SHEEP MODELS OF INTRAUTERINE GROWTH RESTRICTION: FETAL ADAPTATIONS AND CONSEQUENCES

Morrison, Janna L

doi:10.1111/j.1440-1681.2008.04975.x

Cited by 289Pregnancy and preeclampsia studiesBirth, Development, and HealthPrenatal Substance Exposure Effects

SHEEP MODELS OF INTRAUTERINE GROWTH RESTRICTION: FETAL ADAPTATIONS AND CONSEQUENCES

Morrison, Janna L·2008·Clinical and Experimental Pharmacology and Physiology

DOI 10.1111/j.1440-1681.2008.04975.x

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Abstract

SUMMARY: Intrauterine growth restriction (IUGR) has been associated with poor perinatal health outcomes. Animal models have been used to investigate why IUGR is associated with a poor prognosis. The sheep has been used extensively as an experimental model for IUGR with poor placental substrate supply to the fetus induced using a range of methods, including the surgical ablation of the majority of endometrial caruncles prior to conception, experimental induction of maternal hyperthermia, ligation of an umbilical artery or embolization of the placenta in late gestation and maternal overnutrition in the pregnant adolescent ewe. Fetal adaptations to fetal hypoxia and hypoglycaemia include activation of the fetal hypothalamic–pituitary–adrenal (HPA) axis and sympathetic nervous system and an associated increase in circulating cortisol and noradrenaline concentrations. Fetal cardiovascular responses vary according to the method used to induce placental dysfunction. Although an array of experimental models has been used to induce placental dysfunction at different stages of fetal development, each leads to remarkably similar fetal growth, metabolic, neuroendocrine and cardiovascular adaptations and consequences. The extent and range of the fetal physiological adaptations to chronic placental insufficiency are determined by the duration of exposure and the degree of the severity of substrate supply restriction. The present review summarizes how sheep models of IUGR have provided an increased understanding of the nature of the fetal adaptations to IUGR, their longer‐term physiological consequences and how to improve clinical management of IUGR in human pregnancies.

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The placental strategy for coping with hypoxia differs with species, duration, severity and timing of the hypoxic insult, and/or the presence of fetal hypoxemia.
“However, its strategy appears to differ with species, duration, severity and timing of the hypoxic insult, and/or the presence of fetal hypoxemia (393).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [393]

