Adaptation of the Fetal Pancreas to Maternal Diabetes

  • Piero P. Foà
Part of the Endocrinology and Metabolism book series (EAM, volume 2)


Webster’s dictionary defines a parasite as “one living at another’s expense” or as “an organism living in or on another living organism obtaining from it part or all of its organic nutrients and commonly exhibiting some degree of adaptive structural modification” (1). Either definition well describes the mammalian embryo: Aristotle (2) and Leonardo da Vinci (3) knew it and so did Michele Medici, a professor at the Pontifical University of Bologna, who, about 150 years ago, wrote that “the material destined for the nutrition of the fetus is carried by the uterine blood vessels to the placenta and, after being absorbed by the latter, is transported to the fetus thanks to the umbilical vessels… probably without direct commerce of blood” (4). We now know that the composition of this nutritional material is the product of maternal metabolism, suitably modified by a balance of apparently opposite endocrine forces: hyperinsulinism in the fed state, albeit associated with a degree of insulin resistance, and an increased secretion of counterregulatory hormones in the fasted state (5–8). As a result of this shifting equilibrium, the mother stores nutrients during the fed state and mobilizes them during periods of fasting, thus guaranteeing an adequate and constant supply to the growing conceptus. No matter how abundant and well balanced the nutrients, to use them the embryo must develop suitable enzymes, a process regulated partly by the quality and quantity of the nutrients themselves, partly by the manner in which the nutrients are obtained, and partly by hormones that become available as gestation progresses.


Gestational Diabetes Mellitus Diabetic Mother Maternal Diabetes Diabetic Pregnancy Fetal Macrosomia 
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  1. 1.
    Gove PB (1981) Webster’s Third International Dictionary of the English Language Unabridged. Merriam Co, Springfield MA.Google Scholar
  2. 2.
    Aristoteles of Stagira: On the generation of animals. Translated by Peck AL (1963) London, Cambridge MA.Google Scholar
  3. 3.
    Leonardo da Vinci, Quaderni di Anatomia. Cited by Castiglioni A (1948) Storia della Medicina Vol 1. Mondadori, Milano, p 363.Google Scholar
  4. 4.
    Medici M (1836) Manuale di Fisiologia. Tesi e Wambergher, Livorno, p 534.Google Scholar
  5. 5.
    Ward WK, Johnston CLW, Beard JC, Benedetti TG, Halter JB, Porte D Jr (1985) Insulin resistance and impaired insulin secretion in subjects with histories of gestational diabetes mellitus. Diabetes 34: 861 – 869.PubMedCrossRefGoogle Scholar
  6. 6.
    Toyoda N, Murata K, Sugiyama Y (1985) Insulin binding, glucose oxidation and methylglucose transport in isolated adipocytes from pregnant rats near term. Endocrinology 116: 998 – 1002.PubMedCrossRefGoogle Scholar
  7. 7.
    Lerario AC, Wajchenberg BL, El-Andere W, Ohnuma LY, Monaci J, San- kowsky M, Toledo E, Souza IT, Germek O (1985) Sequential studies of glucose tolerance and red blood cell insulin receptors in normal human pregnancy. Diabetes 34: 780 – 786.PubMedCrossRefGoogle Scholar
  8. 8.
    Hjøllund E, Pedersen O, Espersen T, Klebe JG (1986) Impaired insulin receptor binding and postbinding defects of adipocytes from normal and diabetic pregnant women. Diabetes 35: 598 – 603.PubMedCrossRefGoogle Scholar
  9. 9.
    Fiser RH Jr (1976) Glucose homeostasis during the perinatal period. In: New MI, Fiser RH Jr (eds) Diabetes and Other Disorders During Pregnancy and in the Newborn. Liss, New York, pp 33 – 50.Google Scholar
  10. 10.
