental programming, reviews some of the evidence for long-term effects of early life exposures on welfare and productivity in animal production, with a focus on prenatal growth and maternal stress in pig production, and discusses options for intervening to improve long-term outcomes.

Additional keywords: animal welfare, fetal development, mortality.


References

Alexander GR (1964) Studies on the placenta of the sheep (Ovis aries L.). Effect of surgical reduction in the number of caruncles. Journal of Reproduction and Fertility 7, 307–322.
Studies on the placenta of the sheep (Ovis aries L.). Effect of surgical reduction in the number of caruncles.CrossRef | 1:STN:280:DyaF2c7jvVOguw%3D%3D&md5=f2181187eb1b12fa4031db513cd73477CAS |

Almeida FR, Laurenssen B, Pereira LX, Teerds KJ, Soede NM (2015) Effects of birthweight on reproductive system development and onset of puberty in gilts. Reproduction, Fertility and Development
Effects of birthweight on reproductive system development and onset of puberty in gilts.CrossRef |

Ashmore CR, Addis PB, Doerr L (1973) Development of muscle fibres in the fetal pig. Journal of Animal Science 36, 1088–1093.
Development of muscle fibres in the fetal pig.CrossRef | 1:STN:280:DyaE3s3gtlWmtA%3D%3D&md5=1157037fb07be9bdfdea679e8ad0dd79CAS |

Ashworth CJ, Hogg CO, Hoeks CW, Donald RD, Duncan WC, Lawrence AB, Rutherford KM (2011) Pre-natal social stress and post-natal pain affect the developing pig reproductive axis. Reproduction 142, 907–914.
Pre-natal social stress and post-natal pain affect the developing pig reproductive axis.CrossRef | 1:CAS:528:DC%2BC3MXhs1GqtLbL&md5=8c310d74eaf2bdaca90d3eb031807845CAS |

Barker DJP, Osmond C (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 327, 1077–1081.
Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales.CrossRef |

Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. Lancet 334, 577–580.
Weight in infancy and death from ischaemic heart disease.CrossRef |

Bee G (2004) Effect of early gestation feeding, birth weight, and gender of progeny on muscle fiber characteristics of pigs at slaughter. Journal of Animal Science 82, 826–836.
Effect of early gestation feeding, birth weight, and gender of progeny on muscle fiber characteristics of pigs at slaughter.CrossRef | 1:CAS:528:DC%2BD2cXhvVCku7g%3D&md5=ed602d8dae363159ac39bb761bd88125CAS |

Brameld JM, Daniel ZCTR (2008) In utero effects on livestock muscle development and body composition. Australian Journal of Experimental Agriculture 48, 921–929.
In utero effects on livestock muscle development and body composition.CrossRef |

Broekman K 1985 Low birthweight causes high mortality. Pigs February 24 25

Campbell RG, Dunkin AC (1982) The effect of birth weight on the estimated milk intake, growth and body composition of sow-reared piglets. Animal Production 35, 193–197.
The effect of birth weight on the estimated milk intake, growth and body composition of sow-reared piglets.CrossRef |

Chavatte-Palmer P, Richard C, Peugnet P, Robles M, Rousseau-Ralliard D, Tarrade A (2015) The developmental origins of health and disease: importance for animal production. Animal Reproduction 12, 505–520.

Chavatte-Palmer P, Tarrade A, Kiefer H, Duranthon V, Jammes H (2016) Breeding animals for quality products: not only genetics. Reproduction, Fertility and Development 28, 94–111.
Breeding animals for quality products: not only genetics.CrossRef |

Couret D, Prunier A, Mounier A-M, Thomas F, Oswald IP, Merlot E (2009) Comparative effects of a prenatal stress occurring during early or late gestation on pig immune response. Physiology & Behavior 98, 498–504.
Comparative effects of a prenatal stress occurring during early or late gestation on pig immune response.CrossRef | 1:CAS:528:DC%2BD1MXhtFGqsbvO&md5=eb8017cde6a213b238350d9449257f9cCAS |

Da Silva-Buttkus P, van den Hurk R, te Velde ER, Taverne MA (2003) Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter. Reproduction 126, 249–258.
Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter.CrossRef | 1:CAS:528:DC%2BD3sXntFyjtrs%3D&md5=7db69fba0dea692cbbb0d63c7bbce69aCAS |

