Skip to main content

Fetal Growth and Its Restriction

  • Chapter
  • First Online:
  • 1138 Accesses

Part of the book series: Perspectives in Physiology ((PHYSIOL))

Abstract

In his essay “On being the right size,” the British geneticist, biometrician, and popularizer of science John Burdon Sanderson (JBS) Haldane (1892–1964) theorized on and presented some mathematical analysis for the optimal size of various organisms. In addition to consideration of body mass, he included surface area, weight-bearing bone structure, respiratory and circulating mechanisms, and other features of comparative anatomy and physiology (Haldane 1927). His analysis extended from insects to birds to a number of mammals which varied in size from mice to the rhinoceros. Haldane concluded “… that for every type of animal there is an optimal size” (Haldane 1927). A number of studies have disclosed that even for the fetus development follows clearly defined mathematical principles (Roberts 1906; see below). Prior to full maturity, timely growth, both physical and mental, is one of the best indicators of a fully functional physiological system and health. As is appreciated, optimal growth of the embryo-fetus and its various organs is a complex process that is a function of genetic makeup, state of maternal health, the availability of nutrients and oxygen, as well as a multitude of growth factors and hormones of maternal, placental, and fetal origin. In addition, a host of environmental factors that influence epigenetic programming play vital roles in this process. These factors are associated with physiologic, biochemical, and molecular changes, most of which are only poorly understood (Cheek 1975; Timiras 1972; Winick 1972). From mid-century onward, considerable emphasis has been placed on the mechanisms of cell division and multiplication (hyperplasia) and cell enlargement with cytoplasmic growth (hypertrophy) that result in the deposition of new tissue and change in anatomical form (Cheek 1975; Cockburn 1988; Fowden 1989; Winick 1972; Winick and Noble 1965).

We are too late for the gods and too early for the being. Being’s a poem, just begun, is man.

Martin Heidegger 1971

This is a preview of subscription content, log in via an institution.

Notes

  1. 1.

    An intricate knot tied by King Gordius of Phrygia and cut by Alexander the Great (356 BCE-323 BCE) with his sword after hearing an oracle promise that whoever could undo it would be the next ruler of Asia.

References

  • Aarnoudse-Moens, C.S., N. Weisglas-Kuperus, J.B. van Goudoever & J. Oosterlaan. Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics 124:717-728, 2009.

    Article  PubMed  Google Scholar 

  • Abramowicz, M., Kass, E.H. Pathogenesis and prognosis of prematurity. N Engl J Med 275:878-885; 938-943; 1001-1007; 1053-l059, 1966.

    Google Scholar 

  • Acharya, G., R.K. Creasy, R. Resnik, J.D. Iams, C.J. Lockwood, T.R. Moore, M. Greene, editors. Creasy & Resnik's Maternal-Fetal Medicine: Principles and Practice, 7th edn. Elsevier Saunders, Philadelphia, ISBN: 978-1-4557-1137-6, 2015.

    Google Scholar 

  • Aitken, R.J., Bowman, P., Gauld, I. The effect of synchronous and asynchronous egg transfer on foetal weight in mice selected for large and small body size. J Embryol Exp Morphol 37:59-64, 1977.

    Google Scholar 

  • Albaiges, G., H. Missfelder-Lobos, M. Parra, C. Lees, D. Cooper & K.H. Nicolaides. Comparison of color Doppler uterine artery indices in a population at high risk for adverse outcome at 24 weeks’ gestation. Ultrasound Obstet Gynecol 21:170-173, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, G. Studies on the placenta of the sheep (Ovis aries L.). Effect of surgical reduction in the number of caruncles. J Reprod Fertil 7:307-322, 1964.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, G.R., Himes, J.H, Kaufman, R.B., Mor J, Kogan, M. A United States national reference for fetal growth. Obstet Gynecol 87:163–168, 1996.

    Google Scholar 

  • Altman, D.G. & E.C. Coles. Nomograms for precise determination of birth weight for dates. Br J Obstet Gynaecol 87:81-86, 1980.

    Article  CAS  PubMed  Google Scholar 

  • Altman, P.L., Dittmer, D.S. Growth including reproduction and morphological development. Federation of American Societies for Experimental Biology, Washington, DC, 1962.

    Google Scholar 

  • American College of Obstetricians and Gynecologists (ACOG), Intrauterine growth restriction. Clinical management guidelines for obstetrician-gynecologists. Committee on Practice Bulletins—Gynecology. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet 71:85-96, 2001.

    Google Scholar 

  • Amon, E., B.M. Sibai, G.D. Anderson & W.C. Mabie. Obstetric variables predicting survival of the immature newborn (less than or equal to 1000 gm): a five-year experience at a single perinatal center. Am J Obstet Gynecol 156:1380-1389, 1987.

    Article  CAS  PubMed  Google Scholar 

  • Amoroso, E.C. Placentation. In: Marshall’s Physiology of Reproduction. A.S. Parkes (Ed). 3rd edn. London, Longmans, Green, 1952, p. 127-311.

    Google Scholar 

  • Angiolini, E., A. Fowden, P. Coan, I. Sandovici, P. Smith, W. Dean, G. Burton, B. Tycko, W. Reik, C. Sibley & M. Constância. Regulation of placental efficiency for nutrient transport by imprinted genes. Placenta27 Suppl A:S98-S102, 2006.

    Google Scholar 

  • Amiel-Tison, C. Neurological evaluation of the maturity of newborn infants. Archives of Disease in Childhood 43 (227):89-93, 1968.

    Google Scholar 

  • Amiel-Tison, C., Grenier, A. Evaluation neurologigue du nouvcau-ne et clu nounisson. Masson, Paris, 1980.

    Google Scholar 

  • Arnett, D.K., G.W. Evans & W.A. Riley. Arterial stiffness: a new cardiovascular risk factor? Am J Epidemiol 140:669-682, 1994.

    Article  CAS  PubMed  Google Scholar 

  • Arbuckle, T.E., Wilkins, R., & Sherman, G.J. Birth weight percentiles by gestational age in Canada. Obstetrics & Gynecology, 81(1), 39-48, 1993.

    Google Scholar 

  • Assali, N.S., Nuwayhid, B., Brinkman, C.R. Placental insufficiency, problems of etiology, diagnosis and management. European Journal of Obstetrics & Gynecology and Reproductive Biology 5 (1–2):87-91, 1975.

    Google Scholar 

  • Assheton, R. Growth in length. Embryological essays. Cambridge University Press, Cambridge, MA, 1916.

    Google Scholar 

  • Axt-Fliedner, R. Second trimester uterine artery Doppler ultrasound as a screening test for adverse pregnancy outcome. Clin Exp Obstet Gynecol 31:9-11, 2004.

    CAS  PubMed  Google Scholar 

  • Balasch, J. & E. Gratacos. Delayed childbearing: effects on fertility and the outcome of pregnancy. Fetal Diagn Ther 29:263-273, 2011.

    Article  PubMed  Google Scholar 

  • Ballard, J.L., K.K. Novak & M. Driver. A simplified score for assessment of fetal maturation of newly born infants. J Pediatr 95:769-774, 1979.

    Article  CAS  PubMed  Google Scholar 

  • Banks, E.H. & D.A. Miller. Perinatal risks associated with borderline amniotic fluid index. Am J Obstet Gynecol 180:1461-1463, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Barker, D.J. Mothers, Babies and Disease in Later Life. London, BMJ Publishing Group, 1994.

    Google Scholar 

  • Barker, D.J., P.D. Winter, C. Osmond, B. Margetts & S.J. Simmonds. Weight in infancy and death from ischaemic heart disease. Lancet 2:577-580, 1989.

    Article  CAS  PubMed  Google Scholar 

  • Baschat, A.A. Integrated fetal testing in growth restriction: combining multivessel Doppler and biophysical parameters. Ultrasound Obstet Gynecol 21:1-8, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Baschat, A.A. Fetal responses to placental insufficiency: an update. BJOG 111:1031-1041, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Baschat, A.A. Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol 37:501-514, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Baschat, A.A. “Neurodevelopment after fetal growth restriction.” Fetal diagnosis and therapy 36.2: 136–142, 2014.

    Google Scholar 

  • Baschat, A.A., U. Gembruch, I. Reiss, L. Gortner, C.P. Weiner & C.R. Harman. Relationship between arterial and venous Doppler and perinatal outcome in fetal growth restriction. Ultrasound Obstet Gynecol 16:407-413, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Baschat, A.A., Gembruch, U., & Harman, C.R. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound in obstetrics & gynecology, 18(6), 571-577, 2001.

    Google Scholar 

  • Baserga, M., A.L. Bares, M.A. Hale, C.W. Callaway, R.A. McKnight, P.H. Lane & R.H. Lane. Uteroplacental insufficiency affects kidney VEGF expression in a model of IUGR with compensatory glomerular hypertrophy and hypertension. Early Hum Dev 85:361-367, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baserga, M., M.A. Hale, R.A. McKnight, X. Yu, C.W. Callaway & R.H. Lane. Uteroplacental insufficiency alters hepatic expression, phosphorylation, and activity of the glucocorticoid receptor in fetal IUGR rats. Am J Physiol Regul Integr Comp Physiol 289:R1348-R1353, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Baserga, M., M.A. Hale, Z.M. Wang, X. Yu, C.W. Callaway, R.A. McKnight & R.H. Lane. Uteroplacental insufficiency alters nephrogenesis and downregulates cyclooxygenase-2 expression in a model of IUGR with adult-onset hypertension. Am J Physiol Regul Integr Comp Physiol 292:R1943-R1955, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Baserga, M., R. Kaur, M.A. Hale, A. Bares, X. Yu, C.W. Callaway, R.A. McKnight & R.H. Lane. Fetal growth restriction alters transcription factor binding and epigenetic mechanisms of renal 11beta-hydroxysteroid dehydrogenase type 2 in a sex-specific manner. Am J Physiol Regul Integr Comp Physiol 299:R334-R342, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassan, H., O. Stolar, R. Geva, R. Eshel, A. Fattal-Valevski, Y. Leitner, M. Waron, A. Jaffa & S. Harel. Intrauterine growth-restricted neonates born at term or preterm: how different? Pediatr Neurol 44:122-130, 2011.

