Coexistent Maternal Disease and Intrauterine Growth Restriction

  • Janet R. Ashworth
  • Philip N. Baker


A plethora of different coexistent maternal diseases has been linked to the development of IUGR; if any maternal disease is of sufficient severity, IUGR may ensue. Examples of reported associations with IUGR include maternal diabetes, cardiac disease, thyrotoxicosis, asthma, anaemia and chronic hypertension.


Obstet Gynecol Adverse Pregnancy Outcome Recurrent Pregnancy Loss Anticardiolipin Antibody Intrauterine Growth Restriction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Madsen H. Fetal oxygenation in diabetic pregnancy. Dan Med Bull 1986;33:64.PubMedGoogle Scholar
  2. 2.
    Nyland L, Lunell NO, Lewander R et al. Uteroplacental blood flow in diabetic pregnancy: Measurements with indium 113m and a computer linked gamma camera. Am J Obstet Gynecol 1982;144:298.Google Scholar
  3. 3.
    Reece EA, Leguizamon G, Homko C. Pregnancy performance and outcomes associated with diabetic nephropathy. Am J Perinatol 1998;15:413–21.PubMedCrossRefGoogle Scholar
  4. 4.
    Niswander KR, Berendes H, Deutschberger J. Fetal morbidity following potentially anoxygenic obstetric conditions. Organic heart disease. Am J Obstet Gynecol 1967;98:871–6. PubMedGoogle Scholar
  5. 5.
    Vander Spruy ZM Jacobs HS. Management of endocrine disorders in pregnancy. Thyroid and parathyroid disease. Postgrad Med J 1984;60:245–52. CrossRefGoogle Scholar
  6. 6.
    Owens JA. Endocrine and substrate control of fetal growth: placental and maternal influences and insulin-like growth factors. Reprod Fértil Dev 1991;3:501–17.PubMedCrossRefGoogle Scholar
  7. 7.
    Sims CD, Chamberlain GVP, de Swiet M. Lung function tests in bronchial asthma during and after pregnancy. Br J Obstet Gynaecol 1976;88:434–7.Google Scholar
  8. 8.
    Godfrey KM, Redman CWG, Barker DJP, Osmond C. The effect of maternal anaemia and iron deficiency on the ratio of fetal weight to placental weight. Br J Obstet Gynaecol 1991;98:886–91.PubMedCrossRefGoogle Scholar
  9. 9.
    Charache S, Niebyl JR. Pregnancy in sickle cell disease. In: Letsky EA, editor. Haematological disorders in pregnancy. Clinics in haematology, vol 14. London: WB Saunders, 1985;720–46. Google Scholar
  10. 10.
    Sibai BM, Spinnato JA, Watson DL, Hill GA, Anderson GD. Pregnancy outcome in 303 cases with severe preeclampsia. Obstet Gynecol 1984;64:319–25.PubMedGoogle Scholar
  11. 11.
    Wildschutt HIJ, Triffers PE, Hart AAM. The effect of hypertension on fetal growth. Clin Exp Hypertens 1963;B2:37–43.Google Scholar
  12. 12.
    Szymonowicz W, Yu VYH. Severe pre-eclampsia and infants of very low birth weight. Arch Dis Child 1987;62:712–16.PubMedCrossRefGoogle Scholar
  13. 13.
    Redman CWG, Beilin LJ, Bonnar J, Wilkinson RH. Plasma-urate measurements in predicting fetal death in hypertensive pregnancy. Lancet 1976;i: 1370–3. Google Scholar
  14. 14.
    Cooper JC , Milton PJ, Baker PN (1995). Pre-eclampsia; current theories of. In: Asch R, Studd J, editors. Progress in reproductive medicine, vol 2. London: Parthenon, 1995;165–76. Google Scholar
  15. 15.
    Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972;1:177–91.PubMedGoogle Scholar
  16. 16.
    Sheppard BL, Bonnar J. The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation. Br J Obstet Gynaecol 1976;83:948–59.PubMedCrossRefGoogle Scholar
  17. 17.
    Khong TY, DeWolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986;93:1049–59.PubMedCrossRefGoogle Scholar
  18. 18.
    Lunell N-O, Nylund L, Lewander R, Sarby B (1982). Uteroplacental blood flow in pre-eclampsia. Measurements with indium-113m and a computer-linked gamma camera. Clin Exp Hypertens BÍ: 105–117. Google Scholar
  19. 19.
    Francis ST, Duncan K, Moore RW, Baker PN, Johnson IR, Gowland PA. Non-invasive imaging of placental perfusion in normal pregnancies and in pregnancies complicated by intrauterine growth restriction. Lancet 1998;351:1397–400.PubMedCrossRefGoogle Scholar
  20. 20.
    Cameron AD, Nicholson SF, Nimrod CA, Harder JR, Davies DM. Doppler waveforms in the fetal aorta and umbilical artery in patients with hypertension in pregnancy. Am J Obstet Gynecol 1988;158:339–45.PubMedGoogle Scholar
  21. 21.