    Baxter-Grillo D, Blázquez E, Grillo TAI, Sodoyez J-C, Sodoyez-Goffaux F, Foa PP (1981) Functional development of the pancreatic islets. In: Cooperstein SJ, Watkins D (eds) The Islets of Langerhans. Biochemistry, Physiology, and Pathology. Academic Press, New York, pp 35 – 49.Google Scholar
  11. 11.
    Ktorza A, Bihorean MT, Nurjhan N, Picon L, Girard J (1985) Insulin and glucagon during the perinatal period: secretion and metabolic effects on the liver. Biol Neonate 48: 204 – 220.PubMedCrossRefGoogle Scholar
  12. 12.
    Bernard C (1859) Recherches sur l’origine de la glycogénie dans la vie embryonnaire; nouvelle fonction du placenta. Compt Rend Séances Soc Biol (Paris) Kseries 3 ): 101 – 107.Google Scholar
  13. 13.
    Grillo TAI, Shima K (1966) Insulin content and enzyme histochemistry of the human fetal pancreatic islet. J Endocrinol 36: 151 – 158.PubMedCrossRefGoogle Scholar
  14. 14.
    Rastogi GK, Letarte J, Fraser TR (1970) Immunoreactive insulin content of 103 pancreases from foetuses of healthy mothers. Diabetologia 6: 445 – 446.PubMedCrossRefGoogle Scholar
  15. 15.
    Wirdnam PK, Milner RDG (1981) Quantitation of the B and A cell fractions in human pancreas from early fetal life to puberty. Early Hum Dev 5: 299 – 309.PubMedCrossRefGoogle Scholar
  16. 16.
    Stefan Y, Grasso S, Perrelet A, Orci L (1983) A quantitative immunofluorescent study of the endocrine cell populations in the developing human pancreas. Diabetes 32: 293 – 301.PubMedCrossRefGoogle Scholar
  17. 17.
    Milner RDG, Leach FN, Jack PMB (1975) Reactivity of the fetal islet. In: Sutherland HW, Stowers JM (eds) Carbohydrate Metabolism in Pregnancy and the Newborn. Churchill Livingstone, Edinburgh, pp 83 – 104.Google Scholar
  18. 18.
    Kawazu S, Kanazawa Y, Hayashi M, Ikeuchi M, Nakai T, Kosaka K (1980) Monolayer culture of human fetal and adult pancreas. Static and dynamic studies of insulin release in vitro. Horm Metab Res 12: 354 – 360.PubMedCrossRefGoogle Scholar
  19. 19.
    Andersson A, Grill V, Asplund K, Berne C, Agran A, Hellerstrom C (1975) Functional maturation of the pancreatic B cell. In: Camerini-Davalos RA, Cole HS (eds) Early Diabetes in Early Life. Academic Press, New York, pp 49 – 56.Google Scholar
  20. 20.
    Rahier J, Wallon J, Henquin J-C, (1981) Cell populations in the endocrine pancreas of human neonates and infants. Diabetologia 20: 540 – 546.PubMedCrossRefGoogle Scholar
  21. 21.
    Goldman H, Wong I, Patel YC (1982) Study of the structural and biochemical development of human fetal Islets of Langerhans. Diabetes 31: 897 – 902.PubMedCrossRefGoogle Scholar
  22. 22.
    Clark A, Grant AM (1983) Quantitative morphology of endocrine cells in human fetal pancreas. Diabetologia 25: 31 – 35.PubMedCrossRefGoogle Scholar
  23. 23.
    Grasso S, Palumbo G, Messina A, Mazzone D, Rutano G (1975) Human maternal and fetal serum insulin and growth hormone response to glucose and leucine. In: Camerini-Dávalos RA, Cole MS (eds) Early Diabetes in Early Life. Academic Press, New York, pp 537 – 540.Google Scholar
  24. 24.
    Sodoyez-Goffaux F, Sodoyez J-C (1976) Effects of intermittent hyperglycemia in pregnant rats on the functional development of the pancreatic B cells of their offspring. Diabetologia 12: 73 – 76.PubMedCrossRefGoogle Scholar
  25. 25.