    Article  PubMed  Google Scholar 

  • Batalle, D., E. Eixarch, F. Figueras, E. Muñoz-Moreno, N. Bargallo, M. Illa, R. Acosta-Rojas, I. Amat-Roldan & E. Gratacos. Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome. Neuroimage 60:1352-1366, 2012.

    Article  PubMed  Google Scholar 

  • Battaglia, F.C. Circulatory and metabolic changes accompanying fetal growth restriction. In: Fetal and neonatal physiology. R.A. Polin, W.W. Fox & S.H. Abman (Eds). 4th edn, Vol 1. Philadelphia, Elsevier/Saunders, 2011, p. 302-310.

    Chapter  Google Scholar 

  • Battaglia, F.C. & L.O. Lubchenco. A practical classification of newborn infants by weight and gestational age. J Pediatr 71:159-163, 1967.

    Article  CAS  PubMed  Google Scholar 

  • Battaglia, F.C., Simmons, M.A. The low-birth-weight infant. In: Falkner F, Tanner JM (eds), Human growth. Postnatal growth, vol 2. Plenum, New York, pp 507-555, 1978.

    Google Scholar 

  • Battaglia, C., Artini, P. G., D'Ambrogio, G., Galli, P. A., Segre, A., & Genazzani, A. R. Maternal hyperoxygenation in the treatment of intrauterine growth retardation. American journal of obstetrics and gynecology, 167(2), 430-435, 1992.

    Google Scholar 

  • Begermann, M., Zirn, B., Santen, G., Wirthgen, E., Soellner, L., Büttel, H. M., Schweizer, R., van Workum, W., Binder, G., & Eggermann, T. Paternally inherited IGF2 mutation and growth restriction. New England Journal of Medicine, 373(4), 349–356, 2015.

    Google Scholar 

  • Bell, A.W., W.W. Hay, Jr. & R.A. Ehrhardt. Placental transport of nutrients and its implications for fetal growth. J Reprod Fertil Suppl 54:401-410, 1999.

    CAS  PubMed  Google Scholar 

  • Bellamy, C. & UNICEF. The state of the world’s children 2004. New York, United Nations Publications, 2003.

    Google Scholar 

  • Benirschke, K. Twin placenta in perinatal mortality. N Y State J Med 61:1499-1508, 1961.

    Google Scholar 

  • Bernstein, M., J.D. Horbar, G.J. Badger, A. Ohlsson & A. Golan. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 182:198-206, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Bhide A. Fetal growth restriction and developmental delay: current understanding and future possibilities. Ultrasound Obstet Gynecol 38(3):243-245, 2011.

    Google Scholar 

  • Blair, E.M. & K.B. Nelson. Fetal growth restriction and risk of cerebral palsy in singletons born after at least 35 weeks’ gestation. Am J Obstet Gynecol212:520.e1–e7, 2015.

    Article  Google Scholar 

  • Bloomfield, F.H., M.H. Oliver & J.E. Harding. The late effects of fetal growth patterns. Arch Dis Child Fetal Neonatal Ed 91:F299-F304, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Börzsönyi, B., C. Demendi, Z. Nagy, K. Tóth, M. Csanád, A. Pajor, J. Rig, Jr. & J.G. Joó. Gene expression patterns of insulin-like growth factor 1, insulin-like growth factor 2 and insulin-like growth factor binding protein 3 in human placenta from pregnancies with intrauterine growth restriction. J Perinat Med 39:701-707, 2011.

    Article  PubMed  Google Scholar 

  • Börzsönyi, B., C. Demendi, A. Pajor, J. Rigó, Jr., K. Marosi, A. Ágota, Z.B. Nagy & J.G. Joó. Gene expression patterns of the 11β-hydroxysteroid dehydrogenase 2 enzyme in human placenta from intrauterine growth restriction: the role of impaired fetal-maternal glucocorticoid metabolism. Eur J Obstet Gynecol Reprod Biol 161:12-17, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Bottoms, S.F., R.H. Paul, B.M. Mercer, C.A. MacPherson, S.N. Caritis, A.H. Moawad, J.P. Van Dorsten, J.C. Hauth, G.R. Thurnau, M. Miodovnik, P.M. Meis, J.M. Roberts, D. McNellis & J.D. Iams. Obstetric determinants of neonatal survival: Antenatal predictors of neonatal survival and morbidity in extremely low birth weight infant. Am J Obstet Gynecol 180:665-669, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Bourque, D.K., L. Avila, M. Penaherrera, P. von Dadelszen & W.P. Robinson. Decreased placental methylation at the H19/IGF2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta 31:197-202, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Boyle, J.W., F.K. Lotgering & L.D. Longo. Acute embolization of the uteroplacental circulation: uterine blood flow and placental CO diffusing capacity. J Dev Physiol 6:377-386, 1984.

    CAS  PubMed  Google Scholar 

  • Brenner, W.E., D.A. Edelman & C.H. Hendricks. A standard of fetal growth for the United States of America. Am J Obstet Gynecol 126:555-564, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Brodsky, D. & H. Christou. Current concepts in intrauterine growth restriction. J Intensive Care Med 19:307-319, 2004.

    Article  PubMed  Google Scholar 

  • Brody, S. Bioenergetics and growth. With special reference to the efficiency complex in domestic animals. Reinhold Publishing Corporation, New York, 1945.

    Google Scholar 

  • Bubb, K.J., M.L. Cock, M.J. Black, M. Dodic, W.M. Boon, H.C. Parkington, R. Harding & M. Tare. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 578:871-881, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Budin, P. The nursling. Caxton, London, 1907.

    Google Scholar 

  • Calvert, S.J., C.J. Jones, C.P. Sibley, J.D. Aplin & A.E. Heazell. Analysis of syncytial nuclear aggregates in preeclampsia shows increased sectioning artefacts and decreased inter-villous bridges compared to healthy placentas. Placenta 34:1251-1254, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, S. & A. Thoms. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. Br J Obstet Gynaecol 84:165-174, 1977.

    Article  CAS  PubMed  Google Scholar 

  • Cetin, I. & G. Alvino. Intrauterine growth restriction: implications for placental metabolism and transport. A review. Placenta30 Suppl A:S77-S82, 2009.

    Google Scholar 

  • Cetin, I. & P. Antonazzo. The role of the placenta in intrauterine growth restriction (IUGR). Z Geburtshilfe Neonatol 213:84-88, 2009.

    Article  PubMed  Google Scholar 

  • Challis, J.R., L. Fraher, J. Oosterhuis, S.E. White & A.D. Bocking. Fetal and maternal endocrine responses to prolonged reductions in uterine blood flow in pregnant sheep. Am J Obstet Gynecol 160:926-932, 1989.

    Article  CAS  PubMed  Google Scholar 

  • Chamberlain, P.F., F.A. Manning, I. Morrison, C.R. Harman & I.R. Lange. Ultrasound evaluation of amniotic fluid volume. I. The relationship of marginal and decreased amniotic fluid volumes to perinatal outcome. Am J Obstet Gynecol 150:245-249, 1984.

    Article  CAS  PubMed  Google Scholar 

  • Charnock-Jones, D.S., P. Kaufmann & T.M. Mayhew. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 25:103-113, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Chauhan, S.P., J.A. Scardo, N.W. Hendrix, E.F. Magann & J.C. Morrison. Accuracy of sonographically estimated fetal weight with and without oligohydramnios. A case-control study. J Reprod Med 44:969-973, 1999.

    CAS  PubMed  Google Scholar 

  • Cheek, D.B. Fetal and postnatal cellular growth. Hormones and nutrition. Wiley, New York, 1975.

    Google Scholar 

  • Chen, H.Y., C.C. Lu, Y.T. Cheng, F.J. Hsieh & J.Y. Liu. Antenatal measurement of fetal umbilical venous flow by pulsed Doppler and B-mode ultrasonography. J Ultrasound Med 5:319-321, 1986.

    Article  CAS  PubMed  Google Scholar 

  • Clapp, J.F., 3rd, H.H. Szeto, R. Larrow, J. Hewitt & L.I. Mann. Umbilical blood flow response to embolization of the uterine circulation. Am J Obstet Gynecol 138:60-67, 1980.

    Article  PubMed  Google Scholar 

  • Clausson, B., J. Gardosi, A. Francis & S. Cnattingius. Perinatal outcome in SGA births defined by customized versus population-based birthweight standards. BJOG 108:830-834, 2001.

    CAS  PubMed  Google Scholar 

  • Cockburn, F. (ed) Fetal and neonatal growth. Wiley, Chichester, 1988.

    Google Scholar 

  • Cohn, H.E., E.J. Sacks, M.A. Heymann & A.M. Rudolph. Cardiovascular responses to hypoxemia and academia in fetal lambs. Am J Obstet Gynecol 120:817-824, 1974.

    Article  CAS  PubMed  Google Scholar 

  • Cone, T.E. Jr. De Ponderc Infantum Recens Natorum. The history of weighing the newborn infant. Pediatrics 28:490-498, 1961.

    Google Scholar 

  • Constância, M., M. Hemberger, J. Hughes, W. Dean, A. Ferguson-Smith, R. Fundele, F. Stewart, G. Kelsey, A. Fowden, C. Sibley & W. Reik. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945-948, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Corso, M. & M. Thomson. Protein phosphorylation in mitochondria from human placenta. Placenta 22:432-439, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Cosmi, E., S. Visentin, T. Fanelli, A.J. Mautone & V. Zanardo. Aortic intima media thickness in fetuses and children with intrauterine growth restriction. Obstet Gynecol 114:1109-1114, 2009.

    Article  PubMed  Google Scholar 

  • Cubillo, A., R. Halari, A. Smith, E. Taylor & K. Rubia. A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention. Cortex 48:194-215, 2012.

    Article  PubMed  Google Scholar 

  • Dancis, J. Historic perspective [on the weight of premature infants]. Landmarks Perinatol/Neonatol 18:1-3, 1983.