Daniel ZC, Brameld JM, Craigon J, Scollan ND, Buttery PJ (2007) Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition. Journal of Animal Science 85, 1565–1576.
Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition.CrossRef | 1:CAS:528:DC%2BD2sXls1antLc%3D&md5=e5e529dc7103624b1ebd57b548b4e07cCAS |

de Groot J, Kranendonk G, Fillerup M, Hopster H, Boersma W, Hodgson D, van Reenen K, Taverne M (2007) Response to LPS in female offspring from sows treated with cortisol during pregnancy. Physiology & Behavior 90, 612–618.
Response to LPS in female offspring from sows treated with cortisol during pregnancy.CrossRef | 1:CAS:528:DC%2BD2sXisVWhsb4%3D&md5=270e119bb03bf959e72430224f4be803CAS |

de Haas EN, Bolhuis JE, Kemp B, Groothuis TG, Rodenburg TB (2014) Parents and early life environment affect behavioral development of laying hen chickens. PLoS One 9, e90577
Parents and early life environment affect behavioral development of laying hen chickens.CrossRef |

Dwyer CM, Stickland NC (1991) Sources of variation in myofibre number within and between litters of pigs. Animal Production 52, 527–533.
Sources of variation in myofibre number within and between litters of pigs.CrossRef |

Dwyer CM, Fletcher JM, Stickland NC (1993) Muscle cellularity and postnatal growth in the pig. Journal of Animal Science 71, 3339–3343.
Muscle cellularity and postnatal growth in the pig.CrossRef | 1:STN:280:DyaK2c7isVemtA%3D%3D&md5=0305bd437f2e685c86e9772d31ff2fdaCAS |

Dwyer CM, Stickland NC, Fletcher JM (1994) The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. Journal of Animal Science 72, 911–917.
The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth.CrossRef | 1:STN:280:DyaK2c3osVahsA%3D%3D&md5=19ee13d9d9ae061de992cc19c4ebe80eCAS |

Fahey AJ, Brameld JM, Parr T, Buttery PJ (2005a) The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. Journal of Animal Science 83, 2564–2571.
The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb.CrossRef | 1:CAS:528:DC%2BD2MXhtFGmu7nK&md5=33f25f9150c22d08c403dacd40a528eeCAS |

Fahey AJ, Brameld JM, Parr T, Buttery PJ (2005b) Ontogeny of factors associated with proliferation and differentiation of muscle in the ovine fetus. Journal of Animal Science 83, 2330–2338.
Ontogeny of factors associated with proliferation and differentiation of muscle in the ovine fetus.CrossRef | 1:CAS:528:DC%2BD2MXhtVKqsLvL&md5=d8caf34ef495b82b35bb0249b6886179CAS |

Fahmy MH, Bernard C (1971) Causes of mortality in Yorkshire pigs from birth to 20 weeks of age. Canadian Journal of Animal Science 51, 351–359.
Causes of mortality in Yorkshire pigs from birth to 20 weeks of age.CrossRef |

Fahmy MH, Holtmann WB, Maclntyre TM, Moxley JE (1978) Evaluation of piglet mortality in 28 two-breed crosses among eight breeds of pig. Animal Production 26, 277–285.
Evaluation of piglet mortality in 28 two-breed crosses among eight breeds of pig.CrossRef |

Falconer J, Owens JA, Allotta E, Robinson JS (1985) Effect of restriction of placental growth on the concentrations of insulin, glucose and placental lactogen in the plasma of sheep. The Journal of Endocrinology 106, 7–11.
Effect of restriction of placental growth on the concentrations of insulin, glucose and placental lactogen in the plasma of sheep.CrossRef | 1:CAS:528:DyaL2MXksVynsrw%3D&md5=c69dbff067f0416a9f670a582c7958aeCAS |

Funston RN, Summers AF (2013) Epigenetics: setting up lifetime production of beef cows by managing nutrition. Annual Review of Animal Biosciences 1, 339–363.
Epigenetics: setting up lifetime production of beef cows by managing nutrition.CrossRef | 1:STN:280:DC%2BC2M3ntlOgtA%3D%3D&md5=ae453b458bbe8b9dbc43a9e3a884c414CAS |

Gardner IA, Hird DW, Franti CE (1989) Neonatal survival in swine: effects of low birth weight and clinical disease. American Journal of Veterinary Research 50, 792–797.