WEIGHT IN INFANCY AND DEATH FROM ISCHAEMIC HEART DISEASE
Barker, D. J. P., Osmond, C., Winter, P. D., Margetts, B., & Simmonds, S. J. (1989) · The Lancet · doi:10.1016/s0140-6736(89)90710-1 · Cited by 3,574 · see citing works
Fetal origins of adult disease: strength of effects and biological basis
Barker, D., Eriksson, J., Forsén, T., & Osmond, C. (2002) · International Journal of Epidemiology · doi:10.1093/ije/31.6.1235 · Cited by 2,024 · see citing works
Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming
Mcmillen, I. C., & Robinson, J. S. (2005) · Physiological Reviews · doi:10.1152/physrev.00053.2003 · Cited by 1,910 · see citing works
Trajectories of growth among children who have coronary events as adults
Barker, D. J. P., Osmond, C., Forsén, T. J., Kajantie, E., & Eriksson, J. G. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa044160 · Cited by 1,517 · see citing works
Intrauterine growth restriction
Resnik, R. (2002) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(01)01780-x · Cited by 1,022 · see citing works
Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction
Bernstein, I. M., Horbar, J. D., Badger, G. J., Ohlsson, A., & Golan, A. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(00)70513-8 · Cited by 840 · see citing works
Rapid Transition of Cardiac Myocytes from Hyperplasia to Hypertrophy During Postnatal Development
Li, F. (1996) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1996.0163 · Cited by 837 · see citing works
Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976
Rich-Edwards, J. W., Stampfer, M. J., Manson, J. E., ROSNER, B. A., Hankinson, S. E., Colditz, G. A., Hennekens, C. H., & Willett, W. C. (1997) · BMJ · doi:10.1136/bmj.315.7105.396 · Cited by 814 · see citing works
Are there behavioural states in the human fetus?
Nijhuis, J. G., Prechtl, H. F. R., Martin, C. B., & Bots, R. S. G. M. (1982) · Early Human Development · doi:10.1016/0378-3782(82)90106-2 · Cited by 808 · see citing works
Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915-29
Leon, D. A., Lithell, H. O., Vågerö, D., Koupilová, I., Mohsen, R., Berglund, L., Lithell, U.-B., & McKeigue, P. M. (1998) · BMJ · doi:10.1136/bmj.317.7153.241 · Cited by 807 · see citing works
Cardiomyocyte DNA synthesis and binucleation during murine development
Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. T., & Field, L. J. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.5.h2183 · Cited by 718 · see citing works
Fetal growth and coronary heart disease in South India
Stein, C., Fall, C., Kumaran, K., Osmond, C., Barker, D. J. P., & Cox, V. (1996) · The Lancet · doi:10.1016/s0140-6736(96)04547-3 · Cited by 607 · see citing works
Oxygen and placental villous development: Origins of fetal hypoxia
Kingdom, J. C., & Kaufmann, P. (1997) · Placenta · doi:10.1016/s0143-4004(97)90000-x · Cited by 581 · see citing works
Birthweight and the Risk for Type 2 Diabetes Mellitus in Adult Women
Rich-Edwards, J. W., Colditz, G. A., Stampfer, M. J., Willett, W. C., Gillman, M. W., Hennekens, C. H., Speizer, F. E., & Manson, J. E. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-130-4_part_1-199902160-00005 · Cited by 544 · see citing works
The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens
Baschat, A. A., Gembruch, U., & Harman, C. R. (2001) · Ultrasound in Obstetrics & Gynecology · doi:10.1046/j.0960-7692.2001.00591.x · Cited by 435 · see citing works
Foetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sheep
Boddy, K., Dawes, G. S., Fisher, R., Pinter, S., & Robinson, J. S. (1974) · The Journal of Physiology · doi:10.1113/jphysiol.1974.sp010768 · Cited by 433 · see citing works
Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep.
Giussani, D. A., Spencer, J. A., Moore, P. J., Bennet, L., & Hanson, M. A. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019521 · Cited by 361 · see citing works
Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome
Fernandez‐Twinn, D. S., & Ozanne, S. E. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.039 · Cited by 301 · see citing works
Relationship between arterial and venous Doppler and perinatal outcome in fetal growth restriction
Baschat, A., Gembruch, U., Reiss, I. K. M., Gortner, L., Weiner, C. P., & Harman, C. R. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00284.x · Cited by 285 · see citing works
Doppler measurements of fetal and uteroplacental circulations: Relationship with umbilical venous blood gases measured at cordocentesis
Bilardo, C. M., Nicolaides, K. H., & Campbell, S. (1990) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(90)90833-s · Cited by 280 · see citing works
Effect of corticosteroids on brain growth in fetal sheep.
Huang, W.-L., Beazley, L., Quinlivan, J., Evans, S., Newnham, J., & Dunlop, S. (1999) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(99)00265-3 · Cited by 280 · see citing works
The fetal origins of adult disease
Robinson, R. (2001) · BMJ · doi:10.1136/bmj.322.7283.375 · Cited by 272 · see citing works
Fetal growth restriction: adaptations and consequences
McMillen, I. C., Adams, M. B., Ross, J. T., Coulter, C. L., Simonetta, G., Owens, J. A., Robinson, J. S., & Edwards, L. J. (2001) · Reproduction · doi:10.1530/rep.0.1220195 · Cited by 262 · see citing works
Pregnancy outcomes associated with intrauterine growth restriction
Gilbert, W. M., & Danielsen, B. H. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.384 · Cited by 223 · see citing works
Size at birth as a predictor of mortality in adulthood: a follow-up of 350 000 person-years
Kajantie, E., Osmond, C., Barker, D. J. P., Forsén, T., Phillips, D. I. W., & Eriksson, J. G. (2005) · International Journal of Epidemiology · doi:10.1093/ije/dyi048 · Cited by 215 · see citing works
Studies on experimental growth retardation in sheep. The effect of removal of a endometrial caruncles on fetal size and metabolism.
Robinson, J. S., Kingston, E. J., Ct, J., & Thorburn, G. D. (1979) · PubMed · Cited by 212 · see citing works
Attenuated Insulin Release and Storage in Fetal Sheep Pancreatic Islets with Intrauterine Growth Restriction
Limesand, S. W., Rozance, P. J., Zerbe, G. O., Hutton, J. C., & Hay, W. W. (2005) · Endocrinology · doi:10.1210/en.2005-0900 · Cited by 206 · see citing works
Antenatal corticosteroids revisited: repeat courses— National Institutes of Health Consensus Development Conference Statement, August 17–18, 2000
Panel, N. I. O. H. C. D. (2001) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01410-7 · Cited by 206 · see citing works
Fetal umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth
Lackman, F., Capewell, V., Gagnon, R. J., & Richardson, B. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.116686 · Cited by 192 · see citing works
Weights of Placentae From Small-for-Gestational Age Infants Revisited
Heinonen, S. T., Taipale, P., & Saarikoski, S. (2001) · Placenta · doi:10.1053/plac.2001.0630 · Cited by 185 · see citing works
Restriction of placental function alters heart development in the sheep fetus
Morrison, J. L., Botting, K. J., Dyer, J. L., Williams, S. J., Thornburg, K. L., & McMillen, I. C. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00798.2006 · Cited by 184 · see citing works
Self-citation
Plasma Cortisol and Adrenocorticotropin in Appropriate and Small for Gestational Age Fetuses
Economides, D. L., Nicolaides, K. H., Linton, E. A., Perry, L., & Chard, T. (1988) · Fetal Diagnosis and Therapy · doi:10.1159/000263348 · Cited by 179 · see citing works
Placental glucose transport in heat-induced fetal growth retardation
Thureen, P. J., Trembler, K. A., Meschia, G., Makowski, E. L., & Wilkening, R. B. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.3.r578 · Cited by 173 · see citing works
Nutrient partitioning and fetal growth in rapidly growing adolescent ewes
Wallace, J. M., Aitken, R. P., & Cheyne, M. A. (1996) · Reproduction · doi:10.1530/jrf.0.1070183 · Cited by 169 · see citing works
Some aspects of placental function in chronically heat-stressed ewes.
Aw, B., Rb, W., & Meschia, G. (1987) · PubMed · Cited by 169 · see citing works
Human Fetal Kidney Morphometry during Gestation and the Relationship between Weight, Kidney Morphometry and Plasma Active Renin Concentration at Birth
Konje, J. C., Bell, S. C., Morton, J. J., Chazal, R. D., & Taylor, D. J. (1996) · Clinical Science · doi:10.1042/cs0910169 · Cited by 155 · see citing works
Nutritionally Mediated Placental Growth Restriction in the Growing Adolescent: Consequences for the Fetus1
Wallace, J. M., Aitken, R. P., Milne, J. S., & Hay, W. W. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.104.030965 · Cited by 149 · see citing works
STUDIES ON THE PLACENTA OF THE SHEEP ( OVIS ARIES L.)
Alexander, G. M. (1964) · Reproduction · doi:10.1530/jrf.0.0070307 · Cited by 143 · see citing works
Chronic Hypoxia Stimulates Periarterial Sympathetic Nerve Development in Chicken Embryo
Ruijtenbeek, K., le Noble, F. A. C., Janssen, G. M. J., Kessels, C. G. A., Fazzi, G. E., Blanco, C. E., & Mey, J. G. R. D. (2000) · Circulation · doi:10.1161/01.cir.102.23.2892 · Cited by 140 · see citing works
Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep
Wallace, J. M., Bourke, D. A., Aitken, R. P., Leitch, N., & Hay, W. W. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00465.2001 · Cited by 137 · see citing works
Doppler and biophysical assessment in growth restricted fetuses: distribution of test results
Baschat, A., Galan, H. L., Bhide, A., Berg, C., Kush, M. L., Oepkes, D., Thilaganathan, B., Gembruch, U., & Harman, C. R. (2005) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.2657 · Cited by 137 · see citing works
The relationship between transplacental O2 diffusion and placental expression of PlGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction
Regnault, T. R. H., de Vrijer, B., Galan, H. L., Davidsen, M. L., Trembler, K. A., Battaglia, F. C., Wilkening, R. B., & Anthony, R. V. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.039511 · Cited by 136 · see citing works
Intrauterine Growth and its Relationship to Size and Shape at Birth
Hindmarsh, P. C., Geary, M. P., Rodeck, C. H., Kingdom, J. C., & Cole, T. J. (2002) · Pediatric Research · doi:10.1203/00006450-200208000-00020 · Cited by 132 · see citing works
Restriction of placental and fetal growth in sheep alters fetal blood pressure responses to angiotensin II and captopril
Edwards, L. J., Simonetta, G., Owens, J. A., Robinson, J. S., & McMillen, I. C. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.897ab.x · Cited by 131 · see citing works
Placental Restriction Alters the Functional Development of the Pituitary-Adrenal Axis in the Sheep Fetus during Late Gestation
Phillips, I. D., Simonetta, G., Owens, J. A., Robinson, J. S., Clarke, I. J., & McMillen, I. C. (1996) · Pediatric Research · doi:10.1203/00006450-199612000-00014 · Cited by 131 · see citing works
Development and Mechanisms of Fetal Hypoxia in Severe Fetal Growth Restriction
Regnault, T. R. H., de Vrijer, B., Galan, H. L., Wilkening, R. B., Battaglia, F. C., & Meschia, G. (2007) · Placenta · doi:10.1016/j.placenta.2006.06.007 · Cited by 131 · see citing works
Metabolic and endocrine findings in appropriate and small for gestational age fetuses
Economides, D. L., Nicolaides, K. H., & Campbell, S. C. (1991) · Journal of Perinatal Medicine · doi:10.1515/jpme.1991.19.1-2.97 · Cited by 129 · see citing works