    Google Scholar 

  • Dancis, J., J.R. O’Connell & L.E. Holt, Jr. A grid for recording the weight of premature infants. J Pediatr 33:570-572, 1948.

    Article  CAS  PubMed  Google Scholar 

  • Dessì, A., G. Ottonello & V. Fanos. Physiopathology of intrauterine growth retardation: from classic data to metabolomics. J Matern Fetal Neonatal Med 25 (Suppl 5):13-18, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Diczfalusy, E. Endocrine functions of the human fetoplacental unit. Fed Proc 23:791-798, 1964.

    CAS  PubMed  Google Scholar 

  • Diplas, A.I., L. Lambertini, M.J. Lee, R. Sperling, Y.L. Lee, J. Wetmur & J. Chen. Differential expression of imprinted genes in normal and IUGR human placentas. Epigenetics 4:235-240, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Dobell, C. D'Arcy Wentworth Thompson. 1860–1948. Obituary Notices of Fellows of the Royal Society 6 (18):599-617, 1949.

    Google Scholar 

  • Dong, Y. & L.P. Thompson. Differential expression of endothelial nitric oxide synthase in coronary and cardiac tissue in hypoxic fetal guinea pig hearts. J Soc Gynecol Investig 13:483-490, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Dubois, J., M. Benders, C. Borradori-Tolsa, A. Cachia, F. Lazeyras, R. Ha-Vinh Leuchter, S.V. Sizonenko, S.K. Warfield, J.F. Mangin & P.S. Hüppi. Primary cortical folding in the human newborn: an early marker of later functional development. Brain 131:2028-2041, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubowitz, L.M., Dubowitz, V., Goldberg, C. Clinical assessment of gestational age in the new born infant. J Pediatr 77:1-10, 1970.

    Google Scholar 

  • Dunham, E.C., R.M. Jenss & A.U. Christie. A consideration of race and sex in relation to the growth and development of infants. J Pediatr 14:156-160, 1939.

    Article  Google Scholar 

  • Dunn, P.M. & B.A. Wharton. Perinatal Growth: the Quest for an International Standard for Reference. Stockholm, SwedenAlmqvist & Wiksell Periodical Company, 1985.

    Google Scholar 

  • Dyer, J.L., I.C. McMillen, K.E. Warnes & J.L. Morrison. No evidence for an enhanced role of endothelial nitric oxide in the maintenance of arterial blood pressure in the IUGR sheep fetus. Placenta 30:705-710, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum, H., A.P. Yonelinas & C. Ranganath. The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123-152, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esterman, A., M.A. Greco, Y. Mitani, T.H. Finlay, F. Ismail-Beigi & J. Dancis. The effect of hypoxia on human trophoblast in culture: morphology, glucose transport and metabolism. Placenta 18:129-136, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Evseenko, D.A., P. Murthi, J.W. Paxton, G. Reid, B.S. Emerald, K.M. Mohankumar, P.E. Lobie, S.P. Brennecke, B. Kalionis & J.A. Keelan. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J 21:3592-3605, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Falkner, F., Tanner, J.M. (eds) Human growth, vol 1, Principles and prenatal growth. Plenum Publishing Corporation, New York, 1978a.

    Google Scholar 

  • Falkner, F., Tanner, J.M. (cds) Human growth, vol 2, Postnatal growth. Plenum Publishing Corporation, New York, 1978b.

    Google Scholar 

  • Falkner, F., Tanner, J.M. (eds) Human growth, vol 3, Neurobiology and nutrition. Plenum New York, 1979.

    Google Scholar 

  • Feldman, R. & A.I. Eidelman. Neonatal state organization, neuromaturation, mother-infant interaction, and cognitive development in small-for-gestational-age premature infants. Pediatrics 118:e869-e878, 2006.

    Article  PubMed  Google Scholar 

  • Figueras, F., R. Cruz-Martinez, M. Sanz-Cortes, A. Arranz, M. Illa, F. Botet, C. Costas-Moragas & E. Gratacos. Neurobehavioral outcomes in preterm, growth-restricted infants with and without prenatal advanced signs of brain-sparing. Ultrasound Obstet Gynecol 38:288-294, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Figueras, F., D. Oros, R. Cruz-Martinez, N. Padilla, E. Hernandez-Andrade, F. Botet, C. Costas-Moragas & E. Gratacos. Neurobehavior in term, small-for-gestational age infants with normal placental function. Pediatrics 124:e934-e941, 2009.

    Article  PubMed  Google Scholar 

  • Fitzhardinge, P.M., Steven, E.M. The small-for-date infant. II. Neurological and intellectual sequelae. Pediatrics 50:50-57, 1972.

    Google Scholar 

  • Fletcher, A.J., C.M. Edwards, D.S. Gardner, A.L. Fowden & D.A. Giussani. Neuropeptide Y in the sheep fetus: effects of acute hypoxemia and dexamethasone during late gestation. Endocrinology 141:3976-3982, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Fong, K.W., A. Ohlsson, M.E. Hannah, S. Grisaru, J. Kingdom, H. Cohen, M. Ryan, R. Windrim, G. Foster & K. Amankwah. Prediction of perinatal outcome in fetuses suspected to have intrauterine growth restriction: Doppler US study of fetal cerebral, renal, and umbilical arteries. Radiology 213:681-689, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Fowden, A.L. The endocrine regulation of fetal metabolism and growth. In: Gluckman PD, Johnston BM, Nathanielsz PW (eds) Research in perinatal medicine (Vlll). Advances in fetal, physiology: reviews in honor of G.C. Liggins. Perinatology Press. Ithaca, NY. pp 229–243, 1989.

    Google Scholar 

  • Fowden, A.L., D.A. Giussani & A.J. Forhead. Endocrine and metabolic programming during intrauterine development. Early Hum Dev 81:723-734, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Fowden, A.L., D.A. Giussani & A.J. Forhead. Intrauterine programming of physiological systems: causes and consequences. Physiology 21:29-37, 2006a.

    Article  CAS  PubMed  Google Scholar 

  • Fowden, A.L., C. Sibley, W. Reik & M. Constancia. Imprinted genes, placental development and fetal growth. Horm Res 65 Suppl 3:50-58, 2006b.

    CAS  PubMed  Google Scholar 

  • Fowden, A.L., Szemere, J., Hughes, P., Gilmour, R.S., Forhead, A.J. The effects of cortisol on the growth rate of the sheep fetus during late gestation. J Endocrinol 151 :97-105, 1996.

    Google Scholar 

  • Fowden, A.L., Mundy, L., Silver, M. Developmental regulation of glucogenesis in the sheep fetus during late gestation. J Physiol 508:937-947, 1998.

    Google Scholar 

  • Frisk, V., R. Amsel & H.E. Whyte. The importance of head growth patterns in predicting the cognitive abilities and literacy skills of small-for-gestational-age children. Dev Neuropsychol 22:565-593, 2002.

    Article  PubMed  Google Scholar 

  • Gagnon, R., J. Murotsuki, J.R. Challis, L. Fraher & B.S. Richardson. Fetal sheep endocrine responses to sustained hypoxemic stress after chronic fetal placental embolization. Am J Physiol 272:E817-E823, 1997.

    CAS  PubMed  Google Scholar 

  • Gardosi, J., A. Chang, B. Kalyan, D. Sahota & E.M. Symonds. Customised antenatal growth charts. Lancet 339:283-287, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Gardosi, J. & A. Francis. Controlled trial of fundal height measurement plotted on customized antenatal growth charts. Br J Obstet Gynaecol 106:309-317, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Gardosi, J. Customized fetal growth standards: rationale and clinical application. Seminars in Perinatology 28 (1):33–40, 2004.

    Google Scholar 

  • Gardosi, J., Figueras, F., Clausson, B., & Francis, A. The customised growth potential: an international research tool to study the epidemiology of fetal growth. Paediatric and perinatal epidemiology, 25(1), 2-10, 2011.

    Google Scholar 

  • Gardosi, J., V. Madurasinghe, M. Williams, A. Malik & A. Francis. Maternal and fetal risk factors for stillbirth: population based study. BMJ 346:f108, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gascoin-Lachambre, G., C. Buffat, R. Rebourcet, S.T. Chelbi, V. Rigourd, F. Mondon, T.M. Mignot, E. Legras, U. Simeoni, D. Vaiman & S. Barbaux. Cullins in human intra-uterine growth restriction: expressional and epigenetic alterations. Placenta 31:151-157, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Geva, R., R. Eshel, Y. Leitner, A. Fattal-Valevski & S. Harel. Memory functions of children born with asymmetric intrauterine growth restriction. Brain Res 1117:186-194, 2006a.

    Article  CAS  PubMed  Google Scholar 

  • Geva, R., R. Eshel, Y. Leitner, A.F. Valevski & S. Harel. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics 118:91-100, 2006b.

    Article  PubMed  Google Scholar 

  • Gheorghe, C.P., S. Mohan, K. Oberg & L.D. Longo. Gene expression patterns in the hypoxic murine placenta: a role in epigenesis? Reprod Sci 14:223-233, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert, W.M. & B. Danielsen. Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol 188:1596-1599, 2003.

    Article  PubMed  Google Scholar 

  • Gilford, H. On a condition of mixed premature and immature development. Mcd Chir Trans 80:17-46, 1897.

    Google Scholar 

  • Gilford, H. The disorders of post-natal growth and development. Adlard and Son Bartholomew Press, London, 1911.

    Google Scholar 

  • Gill, R.W., B.J. Trudinger, W.J. Garrett, G. Kossoff & P.S. Warren (1981). Fetal umbilical venous flow measured in utero by pulsed Doppler and B-mode ultrasound. I. Normal pregnancies. Am J Obstet Gynecol 139:720-725, 1981.

    Article  CAS  PubMed  Google Scholar 

  • Giussani, D.A., E.J. Camm, Y. Niu, H.G. Richter, C.E. Blanco, R. Gottschalk, E.Z. Blake, K.A. Horder, A.S. Thakor, J.A. Hansell, A.D. Kane, F.B. Wooding, C.M. Cross & E.A. Herrera. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One 7:e31017, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giussani, D.A. & S.T. Davidge. Developmental programming of cardiovascular disease by prenatal hypoxia. J Dev Orig Health Dis 4:328-337, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Giussani, D.A., P.S. Phillips, S. Anstee & D.J. Barker. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res 49:490-494, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Giussani, D.A., C.E. Salinas, M. Villena & C.E. Blanco. The role of oxygen in prenatal growth: studies in the chick embryo. J Physiol 585:911-917, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giussani, D.A., J.A. Spencer & M.A. Hanson. Fetal cardiovascular reflex responses to hypoxaemia. Fetal Matern Med Rev 6:17-37, 1994.

    Article  Google Scholar 

  • Giussani, D.A., J.A. Spencer, P.J. Moore, L. Bennet & M.A. Hanson. Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep. J Physiol 461:431-449, 1993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giussani, D.A., N. Unno, S.L. Jenkins, R.A. Wentworth, J.B. Derks, J.H. Collins & P.W. Nathanielsz. Dynamics of cardiovascular responses to repeated partial umbilical cord compression in late-gestation sheep fetus. Am J Physiol 273:H2351-H2360, 1997.

    CAS  PubMed  Google Scholar 

  • Gluckman, P.D., M.A. Hanson, C. Cooper & K.L. Thornburg. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61-73, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon, H.H., Levine, S.Z. The metabolic basis for the individualized feeding of infants, premature and full-term. The Journal of Pediatrics 25(6):464-475, 1944.

    Google Scholar 

  • Goyal, R., A. Leitzke, D. Goyal, C.P. Gheorghe & L.D. Longo. Antenatal maternal hypoxic stress: epigenetic adaptations in fetal lung renin-angiotensin system. Reprod Sci 18:180-189, 2011a.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goyal, R., R.R. Lister, D. Goyal, C.P. Gheorghe & L.D. Longo. Antenatal maternal hypoxic stress: Adaptations of the placental renin-angiotensin system in the mouse. Placenta 32:134-139, 2011b.

    Article  CAS  PubMed  Google Scholar 

  • Griffin, M., G. Attilakos, R. Greenwood & M. Denbow. Amniotic fluid index in low-risk, post-dates pregnancies. Fetal Diagn Ther 26:212-215, 2009.

    Article  PubMed  Google Scholar 

  • Groom, K.M., K.K. Poppe, R.A. North & L.M. McCowan. Small-for-gestational-age infants classified by customized or population birthweight centiles: impact of gestational age at delivery. Am J Obstet Gynecol197:239.e1–e5, 2007.

    Article  Google Scholar 

  • Gruenwald, P. Chronic fetal distress and placental insufficiency. Biol Neonat 5:215-265, 1963.

    Article  CAS  PubMed  Google Scholar 

  • Gruenwald, P. Growth of the human fetus. I. Normal growth and its variation, Am J Obstet. Gynecol 94:1112–1119, 1966.

    Google Scholar 

  • Gruenwald, P. 32. The Lobular Architecture and Maternal Blood Supply of the Mature Primate Placenta. Obstetrics & Gynecology, 29(3), 444, 1967.

    Google Scholar 

  • Gruenwald, P. Intrauterine growth. In: Physiology of the Perinatal Period, Functional and Biochemical Development in Mammals. U. Stave (Ed). New York, Appleton-Century-Crofts, 1970, p. 3-27.

    Google Scholar 

  • Gruenwald, P., H. Funakawa, S. Mitani, T. Nishimura & S. Takeuchi. Influence of environmental factors on foetal growth in man. Lancet 1:1026-1028, 1967.

    Article  CAS  PubMed  Google Scholar 

  • Guo, L., S. Choufani, J. Ferreira, A. Smith, D. Chitayat, C. Shuman, R. Uxa, S. Keating, J. Kingdom & R. Weksberg. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 320:79-91, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Guttmacher, A.F., Kohl, S.G. The fetus of multiple gestations, Obstct Gynecol 12:528-541, 1958.

    Google Scholar 

  • Haldane, J.B.S. Possible worlds and other essays. Chatto & Windus, London, 1927.

    Google Scholar 

  • Hales, C.N. & D.J. Barker. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35:595-601, 1992.

    Article  CAS  PubMed  Google Scholar 

  • Hales, C.N. & S.E. Ozanne. For debate: Fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure. Diabetologia 46:1013-1019, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Harding, R., Bocking, A.D. Fetal growth and development. Cambridge University Press, Cambridge, MA, 2001.

    Google Scholar 

  • Hassan, W.A., J. Brockelsby, M. Alberry, T. Fanelli, J. Wladimiroff & C.C. Lees. Cardiac function in early onset small for gestational age and growth restricted fetuses. Eur J Obstet Gynecol Reprod Biol 171:262-265, 2013.

    Article  PubMed  Google Scholar 

  • Hecher, K., C.M. Bilardo, R.H. Stigter, Y. Ville, B.J. Hackelöer, H.J. Kok, M.V. Senat & G.H.A. Visser. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 18:564-570, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Heidegger, M. Poetry, Language, Thought, Harper & Row, New York 1971

    Google Scholar 

  • Heidenreich, P.A., J.G. Trogdon, O.A. Khavjou, J. Butler, K. Dracup, M.D. Ezekowitz, E.A. Finkelstein, Y. Hong, S.C. Johnston, A. Khera, D.M. Lloyd-Jones, S.A. Nelson, G. Nichol, D. Orenstein, P.W. Wilson, Y.J. Woo, American Heart Association Advocacy Coordinating Committee, Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Clinical Cardiology, Council on Epidemiology and Prevention, Council on Arteriosclerosis, Thrombosis and Vascular Biology, Council on Cariopulmonary, Critical Care, Perioperative and Resuscitation, Council on Cardiovascular Nursing, Council on the Kidney in Cardiovascular Disease, Council on Cardiovascular Surgery and Anesthesia & Interdisciplinary Council on Quality of Care and Outcomes Research. (2011). Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation 123:933-944, 2011.

    Google Scholar 

  • Heinonen, K., K. Räikkönen, A.K. Pesonen, S. Andersson, E. Kajantie, J.G. Eriksson, D. Wolke & A. Lano. Behavioural symptoms of attention deficit/hyperactivity disorder in preterm and term children born small and appropriate for gestational age: a longitudinal study. BMC Pediatr 10:91, 2010.

    Google Scholar 

  • Hemmings, D.G., S.J. Williams & S.T. Davidge. Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. Am J Physiol Heart Circ Physiol 289:H674-H682, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Herrera, E.A., E.J. Camm, C.M. Cross, J.L. Mullender, F.B. Wooding & D.A. Giussani. Morphological and functional alterations in the aorta of the chronically hypoxic fetal rat. J Vasc Res 49:50-58, 2012.

    Article  PubMed  Google Scholar 

  • Hershkovitz, R., J.C. Kingdom, M. Geary & C.H. Rodeck. Fetal cerebral blood flow redistribution in late gestation: identification of compromise in small fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 15:209-212, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Hershkovitz, R., M. de Swiet & J. Kingdom. Mid-trimester placentation assessment in high-risk pregnancies using maternal serum screening and uterine artery Doppler. Hypertens Pregnancy 24:273-280, 2005.

    Article  PubMed  Google Scholar 

  • Hammond, J. Farm animals, their breeding, growth, and inheritance. Longmans, Green & Co, New York, 1940.

    Google Scholar 

  • Hammond, J. Effect of nutrition on the stage of development of the young at birth in farm animals. In: Wolstenholme GEW, O'Connor M (eds) Ciba Foundation Symposium on somatic stability in the newly born. Little, Brown, Boston, MA, pp 5-15, 1961a.

    Google Scholar 

  • Hammond, J. Short Communication: informal assessment of the veterinary significance of the proceedings. In: Wolstenholme GEW, O'Connor M (eds) Ciba Foundation Symposium on somatic stability in the newly born. Little, Brown, Boston, MA, pp 353-365, 1961b.

    Google Scholar 

  • Hammond, J., Marshall, FHA. Reproduction in the rabbit. Oliver & Boyd, Edinburgh, 1925.

    Google Scholar 

  • Hoffman, H.J., Stark, C.R., Lundin, F.E. Jr, Ashbrook, J.D. Analysis of birth weight, gestational age, and fetal viability, US births, 1968, Obstet Gynccol Surv 29:651–681, 1974.

    Google Scholar 

  • Hutcheon, J.A., X. Zhang, S. Cnattingius, M.S. Kramer & R.W. Platt. Customised birthweight percentiles: does adjusting for maternal characteristics matter? BJOG 115:1397-1404, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Hutcheon, J.A., M. Walker, R.W. Platt. Assessing the value of customized birth weight percentiles. Am J Epidemiol 173(4): 459-467, 2011a.

    Google Scholar 

  • Hutcheon J.A., X. Zhang, R.W. Platt, S. Cnattingius, M.S. Kramer. The case against customised birthweight standards. Paediatr Perinat Epidemiol. 25(1):11-16, 2011b.

    Google Scholar 

  • Iams, J.D. Small for gestational age (SGA) and fetal growth restriction (FGR). Am J Obstet Gynecol 202:513, 2010.

    Article  PubMed  Google Scholar 

  • Iams, J.D. Clinical practice. Prevention of preterm parturition. N Engl J Med 370:254-261, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Illa, M., E. Eixarch, D. Batalle, A. Arbat-Plana, E. Muñoz-Moreno, F. Figueras & E. Gratacos. Long-term functional outcomes and correlation with regional brain connectivity by MRI diffusion tractography metrics in a near-term rabbit model of intrauterine growth restriction. PLoS One 8:e76453, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang, E.A., L.D. Longo & R. Goyal. Antenatal maternal hypoxia: criterion for fetal growth restriction in rodents. Front Physiol 6:176, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones, C.T. & R.O. Robinson. Plasma catecholamines in foetal and adult sheep. J Physiol 248:15-33, 1975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Julian, C.G., I.V. Yang, V.A. Browne, E. Vargas, C. Rodriguez, B.S. Pedersen, L.G. Moore & D.A. Schwartz. Inhibition of peroxisome proliferator-activated receptor γ: a potential link between chronic maternal hypoxia and impaired fetal growth. FASEB J 28:1268-1279, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamitomo, M., J.G. Alonso, T. Okai, L.D. Longo & R.D. Gilbert. Effects of long-term, high-altitude hypoxemia on ovine fetal cardiac output and blood flow distribution. Am J Obstet Gynecol 169:701-707, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Kamitomo, M., L.D. Longo & R.D. Gilbert. Right and left ventricular function in fetal sheep exposed to long-term high-altitude hypoxemia. Am J Physiol 262:H399-H405, 1992.

    CAS  PubMed  Google Scholar 

  • King, L.S. The Medical World of the Eighteenth Century. Huntington, NY, R.E. Krieger, 1958.

    Google Scholar 

  • Kitanaka, T., R.D. Gilbert & L.D. Longo. Maternal responses to long-term hypoxemia in sheep. Am J Physiol 256:R1340-R1347, 1989.

    CAS  PubMed  Google Scholar 

  • Koklu, E., S. Kurtoglu, M. Akcakus, S. Koklu, D. Buyukkayhan, H. Gumus & A. Yikilmaz. Increased aortic intima-media thickness is related to lipid profile in newborns with intrauterine growth restriction. Horm Res 65:269-275, 2006.

    CAS  PubMed  Google Scholar 

  • Kovo, M., Schreiber, L., Elyashiv, O., Ben-Haroush, A., Abraham, G., & Bar, J. Pregnancy outcome and placental findings in pregnancies complicated by fetal growth restriction with and without preeclampsia. Reproductive Sciences, 22(3), 316-321, 2015.

    Google Scholar 

  • Kramer, M.S. Intrauterine growth and gestational duration determinants. Pediatrics 80:502–511, 1987.

    Google Scholar 

  • Kramer, M.S., M. Olivier, F.H. McLean, D.M. Willis & R.H. Usher. Impact of intrauterine growth retardation and body proportionality on fetal and neonatal outcome. Pediatrics 86:707-713, 1990.

    CAS  PubMed  Google Scholar 

  • Kusinski, L. C., Stanley, J. L., Dilworth, M. R., Hirt, C. J., Andersson, I. J., Renshall, L. J., Baker, B. C., Baker, P. N., Sibley, C. P., Wareing, M., & Glazier, J. D. eNOS knockout mouse as a model of fetal growth restriction with an impaired uterine artery function and placental transport phenotype. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 303(1), R86-R93, 2012.

    Google Scholar 

  • Kuzawa, C.W. Modeling fetal adaptation to nutrient restriction: testing the fetal origins hypothesis with a supply-demand model. J Nutr 134:194-200, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Lambertini, L., T.L. Lee, W.Y. Chan, M.J. Lee, A. Diplas, J. Wetmur & J. Chen. Differential methylation of imprinted genes in growth-restricted placentas. Reprod Sci 18:1111-1117, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Lattuada, D., F. Colleoni, A. Martinelli, A. Garretto, R. Magni, T. Radaelli & I. Cetin. Higher mitochondrial DNA content in human IUGR placenta. Placenta 29:1029-1033, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Lawn, J.E., S. Cousens, J. Zupan & Lancet Neonatal Survival Steering Team. 4 million neonatal deaths: When? Where? Why? Lancet 365:891-900, 2005.

    Article  PubMed  Google Scholar 

  • Leeson, C.P., M. Kattenhorn, R. Morley, A. Lucas & J.E. Deanfield. Impact on low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation 103:1264-1268, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Leeson, C.P., P.H. Whincup, D.G. Cook, A.E. Donald, O. Papacosta, A. Lucas & J.E. Deanfield. Flow-mediated dilation in 9- to 11-year-old children: the influence of intrauterine and childhood factors. Circulation 96:2233-2238, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Leiser, R. & P. Kaufmann. Placental structure: in a comparative aspect. Exp Clin Endocrinol 102:122-134, 1994.

    Article  CAS  PubMed  Google Scholar 

  • Leitner, Y., A. Fattal-Valevski, R. Geva, R. Eshel, H. Toledano-Alhadef, M. Rotstein, H. Bassan, B. Radianu, O. Bitchonsky, A.J. Jaffa & S. Harel. Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study. J Child Neurol 22:580-587, 2007.

    Article  PubMed  Google Scholar 

  • Leon, D.A., H.O. Lithell, D. Vâgerö, I. Koupilová, R. Mohsen, L. Berglund, U.B. Lithell & P.M. McKeigue. Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15000 Swedish men and women born in 1915-29. BMJ 317:241-245, 1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lepsch, J., Farias, D. R., dos Santos Vaz, J., Pinto, T. D. J. P., da Silva Lima, N., Vilela, A. A. F., Cunha, M., Factor-Litvak, P., & Kac, G. Serum saturated fatty acid decreases plasma adiponectin and increases leptin throughout pregnancy independently of BMI. Nutrition, 32(7), 740–747, 2016.

    Google Scholar 

  • Li, G., Y. Xiao, J.L. Estrella, C.A. Ducsay, R.D. Gilbert & L. Zhang. Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult rat. J Soc Gynecol Investig 10:265-274, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Lim, A.L., S. Ng, S.C. Leow, R. Choo, M. Ito, Y.H. Chan, S.K. Goh, E. Tng, K. Kwek, Y.S. Chong, P.D. Gluckman & A.C. Ferguson-Smith. Epigenetic state and expression of imprinted genes in umbilical cord correlates with growth parameters in human pregnancy. J Med Genet 49:689-697, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Lin, C.C. & J. Santolaya-Forgas. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol 92:1044-1055, 1998.

    CAS  PubMed  Google Scholar 

  • Lin, C.C., S.J. Su & L.P. River. Comparison of associated high-risk factors and perinatal outcome between symmetric and asymmetric fetal intrauterine growth retardation. Am J Obstet Gynecol 164:1535-1541, 1991.

    Article  CAS  PubMed  Google Scholar 

  • Lindgren, I. & J. Altimiras. Sensitivity of organ growth to chronically low oxygen levels during incubation in Red Junglefowl and domesticated chicken breeds. Poult Sci 90:126-135, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Lodygensky, G.A., M.L. Seghier, S.K. Warfield, C.B. Tolsa, S. Sizonenko, F. Lazeyras & P.S. Hüppi. Intrauterine growth restriction affects the preterm infant’s hippocampus. Pediatr Res 63:438-443, 2008.

    Article  PubMed  Google Scholar 

  • Longo, L.D. Intrauterine growth retardation: a “mosaic” hypothesis of pathophysiology. Semin Perinatol 8:62-72, 1984.

    CAS  PubMed  Google Scholar 

  • Longo, L.D. Respiratory gas exchange in the placenta. In: Handbook of Physiology. The Respiratory System. Gas Exchange (Sect. 3, vol. IV). Bethesda, MD, American Physiological Society, 1987, p. 351-401.

    Google Scholar 

  • Lorijn, R.H. & L.D. Longo. Norepinephrine elevation in the fetal lamb: oxygen consumption and cardiac output. Am J Physiol 239:R115-R122, 1980.

    CAS  PubMed  Google Scholar 

  • Low, J.A., Boston, R.W., Pancham, S.R. Fetal asphyxia during the intrapartum period in intrauterine growth-retarded infants. American Journal of Obstetrics and Gynecology 113 (3):351-357, 1972.

    Google Scholar 

  • Lubchenco, L.O. Assessment of gestational age and development of birth. Pediatr Clin North Am 17:125-145, 1970.

    Article  CAS  PubMed  Google Scholar 

  • Lubchenco, L.O. The High-Risk Infant. A.J. Schaffer & M. Markowitz (Eds). Philadelphia, Saunders, 1976.

    Google Scholar 

  • Lubchenco, L.O., C. Hansman & E. Boyd. Intrauterine growth in length and head circumference as estimated from live births at gestational ages from 26 to 42 weeks. Pediatrics 37:403-408, 1966.

    CAS  PubMed  Google Scholar 

  • Lubchenco, L.O., C. Hansman, M. Dressler & E. Boyd. Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation. Pediatrics 32:793-800, 1963.

    CAS  PubMed  Google Scholar 

  • Lubchenco, L.O., D.T. Searls & J.V. Brazie. Neonatal mortality rate: relationship to birth weight and gestational age. J Pediatr 81:814-822, 1972.

    Article  CAS  PubMed  Google Scholar 

  • Manjarrez, G., I. Cisneros, R. Herrera, F. Vazquez, A. Robles & J. Hernandez. Prenatal impairment of brain serotonergic transmission in infants. J Pediatr 147:592-596, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Manning, F.A. Intrauterine growth retardation. In: Fetal Medicine: Principal and Practice. Norwalk, Appleton and Lange, 1995.

    Google Scholar 

  • Mari, G., F. Hanif, M. Kruger, E. Cosmi, J. Santolaya-Forgas & M.C. Treadwell. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol 29:310-316, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Marsál, K. Intrauterine growth restriction. Curr Opin Obstet Gynecol 14:127-135, 2002.

    Article  PubMed  Google Scholar 

  • Marshall, FHA, Hammond, J. The science of animal breeding in Britain: a shmi history. Longmans, Green and Co, London, 1946.

    Google Scholar 

  • Mayhew, T.M., C. Gregson & D.G. Fagan. Ventricular myocardium in control and growth-retarded human fetuses: growth in different tissue compartments and variation with fetal weight, gestational age, and ventricle size. Hum Pathol 30:655-660, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Mayhew, T.M., J. Wijesekara, P.N. Baker & S.S. Ong. Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta 25:829-833, 2004.

    Article  CAS  PubMed  Google Scholar 

  • McBurney, R.D. The undernourished full term infant; a case report. West J Surg Obstet Gynecol 55:363-370, 1947.

    CAS  PubMed  Google Scholar 

  • McCarthy, C., F.E. Cotter, S. McElwaine, A. Twomey, E.E. Mooney, F. Ryan, J. Vaughan. Altered gene expression patterns in intrauterine growth restriction: potential role of hypoxia. Am J Obstet Gynecol 196:70.e1–e6, 2007.

    Google Scholar 

  • McCowan, L.M., J.E. Harding & A.W. Stewart. Customized birthweight centiles predict SGA pregnancies with perinatal morbidity. BJOG 112:1026-1033, 2005.

    Article  PubMed  Google Scholar 

  • McMinn, J., M. Wei, N. Schupf, J. Cusmai, E.B. Johnson, A.C. Smith, R. Weksberg, H.M. Thaker & B. Tycko. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 27:540-549, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Mellor, D.J. Nutritional and placental determinants of foetal growth rate in sheep and consequences for the newborn lamb. Br Vet J 139:307-324, 1983.

    Article  CAS  PubMed  Google Scholar 

  • Milani, S., A. Bossi, E. Bertino, E. di Battista, A. Coscia, G. Aicardi, C. Fabris & L. Benso. Differences in size at birth are determined by differences in growth velocity during early prenatal life. Pediatr Res 57:205-210, 2005.

    Article  PubMed  Google Scholar 

  • Miller, H.C., Merritt, T.A. Fetal growth in humans. Year Book Medical, Chicago, IL, 1979.

    Google Scholar 

  • Miller, S.L., L.R. Green, D.M. Peebles, M.A. Hanson & C.E. Blanco. Effects of chronic hypoxia and protein malnutrition on growth in the developing chick. Am J Obstet Gynecol 186:261-267, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Minot, C.S. Senescence and Rejuvenation. The Journal of Physiology 12 (2):97-192, 1891.

    Google Scholar 

  • Minot, C.S. The embryological basis of pathology. Science 13:481–498 (Also published in Boston Med Surg J 144:295-305, 1901.

    Google Scholar 

  • Minot, C.S. The problem of age, growth, and death; a study of cytomorphosis, based on Lectures at the Lowell Institute, March 1907. Putnam, New York, 1908.

    Google Scholar 

  • Moore, L.G., S.M. Charles & C.G. Julian. Humans at high altitude: hypoxia and fetal growth. Respir Physiol Neurobiol 178:181-190, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Morgan, H.D., F. Santos, K. Green, W. Dean & W. Reik. Epigenetic reprogramming in mammals. Hum Mol Genet 14 Spec No 1:R47-R58, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Morrison, J.L. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol 35:730-743, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Morrison, S., D.S. Gardner, A.J. Fletcher, M.R. Bloomfield & D.A. Giussani. Enhanced nitric oxide activity offsets peripheral vasoconstriction during acute hypoxaemia via chemoreflex and adrenomedullary actions in the sheep fetus. J Physiol 547:283-291, 2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morton, J.S., C.F. Rueda-Clausen & S.T. Davidge. Mechanisms of endothelium-dependent vasodilation in male and female, young and aged offspring born growth restricted. Am J Physiol Regul Integr Comp Physiol 298:R930-R938, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Morton, J.S., C.F. Rueda-Clausen & S.T. Davidge. Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal hypoxia. J Appl Physiol 110:1073-1082, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Mossman, H.W. Vertebrate Fetal Membranes. New Brunswick, NJ, Rutgers University Press, 1987.

    Book  Google Scholar 

  • Mouillet, J.F., T. Chu, C.A. Hubel, D.M. Nelson, W.T. Parks & Y. Sadovsky. The levels of hypoxia-regulated microRNAs in plasma of pregnant women with fetal growth restriction. Placenta 31:781-784, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray, A.J. Oxygen delivery and fetal-placental growth: beyond a question of supply and demand? Placenta 33 Suppl 2:e16-e22, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Myatt, L. Placental adaptive responses and fetal programming. J Physiol 572:25-30, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nardozza, L.M., E. Araujo Júnior, M.M. Barbosa, A.C. Caetano, D.J. Lee & A.F. Moron. Fetal growth restriction: current knowledge to the general Obs/Gyn. Arch Gynecol Obstet 286:1-13, 2012.

    Article  PubMed  Google Scholar 

  • Nelson, D.M., S.D. Smith, T.C. Furesz, Y. Sadovsky, V. Ganapathy, C.A. Parvin & C.H. Smith. Hypoxia reduces expression and function of system A amino acid transporters in cultured term human trophoblasts. Am J Physiol Cell Physiol 284:C310-C315, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Newman, H.H. The biology of twins (mammals). University of Chicago Press, Chicago, IL, 1917.

    Google Scholar 

  • Newman, H.H. The physiology of twinning. University of Chicago Press, Chicago, IL, 1923.

    Google Scholar 

  • Newman, H.H. Multiple human births. Twins, triplets, quadruplets and quintuplets. Doubleday, Doran & Company, Inc., New York, 1940.

    Google Scholar 

  • North, A.F., Jr. Small-for-dates neonates. I. Maternal, gestational, and neonatal characteristics. Pediatrics 38:1013-1019, 1966.

    PubMed  Google Scholar 

  • Ott, W.J. Intrauterine growth retardation and preterm delivery. American Journal of Obstetrics and Gynecology 168 (6):1710-1717, 1993.

    Google Scholar 

  • Patterson, A.J., M. Chen, Q. Xue, D. Xiao & L. Zhang. Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ Res 107:365-373, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patterson, A.J., D. Xiao, F. Xiong, B. Dixon & L. Zhang. Hypoxia-derived oxidative stress mediates epigenetic repression of PKCε gene in foetal rat. Cardiovasc Res 93:302-310, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Payne, J.F. Thomas Sydenham. London, T. Fisher Unwin, 1900.

    Google Scholar 

  • Paz, I., Gale, R., Laor, A., Danon, Y.L., Stevenson, D.K. & Seidman, D.S. (1995). The cognitive outcome of full-term small for gestational age infants at late adolescence. Obstet Gynecol 85:452-456, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Peeters, L.L., R.E. Sheldon, M.D. Jones, Jr., E.L. Makowski & G. Meschia. Blood flow to fetal organs as a function of arterial oxygen content. Am J Obstet Gynecol 135:637-646, 1979.

    Article  CAS  PubMed  Google Scholar 

  • Perez, R., M. Espinoza, R. Riguelme, J.T. Parer & A.J. Llanos. Arginine vasopressin mediates cardiovascular responses to hypoxemia in fetal sheep. Am J Physiol 256:R1011-R1018, 1989.

    CAS  PubMed  Google Scholar 

  • Phillips, I.D., G. Simonetta, J.A. Owens, J.S. Robinson, I.J. Clarke & I.C. McMillen. Placental restriction alters the functional development of the pituitary-adrenal axis in the sheep fetus during late gestation. Pediatr Res 40:861-866, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Piedrahita, J.A. The role of imprinted genes in fetal growth abnormalities. Birth Defects Res A Clin Mol Teratol 91:682-692, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Postigo, L., G. Heredia, N.P. Illsley, T. Torricos, C. Dolan, L. Echalar, W. Tellez, I. Maldonado, M. Brimacombe, E. Balanza, E. Vargas & S. Zamudio. Where the O2 goes to: preservation of human fetal oxygen delivery and consumption at high altitude. J Physiol 587:693-708, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Rees, S., R. Harding & D. Walker. An adverse intrauterine environment: implications for injury and altered development of the brain. Int J Dev Neurosci 26:3-11, 2008.

    Article  PubMed  Google Scholar 

  • Rees, S., R. Harding & D. Walker. The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int J Dev Neurosci 29:551-563, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reik, W., M. Constância, A. Fowden, N. Anderson, W. Dean, A. Ferguson-Smith, B. Tycko & C. Sibley. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 547:35-44, 2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reik, W. & J. Walter. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2:21-32, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Resnik, R. Intrauterine growth restriction. Obstet Gynecol 99:490-496, 2002.

    PubMed  Google Scholar 

  • Resnik, R. One size does not fit all. Am J Obstet Gynecol 197:221-222, 2007.

    Article  PubMed  Google Scholar 

  • Riddell, M.R., B. Winkler-Lowen, Y. Jiang, L.J. Guilbert & S.T. Davidge. Fibrocyte-like cells from intrauterine growth restriction placentas have a reduced ability to stimulate angiogenesis. Am J Pathol 183:1025-1033, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Rizzo, G., A. Capponi, D. Rinaldo, D. Arduini & C. Romanini. Ventricular ejection force in growth-retarded fetuses. Ultrasound Obstet Gynecol 5:247-255, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Roberts, R.C. On the uniform lineal growth of the human foetus. Lancet 1:295-296, 1906.

    Google Scholar 

  • Robinson, R.J. Assessment of Gestational Age by Neurological Examination. Archives of Disease in Childhood 41 (218):437-447, 1966.

    Google Scholar 

  • Robinson, J.J. The influence of maternal nutrition on ovine foetal growth. Proceedings of the Nutrition Society 36:9-16, 1977.

    Google Scholar 

  • Robinson, J.S., E.J. Kingston, C.T. Jones & G.D. Thorburn. Studies on experimental growth retardation in sheep. The effect of removal of a endometrial caruncles on fetal size and metabolism. J Dev Physiol 1:379-398, 1979.

    CAS  PubMed  Google Scholar 

  • Robinson, J.S., Moore, V.M., Owens, J.A., McMillen, I.C. Origins of fetal growth restriction. Eur 914 J Obstet Gynecol Reprod Biol 92:13-19, 2000.

    Google Scholar 

  • Roex, A., P. Nikpoor, E. van Eerd, N. Hodyl & G. Dekker. Serial plotting on customised fundal height charts results in doubling of the antenatal detection of small for gestational age fetuses in nulliparous women. Aust N Z J Obstet Gynaecol 52:78-82, 2012.

    Article  PubMed  Google Scholar 

  • Roje, D., S. Zekic Tomas, V. Capkun, J. Marusic, J. Resic & I. Kuzmic Prusac. Asymmetrical fetal growth is not associated with altered trophoblast apoptotic activity in idiopathic intrauterine growth retardation. J Obstet Gynaecol Res 40:410-417, 2014.

    Article  PubMed  Google Scholar 

  • Rouwet, E.V., A.N. Tintu, M.W. Schellings, M. van Bilsen, E. Lutgens, L. Hofstra, D.W. Slaaf, G. Ramsay & F.A. Le Noble. Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation 105:2791-2796, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Rueda-Clausen, C.F., J.S. Morton & S.T. Davidge. Effects of hypoxia-induced intrauterine growth restriction on cardiopulmonary structure and function during adulthood. Cardiovasc Res 81:713-722, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Rueda-Clausen, C.F., J.S. Morton, G.D. Lopaschuk & S.T. Davidge. Long-term effects of intrauterine growth restriction on cardiac metabolism and susceptibility to ischaemia/reperfusion. Cardiovasc Res 90:285-294, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Ruijtenbeek, K., C.G. Kessels, B.J. Janssen, N.J. Bitsch, G.E. Fazzi, G.M. Janssen, J. De Mey & C.E. Blanco. Chronic moderate hypoxia during in ovo development alters arterial reactivity in chickens. Pflugers Arch 447:158-167, 2003b.

    Article  CAS  PubMed  Google Scholar 

  • Ruijtenbeek, K., L.C. Kessels, J.G. De Mey & C.E. Blanco. Chronic moderate hypoxia and protein malnutrition both induce growth retardation, but have distinct effects on arterial endothelium-dependent reactivity in the chicken embryo. Pediatr Res 53:573-579, 2003a.

    Article  PubMed  Google Scholar 

  • Ruijtenbeek, K., F.A. le Noble, G.M. Janssen, C.G. Kessels, G.E. Fazzi, C.E. Blanco & J.G. De Mey. Chronic hypoxia stimulates periarterial sympathetic nerve development in chicken embryo. Circulation 102:2892-2897, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Rumbolz, W.L. & L.S. McGoogan. Placental insufficiency and the small undernourished full-term infant. Obstet Gynecol 1:294-301, 1953.

    CAS  PubMed  Google Scholar 

  • Saenger, P., P. Czernichow, I. Hughes & E.O. Reiter. Small for gestational age: short stature and beyond. Endocr Rev 28:219-251, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Saint-Anne Dargassies, S. La maturation neurologique du premature. Etudes Neonatales 4:71-116, 1955.

    Google Scholar 

  • Salinas, C.E., C.E. Blanco, M. Villena, E.J. Camm, J.D. Tuckett, R.A. Weerakkody, A.D. Kane, A.M. Shelley, F.B. Wooding, M. Quy & D.A. Giussani. Cardiac and vascular disease prior to hatching in chick embryos incubated at high altitude. J Dev Orig Health Dis 1:60-66, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Sanders, H.G. Sir John Hammond, CBE, FRS. British Journal of Nutrition 19 (01):149, 1965.

    Google Scholar 

  • Sanz-Cortés, M., F. Figueras, E. Bonet-Carne, N. Padilla, V. Tenorio, N. Bargalló, I. Amat-Roldan & E. Gratacós. Fetal brain MRI texture analysis identifies different microstructural patterns in adequate and small for gestational age fetuses at term. Fetal Diagn Ther 33:122-129, 2013.

    Article  PubMed  Google Scholar 

  • Scammon, R. The first seriatim study of human growth. American Journal of Physical Anthropology 10 (3):329-336, 1927.

    Google Scholar 

  • Schauseil-Zipf, U., W. Hamm, B. Stenzel, A. Bolte & E. Gladtke. Severe intra-uterine growth retardation: obstetrical management and follow up studies in children born between 1970 and 1985. Eur J Obstet Gynecol Reprod Biol 30:1-9, 1989.

    Article  CAS  PubMed  Google Scholar 

  • Schober, M.E., R.A. McKnight, X. Yu, C.W. Callaway, X. Ke & R.H. Lane. Intrauterine growth restriction due to uteroplacental insufficiency decreased white matter and altered NMDAR subunit composition in juvenile rat hippocampi. Am J Physiol Regul Integr Comp Physiol 296:R681-R692, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Seeds, J.W. Impaired fetal growth: definition and clinical diagnosis. Obstet Gynecol 64:303-310, 1984.

    CAS  PubMed  Google Scholar 

  • Sharma, S.K., J.L. Lucitti, C. Nordman, J.P. Tinney, K. Tobita & B.B. Keller. Impact of hypoxia on early chick embryo growth and cardiovascular function. Pediatr Res 59:116-120, 2006.

    Article  PubMed  Google Scholar 

  • Sibley, C.P., P.M. Coan, A.C. Ferguson-Smith, W. Dean, J. Hughes, P. Smith, W. Reik, G.J. Burton, A.L. Fowden & M. Constância. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci USA 101:8204-8208, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sibley, C.P., M.A. Turner, I. Cetin, P. Ayuk, C.A. Boyd, S.W. D’Souza, J.D. Glazier, S.L. Greenwood, T. Jansson & T. Powell. Placental phenotypes of intrauterine growth. Pediatr Res 58:827-832, 2005.

    Article  PubMed  Google Scholar 

  • Singla, P.N., M. Tyagi, A. Kumar, D. Dash & R. Shankar. Fetal growth in maternal anaemia. J Trop Pediatr 43:89-92, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Sitras, V., R. Paulssen, J. Leirvik, A. Vårtun & G. Acharya. Placental gene expression profile in intrauterine growth restriction due to placental insufficiency. Reprod Sci 16:701-711, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Skilton, M.R., N. Evans, K.A. Griffiths, J.A. Harmer & D.S. Celermajer. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet 365:1484-1486, 2005.

    Article  PubMed  Google Scholar 

  • Slater, W.K., Edwards, J. John Hammond. 1889-1964. Biographical Memoirs of Fellows of the Royal Society 11 (0):100-113, 1965.

    Google Scholar 

  • Soleymanlou, N., I. Jurisica, O. Nevo, F. Ietta, X. Zhang, S. Zamudio, M. Post & I. Caniggia. Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab 90:4299-4308, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Stoch, M.B., Smythe, P.M. Does Undernutrition During Infancy Inhibit Brain Growth and subsequent intellectual development? Arch Dis Child 38:546-552, 1963.

    Google Scholar 

  • Strauss, R.S. Adult functional outcome of those born small for gestational age: twenty-six-year follow-up of the 1970 British Birth Cohort. JAMA 283:625-632, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Struwe, E., G. Berzl, R. Schild, H. Blessing, L. Drexel, B. Hauck, A. Tzschoppe, M. Weidinger, M. Sachs, C. Scheler, E. Schleussner & J. Dotsch. Microarray analysis of placental tissue in intrauterine growth restriction. Clin Endocrinol 72:241-247, 2010.

    Article  CAS  Google Scholar 

  • Sung, I.K., B. Vohr & W. Oh. Growth and neurodevelopmental outcome of very low birth weight infants with intrauterine growth retardation: comparison with control subjects matched by birth weight and gestational age. J Pediatr 123:618-624, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Sutton, M.S., M.A. Theard, S.J. Bhatia, T. Plappert, D.H. Saltzman & P. Doubilet. Changes in placental blood flow in the normal human fetus with gestational age. Pediatr Res 28:383-387, 1990.

    Article  CAS  PubMed  Google Scholar 

  • Swanson, A.M., & David, A.L. Animal models of fetal growth restriction: considerations for translational medicine. Placenta, 36(6), 623-630, 2015.

    Google Scholar 

  • Sweeting, H.N. Measurement and definitions of obesity in childhood and adolescence: a field guide for the uninitiated. Nutr J 6:32, 2007.

    Google Scholar 

  • Takenaka, S., Ventura, W., Sterrantino, A. F., Kawashima, A., Koide, K., Hori, K., Farina, A., & Sekizawa, A. Prediction of fetal growth restriction by analyzing the messenger RNAs of angiogenic factor in the plasma of pregnant women. Reproductive Sciences, 22(6), 743-749, 2015.

    Google Scholar 

  • Tanner, J.M. Standards for birth weight or intra-uterine growth. Pediatrics 46:1-6, 1970.

    Google Scholar 

  • Tanner, J.M. Foetus into Man: Physical Growth from Conception to Maturity. Cambridge, Harvard University Press, 1978.

    Google Scholar 

  • Tanner, J.M. A concise history of growth studies from buffon to boas. In: Falkner F, Tanner JM (eds) Human growth. Neurobiology and nutrition, vol.3. Plenum, New York, pp 515-593, 1979.

    Google Scholar 

  • Tanner, J.M. A history of the study of human growth. Cambridge University Press, Cambridge, MA, 1981.

    Google Scholar 

  • Tanner, J.M. Foetus into man: physical growth from conception to maturity. Harvard University Press, Cambridge, MA, 1990.

    Google Scholar 

  • Thakor, A.S., H.G. Richter, A.D. Kane, C. Dunster, F.J. Kelly, L. Poston & D.A. Giussani. Redox modulation of the fetal cardiovascular defence to hypoxaemia. J Physiol 588:4235-4247, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thaler, I., D. Manor, J. Itskovitz, S. Rottem, N. Levit, I. Timor-Tritsch & J.M. Brandes. Changes in uterine blood flow during human pregnancy. Am J Obstet Gynecol 162:121-125, 1990.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, A., Saint-Anne Dargassies, S. Etude neurologiques sur le nouveau-ne ct lc jeunc nourrisson. Masson, Paris, 1952.

    Google Scholar 

  • Thompson, D.W. The British Association for the Advancement of Science. Magnalia naturae; or, the greater problems of biology. Science 34:417-428, 1911.

    Google Scholar 

  • Thompson, D.W. Morphology and mathematics. Trans R Soc Edinb 50:857-895, 1915.

    Google Scholar 

  • Thompson, D.W. On growth and form. Cambridge University Press, Cambridge, MA, 1917.

    Google Scholar 

  • Thompson, D.W. “On growth and form. The complete revised edition. Republished in 1992.” (1942).

    Google Scholar 

  • Thompson, R.D. D'arcy Wentworth Thompson. In: Gillispie CC (ed) Dictionary or scientific, 1976.