Gatford KL, Ekert JE, Blackmore K, De Blasio MJ, Boyce JM, Owens JA, Campbell RG, Owens PC (2003) Variable maternal nutrition and growth hormone treatment in the second quarter of pregnancy in pigs alter semitendinosus muscle in adolescent progeny. British Journal of Nutrition 90, 283–293.
Variable maternal nutrition and growth hormone treatment in the second quarter of pregnancy in pigs alter semitendinosus muscle in adolescent progeny.CrossRef | 1:CAS:528:DC%2BD3sXmsFymt7w%3D&md5=4e8f0d7a66a6b0427cfac7ad79f2faa4CAS |

Gatford KL, Boyce JM, Blackmore K, Smits RJ, Campbell RG, Owens PC (2004) Long-term, but not short-term, treatment with somatotropin during pregnancy in underfed pigs increases the body size of progeny at birth. Journal of Animal Science 82, 93–101.
Long-term, but not short-term, treatment with somatotropin during pregnancy in underfed pigs increases the body size of progeny at birth.CrossRef | 1:CAS:528:DC%2BD2cXlsFWkug%3D%3D&md5=6235d9dc1d79446574e2db8e5d55daedCAS |

Gondret F, Lefaucheur L, Louveau I, Lebret B, Pichodo X, Le Cozler Y (2005) Influence of piglet birth weight on postnatal growth performance, tissue lipogenic capacity and muscle histological traits at market weight. Livestock Production Science 93, 137–146.
Influence of piglet birth weight on postnatal growth performance, tissue lipogenic capacity and muscle histological traits at market weight.CrossRef |

Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B (2006) Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. Journal of Animal Science 84, 93–103.
Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs.CrossRef | 1:CAS:528:DC%2BD28XjvFynuw%3D%3D&md5=149a9b600c20643d846d5dd11530bf71CAS |

Greenwood PL, Bell AW (2003) Consequences of intra-uterine growth retardation for postnatal growth, metabolism and pathophysiology. Reproduction 61, 195–206.

Hales CN, Barker DJP, Clark PMS, Cox LJ, Fall C, Osmond C, Winter PD (1991) Fetal and infant growth and impaired glucose tolerance at age 64. British Medical Journal 303, 1019–1022.
Fetal and infant growth and impaired glucose tolerance at age 64.CrossRef | 1:STN:280:DyaK38%2Fmtlakuw%3D%3D&md5=5df19f3b83404b432e5e9fc665935d87CAS |

Handel SE, Stickland NC (1988) Catch-up growth in pigs: a relationship with muscle cellularity. Animal Production 47, 291–295.
Catch-up growth in pigs: a relationship with muscle cellularity.CrossRef |

Hanson MA, Gluckman PD (2014) Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiological Reviews 94, 1027–1076.
Early developmental conditioning of later health and disease: physiology or pathophysiology?CrossRef | 1:CAS:528:DC%2BC2cXitFansbnO&md5=5d0187d3b79ebdedf5ba740522a6465eCAS |

Haussmann MF, Carroll JA, Weesner GD, Daniels MJ, Matteri RL, Lay DC (2000) Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic–pituitary–adrenal (HPA) axis. Journal of Animal Science 78, 2399–2411.
Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamic–pituitary–adrenal (HPA) axis.CrossRef | 1:CAS:528:DC%2BD3cXms1yjsrY%3D&md5=0fe5b30d1a58ef7f36c50eb3c8c9ff20CAS |

Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General and Comparative Endocrinology 135, 365–371.
Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype.CrossRef | 1:CAS:528:DC%2BD2cXjtVCitA%3D%3D&md5=355e97964934d9d7a03ff624ecc5fb47CAS |

Hegarty PVJ, Allen CE (1978) Effect of pre-natal runting on the postnatal development of skeletal muscles in swine and rats. Journal of Animal Science 46, 1634–1640.
Effect of pre-natal runting on the postnatal development of skeletal muscles in swine and rats.CrossRef | 1:STN:280:DyaE1M%2FgsFeqsg%3D%3D&md5=26f7710fa75760e2874c085ec4fd0b0aCAS |

Hemsworth PH, Winfield CG, Mullaney PD (1976) Within-litter variation in the performance of piglets to three weeks of age. Animal Production 22, 351–357.
Within-litter variation in the performance of piglets to three weeks of age.CrossRef |

Henriksen R, Groothuis TG, Rettenbacher S (2011) Elevated plasma corticosterone decreases yolk testosterone and progesterone in chickens: linking maternal stress and hormone-mediated maternal effects. PLoS One 6, e23824
Elevated plasma corticosterone decreases yolk testosterone and progesterone in chickens: linking maternal stress and hormone-mediated maternal effects.CrossRef | 1:CAS:528:DC%2BC3MXhtF2gu73I&md5=ee6a99967e02cf279564f125025d40afCAS |

Henriksen R, Rettenbacher S, Groothuis TGG (2013) Maternal corticosterone elevation during egg formation in chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition. General and Comparative Endocrinology 191, 83–91.
Maternal corticosterone elevation during egg formation in chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition.CrossRef | 1:CAS:528:DC%2BC3sXhtlWjtbbM&md5=3e14b5d65a5a21ff8acbbf685dd7e8fcCAS |

Heyer A, Andersson HK, Lindberg JE, Lundström K (2004) Effect of extra maternal feed supply in early gestation on sow and piglet performance and production and meat quality of growing/finishing pigs. Acta Agriculturae Scandinavica: Section A. Animal Science 54, 44–55.
Effect of extra maternal feed supply in early gestation on sow and piglet performance and production and meat quality of growing/finishing pigs.CrossRef |

Hunter DS, Hazel SJ, Kind KL, Owens JA, Pitcher JB, Gatford KL (2016) Programming the brain: common outcomes and gaps in knowledge from animal studies of IUGR. Physiology & Behavior 164, 233–248.
Programming the brain: common outcomes and gaps in knowledge from animal studies of IUGR.CrossRef | 1:CAS:528:DC%2BC28XhtVWksLrE&md5=ef178e90a2fd2924749e993efede2fedCAS |

Hynd PI, Weaver S, Edwards NH, Heberle ND, Bowling M (2016) Developmental programming: a new frontier for the poultry industry? Animal Production Science 56, 1233–1238.
Developmental programming: a new frontier for the poultry industry?CrossRef |

Ibáñez L, Ong K, Dunger DB, de Zegher F (2006) Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. The Journal of Clinical Endocrinology and Metabolism 91, 2153–2158.
Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children.CrossRef |

Ison SH, D’Eath RB, Robson SK, Baxter EM, Ormandy E, Douglas AJ, Russell JA, Lawrence AB, Jarvis S (2010) ‘Subordination style’ in pigs? The response of pregnant sows to mixing stress affects their offspring’s behaviour and stress reactivity. Applied Animal Behaviour Science 124, 16–27.
‘Subordination style’ in pigs? The response of pregnant sows to mixing stress affects their offspring’s behaviour and stress reactivity.CrossRef |

Jarvis S, Moinard C, Robson SK, Baxter E, Ormandy E, Douglas AJ, Seckl JR, Russell JA, Lawrence AB (2006) Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Hormones and Behavior 49, 68–80.
Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour.CrossRef | 1:CAS:528:DC%2BD2MXhtlCrsbfL&md5=13311f42e2b4a9d9a2943c8415582886CAS |

Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, Phillips DIW (2006) Fetal growth and the adrenocortical response to psychological stress. The Journal of Clinical Endocrinology and Metabolism 91, 1868–1871.
Fetal growth and the adrenocortical response to psychological stress.CrossRef | 1:CAS:528:DC%2BD28XkslCnur8%3D&md5=c6b343987da872df8613ce2902e5af12CAS |

Kanitz E, Otten W, Tuchscherer M (2006) Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. The Journal of Endocrinology 191, 207–220.
Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol.CrossRef | 1:CAS:528:DC%2BD28Xht1eju7bJ&md5=dac87c13a9f607b786d343ccd58acb02CAS |

Knol EF, Ducro BJ, van Arendonk JAM, van der Lende T (2002) Direct, maternal and nurse sow genetic effects on farrowing-, pre-weaning- and total piglet survival. Livestock Production Science 73, 153–164.
Direct, maternal and nurse sow genetic effects on farrowing-, pre-weaning- and total piglet survival.CrossRef |

Kranendonk G, Hopster H, Fillerup M, Ekkel ED, Mulder EJ, Wiegant VM, Taverne MA (2006a) Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation. Domestic Animal Endocrinology 30, 218–238.
Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation.CrossRef | 1:CAS:528:DC%2BD28XitVartL4%3D&md5=f3b0d237282dce3e46bb9676d9567210CAS |

Kranendonk G, Hopster H, Fillerup M, Ekkel ED, Mulder EJH, Taverne MAM (2006b) Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring. Hormones and Behavior 49, 663–672.
Cortisol administration to pregnant sows affects novelty-induced locomotion, aggressive behaviour, and blunts gender differences in their offspring.CrossRef | 1:CAS:528:DC%2BD28XksVCqurY%3D&md5=c6553ba6d9f06f06f9bbed74187f7ee5CAS |

Kranendonk G, Van der Mheen H, Fillerup M, Hopster H (2007) Social rank of pregnant sows affects their body weight gain and behavior and performance of the offspring. Journal of Animal Science 85, 420–429.
Social rank of pregnant sows affects their body weight gain and behavior and performance of the offspring.CrossRef | 1:CAS:528:DC%2BD2sXht1els70%3D&md5=a3a72a7cfe42bc271d93b29a202aa814CAS |

Kranendonk G, Mulder EJ, Parvizi N, Taverne MA (2008) Prenatal stress in pigs: experimental approaches and field observations. Experimental and Clinical Endocrinology & Diabetes 116, 413–422.
Prenatal stress in pigs: experimental approaches and field observations.CrossRef | 1:CAS:528:DC%2BD1cXht1Sgtb3N&md5=563303145742f26b65f330a4bf93a762CAS |

Ladinig A, Foxcroft G, Ashley C, Lunney JK, Plastow G, Harding JC (2014) Birth weight, intrauterine growth retardation and fetal susceptibility to porcine reproductive and respiratory syndrome virus. PLoS One 9, e109541
Birth weight, intrauterine growth retardation and fetal susceptibility to porcine reproductive and respiratory syndrome virus.CrossRef |

Liu J, He J, Yu J, Mao X, Zheng P, Huang Z, Yu B, Chen D (2014) Birth weight alters the response to postnatal high-fat diet-induced changes in meat quality traits and skeletal muscle proteome of pigs. British Journal of Nutrition 111, 1738–1747.
Birth weight alters the response to postnatal high-fat diet-induced changes in meat quality traits and skeletal muscle proteome of pigs.CrossRef | 1:CAS:528:DC%2BC2cXmtVWnurY%3D&md5=72938d19bc5d79c1a4217593216dd8c8CAS |

Mack LA, Lay DC, Eicher SD, Johnson AK, Richert BT, Pajor EA (2014) Growth and reproductive development of male piglets are more vulnerable to midgestation maternal stress than that of female piglets. Journal of Animal Science 92, 530–548.
Growth and reproductive development of male piglets are more vulnerable to midgestation maternal stress than that of female piglets.CrossRef | 1:CAS:528:DC%2BC2cXjs1Kmsr4%3D&md5=6b5052d1b02782aa12591943825ade5aCAS |

Magnabosco D, Bernardi ML, Wentz I, Cunha ECP, Bortolozzo FP (2016) Low birth weight affects lifetime productive performance and longevity of female swine. Livestock Science 184, 119–125.
Low birth weight affects lifetime productive performance and longevity of female swine.CrossRef |

Metges CC, Gors S, Martens K, Krueger R, Metzler-Zebeli BU, Nebendahl C, Otten W, Kanitz E, Zeyner A, Hammon HM, Pfuhl R, Nurnberg G (2015) Body composition and plasma lipid and stress hormone levels during 3 weeks of feed restriction and refeeding in low birth weight female pigs. Journal of Animal Science 93, 999–1014.
Body composition and plasma lipid and stress hormone levels during 3 weeks of feed restriction and refeeding in low birth weight female pigs.CrossRef | 1:CAS:528:DC%2BC2MXntVGjurg%3D&md5=3889545435df1c09ee5daec1f059f448CAS |

Morise A, Louveau I, Le Huerou-Luron I (2008) Growth and development of adipose tissue and gut and related endocrine status during early growth in the pig: impact of low birth weight. animal 2, 73–83.
Growth and development of adipose tissue and gut and related endocrine status during early growth in the pig: impact of low birth weight.CrossRef | 1:STN:280:DC%2BC38vpt1agtw%3D%3D&md5=c341705fdc256a0c2dd803e3572d225aCAS |

Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JL, Hildebrandt TB, Lonergan P, Ireland JJ, Evans AC (2013) Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biology of Reproduction 88, 92
Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring.CrossRef |

Muir JL, Pfister HP, Ivinskis A (1985) Effects of prepartum stress and postpartum enrichment on mother–infant interaction and offspring problem-solving ability in Rattus norvegicus. Journal of Comparative Psychology 99, 468–478.
Effects of prepartum stress and postpartum enrichment on mother–infant interaction and offspring problem-solving ability in Rattus norvegicus.CrossRef |

Nissen PM, Oksbjerg N (2011) Birth weight and postnatal dietary protein level affect performance, muscle metabolism and meat quality in pigs. animal 5, 1382–1389.
Birth weight and postnatal dietary protein level affect performance, muscle metabolism and meat quality in pigs.CrossRef | 1:CAS:528:DC%2BC3MXht1Cjsb3P&md5=221555bef065e5d76a5de17e2bf1d3fbCAS |

Nissen PM, Danielsen VO, Jorgensen PF, Oksbjerg N (2003) Increased maternal nutrition of sows has no beneficial effects on muscle fiber number or postnatal growth and has no impact on the meat quality of the offspring. Journal of Animal Science 81, 3018–3027.
Increased maternal nutrition of sows has no beneficial effects on muscle fiber number or postnatal growth and has no impact on the meat quality of the offspring.CrossRef | 1:CAS:528:DC%2BD3sXpslSjsro%3D&md5=c6247fcb12585fd79145951819031f66CAS |

Nissen PM, Jorgensen PF, Oksbjerg N (2004) Within-litter variation in muscle fiber characteristics, pig performance, and meat quality traits. Journal of Animal Science 82, 414–421.
Within-litter variation in muscle fiber characteristics, pig performance, and meat quality traits.CrossRef | 1:CAS:528:DC%2BD2cXhtFSmtbw%3D&md5=c5a2e309e840e6ea1e028683481eb42dCAS |

Ong KKL, Ahmed ML, Emmett PM, Preece MA, Dunger DB (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. British Medical Journal 320, 967–971.
Association between postnatal catch-up growth and obesity in childhood: prospective cohort study.CrossRef | 1:STN:280:DC%2BD3c3hs1OmtA%3D%3D&md5=161358b81c3104b5f32da1cfa8ca86c0CAS |

Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ (1993) Early growth and death from cardiovascular disease in women. British Medical Journal 307, 1519–1524.
Early growth and death from cardiovascular disease in women.CrossRef | 1:STN:280:DyaK2c7gtVOmsQ%3D%3D&md5=6a584efee741532f990ea505b087a78eCAS |

Otten W, Kanitz E, Tuchscherer M, Nurnberg G (2001) Effects of prenatal restraint stress on hypothalamic–pituitary–adrenocortical and sympatho–adrenomedullary axis in neonatal pigs. Animal Science 73, 279–287.
Effects of prenatal restraint stress on hypothalamic–pituitary–adrenocortical and sympatho–adrenomedullary axis in neonatal pigs.CrossRef | 1:CAS:528:DC%2BD38XitFChug%3D%3D&md5=dfc85988591375c66d8ce088921bf34eCAS |

Peter RF, Gugusheff J, Wooldridge AL, Gatford KL, Muhlhausler BS (2017) Placental restriction in multi-fetal pregnancies and between-twin differences in size at birth alter neonatal feeding behaviour in the sheep. Journal of Developmental Origins of Health and Disease 8, 357–369.
Placental restriction in multi-fetal pregnancies and between-twin differences in size at birth alter neonatal feeding behaviour in the sheep.CrossRef | 1:STN:280:DC%2BC1cvltFKrtw%3D%3D&md5=a1e16928f1229b5576f1291fab3b2b81CAS |

Pettigrew JE, Cornelius SG, Moser RL, Heeg TR, Hanke HE, Miller KP, Hagen CD (1986) Effects of oral doses of corn oil and other factors on preweaning survival and growth of piglets. Journal of Animal Science 62, 601–612.
Effects of oral doses of corn oil and other factors on preweaning survival and growth of piglets.CrossRef | 1:STN:280:DyaL287psFGrsw%3D%3D&md5=ec48e0fd20de28c6955ebdcaa5cbfc1bCAS |

Phillips DIW, Walker BR, Reynolds RM, Flanagan DEH, Wood PJ, Osmond C, Barker DJP, Whorwood CB (2000) Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension 35, 1301–1306.
Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations.CrossRef | 1:CAS:528:DC%2BD3cXksVCnt7g%3D&md5=81c8573b9dc6a7cb36cbc9a7b206ca6eCAS |

Poore K, Fowden AL (2002) The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 45, 1247–1254.
The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age.CrossRef | 1:CAS:528:DC%2BD38XntFegurY%3D&md5=f0fa9abffcc0f7d5aa455cf978e58459CAS |