Birth Weight, Infant Weight Gain, and Cause-specific Mortality
Syddall, H. E., Sayer, A. A., Simmonds, S. J., Osmond, C., Cox, V., Dennison, E. M., Barker, D. J. P., & Cooper, C. C. (2005) · American Journal of Epidemiology · doi:10.1093/aje/kwi137 · Cited by 128 · see citing works
Placental weight, birth measurements, and blood pressure at age 8 years.
Moore, V., Miller, A., BOULTON, T. J. C., COCKINGTON, R. A., Craig, I. H., Magarey, A., & Robinson, J. S. (1996) · Archives of Disease in Childhood · doi:10.1136/adc.74.6.538 · Cited by 127 · see citing works
Chronic fetal placental embolization and hypoxemia cause hypertension and myocardial hypertrophy in fetal sheep
Murotsuki, J., Challis, J. R. G., Han, V. K. M., Fraher, L. J., & Gagnon, R. J. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.272.1.r201 · Cited by 126 · see citing works
Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb
Blasio, M. J. D., Gatford, K. L., Robinson, J. S., & Owens, J. A. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00430.2006 · Cited by 122 · see citing works
Investigating the causes of low birth weight in contrasting ovine paradigms
Wallace, J. M., Regnault, T. R. H., Limesand, S. W., Hay, W. W., & Anthony, R. V. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.082032 · Cited by 121 · see citing works
Circulating insulin-like growth factors-I and -II and substrates in fetal sheep following restriction of placental growth
Owens, J. A., Kind, K. L., Carbone, F., Robinson, J. S., & Owens, P. C. (1994) · Journal of Endocrinology · doi:10.1677/joe.0.1400005 · Cited by 121 · see citing works
Fetal Growth Restriction Has Long-Term Effects on Postnatal Lung Structure in Sheep
Maritz, G. S., Cock, M. L., Louey, S., Suzuki, K., & Harding, R. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000106314.99930.65 · Cited by 121 · see citing works
Placental Expression of VEGF, PlGF and their Receptors in a Model of Placental Insufficiency—Intrauterine Growth Restriction (PI-IUGR)
Regnault, T. R. H., Orbus, R. J., de Vrijer, B., Davidsen, M. L., Galan, H. L., Wilkening, R. B., & Anthony, R. V. (2002) · Placenta · doi:10.1053/plac.2001.0757 · Cited by 119 · see citing works
The Effects of Maternal Betamethasone Administration on the Intrauterine Growth-Restricted Fetus
Miller, S., Chai, M., Loose, J. M., Castillo-Meléndez, M., Walker, D. W., Jenkin, G., & Wallace, E. M. (2006) · Endocrinology · doi:10.1210/en.2006-1058 · Cited by 106 · see citing works
The relationship between birth weight and blood pressure amplifies from childhood to adulthood
Moore, V., Cockington, R. A., Ryan, P., & Robinson, J. S. (1999) · Journal of Hypertension · doi:10.1097/00004872-199917070-00003 · Cited by 105 · see citing works
Circulatory responses to prolonged hypoxemia in fetal sheep
Bocking, A. D., Gagnon, R., White, S. E., Homan, J., Milne, K. M., & Richardson, B. S. (1988) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(88)90567-4 · Cited by 104 · see citing works
Evaluation of the centrifuged and Gram-stained smear, urinalysis, and reagent strip testing to detect asymptomatic bacteriuria in obstetric patients
McNair, R. D., MacDonald, S. R., Dooley, S. L., & Peterson, L. R. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.105440 · Cited by 104 · see citing works
Restriction of placental growth results in greater hypotensive response to α‐adrenergic blockade in fetal sheep during late gestation
Danielson, L., McMillen, I. C., Dyer, J. L., & Morrison, J. L. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.080523 · Cited by 103 · see citing works
Self-citation
Blood redistribution in the fetal brain during chronic hypoxia
Dubiel, M., Gunnarsson, G. Ö., & Gudmundsson, S. (2002) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2002.00758.x · Cited by 103 · see citing works
Fetal Brain Injury Following Prolonged Hypoxemia and Placental Insufficiency: A Review
Rees, S. M., Mallard, C. E., Breen, S. J., Stringer, M., Cock, M. L., & Harding, R. (1998) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(98)01001-0 · Cited by 100 · see citing works
Effects of betamethasone administration to the fetal sheep in late gestation on fetal cerebral blood flow
Schwab, M. G., Roedel, M., Anwar, M. A., Müller, T. M., Schubert, H., Buchwalder, L. F., Walter, B., & Nathanielsz, P. W. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00619.x · Cited by 97 · see citing works
Fetal endocrine responses to chronic placental embolization in the late-gestation ovine fetus
Gagnon, R. J., Challis, J. R. G., Johnston, L., & Fraher, L. J. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(94)70309-4 · Cited by 97 · see citing works
Placental Insufficiency and Fetal Growth Restriction Lead to Postnatal Hypotension and Altered Postnatal Growth in Sheep
Louey, S., Cock, M. L., Stevenson, K. M., & Harding, R. (2000) · Pediatric Research · doi:10.1203/00006450-200012000-00018 · Cited by 95 · see citing works
Demonstration of fetal coronary blood flow by Doppler ultrasound in relation to arterial and venous flow velocity waveforms and perinatal outcome – the ‘heart‐sparing effect’
Baschat, A., Gembruch, U., Reiss, I. K. M., Gortner, L., & Diedrich, K. (1997) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.1997.09030162.x · Cited by 94 · see citing works
The fetal cardiovascular response to antenatal steroids in severe early-onset intrauterine growth restriction
Simchen, M. J., Alkazaleh, F., Adamson, S. L., Windrim, R. C., Telford, J., Beyene, J., & Kingdom, J. C. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2003.08.011 · Cited by 93 · see citing works
Fetal hypertension and abnormal Doppler velocimetry in an ovine model of intrauterine growth restriction
Galan, H. L., Anthony, R. V., Rigano, S., Parker, T. A., de Vrijer, B., Ferrazzi, E. M., Wilkening, R. B., & Regnault, T. R. H. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.05.088 · Cited by 93 · see citing works
Impact of Placental Restriction on the Development of the Sympathoadrenal System
Simonetta, G., Rourke, A. K., Owens, J. A., Robinson, J. S., & McMillen, I. C. (1997) · Pediatric Research · doi:10.1203/00006450-199712000-00015 · Cited by 92 · see citing works
Placental glucose transport in growth-restricted pregnancies induced by overnourishing adolescent sheep
Wallace, J. M., Bourke, D. A., Aitken, R. P., Milne, J. S., & Hay, W. W. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.023333 · Cited by 86 · see citing works
Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto‐placental growth in the sheep
MacLaughlin, S. M., Walker, S. K., Roberts, C. T., Kleemann, D. O., & McMillen, I. C. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.084996 · Cited by 86 · see citing works
The association of ambient outdoor temperature throughout pregnancy and offspring birthweight: findings from the Aberdeen Children of the 1950s cohort
Lawlor, D. A., Leon, D. A., & Smith, G. D. (2005) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2004.00488.x · Cited by 82 · see citing works
Umbilical blood flow response to embolization of the uterine circulation
Clapp, J. F., Szeto, H. H., Larrow, R. W., Hewitt, J. R., & Mann, L. I. (1980) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(80)90011-3 · Cited by 79 · see citing works
Characterization of Glucose Transporter 8 (GLUT8) in the Ovine Placenta of Normal and Growth Restricted Fetuses
Limesand, S. W., Regnault, T. R. H., & Hay, W. W. (2003) · Placenta · doi:10.1016/j.placenta.2003.08.012 · Cited by 79 · see citing works
Fetal adrenal medulla catecholamine response to hypoxia-direct and neural components
Cheung, C. Y. (1990) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1990.258.6.r1340 · Cited by 79 · see citing works
Nephron Endowment and Filtration Surface Area in the Kidney after Growth Restriction of Fetal Sheep
Mitchell, E., Louey, S., Cock, M. L., Harding, R., & Black, M. J. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000120681.61201.b4 · Cited by 72 · see citing works
Carotid sinus nerve section and the increase in plasma cortisol during acute hypoxia in fetal sheep.
Giussani, D. A., McGARRIGLE, H. H. G., Moore, P. J., Bennet, L., Spencer, J. A., & Hanson, M. A. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020172 · Cited by 69 · see citing works
Fetal placental embolization in the late-gestation ovine fetus: Alterations in umbilical blood flow and fetal heart rate patterns
Gagnon, R., Johnston, L., & Murotsuki, J. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70252-1 · Cited by 69 · see citing works
Early growth, and coronary heart disease and type 2 diabetes: experiences from the Helsinki Birth Cohort Studies
Eriksson, J. G. (2006) · International Journal of Obesity · doi:10.1038/sj.ijo.0803515 · Cited by 69 · see citing works
Antenatal Corticosteroids Revisited
Panel, N. I. O. H. C. D. (2001) · Obstetrics and Gynecology · doi:10.1097/00006250-200107000-00027 · Cited by 67 · see citing works
Altered Placental and Fetal Expression of IGFs and IGF-Binding Proteins Associated With Intrauterine Growth Restriction in Fetal Sheep During Early and Mid-Pregnancy
de Vrijer, B., Davidsen, M. L., Wilkening, R. B., Anthony, R. V., & Regnault, T. R. H. (2006) · Pediatric Research · doi:10.1203/01.pdr.0000242364.78002.71 · Cited by 63 · see citing works
Fetal heart rate patterns in growth-restricted fetal sheep induced by chronic fetal placental embolization
Murotsuki, J., Bocking, A. D., & Gagnon, R. J. (1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70486-1 · Cited by 62 · see citing works
Effect of restriction of placental growth on expression of IGFs in fetal sheep: relationship to fetal growth, circulating IGFs and binding proteins
Kind, K. L., Owens, J. A., Robinson, J. S., Quinn, K. J., Grant, P. A., WALTON, P. E., Gilmour, R. S., & Owens, P. C. (1995) · Journal of Endocrinology · doi:10.1677/joe.0.1460023 · Cited by 62 · see citing works
Basic science: Chronic fetal hypoxia increases activin A concentrations in the late‐pregnant sheep
Supramaniam, V. G., Jenkin, G., Loose, J. M., Wallace, E. M., & Miller, S. (2005) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2005.00791.x · Cited by 58 · see citing works
Altered arterial concentrations of placental hormones during maximal placental growth in a model of placental insufficiency
Regnault, T. R. H., Orbus, R. J., Battaglia, F., Wilkening, R. B., & Anthony, R. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1620433 · Cited by 58 · see citing works
Models of fetal growth restriction
Schröder, H. J. (2003) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(03)00170-2 · Cited by 58 · see citing works
Effects of long-term hypoxemia on pituitary-adrenal function in fetal sheep
Murotsuki, J., Gagnon, R. J., Matthews, S. G., & Challis, J. R. G. (1996) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1996.271.4.e678 · Cited by 58 · see citing works
High gestational weight gain does not improve birth weight in a cohort of African American adolescents
Nielsen, J. N., O'Brien, K. O., Witter, F. R., Chang, S.-C., Mancini, J., Nathanson, M. S., & Caulfield, L. E. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.1.183 · Cited by 54 · see citing works
The ultrastructural development of the glomerular filtration barrier in the rat kidney: A morphometric analysis
Larsson, L., & Maunsbach, A. B. (1980) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(80)90074-x · Cited by 53 · see citing works