    Trudinger BJ, Cook, CM. Doppler umbilical and uterine flow waveforms in severe pregnancy hypertension. Br J Obstet Gynaecol 1990;97:142–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Zacutti, A., Borruto, F., & Bottacci, G. Umbilical bloodflow and placental pathology. Clin Exp Obstet Gynecol 1992;19:63–9.PubMedGoogle Scholar
  23. 23.
    Brosens I, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977;84:656–63.PubMedGoogle Scholar
  24. 24.
    Nylund L, Lunell N-O, Lewander R, Sarby B. Uteroplacental blood flow index in intrauterine growth retardation of fetal or maternal origin. Br J Obstet Gynaecol 1983;90:16–20.PubMedCrossRefGoogle Scholar
  25. 25.
    McCarthy A, Woolfson RG, Raju SK, Poston L. Abnormal endothelial cell function of resistance arteries from women with preeclampsia. Am J Obstet Gynecol 1993;168:1323.PubMedGoogle Scholar
  26. 26.
    Wilcox MA, Johnson IR, Maynard PV, Smith SJ, Chilvers CED. The individualised birthweight ratio: a more logical outcome measure of pregnancy than birthweight alone. Br J Obstet Gynaecol 1993;100:342–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Ashworth JR, Warren AY, Baker PN, Johnson IR. Loss of endothelium-dependent relaxation in myometrial resistance arteries in pre-eclampsia. Br J Obstet Gynaecol 1997;104:1152–8.PubMedCrossRefGoogle Scholar
  28. 28.
    Roberts JM, Redman CWG. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 1993;341:1447–51.PubMedCrossRefGoogle Scholar
  29. 29.
    Baker PN, Davidge ST, Roberts JM. Plasma from women with preeclampsia increases endothelial cell nitric oxide production. Hypertension 1995;26:244–8.PubMedGoogle Scholar
  30. 30.
    Ashworth JR, Warren AY, Johnson IR, Baker PN. Plasma from pre-eclamptic women induces a functional change in myometrial resistance arteries. Br J Obstet Gynaecol 1998;105:459–61.PubMedCrossRefGoogle Scholar
  31. 31.
    Cnattingius S, Mills JL, Yuen J, Eriksson O, Salonen H. The paradoxical effect of smoking in preeclamptic pregnancies: smoking reduces the incidence but increases the rates of perinatal mortality, abruptio placentae and intrauterine growth restriction. Am J Obstet Gynecol 1997;177:156–61.PubMedCrossRefGoogle Scholar
  32. 32.
    Eskenazi B, Fenster L, Sidney S, Elkin E. Fetal growth retardation in infants of multiparous and nulliparous women with preeclampsia. Am J Obstet Gynecol 1993;169:1112–18.PubMedGoogle Scholar
  33. 33.
    MacGillivray I. Some observations on the incidence of preeclampsia. J Obstet Gynaecol Br Commonwlth 1958;65:536–9.CrossRefGoogle Scholar
  34. 34.
    Feeney JG, Scott JS. Pre-eclampsia and changed paternity. Eur J Obstet, Gynaecol Reprod Biol 1980;11:35–8.CrossRefGoogle Scholar
  35. 35.
    Redman CWG. Immunological aspects of pre-eclampsia. Bailiere’s Clin Obstet Gynaecol 1992;6:601–15.CrossRefGoogle Scholar
  36. 36.
    Petrucco O. Aetiology of pre-eclampsia. In: Studd J, editor. Progress in obstetrics and gynaecology. Edinburgh: Churchill Livingstone, 1981;51–69.Google Scholar
  37. 37.
    Haeger M, Unander M, Bengtsson A. Complement activation in relation to development of pre-eclampsia. Obstet Gynecol 1991;78:46–9.PubMedGoogle Scholar
  38. 38.
    El-Roeiy A, Myers SA, Gleicher N. The relationship between autoantibodies and intrauterine growth retardation in hypertensive disorders of pregnancy. Am J Obstet Gynecol 1991;164:1253–61.PubMedGoogle Scholar
  39. 39.
    Pangborn MC. A new serologically active phospholipid from beef heart. Proc Soc Exp Biol Med 1941;48:484–6.Google Scholar
  40. 40.
    Johnstone FD Kilpatrick DC, Burns SM. Anticardiolipin antibodies and pregnancy outcome in women with human immunodeficiency virus infection. Obstet Gynecol 1992;80:92–6.PubMedGoogle Scholar
  41. 41.
    McNeil HP, Chesterman CN, Krills SA. Immunology and clinical importance of antiphospholipid antibodies. Adv Immunol 1991;49:193–280.PubMedCrossRefGoogle Scholar
  42. 42.
    Conley CL, Hartman RC. Hemorrhagic disorder caused by circulating anticoagulant in patients with disseminated lupus erythematosus. J Clin Invest 1952;31:621–2.Google Scholar
  43. 43.
    Feinstein DI, Rapaport SI. Acquired inhibitors of blood coagulation. Proc Hemast Thromb 1972;1:75–95.Google Scholar
  44. 44.