Poore K, Fowden AL (2004) Insulin sensitivity in juvenile and adult Large White pigs of low and high birthweight. Diabetologia 47, 340–348.
Insulin sensitivity in juvenile and adult Large White pigs of low and high birthweight.CrossRef | 1:STN:280:DC%2BD2c7gtVamtQ%3D%3D&md5=7193d943ba89a29083c40f315137d264CAS |

Powell SE, Aberle ED (1980) Effects of birth weight on growth and carcass composition of swine. Journal of Animal Science 50, 860–868.
Effects of birth weight on growth and carcass composition of swine.CrossRef | 1:STN:280:DyaL3c3islGnug%3D%3D&md5=22c57b5fc27a430b58046dbfbc535ab8CAS |

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

Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. Journal of Animal Science 84, E113–E123.
Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis.CrossRef |

Rehfeldt C, Nissen PM, Kuhn G, Vestergaard M, Ender K, Oksbjerg N (2004) Effects of maternal nutrition and porcine growth hormone (pGH) treatment during gestation on endocrine and metabolic factors in sows, fetuses and pigs, skeletal muscle development, and postnatal growth. Domestic Animal Endocrinology 27, 267–285.
Effects of maternal nutrition and porcine growth hormone (pGH) treatment during gestation on endocrine and metabolic factors in sows, fetuses and pigs, skeletal muscle development, and postnatal growth.CrossRef | 1:CAS:528:DC%2BD2cXnvV2rsbw%3D&md5=aa4abb759af99d2bda8290eb45e746b3CAS |

Rettenbacher S, Mostl E, Hackl R, Palme R (2005) Corticosterone in chicken eggs. Annals of the New York Academy of Sciences 1046, 193–203.
Corticosterone in chicken eggs.CrossRef | 1:CAS:528:DC%2BD2MXhtVWjtLzL&md5=1c9530d24f6ee2e17881c99419d5a25fCAS |

Richter VF, Briffa JF, Moritz KM, Wlodek ME, Hryciw DH (2016) The role of maternal nutrition, metabolic function and the placenta in developmental programming of renal dysfunction. Clinical and Experimental Pharmacology & Physiology 43, 135–141.
The role of maternal nutrition, metabolic function and the placenta in developmental programming of renal dysfunction.CrossRef | 1:CAS:528:DC%2BC2MXhvF2kt7fO&md5=14dad4df43a4e455fd0224d05cd9a6a2CAS |

Ritacco G, Radecki SV, Schoknecht PA (1997) Compensatory growth in runt pigs is not mediated by insulin-like growth factor I. Journal of Animal Science 75, 1237–1243.
Compensatory growth in runt pigs is not mediated by insulin-like growth factor I.CrossRef | 1:CAS:528:DyaK2sXjsV2mu7w%3D&md5=efe00a38ab93a7e925b751b5f479dc9dCAS |

Roberts CT (2010) IFPA award in placentology lecture: complicated interactions between genes and the environment in placentation, pregnancy outcome and long term health. Placenta 31, S47–S53.
IFPA award in placentology lecture: complicated interactions between genes and the environment in placentation, pregnancy outcome and long term health.CrossRef |

Robinson DL, Cafe LM, Greenwood PL (2013) Meat science and muscle biology symposium: developmental programming in cattle: consequences for growth, efficiency, carcass, muscle, and beef quality characteristics. Journal of Animal Science 91, 1428–1442.
Meat science and muscle biology symposium: developmental programming in cattle: consequences for growth, efficiency, carcass, muscle, and beef quality characteristics.CrossRef | 1:CAS:528:DC%2BC3sXmsFKnu7s%3D&md5=f35b7b8eb363c02d71676e89e105c9ceCAS |

Roseboom TJ, van der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJP, Bleker OP (2001) Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Molecular and Cellular Endocrinology 185, 93–98.
Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview.CrossRef | 1:CAS:528:DC%2BD3MXovFyqtL0%3D&md5=54d7c7ef9ac83678ff57887b7ef3e793CAS |

Selling KE, Carstensen J, Finnstrom O, Sydsjo G (2006) Intergenerational effects of preterm birth and reduced intrauterine growth: a population-based study of Swedish mother–offspring pairs. BJOG 113, 430–440.
Intergenerational effects of preterm birth and reduced intrauterine growth: a population-based study of Swedish mother–offspring pairs.CrossRef | 1:STN:280:DC%2BD287msVKrsA%3D%3D&md5=755935a1d05986c389f3c1b0051c19d5CAS |