The effect of mild hypoxemia maintained for twenty-four hours on maternal and fetal glucose, lactate, cortisol, and arginine vasopressin in pregnant sheep at 122 to 139 days' gestation
Towell, M. E., Figueroa, J., Markowitz, S. D., Elias, B., & Nathanielsz, P. W. (1987) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(87)80261-2 · Cited by 52 · see citing works
EFFECTS OF SINGLE UMBILICAL ARTERY LIGATION IN THE LAMB FETUS
Emmanouilides, G. C., Townsend, D. E., & Bauer, R. A. (1968) · PEDIATRICS · doi:10.1542/peds.42.6.919 · Cited by 51 · see citing works
Glucose metabolism in pregnant sheep when placental growth is restricted
Owens, J. A., Falconer, J. S., & Robinson, J. S. (1989) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1989.257.2.r350 · Cited by 48 · see citing works
Evaluation of third trimester uterine artery flow velocity indices in relationship to perinatal complications
Ghosh, G., Bręborowicz, A., Brązert, M., Maczkiewicz, M., Kobelski, M., Dubiel, M., & Gudmundsson, S. (2006) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050600852510 · Cited by 44 · see citing works
Fetal sheep endocrine responses to sustained hypoxemic stress after chronic fetal placental embolization
Gagnon, R. J., Murotsuki, J., Challis, J. R. G., Fraher, L. J., & Richardson, B. S. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.272.5.e817 · Cited by 44 · see citing works
The fetal origins of adult disease: from sceptic to convert
Gillman, M. W., & Rich-Edwards, J. W. (2000) · Paediatric and Perinatal Epidemiology · doi:10.1046/j.1365-3016.2000.00265.x · Cited by 43 · see citing works
Effects Of Intra‐Uterine Growth Restriction On The Control Of Breathing And Lung Development After Birth
Harding, R., Tester, M., Moss, T. J. M., DAVEY, M. G., Louey, S., Joyce, B. J., Hooper, S. B., & Maritz, G. S. (2000) · Clinical and Experimental Pharmacology and Physiology · doi:10.1046/j.1440-1681.2000.03191.x · Cited by 40 · see citing works
Fetal growth and systolic blood pressure in young adulthood: the Swedish Young Male Twins Study
Kark, M., Rasmussen, F. E., Stavola, B. L. D., & Leon, D. A. (2002) · Paediatric and Perinatal Epidemiology · doi:10.1046/j.1365-3016.2002.00424.x · Cited by 37 · see citing works
Regional Blood Flow and the Endocrine Response to Sustained Hypoxemia in the Preterm Ovine Fetus
Richardson, B. S., Korkola, S. J., Asano, H., Challis, J. R. G., Polk, D. H., & Fraser, M. (1996) · Pediatric Research · doi:10.1203/00006450-199608000-00024 · Cited by 34 · see citing works
Fetal adrenal and middle cerebral artery Doppler velocimetry in high‐risk pregnancy
Dubiel, M., Breborowicz, G., Maršál, K., & Gudmundsson, S. (2000) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2000.00278.x · Cited by 34 · see citing works
Cotyledon and binucleate cell nitric oxide synthase expression in an ovine model of fetal growth restriction
Galan, H. L., Regnault, T. R. H., Cras, T. D. L., Tyson, R. W., Anthony, R. V., Wilkening, R. B., & Abman, S. H. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.6.2420 · Cited by 34 · see citing works
Polyuria and impaired renal blood flow after asphyxia in preterm fetal sheep
Quaedackers, J. S. L. T., Roelfsema, V., Hunter, C. J., Heineman, E., Gunn, A. J., & Bennet, L. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00592.2003 · Cited by 33 · see citing works
Evaluation of fetal circulation redistribution in pregnancies with absent or reversed diastolic flow in the umbilical artery
Dubiel, M., Bręborowicz, G. H., & Gudmundsson, S. (2003) · Early Human Development · doi:10.1016/s0378-3782(03)00006-9 · Cited by 32 · see citing works
Overnourishing pregnant adolescent ewes preserves perirenal fat deposition in their growth-restricted fetuses
Matsuzaki, M., Milne, J. S., Aitken, R. P., & Wallace, J. M. (2006) · Reproduction Fertility and Development · doi:10.1071/rd05067 · Cited by 31 · see citing works
Fetal brain sparing is strongly related to the degree of increased placental vascular impedance
Cheema, R., Dubiel, M., & Gudmundsson, S. (2006) · Journal of Perinatal Medicine · doi:10.1515/jpm.2006.061 · Cited by 30 · see citing works
Chemoreflex Contribution to Adrenocortical Function during Acute Hypoxemia in the Llama Fetus at 0.6 to 0.7 of Gestation
Riquelme, R. A., Llanos, J. A., McGARRIGLE, H. H. G., Sanhueza, E. M., Hanson, M. A., & Giussani, D. A. (1998) · Endocrinology · doi:10.1210/endo.139.5.6010 · Cited by 29 · see citing works
Effect of a high maternal dietary intake during mid-gestation on components of the utero-placental insulin-like growth factor (IGF) system in adolescent sheep with retarded placental development
Gadd, T., Aitken, R. J., Wallace, J. M., & Wathes, D. C. (2000) · Reproduction · doi:10.1530/jrf.0.1180407 · Cited by 26 · see citing works
Human Fetal Weight and Placental Weight Growth Curves
Bonds, D. R., Mwape, B., Kumar, S., & Gabbe, S. G. (2009) · Biology of the Neonate · doi:10.1159/000242016 · Cited by 25 · see citing works
Postnatal Development of Arterial Pressure: Influence of the Intrauterine Environment
Louey, S., Cock, M. L., & Harding, R. (2003) · Archives of Physiology and Biochemistry · doi:10.1076/apab.111.1.53.15137 · Cited by 25 · see citing works
Cerebral oxidative metabolism in fetal sheep with prolonged and graded hypoxemia.
Bs, R., Carmichael, L., Homan, J., & Patrick, J. E. (1993) · PubMed · Cited by 25 · see citing works
Cerebral circulatory responses of near-term ovine fetuses during sustained fetal placental embolization
Gagnon, R. J., Lamb, T., & Richardson, B. S. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.273.4.h2001 · Cited by 24 · see citing works
Umbilical Blood Flow and Glucose Uptake in Lamb Fetus Following Single Umbilical Artery Ligation
Oh, W., Omori, K., Hobel, C. J., Erenberg, A. P., & Emmanouilides, G. C. (2009) · Biology of the Neonate · doi:10.1159/000240741 · Cited by 23 · see citing works
Restriction of Fetal Growth has a Differential Impact on Fetal Prolactin and Prolactin Receptor mRNA Expression
Phillips, I., Anthony, R. V., Simonetta, G., Owens, J. A., Robinson, J. S., & McMillen, I. C. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2001.00608.x · Cited by 23 · see citing works
Birth outcomes in adolescent pregnancy in an area with intense malaria transmission in Tanzania
Wort, U. U., Warsame, M., & Brabin, B. J. (2006) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/00016340600756870 · Cited by 23 · see citing works
Effect of chronic hypoxemia on the regulation of nitric-oxide synthase in the fetal sheep brain
Aguan, K., Murotsuki, J., Gagnon, R. J., Thompson, L. P., & Weiner, C. P. (1998) · Developmental Brain Research · doi:10.1016/s0165-3806(98)00145-x · Cited by 21 · see citing works
The fetal sound environment during vibroacoustic stimulation in labor: effect on fetal heart rate response.
Gagnon, R. J., Benzaquen, S., & Hunse, C. (1992) · PubMed · Cited by 20 · see citing works
Regional changes in kynurenic acid, quinolinic acid, and glial fibrillary acidic protein concentrations in the fetal sheep brain after experimentally induced placental insufficiency
Nicholls, T., Lacey, B., Nitsos, I., Smythe, G. A., & Walker, D. W. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.108862 · Cited by 19 · see citing works
Coronary blood flow in fetuses with intrauterine growth restriction.
Baschat, A., Gembruch, U., & Harman, C. R. (1998) · PubMed · Cited by 19 · see citing works
Differential Effects of Placental Restriction on IGF‐II, ACTH Receptor and Steroidogenic Enzyme mRNA Levels in the Foetal Sheep Adrenal
Ross, Phillips, Simonetta, Owens, J. A., Робинсон, & McMillen (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00429.x · Cited by 17 · see citing works
Role of catecholamines in mediating fetal blood volume decrease during acute hypoxia
Brace, R. A., & Cheung, C. Y. (1987) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1987.253.4.h927 · Cited by 17 · see citing works
The ovine fetoplacental endocrine response to placental damage
Clapp, J. F., Auletta, F. J., Farnham, J., Larrow, R. W., & Mann, L. I. (1982) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(82)90393-3 · Cited by 16 · see citing works
Cortisol Differentially Regulates Pituitary‐Adrenal Function in the Sheep Fetus after Disconnection of the Hypothalamus and Pituitary
Ross, J. T., Phillips, I., Owens, J. A., & McMillen, I. C. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.00623.x · Cited by 16 · see citing works
Kynurenine production and catabolism in fetal sheep with embolized or nonembolized placentas
Nicholls, T., Nitsos, I., Smythe, G. A., & Walker, D. W. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.117969 · Cited by 16 · see citing works
Placental Restriction Increases the Expression of Prostaglandin Endoperoxide G/H Synthase-2 and EP2 mRNA in the Fetal Sheep Kidney during Late Gestation
Williams, S., McMillen, I. C., Zaragoza, D. B., & Olson, D. M. (2002) · Pediatric Research · doi:10.1203/00006450-200212000-00012 · Cited by 14 · see citing works
Effect of a high maternal dietary intake during mid-gestation on components of the utero-placental insulin-like growth factor (IGF) system in adolescent sheep with retarded placental development
Gadd, T., Aitken, R. P., Wallace, J. M., et al. (2000) · Reproduction · doi:10.1530/reprod/118.2.407 · Cited by 14 · see citing works
Morphologic Alterations in Ovine Placenta and Fetal Liver Following Induced Severe Placental Insufficiency
Cheung, C. Y., Bogić, L., Gagnon, R. J., Harding, R., & Brace, R. A. (2004) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2004.06.010 · Cited by 13 · see citing works
Effect of hyperthermia on the plasma concentrations of prolactin and cortisol in the fetal lamb and pregnant ewe during late gestation.
Dw, W., Davies, A., & McMillen, I. C. (1990) · PubMed · Cited by 12 · see citing works
Trends in incidence of delivery of low birth weight infants in Benin City, southern Nigeria
Onyiriuka, A. (2006) · Nigerian Postgraduate Medical Journal · doi:10.4103/1117-1936.180543 · Cited by 12 · see citing works
Effect of graded hypoxia on activin A, prostaglandin E2 and cortisol levels in the late-pregnant sheep
Supramaniam, V. G., Jenkin, G., Wallace, E. M., O’Connor, A. E., de Kretser, D. M., & Miller, S. (2004) · Reproduction Fertility and Development · doi:10.1071/rd03110 · Cited by 10 · see citing works
Haemodynamic changes in IUGR fetus with chronic hypoxia evaluated by fetal heart-rate monitoring and Doppler measurement of blood flow velocity
Mori, A., Iwashita, M., & Takeda, Y. (1993) · Medical & Biological Engineering & Computing · doi:10.1007/bf02446650 · Cited by 9 · see citing works
In Vivo Techniques for Studying Fetoplacental Nutrient Uptake, Metabolism, and Transport
Regnault, T. R. H., & Hay, W. W. (2006) · Humana Press eBooks · doi:10.1385/1-59259-989-3:205 · Cited by 7 · see citing works
Prolactin and the expression of suppressor of cytokine signaling-3 in the sheep adrenal gland before birth
Gentili, S., Schwartz, J., Waters, M. J., & McMillen, I. C. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00252.2006 · Cited by 5 · see citing works
Restriction of Fetal Growth has a Differential Impact on Fetal Prolactin and Prolactin Receptor mRNA Expression
Phillips, I., Anthony, R. V., Simonetta, G., et al. (2001) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2001.00608.x · Cited by 4 · see citing works