    Triplett DA, Brandt JT, Musgrove KA, Orr CA. The relationship between lupus anticoagulants and antibodies to phospholipid. JAMA 1988;259:550–4.PubMedCrossRefGoogle Scholar
  45. 45.
    Triplett DA, Brandt J. Laboratory identification of the lupus anticoagulant. Br J Haematol 1989;73:139–42.PubMedCrossRefGoogle Scholar
  46. 46.
    Lockwood CJ, Rand JH. The immunology and obstetrical consequences of antiphospholipid antibodies. Obstet Gynecol 1994;49:432–41.Google Scholar
  47. 47.
    Gharavi AE, Harris EN, Asherson RA. Anticardiolipin antibodies: Isotope distribution and phospholipid specificity. Ann Rheum Dis 1987;46:1–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Love PE, Santoro SA. Antiphospholipid antibodies: Anticardiolipin and the lupus anticoagulant in systemic lupus erythematosus (SLE) and in non-SLE disorders. Ann Intern Med 1990;112:682–98.PubMedGoogle Scholar
  49. 49.
    Yasuda M, Takakuwa K, Tokunaga A, Tanaka K. Prospective studies of the association between anticardiolipin antibody and outcome of pregnancy. Obstet Gynecol 1995;86:555–9.PubMedGoogle Scholar
  50. 50.
    Polzin WJ, Kopelman JN, Robinson RD. The association of antiphospholipid antibodies with pregnancies complicated by fetal growth restriction. Obstet Gynecol 1991;78:1108–11.PubMedGoogle Scholar
  51. 51.
    Bendon RW, Hayden LE, Hurtubise PE. Prenatal screening for anticardiolipin antibody. Am J Perinatol 1990;7:245–50.PubMedCrossRefGoogle Scholar
  52. 52.
    Toyoshima K, Makino T, Sugi T. Correlation between trimester of fetal wastage and anticardiolipin antibody titer. Int J Fértil 1991;36:89–93.PubMedGoogle Scholar
  53. 53.
    Infante-Rivard C, David M, Gauthier R, Rivard G-E. Lupus anticoagulants, anticardiolipin antibodies, and fetal loss. N Engl J Med 1991;325:1063–6.PubMedCrossRefGoogle Scholar
  54. 54.
    Haddow JE, Rote NS, Dostal-Johnson D, Palomaki GE, Pulkkinen AJ, Knight GJ. Lack of an association between late fetal death and antiphospholipid antibody measurements in the second trimester. Am J Obstet Gynecol 1991;165:1308–12.PubMedGoogle Scholar
  55. 55.
    Lockshin MD, Sammaritano LR. Antiphospholipid antibodies and fetal loss [letter]. N Engl J Med 1992;326:951–3.PubMedCrossRefGoogle Scholar
  56. 56.
    De Wolf F, Carreras LO, Moerman P, Vermylen J, Van Assche A, Renaer M. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss, and a lupus anticoagulant. Am J Obstet Gynecol 1982;142:829–34.PubMedGoogle Scholar
  57. 57.
    De Carolis S, Caruso A, Ferrazzani S, Carducci B, De Santis L, Mancuso S. Poor pregnancy outcome and anticardiolipin antibodies. Fetal Diagn Ther 1994;9:296–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Katano K, Aoki A, Sasa H, Ogasawara M, Matsuura E, Yagami Y. Beta 2-Glycoprotein I-dependent anticardiolipin antibodies as a predictor of adverse pregnancy outcomes in healthy pregnant women. Human Reprod 1996;11:509–12.Google Scholar
  59. 59.
    Cowchock FS, Reece EA, Balaban D, Branch DW, Plouffe L. Repeated fetal losses associated with antiphospholipid antibodies: a collaborative randomized trial comparing prednisolone with low-dose heparin treatment. Am J Obstet Gynecol 1992;166:1318–23.PubMedGoogle Scholar
  60. 60.
    Stirling Y, Woolf L, North WR, Seghatatchian MJ, Meade TW. Haemostasis in normal pregnancy. Thromb Haemost 1984;52:176–82.PubMedGoogle Scholar
  61. 61.
    Weiner CP . Evaluation of clotting disorders during pregnancy. In: Sciarra J J, Eschenbach DA, Depp R, editors.Gynecology and obstetrics, vol 3. Hagerstown MD, Harper & Row, 1990;1. Google Scholar
  62. 62.
    Maki M. Coagulation, fibrinolysis, platelet and kinin-forming systems during toxaemia of pregnancy. Biol Res Preg 1983;4:152–4.Google Scholar
  63. 63.
    Weiner CP, Brant J. Plasma antithrombin III activity: an aid in the diagnosis of pre-eclampsia-eclampsia. Am J Obstet Gynecol 1982;142:275–81.PubMedGoogle Scholar
  64. 64.
    Saleh AA, Bottoms SF, Welch RA, Ali MA, Mariona FG, Mammen EF. Preeclampsia, delivery, and the haemostatic system. Am J Obstet Gynecol 1987;157:331–6.PubMedGoogle Scholar
  65. 65.
    Brant JT. Current concepts of coagulation. