The role of free radicals and membrane lipids in diabetes-induced congenital malformations

Journal of the Society for Gynecologic Investigation

Volumn 5, Issue 4, 1998, Pages 178-187

  Reece, E Albert ^a,b   Homko, Carol J ^a,b   Wu, Ying King ^a,b   Wiznitzer, Arnon ^a,b  

^a Division of Maternal Fetal Medicine   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Arachidonic acid; Diabetes; Embryopathy; Preconception counseling; Pregnancy

Indexed keywords

ARTICLE; CONGENITAL MALFORMATION; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; HEALTH PROGRAM; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; KETOACIDOSIS; MATERNAL DIABETES MELLITUS; OXIDATION REDUCTION REACTION; PRENATAL CARE; PRIORITY JOURNAL; TERATOGENICITY; TREATMENT PLANNING;

ABNORMALITIES; ANIMALS; FEMALE; FREE RADICALS; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIA; INOSITOL; MEMBRANE LIPIDS; PREGNANCY; PREGNANCY IN DIABETICS; YOLK SAC;

EID: 0031874953     PISSN: 10715576     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1071-5576(98)00008-2     Document Type: Article

References (84)

1. Kitzmiller J.L., Cloherty J.P., Younger M.D., et al. Diabetic pregnancy and perinatal morbidity. Am J Obstet Gynecol. 131:1978;560-580.
2. Hoet JJ, Beard RW. Clinical perspectives in the care of the pregnant diabetic patient. In: Pregnancy metabolism, diabetes and the fetus. Ciba Foundation Series 63. Excerpta Medica 1979:283-300.
3. Reece E.A., Hobbins J.C. Diabetic embryopathy Pathogenesis, prenatal diagnosis, and prevention . Obstet Gynecol Surv. 41:1986;325-335.
4. Horton W.E. Jr, Sadler T.W. Effects of maternal diabetes on early embryogenesis alterations in morphogenesis produced by the ketone body, beta-hydroxybutyrate . Diabetes. 32:1983;610.
5. Kalter H., Warkany J. Congenital malformations etiologic factors and their role in prevention . N Engl J Med. 308:1983;424-431.
6. Freinkel N., Cockroft D.L., Lewis N.J., et al. The 1986 McCollum Award Lecture fuel-mediated teratogenesis during early organogenesis . Am J Clin Nutr. 44:1986;986-995.
7. Baker L., Egler J.M., Klein S.H., Goldman A.S. Meticulous control of diabetes during organogenesis prevents congenital lumbosacral defects in rats. Diabetes. 30:1981;955.
8. Cockroft D.L., Coppola P.T. Teratogenic effects of excess glucose on head-fold rat embryos in culture. Teratology. 16:1977;141-146.
9. Freinkel N. Diabetic embryopathy and fuel-mediated organ teratogenesis lessons from animal models . Horm Metab Res. 20:1988;473-475.
10. Reece E.A., Pinter E., Leranth C.Z., et al. Ultrastructural analysis of malformations of the embryonic neural axis induced by in vitro hyperglycemic conditions. Teratology. 32:1985;363-373.
11. Rose B.I., Graff S., Spencer R., et al. Major congenital anomalies in infants and glycosylated hemoglobin levels in insulin-requiring diabetic mothers. J Perinatol. 8:1988;309-311.
12. Key T.C., Giuffrida R., Moore T.R. Predictive value of early pregnancy glycohemoglobin in the insulin-treated diabetic patient. Am J Obstet Gynecol. 156:1987;1096-2000.
13. Lucas M.J., Leveno K.J., Williams L., et al. Early pregnancy glycosylated hemoglobin, severity of diabetes, and fetal malformations. Am J Obstet Gynecol. 161:1989;426-431.
14. Miller E., Hare J.W., Cloherty J.P., et al. Elevated maternal hemoglobin A1c in early pregnancy and major congenital anomalies in infants of diabetic mothers. N Engl J Med. 304:1988;1331-1333.
15. Ylinen K., Aula P., Stenman U.H., Desaniemi-Kuokkanen T., Teramo K. Risk of minor and major fetal malformations in diabetics with high haemoglobin A1c values in early pregnancy. BMJ. 289:1984;345-346.
16. Leslie R.D.G., Pyke D.A., John P.N., White J.M. Hemoglobin A1 in diabetic pregnancy. Lancet. 2:1978;958-959.
17. Midovnik M., Mimouni F., St. John Dignan P., et al. Major Malformations in infants of IDDM women vasculopathy and early first-trimester poor glycemic control . Diabetes Care. 11:1988;713-718.