    Sodoyez-Goffaux F, Sodoyez J-C, Devos CJ (1979) Insulin secretion and metabolism during the perinatal period in the rat. Evidence for a placental role in fetal hyperinsulinism. J Clin Invest 63:1095–1102.Google Scholar
  26. 26.
    Oliven A, King KC, Kalhan SC (1986) Gastrointestinal enhanced insulin release in response to glucose in newborn infants. J. Pediatr Gastroenterol Nutr 5: 220 – –225.PubMedCrossRefGoogle Scholar
  27. 27.
    Lambert AE, Orci L, Renold AE (1970) Some factors controlling diffentiation and/or modulation of rat pancreatic islet cells. In: Camerini-Dávalos RA, Cole HS (eds) Early Diabetes. Academic Press, New York, pp 35 – 43.Google Scholar
  28. 28.
    Lucas A (1986) Breastfeeding and gut hormones. In: Filer LJ Jr, Fomon SJ (eds) The Breastfed Infant: A Model of Performance. 91st Ross Conf Ped Res, Ross Laboratories, Columbus OH, pp 73 – 87.Google Scholar
  29. 29.
    Blázquez E, Simon FA, Blazques M, Foà PP (1974) Changes in serum growth hormone levels from fetal to adult age in the rat. Proc Soc Exp Biol Med 147: 780 – 783.PubMedCrossRefGoogle Scholar
  30. 30.
    Ashton IK, Zapf J, Einschenk TJ, MacKenzie IZ (1985) Insulin-like growth factors (IGF) 1 and 2 in human fetal plasma and relationship to gestational age and fetal size during midpregnancy. Acta Endocrinol (Copenh) 110: 558 – 563.Google Scholar
  31. 31.
    Bennett A, Wilson DM, Lin F, Nagashima R, Rosenfeld RG, Hintz RL (1983) Levels of insulin-like growth factors I and II in human cord blood. J Clin Endocrinol Metab 57: 609 – 612.PubMedCrossRefGoogle Scholar
  32. 32.
    Lin K-S, Wang C-Y, Mills N, Gyves M, Ilan J (1985) Insulin-related genes expressed in human placenta from normal and diabetic pregnancies. Proc Natl Acad Sci USA 82: 3868 – 3870.CrossRefGoogle Scholar
  33. 33.
    Underwood LE, D’Ercole AJ (1984) Insulin and insulin-like growth factors/ somatomedins in fetal and neonatal development. J Clin Endocrinol Metab 13: 69 – 89.CrossRefGoogle Scholar
  34. 34.
    Chernausek SD, Chatelain PG, Svoboda ME, Underwood LE, Van Wyk JJ (1985) Efficient purification of somatomedin C/insulin-like growth factor I using immunoaffinity chromatography. Biochem Biophys Res Commun 126: 282 – 288.PubMedCrossRefGoogle Scholar
  35. 35.
    Hill DJ, Milner RDG (1985) Insulin as a growth factor. Pediatr Res 19: 879 – 886.PubMedCrossRefGoogle Scholar
  36. 36.
    Sheppard MS, Bala RM (1986) Profile of serum immunoreactive insulin-like growth factor I during gestation in Wistar rats. Can J Physiol Pharmacol 64: 521 – 524.PubMedCrossRefGoogle Scholar
  37. 37.
    Fant M, Munro H, Moses AC (1986) An autocrine/paracrine role for insulinlike growth factors in the regulations of human placental growth. J Clin Endocrinol Metab 63: 499 – 505.PubMedCrossRefGoogle Scholar
  38. 38.
    Freemark M, Comer M, Handwergen S (1986) Placental lactogen and GH receptors in sheep liver: striking differences in ontogeny and function. Am J Physiol 251. E328 – E333.PubMedGoogle Scholar
  39. 39.