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Nutrition and brain development in early life
Prado, E. L., & Dewey, K. G. (2014) · Nutrition Reviews · doi:10.1111/nure.12102 · Cited by 1,036 · see citing works
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome
Miller, S. L., Huppi, P. S., & Mallard, C. (2016) · The Journal of Physiology · doi:10.1113/jp271402 · Cited by 620 · see citing works
FIGO (International Federation of Gynecology and Obstetrics) initiative on fetal growth: Best practice advice for screening, diagnosis, and management of fetal growth restriction
Melamed, N., Baschat, A., Yinon, Y., Athanasiadis, A. P., Mecacci, F., Figueras, F., Berghella, V., Nazareth, A., Tahlak, M., McIntyre, D. H., et al. (2021) · International Journal of Gynecology & Obstetrics · doi:10.1002/ijgo.13522 · Cited by 590 · see citing works
Neonatal Morbidities of Fetal Growth Restriction: Pathophysiology and Impact
Malhotra, A., Allison, B. J., Castillo-Melendez, M., Jenkin, G., Polglase, G. R., & Miller, S. L. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00055 · Cited by 453 · see citing works
The fetal brain sparing response to hypoxia: physiological mechanisms
Giussani, D. A. (2015) · The Journal of Physiology · doi:10.1113/jp271099 · Cited by 393 · see citing works
Invited review: Heat stress effects during late gestation on dry cows and their calves
Tao, S., & Dahl, G. E. (2013) · Journal of Dairy Science · doi:10.3168/jds.2012-6278 · Cited by 342 · see citing works
Impact of Oxidative Stress in Fetal Programming
Thompson, L. P., & Al-Hasan, Y. M. (2012) · Journal of Pregnancy · doi:10.1155/2012/582748 · Cited by 300 · see citing works
Developmental Programming of Cardiovascular Dysfunction by Prenatal Hypoxia and Oxidative Stress
Giussani, D. A., Camm, E. J., Niu, Y., Richter, H. G., Blanco, C. E., Gottschalk, R., Blake, E. Z., Horder, K. A., Thakor, A. S., Hansell, J. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031017 · Cited by 278 · see citing works
Placental Adaptations in Growth Restriction
Zhang, S., Regnault, T. R. H., Barker, P., Botting, K. J., McMillen, I. C., McMillan, C., Roberts, C. T., & Morrison, J. L. (2015) · Nutrients · doi:10.3390/nu7010360 · Cited by 261 · see citing works
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Fetal growth restriction, catch-up growth and the early origins of insulin resistance and visceral obesity
Morrison, J. L., Duffield, J. A., Mühlhäusler, B. S., Gentili, S., & McMillen, I. C. (2009) · Pediatric Nephrology · doi:10.1007/s00467-009-1407-3 · Cited by 190 · see citing works
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Developmental programming of cardiovascular disease by prenatal hypoxia
Giussani, D. A., & Davidge, S. T. (2013) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s204017441300010x · Cited by 182 · see citing works
Role of the hypothalamic–pituitary–adrenal axis in developmental programming of health and disease
Xiong, F., & Zhang, L. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.11.002 · Cited by 177 · see citing works
Improving pregnancy outcomes in humans through studies in sheep
Morrison, J. L., Berry, M. J., Botting, K. J., Darby, J. R. T., Frasch, M. G., Gatford, K. L., Giussani, D. A., Gray, C. L., Harding, R., Herrera, E. A., et al. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00391.2017 · Cited by 171 · see citing works
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Let's talk about placental sex, baby: understanding mechanisms that drive female- and male-specific fetal growth and developmental outcomes
Meakin, A. S., Cuffe, J. S. M., Darby, J. R. T., Morrison, J. L., & Clifton, V. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126386 · Cited by 158 · see citing works
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Baboons as a Model to Study Genetics and Epigenetics of Human Disease
Cox, L. A., Comuzzie, A. G., Havill, L. M., Karere, G. M., Spradling, K. D., Mahaney, M. C., Nathanielsz, P. W., Nicolella, D. P., Shade, R. E., Voruganti, S., et al. (2013) · ILAR Journal · doi:10.1093/ilar/ilt038 · Cited by 161 · see citing works
Guinea pig models for translation of the developmental origins of health and disease hypothesis into the clinic
Morrison, J. L., Botting, K. J., Darby, J. R. T., David, A. L., Dyson, R. M., Gatford, K. L., Gray, C. L., Herrera, E. A., Hirst, J. J., Kim, B., et al. (2018) · The Journal of Physiology · doi:10.1113/jp274948 · Cited by 148 · see citing works
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Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations
Cheong, J. N., Wlodek, M. E., Moritz, K. M., & Cuffe, J. S. M. (2016) · The Journal of Physiology · doi:10.1113/jp271745 · Cited by 148 · see citing works
Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction
Lemley, C. O., Meyer, A. M., Camacho, L. E., Neville, T. L. L., Newman, D. J., Caton, J. S. S., & Vonnahme, K. A. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00407.2011 · Cited by 144 · see citing works
Brain Development, Intelligence and Cognitive Outcome in Children Born Small for Gestational Age
de Bie, H. M. A., Oostrom, K. J., & de Waal, H. A. D. (2010) · Hormone Research in Paediatrics · doi:10.1159/000271911 · Cited by 132 · see citing works
Long-Term Follow-Up of Intrauterine Growth Restriction: Cardiovascular Disorders
Demicheva, E., & Crispi, F. (2013) · Fetal Diagnosis and Therapy · doi:10.1159/000353633 · Cited by 126 · see citing works
Impact of chronic hypoxemia on blood flow to the brain, heart, and adrenal gland in the late-gestation IUGR sheep fetus
Poudel, R., McMillen, I. C., Holman, S. L., Zhang, S., & Morrison, J. L. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00036.2014 · Cited by 117 · see citing works
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Intrauterine growth restriction delays surfactant protein maturation in the sheep fetus
Orgeig, S., Crittenden, T. A., Marchant, C., McMillen, I. C., & Morrison, J. L. (2010) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00226.2009 · Cited by 113 · see citing works
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OXIDATIVE STRESS AND REPRODUCTIVE FUNCTION: Reactive oxygen species in the mammalian pre-implantation embryo
Deluao, J. C., Winstanley, Y. E., Robker, R. L., Pacella‐Ince, L., Gonzalez, M. B., & McPherson, N. O. (2022) · Reproduction · doi:10.1530/rep-22-0121 · Cited by 112 · see citing works
Chronic Hypoxemia in Late Gestation Decreases Cardiomyocyte Number but Does Not Change Expression of Hypoxia‐Responsive Genes
Botting, K. J., McMillen, I. C., Forbes, H., Nyengaard, J. R., & Morrison, J. L. (2014) · Journal of the American Heart Association · doi:10.1161/jaha.113.000531 · Cited by 111 · see citing works
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The maternal cortisol awakening response in human pregnancy is associated with the length of gestation
Buß, C., Entringer, S., Reyes, J. F., Chicz-DeMet, A., Sandman, C. A., Waffarn, F., & Wadhwa, P. D. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.06.063 · Cited by 106 · see citing works
Ecological Momentary Assessment of Maternal Cortisol Profiles Over a Multiple-Day Period Predicts the Length of Human Gestation
Entringer, S., Buß, C., Andersen, J. P., Chicz-DeMet, A., & Wadhwa, P. D. (2011) · Psychosomatic Medicine · doi:10.1097/psy.0b013e31821fbf9a · Cited by 104 · see citing works
Early origins of heart disease: Low birth weight and determinants of cardiomyocyte endowment
Botting, K. J., Wang, K., Padhee, M., McMillen, I. C., Summers-Pearce, B., Rattanatray, L., Cutri, N., Posterino, G. S., Brooks, D. A., & Morrison, J. L. (2011) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2011.05649.x · Cited by 92 · see citing works
Self-citation
A Pig Model of the Preterm Neonate: Anthropometric and Physiological Characteristics
Eiby, Y. A., Wright, L. L., Kalanjati, V. P., Miller, S. M., Bjorkman, S. T., Keates, H., Lumbers, E. R., Colditz, P. B., & Lingwood, B. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068763 · Cited by 89 · see citing works
The peripheral chemoreflex: indefatigable guardian of fetal physiological adaptation to labour
Lear, C. A., Wassink, G., Westgate, J. A., Nijhuis, J. G., Ugwumadu, A. H. N., Galinsky, R., Bennet, L., & Gunn, A. J. (2018) · The Journal of Physiology · doi:10.1113/jp274937 · Cited by 89 · see citing works
Antenatal Steroids and the IUGR Fetus: Are Exposure and Physiological Effects on the Lung and Cardiovascular System the Same as in Normally Grown Fetuses?
Morrison, J. L., Botting, K. J., Soo, P. S., McGillick, E. V., Hiscock, J. J., Zhang, S., McMillen, I. C., & Orgeig, S. (2012) · Journal of Pregnancy · doi:10.1155/2012/839656 · Cited by 83 · see citing works
Self-citation
Hormonal and nutritional drivers of intrauterine growth
Sferruzzi-Perri, A. N., Vaughan, O. R., Forhead, A. J., & Fowden, A. L. (2013) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835e3643 · Cited by 82 · see citing works
Near to One's Heart: The Intimate Relationship Between the Placenta and Fetal Heart
Camm, E. J., Botting, K. J., & Sferruzzi-Perri, A. N. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00629 · Cited by 82 · see citing works
Effect of antipsychotic treatment on Insulin-like Growth Factor-1 and cortisol in schizophrenia: A longitudinal study
Venkatasubramanian, G., Chittiprol, S., Neelakantachar, N., Shetty, T., & Gangadhar, B. N. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.01.033 · Cited by 82 · see citing works
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George, L. A., Uthlaut, A. B., Long, N., Zhang, L., Ma, Y., Smith, D. T., Nathanielsz, P. W., & Ford, S. P. (2010) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-8-75 · Cited by 77 · see citing works
Preterm growth restriction and bronchopulmonary dysplasia: the vascular hypothesis and related physiology
Sehgal, A., Gwini, S. M., Menahem, S., Allison, B. J., Miller, S., & Polglase, G. R. (2018) · The Journal of Physiology · doi:10.1113/jp276040 · Cited by 76 · see citing works
Pharmacological models and approaches for pathophysiological conditions associated with hypoxia and oxidative stress
Farías, J. G., Herrera, E. A., Carrasco‐Pozo, C., Sotomayor‐Zárate, R., Cruz, G., Morales, P., & Castillo, R. L. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.11.006 · Cited by 77 · see citing works
Are Twins Growth Restricted?
Mühlhäusler, B. S., Hancock, S. N., Bloomfield, F. H., & Harding, R. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e31821f6cfd · Cited by 73 · see citing works
Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen
Siqueira, L. G. B., Dikmen, S., Ortega, M. S., & Hansen, P. J. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-12539 · Cited by 70 · see citing works
A Narrative Review of Placental Contribution to Adverse Pregnancy Outcomes in Women With Polycystic Ovary Syndrome
Kelley, A. S., Smith, Y. R., & Padmanabhan, V. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00383 · Cited by 73 · see citing works
Clinical and molecular characterization of a re‐established line of sheep exhibiting hemophilia A
Porada, C. D., Sanada, C. D., Long, C. R., WOOD, J. A., DESAI, J., Frederick, N. M., Millsap, L., Bormann, C. L., Menges, S., Hanna, C. B., et al. (2009) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2009.03697.x · Cited by 66 · see citing works
Effects of intrauterine growth retardation and Bacillus subtilis PB6 supplementation on growth performance, intestinal development and immune function of piglets during the suckling period
Hu, L., Xie, P. P., Chen, H., Yan, C., Liu, Y., Xu, Q., Fang, Z., Lin, Y., Xu, S., Feng, B., et al. (2016) · European Journal of Nutrition · doi:10.1007/s00394-016-1223-z · Cited by 65 · see citing works
Chronic Protein Restriction in Mice Impacts Placental Function and Maternal Body Weight before Fetal Growth
González, P., Gasperowicz, M., Barbeito‐Andrés, J., Klenin, N., Cross, J. C., & Hallgrímsson, B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152227 · Cited by 62 · see citing works
Evolution, Development, and Function of the Pulmonary Surfactant System in Normal and Perturbed Environments
Orgeig, S., Morrison, J. L., & Daniels, C. B. (2015) · Comprehensive physiology · doi:10.1002/cphy.c150003 · Cited by 67 · see citing works
Self-citation
REPRODUCTION SYMPOSIUM: Developmental programming of reproductive and metabolic health1,2
Padmanabhan, V., & Veiga‐Lopez, A. (2014) · Journal of Animal Science · doi:10.2527/jas.2014-7637 · Cited by 63 · see citing works
Cardiorespiratory consequences of intrauterine growth restriction: Influence of timing, severity and duration of hypoxaemia
Darby, J. R. T., Varcoe, T. J., Orgeig, S., & Morrison, J. L. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.01.080 · Cited by 60 · see citing works
Self-citation
Early determinants of cardiovascular disease
Santos, M. S., & Joles, J. A. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.03.003 · Cited by 57 · see citing works
A review of inter- and intraspecific variation in the eutherian placenta
Gundling, W. E., & Wildman, D. E. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0072 · Cited by 58 · see citing works
Prenatal Hypoxia and Placental Oxidative Stress: Insights from Animal Models to Clinical Evidences
Silvestro, S., Calcaterra, V., Pelizzo, G., Bramanti, P., & Mazzon, E. (2020) · Antioxidants · doi:10.3390/antiox9050414 · Cited by 56 · see citing works
Developmental programing: impact of testosterone on placental differentiation
Beckett, E. M., Astapova, O., Steckler, T. L., Veiga‐Lopez, A., & Padmanabhan, V. (2014) · Reproduction · doi:10.1530/rep-14-0055 · Cited by 55 · see citing works
Models of Intrauterine growth restriction and fetal programming in rabbits