18. Greene M.F., Hare J.W., Cloherty J.P., Benacevraf B.R., Soeldner J.S. First-trimester hemoglobin A, and risk for major malformation and spontaneous abortion in diabetic pregnancy. Teratology. 39:1989;225-231.
19. Rosenn B., Miodovnik M., Combs C.A., Khoury J., Siddiqi T.A. Glycemic thresholds for spontaneous abortion and congenital malformations in insulin-dependent diabetes mellitus. Obstet Gynecol. 84:1994;15-20.
20. Smoak A.W., Sadler T.W. Embryopathic effects of short-term exposure to hypoglycemia in mouse embryos in vitro. Am J Obstet Gynecol. 163:1990;619-624.
21. Akazawa M., Akazawa S., Hasimoto M. Effects of brief exposure to insulin-induced hypoglycemic serum during organogenesis in rat embryo culture. Diabetes. 38:1989;1573-1578.
22. Buchanan T.A., Schemmer J.K., Freinkel N. Embryotoxic effects of brief maternal insulin-hypoglycemic serum during organogenesis in rat embryo culture. J Clin Invest. 78:1986;643-649.
23. Kimmerle R., Heinemann L., Delecki A., Berger M. Severe hypoglycemia incidence and predisposing factors in 85 pregnancies of Type I diabetic women. Diabetes Care. 15:1992;1034-1037.
24. Rayburn W., Piehl E., Jacober S., Schork A., Ploughaman L. Severe hypoglycemia during pregnancy Its frequency and predisposing factors in diabetic women . Int J Gynaecol Obstet. 24:1986;263-268.
25. Impastato D.J., Gabriel A.R., Lardaro E.H. Electric and insulin shock therapy during pregnancy. Dis Nerv Syst. 25:1964;542-546.
26. Mills J.L., Knopp R.H., Simpson J.L., et al. The NICHD Diabetes in Early Pregnancy Study lack of relation of increased malformation rates in infants of diabetic mothers to glycemic control during organogenesis . N Engl J Med. 318:1988;671-676.
27. Pedersen J. The pregnant diabetic and her newborn, 2nd ed. 1977;Williams and Wilkins, Baltimore.
28. Kitzmiller J.L., Gavin L.A., Gin G.D., et al. Preconception management of diabetes continued through early pregnancy prevents the excess frequency of major congenital anomalies in infants of diabetic mothers. JAMA. 265:1991;731-736.
29. Freinkel N., Cockroft D.L., Lewis N.J., et al. The 1986 McCollum Award Lecture. Fuel-mediated teratogenesis during early organogenesis the effects of increased concentrations of glucose, ketones, or somatomedin inhibitor during rat embryo culture . Am J Clin Nutr. 44:1986;986-995.
30. Horton W.E. Jr, Sadler T.W., Hunter E.S. III. Effects of hyperketonemia on mouse embryonic and fetal glucose metabolism in vitro. Teratology. 31:1985;227-233.
31. Lewis N.J., Akazawa S., Freinkel N. Teratogenesis from β-hydroxybutyrate during organogenesis in rat embryo organ culture and enhancement by subteratogenic glucose. Diabetes. 32:(Suppl):1983;11A.
32. Rizzo T., Metzger B.E., Burns W.J. Correlations between antepartum maternal metabolism and intelligence of offspring. N Engl J Med. 325:1991;911-916.
33. Sadler T.W., Phillips L.S., Balkan W., et al. Somatomedin inhibitors from diabetic rat serum alter growth and development of mouse embryos in culture. Diabetes. 35:1986;861.
34. Hunter E.S., Phillips L.S., Goldstein S., et al. Altered visceral yolk sac function produced by a low-molecular-weight somatomedin inhibitor. Teratology. 43:1991;331-340.
35. Landaeur W. Is insulin a teratogen? Teratology. 5:1972;129-135.
36. Eriksson U.J. Diabetes in pregnancy effects of post-implantation embryos . Isr J Med Sci. 27:1991;478-486.
37. Beckman D.A., Koszalka T.R., Jensen M., Brent R.L. Experimental manipulation of the rodent visceral yolk sac. Teratology. 41:1990;395-404.
38. Brent R.L., Beckman D.A., Jensen M., Koszalka T.R. Experimental yolk sac dysfunction as a model for studying nutritional disturbances in the embryo during early organogenesis. Teratology. 41:1990;405-413.
39. Pinter E., Reece E.A., Leranth C.Z., Sanyal M.K., Hobbins J.C., Mahoney M.J., Naftolin F. Yolk sac failure in embryopathy due to hyperglycemia ultrastructural analysis of yolk sac differentiation associated with embryopathy in rat conceptuses under hyperglycemic conditions . Teratology. 33:1986;73-84.
40. Reece E.A., Pinter E., Leranth C.Z. Yolk sac failure in embryopathy due to hyperglycemia horseradish peroxidase uptake in the assessment of yolk sac function . Obstet Gynecol. 74:1989;755-762.
41. Reece E.A., Pinter E., Homko C., Wu Y.-K., Naftolin F. The yolk sac theory closing the circle on why diabetes-associated malformations occur . J Soc Gynecol Invest. 1:1994;3-13.
42. Beck F., Lloyd J.B., Griffiths A. Lysosmal enzyme inhibitation by trypan blue a theory of teratogenesis . Science. 101:1967;461-478.
43. Hod M., Star S., Passonnequ J.V., et al. Effect of hyperglycemia on sorbitol and myo-inositol content of cultured rat conceptus failure of aldose reductase inhibitors to modify myo-inositol depletion and dysmorphogenesis . Biochem Biophys Res Commun. 140:1986;974-980.
44. Hod M., Star S., Passonnequ J.V., et al. Glucose-induced dysmorphogenesis in the cultured rat conceptus prevention by supplementation with myo-inositol . Isr J Med Sci. 26:1990;541-544.
45. Reece E.A., Khandelwal M., Wu Y.K., Borenstein M. Dietary intake of myo-inositol reduces the incidence of embryopathy in offspring of diabetic rats. Am J Obstet Gynecol. 176:1997;790-797.
46. Khandelwal M., Wu Y.K., Borenstein M., Reece E.A. Dietary phospholipid therapy, hyperglycemia-induced membrane changes and associated diabetic embryopathy. Teratology. 57:1998;79-84.
47. Sussman I., Matschinsky F.M. Diabetes affects sorbitol and myo-inositol levels of neuroectodermal tissue during embryogenesis. Diabetes. 37:1988;974-981.
48. Goldman A.S., Baker L., Piddington R., et al. Hyperglycemia-induced teratogenesis is mediated by a functional deficiency of arachidonic acid. Proc Natl Acad Sci USA. 82:1985;8827-8831.
49. Pinter E., Reece E.A., Ogburn P.L. Jr, et al. Fatty acid content of yolk sac and embryo in hyperglycemia-induced embryopathy and effect of arachidonic acid supplementation. Am J Obstet Gynecol. 159:1988;1484-1490.
50. Reece E.A., Wu Y.K., Borenstein M., Aksoy M., Sloskey G. Dietary polyunsaturated fatty acid (PUFA) prevents malformations in offspring. Am J Obstet Gynecol. 175:1996;818-823.
51. Kay E.D., Goldman A.S., Daniel J.C. Arachidonic acid reversal of phenytoin-induced neural tube and craniofacial defects in vitro in mice. J Craniofac Genet Dev Biol. 8:1988;135-141.
52. Eriksson U.J. Diabetes in pregnancy effects on post implantation embryos . Isr J Med Sci. 27:1991;478-486.
53. Eriksson U.J., Hakan Borg L.A., Forsberg H., Styrud J. Diabetic Embryopathy studies with animal and in vitro models . Diabetes. 40:(Suppl 2):1991;94-98.
54. Hagay Z.J., Weiss I., Zusman I., et al. Prevention of diabetic embryopathy by over expression of the free radical scavenging enzyme superoxide dismutase in transgenic mouse embryos. Am J Obstet Gynecol. 173:1995;1036-1041.
55. Eriksson U.J., Borg L.A.H., Hagay Z., Groner Y. Increased superoxide dismutase (SOD) activity in embryos of transgenic mice protects from the teratogenic effects of a diabetic environment. Diabetes. 42:(Suppl 1):1993;85A.
56. Sivan E., Wu Y.K., Homko C.J., Reece E.A. Dietary vitamin E prophylaxis and diabetic embryopathy morphological, biochemical and milecular analyses . Am J Obstet Gynecol. 175:1996;793-799.
57. Wiznitzer A, Hershkovitz R, Mimmom E, et al. The antioxidant lipioc acid prevents malformations in offspring of diabetic rats (abstract). Society of P.O., Hawaii, Am J Obstet Gynecol 1966:174:310.
58. Cagliero E., Forsberg H., Sala R., Lorenzi M., Eriksson U.J. Maternal diabetes induces increased expression of extracellular matrix components in rat embryos. Diabetes. 42:1993;975-980.
59. Lee A.T., Plump A., DeSimone C., Cerami A., Bucala R. A role for DNA mutations in diabetes-associated teratogenesis in transgenic embryos. Diabetes. 44:1995;20-24.
60. Reece E.A., Wiznitzer A., Homko C.J., Hagay Z., Wu Y.K. Synchronization of the factors critical for diabetic teratogenesis an in vitro model . Am J Obstet Gynecol. 174:1996;1284-1288.
61. Eriksson U.J., Dahlstrom V.E., Lithell H.O. Diabetes in pregnancy influence of genetic background and maternal diabetic state on the incidence of skeletal malformations in the fetal rat . Acta Endocrinol. 277:1986;66-73.
62. Eriksson U.J. Importance of genetic predisposition and maternal environment for the occurrence of congenital malformations in offspring of diabetic rats. Teratology. 37:1988;365-374.
63. Comess L.J., Bennett P.H., Burch T.A., Miller M. Congenital anomalies and diabetes in the Pima Indians of Arizona. Diabetes. 18:1969;471-477.
64. Chung C.S., Myrianthopoulos N.C. Factors affecting risks of congenital malformations. II. Effect of maternal diabetes on congenital malformations. Birth Defects. 11:1975;23.
65. McCarter C., Kessler I.I., Cromstock G.W. Diabetes mellitus a teratogen or coteratogen . Am J Epidem. 123:1987;195-205.
66. Fuhrmann K., Reiher H., Semmler K., et al. Prevention of congenital malformations in infants of insulin-dependent diabetic mothers. Diabetes Care. 6:1983;219-223.
67. Kitzmiller J.L., Gavin L.A., Gin G.D., et al. Preconception management of diabetes continued through early pregnancy prevents the excess frequency of major congenital anomalies in infants of diabetic mothers. JAMA. 265:1991;731-736.
68. Mills J.L., Knopp R.H., Simpson J.L., et al. Lack of relation of increased malformation rates in infants of diabetic mothers to glycemic control during organogenesis. N Engl J Med. 318:1988;671-676.
69. Goldman J.A., Dicker D., Feldberg D., et al. Pregnancy outcome in patients with insulin-dependent diabetes mellitus with preconceptional diabetic control a comparative study . Am J Obstet Gynecol. 155:1986;293-297.
70. Damm P., Molsted-Pederson L. Significant decrease in congenital malformations in newborn infants of an unselected population of diabetic women. Am J Obstet Gynecol. 161:1989;1163-1167.
71. Steel J.M., Johnstone F.D., Smith A.F. Five years experience of a "prepregnancy" clinic for insulin dependent diabetics. BMJ. 1982;285-353.
72. Steel J.M., Johnstone F.D., Hepburn D.A., Smith A.F. Can prepregnancy care of diabetic women reduce the risk of abnormal babies? BMJ. 301:1991;1070-1073.
73. Wilhoite M.B., Bennett H.W. Jr, Palomaki G.E., Zaremba M.M., Herman W.H., Williams J.R., Spear N.H. The impact of preconception counseling on pregnancy outcomes. Diabetes Care. 16:1993;450-455.
74. Hollingsworth DR. Preconception and early post-conception counseling. In: Hollingsworth DR, ed. Pregnancy, diabetes and birth: a management guide. Baltimore: Williams & Wilkins, 1992.
75. Janz N.K., Herman W.H., Becker M.P., et al. Diabetes and pregnancy factors associates with seeking preconception care . Diabetes Care. 18:1995;157-165.
76. St. James P.J., Younger M.D., Hamilton B.D., et al. Unplanned pregnancies in young women with diabetes. Diabetes Care. 16:1993;1572-1578.
77. King R.C., Dobree J.H., Kok D.A., Foulds W.S., Dangerfield W.G. Exudative diabetic retinopathy Spontaneous changes and effects of a corn oil diet . Br J Opthalmol. 47:1963;666-672.
78. Howard-Williams J., Patel P., Jelfs R., et al. Polyunsaturated fatty acids and diabetic retinopathy. Br J Opthalmol. 69:1985;15-18.
79. Houtsmuller A.J., van Hal-Ferwerda J., Kahn K.J., Henkes H.E. Favorable influences of linoleic acid on the progression of diabetic micro- and macro-angiopathy in adult onset diabetes mellitus. Prog Lipid Res. 20:1982;377-386.
80. Keen H., Payan J., Allawi J., et al. Treatment of diabetic neuropathy with gamma-linolenic acid. Diabetes Care. 16:1993;8-15.
81. Cerirllo A., Guigliano D., Quatraro A., Donzella C., Dipalo G., Lefebve P.J. Vitamin E reduction of protein glycosylation in diabetes. Diabetes Care. 14:1991;68-72.
82. Reece E.A., Homko C.J., Wu Y.-K. Multifactorial basis of the syndrome of diabetic embryopathy. Teratology. 54:1996;179.
83. Fuhrmann K., Reiber H., Semmler K., et al. The effect of intensified conventional insulin therapy before and during pregnancy on the malformation rate of offspring of diabetic mothers. Exp Clin Endocrinol. 83:1984;173-177.
84. Reece E.A., Homko C.J., Wu Y.-K., Wiznitzer A. Metabolic fuel mixtures and diabetic embryopathy. Clinics Perinatol. 20:1993;517-532.