    Blázquez E, Rubalcava B, Montesano R, Orci L, Unger RH (1976) Development of insulin and glucagon binding and the adenylate cyclase response in liver membranes of the prenatal, postnatal and adult rat: evidence of glucagon “resistance”. Endocrinology 98: 1014 – 1023.PubMedCrossRefGoogle Scholar
  40. 40.
    Thorsson AV, Hintz RL (1977) Insulin receptors in the newborn. Increase in receptor affinity and number. N Engl J Med 297: 908 – 912.PubMedCrossRefGoogle Scholar
  41. 41.
    Kappy MS, Plotnick LP, Milley JR, Rosenberg A, Molteni RA, Jones MD Jr,Simmons MA (1981) Ontogeny of erythrocyte insulin binding in the sheep. Endocrinology 109: 611 – 617.PubMedCrossRefGoogle Scholar
  42. 42.
    Vinicor F, Kiedrowski L (1982) Characterization of the hepatic receptor for insulin in the perinatal rat. Endocrinology 110: 782 – 790.PubMedCrossRefGoogle Scholar
  43. 43.
    Ganguli S, Sinha M, Sperling MA (1984) Ontogeny of insulin and glucagon receptors and the adenylate cyclase system in guinea pig liver. Pediatr Res 18: 558 – 565.PubMedCrossRefGoogle Scholar
  44. 44.
    Morriss FH Jr, Tuchman C, Crandell SS, Riddle LM, Fitzgerald BJ, West MS (1986) Ontogeny of ovine fetal liver and kidney plasma membrane insulin receptors and fetal growth. Proc Soc Exp Biol Med 181: 24 – 32.PubMedCrossRefGoogle Scholar
  45. 45.
    Unterman T, Goewert RR, Baumann G, Freinkel N (1986) Insulin receptors in embryo and extra-embryonic membranes of early somite rat conceptus. Diabetes 35: 1193 – 1199.PubMedCrossRefGoogle Scholar
  46. 46.
    Greengard O (1975) Enzymatic differentiation during hepatic development. In: Camerini-Dávalos RA, Cole HS (eds) Early Diabetes in Early Life. Academic Press, New York pp 9 – 14.Google Scholar
  47. 47.
    Shelley HJ, Bassett JM, Milner RDG (1975) Control of carbohydrate metabolism in the fetus and newborn. Br Med Bull 31: 37 – 43.PubMedGoogle Scholar
  48. 48.
    Cuezva JM, Valcarce C, Medina JM (1985) Substrates availability for maintenance of energy homeostasis in the immediate postnatal period of the fasted newborn rat. In: Jonas CT, Nathanielsz PW (eds) The Physiological Development of the Fetus and Newborn. Academic Press, New York pp 63 – 69.Google Scholar
  49. 49.
    Räiha NCR (1979) Hormonal regulation of perinatal enzyme differentiation in the mammalian liver. In: Elliott K, O’Connor M (eds) Pregnancy Metabolism, Diabetes and the Fetus. Ciba Found Symp 63, Excerpta Med, Amsterdam pp 137 – 160.Google Scholar
  50. 50.
    Ruiz-Bravo N, Ernest MJ (1985) Multihormonal control of tyrosine aminotransferase activity in developing rat liver. Endocrinology 116: 2489 – 2496.PubMedCrossRefGoogle Scholar
  51. 51.
    Denne SC, Kalhan SC (1986) Glucose carbon recycling and oxidation in human newborns. Am J Physiol 251: E71 - E77.PubMedGoogle Scholar
  52. 52.
    Helman AM, Giraud P, Nicolaidis S, Oliver C, Assan R (1983) Glucagon release after stimulation of the lateral hypothalamic area in rats: predominant 0-ad- renergic transmission and involvement of endorphin pathways. Endocrinology 113: 1 - 6.PubMedCrossRefGoogle Scholar
  53. 53.
    Stark RI, Wardlaw SL, Daniel SS (1986) Characterization of plasma β-en- dorphin immunoreactivity in the fetal lamb: effects of gestational age and hypoxia. Endocrinology 119: 755 – 761.PubMedCrossRefGoogle Scholar
  54. 54.