López‐Tello, J., Arias‐Álvarez, M., Gonzalez‐Bulnes, A., & Sferruzzi-Perri, A. N. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23271 · Cited by 54 · see citing works
Early developmental influences on hepatic organogenesis
Hyatt, M. A., Budge, H., & Symonds, M. E. (2008) · Organogenesis · doi:10.4161/org.4.3.6849 · Cited by 50 · see citing works
Navigating redox imbalance: the role of oxidative stress in embryonic development and long-term health outcomes
Divvela, S. S. K., Gallorini, M., Gellisch, M., Patel, G. D., Saso, L., & Brand‐Saberi, B. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1521336 · Cited by 50 · see citing works
Fetal growth, birth size and energetic cost of gestation in southern right whales
Christiansen, F., Uhart, M. M., Bejder, L., Clapham, P., Ivashchenko, Y., Tormosov, D., Lewin, N., & Sironi, M. (2022) · The Journal of Physiology · doi:10.1113/jp282351 · Cited by 48 · see citing works
The vulnerable developing brain
Giussani, D. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019726108 · Cited by 48 · see citing works
Fetoplacental biometry and umbilical artery Doppler velocimetry in the overnourished adolescent model of fetal growth restriction
Carr, D. J., Aitken, R. P., Milne, J. S., David, A. L., & Wallace, J. M. (2012) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2012.05.008 · Cited by 47 · see citing works
BOLD MRI in sheep fetuses: a non‐invasive method for measuring changes in tissue oxygenation
Sørensen, A., Pedersen, M., Tietze, A., Ottosen, L. D. M., Duus, L., & Uldbjerg, N. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7322 · Cited by 47 · see citing works
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Keswani, S. G., Balaji, S., Katz, A. B., King, A., Omar, K., Habli, M. A., Klanke, C. A., & Crombleholme, T. M. (2015) · Human Gene Therapy · doi:10.1089/hum.2014.065 · Cited by 46 · see citing works
Suppression of trophoblast uterine spiral artery remodeling by estrogen during baboon pregnancy: impact on uterine and fetal blood flow dynamics
Aberdeen, G. W., Bonagura, T. W., Harman, C. R., Pepe, G. J., & Albrecht, E. D. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00590.2011 · Cited by 46 · see citing works
Increased lung prolyl hydroxylase and decreased glucocorticoid receptor are related to decreased surfactant protein in the growth-restricted sheep fetus
Orgeig, S., McGillick, E. V., Botting, K. J., Zhang, S., McMillen, I. C., & Morrison, J. L. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00275.2014 · Cited by 44 · see citing works
Self-citation
ASAS-SSR Triennnial Reproduction Symposium: Looking Back and Moving Forward—How Reproductive Physiology has Evolved: Fetal origins of impaired muscle growth and metabolic dysfunction: Lessons from the heat-stressed pregnant ewe1
Yates, D. T., Petersen, J. L., Schmidt, T. B., Cadaret, C. N., Barnes, T. L., Posont, R. J., & Beede, K. A. (2018) · Journal of Animal Science · doi:10.1093/jas/sky164 · Cited by 43 · see citing works
Fetal Growth Restriction and Hypertension in the Offspring: Mechanistic Links and Therapeutic Directions
Sehgal, A., Alexander, B. T., Morrison, J. L., & South, A. M. (2020) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2020.05.028 · Cited by 47 · see citing works
Self-citation
Third Trimester Fetal Heart Rate and Doppler Middle Cerebral Artery Blood Flow Velocity Characteristics During Prenatal Selective Serotonin Reuptake Inhibitor Exposure
Rurak, D. W., Lim, K. I., Sanders, A. P., Brain, U. M., Riggs, W. K., & Oberlander, T. F. (2011) · Pediatric Research · doi:10.1203/pdr.0b013e31821ba11a · Cited by 45 · see citing works
Prenatal origins of postnatal variation in growth, development and productivity of ruminants
Bell, A. W., & Greenwood, P. L. (2016) · Animal Production Science · doi:10.1071/an15408 · Cited by 45 · see citing works
Feasibility of phase-contrast cine magnetic resonance imaging for measuring blood flow in the sheep fetus
Duan, A. Q., Darby, J. R. T., Soo, J. Y., Lock, M. C., Zhu, M. Y., Flynn, L. V., Perumal, S. R., Macgowan, C. K., Selvanayagam, J. B., Morrison, J. L., et al. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00273.2017 · Cited by 44 · see citing works
Self-citation
Complex patterns of cell growth in the placenta in normal pregnancy and as adaptations to maternal diet restriction
Eaton, M., Davies, A., Devine, J., Zhao, X., Simmons, D. G., Maríusdóttir, E., Natale, D. R. C., Matyas, J. R., Bering, E. A., Workentine, M. L., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0226735 · Cited by 44 · see citing works
Maternal undernutrition in late gestation increases IGF2 signalling molecules and collagen deposition in the right ventricle of the fetal sheep heart
Darby, J. R. T., McMillen, I. C., & Morrison, J. L. (2018) · The Journal of Physiology · doi:10.1113/jp275806 · Cited by 43 · see citing works
Self-citation
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Sales, F., Peralta, Ó. A., Narbona, E., McCoard, S. A., Reyes, M. D. L., Gonzalez‐Bulnes, A., & Parraguez, V. H. (2018) · Animals · doi:10.3390/ani8110217 · Cited by 43 · see citing works
Chronic anemic hypoxemia attenuates glucose-stimulated insulin secretion in fetal sheep
Benjamin, J. S., Culpepper, C., Brown, L. D., Wesolowski, S. R., Jonker, S. S., Davis, M. A., Limesand, S. W., Wilkening, R. B., Hay, W. W., & Rozance, P. J. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00484.2016 · Cited by 42 · see citing works
Cardiac and vascular disease prior to hatching in chick embryos incubated at high altitude
Salinas, C. E., Blanco, C. E., Villena, M., Camm, E. J., Tuckett, J. D., Weerakkody, R. A., Kane, A. D., Shelley, A. M., Wooding, F. B. P., Quy, M. T., et al. (2009) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174409990043 · Cited by 42 · see citing works
Early restriction of placental growth results in placental structural and gene expression changes in late gestation independent of fetal hypoxemia
Zhang, S., Barker, P., Botting, K. J., Roberts, C. T., McMillan, C. M., McMillen, I. C., & Morrison, J. L. (2016) · Physiological Reports · doi:10.14814/phy2.13049 · Cited by 42 · see citing works
Self-citation
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Lear, C. A., Westgate, J. A., Ugwumadu, A. H. N., Nijhuis, J. G., STONE, P. R., Georgieva, A., Ikeda, T., Wassink, G., Bennet, L., & Gunn, A. J. (2018) · Seminars in Pediatric Neurology · doi:10.1016/j.spen.2018.05.002 · Cited by 41 · see citing works
Prenatal hypoxia impairs cardiac mitochondrial and ventricular function in guinea pig offspring in a sex-related manner
Thompson, L. P., Chen, L., Polster, B. M., Pinkas, G. A., & Song, H. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00224.2018 · Cited by 41 · see citing works
Systematic review: Impact of resveratrol exposure during pregnancy on maternal and fetal outcomes in animal models of human pregnancy complications—Are we ready for the clinic?
Darby, J. R. T., Dollah, M. H. B. M., Regnault, T. R. H., Williams, M., & Morrison, J. L. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.04.020 · Cited by 41 · see citing works
Self-citation
2011 AND 2012 EARLY CAREERS ACHIEVEMENT AWARDS: Placental programming: How the maternal environment can impact placental function1,2
Vonnahme, K. A., Lemley, C. O., Shukla, P., & O'Rourke, S. T. (2013) · Journal of Animal Science · doi:10.2527/jas.2012-5929 · Cited by 40 · see citing works
Myoblast replication is reduced in the IUGR fetus despite maintained proliferative capacity in vitro
Soto, S. M., Blake, A. C., Wesolowski, S. R., Rozance, P. J., Bjorkman, K. K., Gao, B., Hetrick, B., McCurdy, C. E., Garza, N. G., Hay, W. W., et al. (2017) · Journal of Endocrinology · doi:10.1530/joe-16-0123 · Cited by 40 · see citing works
Chronic hypoxia alters maternal uterine and fetal hemodynamics in the full-term pregnant guinea pig
Turan, Ş., Aberdeen, G. W., & Thompson, L. P. (2017) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00056.2017 · Cited by 39 · see citing works
Implications of maternal conditions and pregnancy course on offspring’s medical problems in adult life
von Ehr, J., & von Versen‐Höynck, F. (2016) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-016-4178-7 · Cited by 39 · see citing works
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Dahl, G. E., Skibiel, A. L., & Laporta, J. (2019) · Veterinary Clinics of North America Food Animal Practice · doi:10.1016/j.cvfa.2019.02.005 · Cited by 39 · see citing works
Lower oxygen consumption and Complex I activity in mitochondria isolated from skeletal muscle of fetal sheep with intrauterine growth restriction
Pendleton, A. L., Antolic, A. T., Kelly, A. C., Davis, M. A., Camacho, L. E., Doubleday, K., Anderson, M. J., Langlais, P. R., Lynch, R. M., & Limesand, S. W. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00057.2020 · Cited by 39 · see citing works
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Rock, C. R., White, T. A., Piscopo, B. R., Sutherland, A. E., Miller, S., Camm, E. J., & Allison, B. J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147555 · Cited by 39 · see citing works
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Carr, D. J., Aitken, R. P., Milne, J. S., David, A. L., & Wallace, J. M. (2011) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2011.06.016 · Cited by 35 · see citing works
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McGillick, E. V., Orgeig, S., & Morrison, J. L. (2015) · The Journal of Physiology · doi:10.1113/jp271113 · Cited by 34 · see citing works
Self-citation
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Knight, L. C., & Dilger, R. N. (2018) · Nutrients · doi:10.3390/nu10050632 · Cited by 35 · see citing works
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Meyer, K. M., Koch, J. M., Ramadoss, J., Kling, P. J., & Magness, R. R. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.085381 · Cited by 34 · see citing works
Sex-dependent effects of developmental hypoxia on cardiac mitochondria from adult murine offspring
Hellgren, K. T., Premanandhan, H., Quinn, C. J., Trafford, A. W., & Galli, G. L. J. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.11.004 · Cited by 34 · see citing works
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Mordhorst, B. R., & Prather, R. S. (2017) · doi:10.1002/9781118881286.ch9 · Cited by 33 · see citing works
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McGillick, E. V., Orgeig, S., & Morrison, J. L. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00469.2015 · Cited by 32 · see citing works
Self-citation
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Byrne, M., Aughwane, R., James, J. L., Hutchinson, J. C., Arthurs, O. J., Sebire, N. J., Sebastien Ourselin, A., David, A. L., Melbourne, A., & Clark, A. R. (2021) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2021.110630 · Cited by 32 · see citing works
An MRI approach to assess placental function in healthy humans and sheep
Saini, B. S., Darby, J. R. T., Marini, D., Portnoy, S., Lock, M. C., Soo, J. Y., Holman, S. L., Perumal, S. R., Wald, R. M., Windrim, R. C., et al. (2021) · The Journal of Physiology · doi:10.1113/jp281002 · Cited by 32 · see citing works
Self-citation
Maternal chronic hypoxia increases expression of genes regulating lung liquid movement and surfactant maturation in male fetuses in late gestation
McGillick, E. V., Orgeig, S., Allison, B. J., Brain, K. L., Niu, Y., Itani, N., Skeffington, K. L., Kane, A. D., Herrera, E. A., Giussani, D. A., et al. (2017) · The Journal of Physiology · doi:10.1113/jp273842 · Cited by 31 · see citing works
Self-citation
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Awonuga, A. O., Camp, O. G., Abu‐Soud, H. M., Rappolee, D. A., Puscheck, E. E., & Diamond, M. P. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01224-w · Cited by 29 · see citing works
Intrauterine growth restriction elevates circulating acylcarnitines and suppresses fatty acid metabolism genes in the fetal sheep heart
Drake, R., Louey, S., & Thornburg, K. L. R. (2021) · The Journal of Physiology · doi:10.1113/jp281415 · Cited by 29 · see citing works
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McGillick, E. V., Orgeig, S., Williams, M., & Morrison, J. L. (2016) · Reproductive Sciences · doi:10.1177/1933719116660842 · Cited by 28 · see citing works
Self-citation
Prenatal development of the pulmonary surfactant system and the influence of hypoxia
Orgeig, S., Morrison, J. L., & Daniels, C. B. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.05.015 · Cited by 25 · see citing works
Self-citation
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Wang, K. C. W., Botting, K. J., Padhee, M., Zhang, S., McMillen, I. C., Suter, C. M., Brooks, D. A., & Morrison, J. L. (2012) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2012.05743.x · Cited by 26 · see citing works
Self-citation
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Harvey, T. J., Murphy, R. M., Morrison, J. L., & Posterino, G. S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138388 · Cited by 26 · see citing works
Self-citation
Postnatal β2 adrenergic treatment improves insulin sensitivity in lambs with IUGR but not persistent defects in pancreatic islets or skeletal muscle
Yates, D. T., Camacho, L. E., Kelly, A. C., Steyn, L. V., Davis, M. A., Antolic, A. T., Anderson, M. J., Goyal, R., Allen, R. E., Papas, K. K., et al. (2019) · The Journal of Physiology · doi:10.1113/jp278726 · Cited by 26 · see citing works
Lower citrate synthase activity, mitochondrial complex expression, and fewer oxidative myofibers characterize skeletal muscle from growth-restricted fetal sheep
Stremming, J., Chang, E. I., Knaub, L. A., Armstrong, M., Baker, P. R., Wesolowski, S. R., Reisdorph, N. A., Reusch, J. E. B., & Brown, L. D. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00222.2021 · Cited by 29 · see citing works