Sinclair KD, Rutherford KM, Wallace JM, Brameld JM, Stoger R, Alberio R, Sweetman D, Gardner DS, Perry VE, Adam CL, Ashworth CJ, Robinson JE, Dwyer CM (2016) Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod. Fertil. Dev. 28, 1443–1478.
Epigenetics and developmental programming of welfare and production traits in farm animals.CrossRef | 1:CAS:528:DC%2BC28Xhtl2msbbK&md5=4a4851ac8ce542c3db8bcf1f41f9da1cCAS |

Thompson JG, Gardner DK, Pugh PA, McMillan WH, Tervit HR (1995) Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biology of Reproduction 53, 1385–1391.
Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos.CrossRef | 1:CAS:528:DyaK2MXpsVeisrs%3D&md5=8dac2711b2ecb8b85908f46e7c962af5CAS |

Thompson KM, Simons EA, Badizadegan K, Reef SE, Cooper LZ (2014) Characterization of the risks of adverse outcomes following rubella infection in pregnancy. Risk Analysis
Characterization of the risks of adverse outcomes following rubella infection in pregnancy.CrossRef |

Tuchscherer M, Kanitz E, Otten W, Tuchscherer A (2002) Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs. Veterinary Immunology and Immunopathology 86, 195–203.
Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs.CrossRef | 1:CAS:528:DC%2BD38XjsVSqtb0%3D&md5=49c0e72c9ec25076bc6022ee7854d5b1CAS |

van der Lende T, de Jager D (1991) Death risk and preweaning growth of piglets in relation to the within-litter weight distribution at birth. Livestock Production Science 28, 73–84.
Death risk and preweaning growth of piglets in relation to the within-litter weight distribution at birth.CrossRef |

Verdon M, Hansen CF, Rault JL, Jongman E, Hansen LU, Plush K, Hemsworth PH (2015) Effects of group housing on sow welfare: a review. Journal of Animal Science 93, 1999–2017.
Effects of group housing on sow welfare: a review.CrossRef | 1:CAS:528:DC%2BC2MXhtVCkt7nO&md5=59e1f2cd267c70cf4aadd85472780b0aCAS |

Wallace JM, Regnault TR, Limesand SW, Hay WW, Anthony RV (2005) Investigating the causes of low birth weight in contrasting ovine paradigms. The Journal of Physiology 565, 19–26.
Investigating the causes of low birth weight in contrasting ovine paradigms.CrossRef | 1:CAS:528:DC%2BD2MXkslyrurc%3D&md5=43aa156d105f141ac7dbbf2c0544f4adCAS |

Widdowson EM (1971) Intra-uterine growth retardation in the pig. I. Organ size and cellular development at birth and after birth to maturity. Biology of the Neonate 19, 329–340.
Intra-uterine growth retardation in the pig. I. Organ size and cellular development at birth and after birth to maturity.CrossRef | 1:STN:280:DyaE387ptFahsA%3D%3D&md5=1e96ae1ab0566d21b679d5874060c320CAS |

Wigmore PMC, Stickland NC (1983) Muscle development in large and small pig fetuses. Journal of Anatomy 137, 235–245.

Wolter BF, Ellis M, Corrigan BP, DeDecker JM (2002) The effect of birth weight and feeding of supplemental milk replacer to piglets during lactation on preweaning and postweaning growth performance and carcass characteristics. Journal of Animal Science 80, 301–308.
The effect of birth weight and feeding of supplemental milk replacer to piglets during lactation on preweaning and postweaning growth performance and carcass characteristics.CrossRef | 1:CAS:528:DC%2BD38XmvFSqtLo%3D&md5=2b3c99b1ae83cd94a431d0533f60a4daCAS |

Zhong X, Li W, Huang X, Zhang L, Yimamu M, Raiput N, Zhou Y, Wang T (2012) Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation. Cell Stress & Chaperones 17, 495–505.
Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation.CrossRef | 1:CAS:528:DC%2BC38Xot1ylt7k%3D&md5=87af8296d2479081b96e70f9b5506573CAS |

Zuena AR, Zinni M, Giuli C, Cinque C, Alema GS, Giuliani A, Catalani A, Casolini P, Cozzolino R (2016) Maternal exposure to environmental enrichment before and during gestation influences behaviour of rat offspring in a sex-specific manner. Physiology & Behavior 163, 274–287.
Maternal exposure to environmental enrichment before and during gestation influences behaviour of rat offspring in a sex-specific manner.CrossRef | 1:CAS:528:DC%2BC28Xos1antL0%3D&md5=b2906c61d4c03d56eb19b636b364987aCAS |



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