    Blazquez E, Lipshaw LA, Blázquez M, Foa PP (1975) The synthesis and release of insulin in fetal, nursing and young adult rats: studies in vivo and in vitro. Pediatr Res 9: 17 – 25.Google Scholar
  55. 55.
    Begum N, Tepperman HM, Tepperman J (1985) Insulin-induced internalization and replacement of insulin receptors in adipocytes of rats adapted to fat feeding. Diabetes 34: 1272 – 1277.PubMedCrossRefGoogle Scholar
  56. 56.
    Schwartz R, Susa J (1980) Fetal macrosomia. Animal models. Diabetes Care 3: 430 – 432.PubMedCrossRefGoogle Scholar
  57. 57.
    Freinkel N, Lewis NJ, Johnson R, Swenne R, Bone A, Hellerstrom C (1984) Differential effects of age versus glycemic stimulation on the maturation of insulin stimulus-secretion coupling during culture of fetal rat islet. Diabetes 33: 1028 – 1038.PubMedCrossRefGoogle Scholar
  58. 58.
    Russell G, Dawodu AK, Shennan AT (1984) Glucose homeostasis in the heavy- for-date neonate. In: Sutherland HW, Stowers JM (eds) Carbohydrate Metabolism in Pregnancy and the Newborn. Churchill Livingstone, Edinburgh, pp 150 – 151.Google Scholar
  59. 59.
    Cella SG, Locatelli V, de Gennaro V, Puggioni R, Pintor C, Müller EE (1985) Human pancreatic growth hormone (GH)-releasing hormone stimulates GH synthesis and release in infant rats. An in vivo study. Endocrinology 116: 574 – 577.PubMedCrossRefGoogle Scholar
  60. 60.
    Domenech M, Gruppuso PA, Susa JB, Schwartz T (1985) Induction in utero of hepatic glucose 6-phosphatase by fetal hypoinsulinemia. Biol Neonate 47: 92 – 98.PubMedCrossRefGoogle Scholar
  61. 61.
    Szabo AJ, Szabo O (1974) Placental free-fatty-acid transfer and fetal adipose tissue development: an explanation of fetal adiposity in infants of diabetic mothers. Lancet 11: 498 – 499.CrossRefGoogle Scholar
  62. 62.
    Freinkel N (1980) The Banting Lecture 1980: Of pregnancy and progeny. Diabetes 29: 1023 – 1035.CrossRefGoogle Scholar
  63. 63.
    Metzger BE, Phelps RL, Freinkel N, Navikas IA (1980) Effects of gestational diabetes on diurnal profiles of plasma glucose, lipids, and individual amino acids. Diabetes Care 3: 402 – 409.PubMedGoogle Scholar
  64. 64.
    Freinkel N, Dooley SL, Metzger BE (1985) Care of the pregnant woman with insulin-dependent diabetes mellitus. N Engl J Med 313: 96 – 101.PubMedCrossRefGoogle Scholar
  65. 65.
    Freinkel N, Metzger BE, Phelps RL, Simpson JL, Martin AO, Radvany R, Ober C, Dooley SL, Depp RO, Belton A (1986) Gestational diabetes mellitus: a syndrome with phenotypic and genotypic heterogeneity. Horm Metab Res 18: 427 – 430.PubMedCrossRefGoogle Scholar
  66. 66.
    Heding LG, Persson B, Stangenberg M (1980) B-cell function in newborn infants of diabetic mothers. Diabetologia 19: 427 – 432.PubMedCrossRefGoogle Scholar
  67. 67.
    Tallarigo L, Giampietro O, Penno G, Miccoli R, Gregori G, Navalesi R (1986) Relation of glucose tolerance to complications of pregnancy in nondiabetic women. N Engl J Med 315: 984 – 992.CrossRefGoogle Scholar
  68. 68.
    Philipps AF, Rosenkrantz TS, Grunnet ML, Connolly ME, Porte PJ, Raye JR (1986) Effects of fetal insulin secretory deficiency on metabolism in fetal lamb. Diabetes 35: 964 – 972.PubMedCrossRefGoogle Scholar
  69. 69.
    Freinkel N, Metzger BE (1979) Pregnancy as a tissue culture experience: the critical implications of maternal metabolism for fetal development. In: Elliott K, O’Connor M (eds) Pregnancy Metabolism, Diabetes and the Fetus. Ciba Found Symp 63, Excerpta Med, Amsterdam pp 3 – 28.Google Scholar
  70. 70.
    Pedersen J (1952) Diabetes and Pregnancy. Blood Sugar of Newborn Infants. A thesis. Danish Science Press, Copenhagen.Google Scholar
  71. 71.
    Pedersen J (1967) The pregnant diabetic and her newborn. Problems and management. Munksgaard, Copenhagen, pp 219.Google Scholar
  72. 72.
    Dubrueil G, Anderodias J (1920) Ilôts de Langerhans géants chez un nouveauné issu de mère glycosurique. Compt Rend Séances Soc Biol (Paris) 83: 1490 – 1493.Google Scholar
  73. 73.
    Van Assche FA (1975) The fetal endocrine pancreas. In: Sutherland HW, Stowers JM (eds) Carbohydrate Metabolism in Pregnancy and the Newborn. Churchill Livingstone, Edinburgh, pp 68 – 82.Google Scholar
  74. 74.
    Milner RDG, Wirdnam, PK, Tsanakas Y (1981) Quantitative morphology of B, A, D and PP cells in infants of diabetic mothers. Diabetes 30: 271 – 274.PubMedCrossRefGoogle Scholar
  75. 75.
    v Dorsche HH, Reiher H, Hahn H-J (1984) Quantitativ-histolgische Unter- suchugen des fetalen menschlichen Pankreas von stoffwechselgesunden Frauen und insulinabhängingen Diabetikerinnen. Acta Anat 118: 139 – 143.CrossRefGoogle Scholar
  76. 76.
    Hill DE (1979) Effect of insulin on fetal growth. In: Merkatz IR, Adam PAJ (eds) The Diabetic Pregnancy. A Perinatal Perspective. Grune & Stratton, New York, pp 155 – 165.Google Scholar
  77. 77.
    Heding LG, Persson B, Stangenberg M (1980) B-cell function in newborn infants of diabetic mothers. Diabetologia 19: 427 – 432.PubMedCrossRefGoogle Scholar
  78. 78.
    Reiher H, Fuhrmann K, Noack S, Besch W, Hahn H-J (1984) The in vitro insulin secretion of human fetal pancreatic slices from diabetic and non-diabetic women. A methodical study. Exp Clin Endocrinol 83: 110 – 112.PubMedCrossRefGoogle Scholar
  79. 79.
    Freinkel N, Metzger BE, Phelps RL, Dooley SL, Ogata ES, Radvany RM, Belton A (1985) Gestational diabetes mellitus. Heterogeneity of maternal age, weight, insulin secretion, HLA antigen and islet cell antibodies and the impact of maternal metabolism in pancretic B-cell and somatic development in the offspring. Diabetes 34 (suppl 2): 1 – 7.PubMedCrossRefGoogle Scholar
  80. 80.
    Shima K, Price S, Foà PP (1966) Serum insulin concentration and birth weight in human infants. Proc Soc Exp Biol Med 121: 55 – 59.PubMedCrossRefGoogle Scholar
  81. 81.
    Lacy PE, Wright PH (1965) Allergic interstitial pancreatitis in rats injected with guinea pig anti-insulin serum. Diabetes 14: 634 – 642.PubMedGoogle Scholar
  82. 82.