    Google Scholar 

  • Thompson, L.P., K. Aguan, G. Pinkas & C.P. Weiner. Chronic hypoxia increases the NO contribution of acetylcholine vasodilation of the fetal guinea pig heart. Am J Physiol Regul Integr Comp Physiol 279:R1813-R1820, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, L.P., Y. Dong & L. Evans. Chronic hypoxia increases inducible NOS-derived nitric oxide in fetal guinea pig hearts. Pediatr Res 65:188-192, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, J.A., Sarr, O., Piorkowska, K., Gros, R., & Regnault, T.R. Low birth weight followed by postnatal over-nutrition in the guinea pig exposes a predominant player in the development of vascular dysfunction. The Journal of physiology, 592(24), 5429-5443, 2014.

    Google Scholar 

  • Thornton, J.G., J. Hornbuckle, A. Vail, D.J. Spiegelhalter, M. Levene & GRIT Study Group Infant wellbeing at 2 years of age in the Growth Restriction Intervention Trial (GRIT): multicentred randomised controlled trial. Lancet 364:513-520, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Thureen, P.J., K.A. Trembler, G. Meschia, E.L. Makowski & R.B. Wilkening. Placental glucose transport in heat-induced fetal growth retardation. Am J Physiol 263:R578-R585, 1992.

    CAS  PubMed  Google Scholar 

  • Timiras, P.S. Developmental physiology and aging. Macmillan Company, New York, 1972.

    Google Scholar 

  • Tissot van Patot, M.C., G. Ebensperger, M. Gassmann & A.J. Llanos. The hypoxic placenta. High Alt Med Biol 13:176-184, 2012.

    Article  Google Scholar 

  • Tzschoppe, A.A., E. Struwe, H.G. Dörr, T.W. Goecke, M.W. Beckmann, R.L. Schild & J. Dötsch. Differences in gene expression dependent on sampling site in placental tissue of fetuses with intrauterine growth restriction. Placenta 31:178-185, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Tzschoppe, A., E. Struwe, W. Rascher, H.G. Dörr, R.L. Schild, T.W. Goecke, M.W. Beckmann, B. Hofner, J. Kratzsch & J. Dötsch. Intrauterine growth restriction (IUGR) is associated with increased leptin synthesis and binding capability in neonates. Clin Endocrinol 74:459-466, 2011.

    Article  CAS  Google Scholar 

  • Unno, N., D.A. Giussani, W.K. Hing, X.Y. Ding, J.H. Collins & P.W. Nathanielsz. Changes in adrenocorticotropin and cortisol responsiveness after repeated partial umbilical cord occlusions in the late gestation ovine fetus. Endocrinology 138:259-263, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Unterscheider, J., Daly, S., Geary, M.P., Kennelly, M.M., McAuliffe, F.M., O’donoghue, K., Hunter, A., Morrison, J.J., Burke, G., Dicker, P., & Tully, E.C. Predictable progressive Doppler deterioration in IUGR: does it really exist?. American journal of obstetrics and gynecology, 209(6), 539-e1, 2013.

    Google Scholar 

  • Usher, R.H. Clinical and therapeutic aspects of fetal malnutrition. Pediatr Clin North Am 17:169-183, 1970.

    Article  CAS  PubMed  Google Scholar 

  • Usher, R. & F. McLean. Intrauterine growth of live-born Caucasian infants at sea level: Standards obtained from measurements in 7 dimensions of infants born between 25 and 44 weeks of gestation J Pediatr 74:901-910, 1969.

    Article  CAS  PubMed  Google Scholar 

  • Usher, R., F. McLean & K.E. Scott. Judgment of fetal age. II. Clinical significance of gestational age and an objective method for its assessment. Pediatr Clin North Am 13:835-848, 1966.

    Article  CAS  PubMed  Google Scholar 

  • Veille, J.C., R. Hanson, M. Sivakoff, H. Hoen & M. Ben-Ami. Fetal cardiac size in normal, intrauterine growth retarded, and diabetic pregnancies. Am J Perinatol 10:275-279, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Villamor, E., C.G. Kessels, K. Ruijtenbeek, R.J. van Suylen, J. Belik, J.G. de Mey & C.E. Blanco. Chronic in ovo hypoxia decreases pulmonary arterial contractile reactivity and induces biventricular cardiac enlargement in the chicken embryo. Am J Physiol Regul Integr Comp Physiol 287:R642-R651, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Villar, J. & J.M. Belizan. The timing factor in the pathophysiology of the intrauterine growth retardation syndrome. Obstet Gynecol Surv 37:499-506, 1982.

    Article  CAS  PubMed  Google Scholar 

  • Wallace, J.M., T.R. Regnault, S.W. Limesand, W.W. Hay, Jr. & R.V. Anthony. Investigating the causes of low birth weight in contrasting ovine paradigms. J Physiol 565:19-26, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walton, A. Notes on artificial insemination of sheep, cattle & horses. The Holborn Surgical Instrument Co. Ltd., London, 1936.

    Google Scholar 

  • Walton, A., Hammond, J. The Maternal Effects on Growth and Confirmation in Shire Horse-Shetland Pony Crosses. Proceedings of the Royal Society B: Biological Sciences 125 (840):311-335, 1938.

    Google Scholar 

  • Ward, J.W., Wooding, F.B.P., Fowden, A.L. Ovine fete-placental metabolism. J Physiol (Lond) 554:529-541, 2004.

    Google Scholar 

  • Warkany, J., B.B. Monroe & B.S. Sutherland. Intrauterine growth retardation. Am J Dis Child 102:249-279, 1961.

    CAS  PubMed  Google Scholar 

  • Weaver, L.T. In the balance: weighing babies and the birth of the infant welfare clinic. Bull Hist Med 84:30-57, 2010.

    Google Scholar 

  • Wells, J.C. Historical cohort studies and the early origins of disease hypothesis: making sense of the evidence. Proc Nutr Soc 68:179-188, 2009a.

    Article  PubMed  Google Scholar 

  • Wells, J.C. Thrift: a guide to thrifty genes, thrifty phenotypes and thrifty norms. Int J Obes 33:1331-1338, 2009b.

    Article  CAS  Google Scholar 

  • Wells, J.C. Maternal capital and the metabolic ghetto: An evolutionary perspective on the transgenerational basis of health inequalities. Am J Hum Biol 22:1-17, 2010.

    Article  PubMed  Google Scholar 

  • Wells, J.C. The thrifty phenotype: An adaptation in growth or metabolism? Am J Hum Biol 23:65-75, 2011.

    Article  PubMed  Google Scholar 

  • West Midlands Perinatal Institute West Midlands PEER-Perinatal KPI Report Q2 2010/11, 2011. Available at: www.pi.nhs.uk/pnm/maternitydata/Q2_2010-11_Perinatal_KPI_report.pdf

  • Wilkening, R.B. & G. Meschia. Fetal oxygen uptake, oxygenation, and acid-base balance as a function of uterine blood flow. Am J Physiol 244:H749-H755, 1983.

    CAS  PubMed  Google Scholar 

  • Williams, R.L. Intrauterine growth curves: intra- and international comparisons with different ethnic groups in California. Prev Med 4:163-172, 1975.

    Google Scholar 

  • Williams, R.L., Creasy, R.K., Cunningham, G.C., Hawes, W.E., Norris, F.D., & Tashiro, M. Fetal growth and perinatal viability in California. Obstetrics & Gynecology, 59(5), 624-634, 1982.

    Google Scholar 

  • Williams, S.J., M.E. Campbell, I.C. McMillen & S.T. Davidge. Differential effects of maternal hypoxia or nutrient restriction on carotid and femoral vascular function in neonatal rats. Am J Physiol Regul Integr Comp Physiol 288:R360-R367, 2005a.

    Article  CAS  PubMed  Google Scholar 

  • Williams, S.J., D.G. Hemmings, J.M. Mitchell, I.C. McMillen & S.T. Davidge. Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol 565:125-135, 2005b.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winick, M. (ed) Nutrition and development. Wiley, New York, 1972.

    Google Scholar 

  • Winick, M., Noble, A. Quantitative changes in DNA, RNA, and protein during prenatal and postnatal growth in the rat. Developmental Biology 12(3):451-466, 1965.

    Google Scholar 

  • Wollmann, H.A. Intrauterine growth restriction: definition and etiology. Horm Res 49 Suppl 2:1-6, 1998.

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization (WHO) Expert Group on Prematurity: final report [on a meeting held in] Geneva, 17–21 April 1950. World Health Organization, Geneva, 1950

    Google Scholar 

  • World Health Organization (WHO). World Health Statistics, Geneva, World Health Organization, 2012.

    Google Scholar 

  • Xu, Y., S.J. Williams, D. O’Brien & S.T. Davidge. Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J 20:1251-1253, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Xue, Q. & L. Zhang. Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C epsilon J Pharmacol Exp Ther 330:624-632, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yerushalmy, J., B.J. van den Berg, Erhardt, C.L. & Jacobziner, H Birth weight and gestation as indices of “immaturity”: neonatal mortality and congenital anomalies of the “immature”. Am J Dis Child 109:43-57, 1965.

    Article  CAS  PubMed  Google Scholar 

  • Zamudio, S., Y. Wu, F. Ietta, A. Rolfo, A. Cross, T. Wheeler, M. Post, N.P. Illsley & I. Caniggia. Human placental hypoxia-inducible factor-1alpha expression correlates with clinical outcomes in chronic hypoxia in vivo. Am J Pathol 170:2171-2179, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., M. Merialdi, L.D. Platt & M.S. Kramer. Defining normal and abnormal fetal growth: promises and challenges. Am J Obstet Gynecol 202:522-528, 2010

    Article  PubMed  PubMed Central  Google Scholar 

  • Zubrick, S.R., J.J. Kurinczuk, B.M. McDermott, R.S. McKelvey, S.R. Silburn & L.C. Davies. Fetal growth and subsequent mental health problems in children aged 4 to 13 years. Dev Med Child Neurol 42:14-20, 2000.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2018 The American Physiological Society

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Longo, L.D. (2018). Fetal Growth and Its Restriction. In: The Rise of Fetal and Neonatal Physiology . Perspectives in Physiology. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-7483-2_12

Download citation

Publish with us

Policies and ethics