Ruminant models of prenatal growth restriction
Anthony, R., Scheaffer, A., Wright, C., & Regnault, T. R. H. (2019) · Bioscientifica Proceedings · doi:10.1530/biosciprocs.5.014 · Cited by 98 · see citing works
Investigating the causes of low birth weight in contrasting ovine paradigms
Wallace, J. M., Regnault, T. R. H., Limesand, S. W., Hay, W. W., & Anthony, R. V. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.082032 · Cited by 121 · see citing works
An Animal Model of Placental Insufficiency-Induced Intrauterine Growth Restriction
Barry, J. S., Rozance, P. J., & Anthony, R. V. (2008) · Seminars in Perinatology · doi:10.1053/j.semperi.2007.11.004 · Cited by 90 · see citing works
Fetal growth restriction: adaptations and consequences
McMillen, I. C., Adams, M. B., Ross, J. T., Coulter, C. L., Simonetta, G., Owens, J. A., Robinson, J. S., & Edwards, L. J. (2001) · Reproduction · doi:10.1530/rep.0.1220195 · Cited by 262 · see citing works
Intrauterine fetal growth restriction, adaptation and programming–a review
Kasimanickam, R. K., Kasimancikam, V. R., & Kastelic, J. P. (2012) · Clinical Theriogenology · doi:10.58292/ct.v4.11256