    Klöppel G, Freytag G, Bommer G (1972) Enzymehistochemical studies on the pancreatic islets in mice injected with anti-insulin serum. Diabetologia 8: 19 – 28.PubMedCrossRefGoogle Scholar
  83. 83.
    Roth J, Kahn CR, King GL, Meggesi K (1979) Receptors in infants of diabetic mothers. In: Cornblath M, Kaye R, Little B, Segal S (eds) Workshop on Fetal Development in the Infant of the Diabetic Mother. Juvenile Diabetes Found pp 28 – 40.Google Scholar
  84. 84.
    Haust MD (1981) Maternal diabetes mellitus. Effects on the fetus and placenta. In: Naeye RL, Kissane JM, Kaufman N (eds) Perinatal Diseases. Williams & Wilkins, Baltimore, pp 201 – 285.Google Scholar
  85. 85.
    Phillips LS, Vassilopoulou-Sellin R, Reichard LA (1979) Nutrition and somatomedin. VIII. The “somatomedin inhibitor” in diabetic rat serum is a general inhibitor of growing cartilage. Diabetes 28: 919 – 924.PubMedCrossRefGoogle Scholar
  86. 86.
    Sadler TW, Phillips LS, Balkan W, Goldstein S (1986) Somatomedin inhibitors from diabetic rat serum alter growth and development of mouse embryos in culture. Diabetes 35: 861 – 865.PubMedCrossRefGoogle Scholar
  87. 87.
    Cornblath M, Pildes RS, Warmer RA (1970) Infants of the diabetic mother. In: Camerini-Dávalos RA, Cole HS (eds): Early Diabetes. Academic Press, New York, pp 241 – 252.Google Scholar
  88. 88.
    Neufeld ND, Corbo LM (1986) Insulin-receptor development in normal and diabetic pregnancies. Role of membrane fluidity. Diabetes 35: 1020 – 1026.PubMedCrossRefGoogle Scholar
  89. 89.
    Gewolb IH, Merdian W, Warshaw JB, Enders AC (1986) Fine structural abnormalities of the placenta in diabetic rats. Diabetes 35: 1254 – 1261.PubMedCrossRefGoogle Scholar
  90. 90.
    Heinze E, Brenner R, Nguyen-Thi Ch, Vetter U, Leupold D, Pohlandt F (1986) Skeletal growth in fetal rats. Effects of glucose and amino acids. Diabetes 35: 222 – 227.PubMedCrossRefGoogle Scholar
  91. 91.
    Buchanan TA, Schemmer JK, Freinkel N (1986) Embryotoxic effects of brief maternal insulin-hypoglycemia during organogenesis in the rat. J Clin Invest 78: 643 – 649.PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    Fuhrmann K, Reiher H, v Dorsche HH (1985) Hyperinsulinemia in the fetus of the diabetic mother. Is prevention possible? In: Serano-Rios M, Lefebvre PJ (eds) Diabetes 1985. Excerpta Med, Amsterdam, pp 598 – 603.Google Scholar
  93. 93.
    Farquhar JW (1969) The infant of the diabetic mother. Postgrad Med J 45: 806 – 811.Google Scholar
  94. 94.
    Shah MPK, Farquhar JW (1975) Children of diabetic mothers. Subsequent weight. In: Camerini-Dávalos RA, Cole HS (eds), Early Diabetes in Early Life. Academic Press, New York, pp 587 – 593.Google Scholar
  95. 95.
    Bihoreau MT, Ktorza A, Kinebanyan MF, Picon L (1986) Impaired glucose homeostasis in adult rats from hyperglycemic mothers. Diabetes 35: 979 – 984.PubMedCrossRefGoogle Scholar
  96. 96.
    Abbott WGH, Thuillez P, Howard BV, Salans LB, Cushman SW, Reaven GW, Foley JE (1986) Body composition, adipocyte size, free fatty acid concentration and glucose tolerance in children of diabetic pregnancies. Diabetes 35: 1077 – 1080.PubMedCrossRefGoogle Scholar

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  • Piero P. Foà

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