Authors: Morrison, J. L.
Affiliations: University of South Australia (AU)
Corresponding author: Morrison, Janna L
ORCID: Morrison, Janna L
Venue: Clinical and Experimental Pharmacology and Physiology
Publisher: Wiley
Published: 2008-05-21
Volume: 35
Issue: 7
Pages: 730-743
ISSN: 0305-1870 (ISSN-L)
1440-1681
DOI: 10.1111/j.1440-1681.2008.04975.x
OpenAlex: W2054055548
Cited by: 289
References: 132
Citations by year: 2026: 8 · 2025: 19 · 2024: 15 · 2023: 21 · 2022: 14 · 2021: 24 · 2020: 24 · 2019: 11 · 2018: 24 · 2017: 16 · 2016: 22 · 2015: 20 · 2014: 8 · 2013: 16 · 2012: 16
FWCI: 1.54
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Clinical and Experimental Pharmacology and Physiology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Keywords: fetal growth restriction, sheep model, placental insufficiency, fetal hypoxia, cortisol, norepinephrine, sympathetic nervous system, maternal hyperthermia, maternal overnutrition, fetal cardiovascular response, perinatal outcomes
MeSH terms: Adaptation, Physiological, Animals, Disease Models, Animal, Female, Fetal Growth Retardation, Humans, Placental Insufficiency, Pregnancy, Sheep, Overnutrition

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SHEEP MODELS OF INTRAUTERINE GROWTH RESTRICTION: FETAL ADAPTATIONS AND CONSEQUENCES

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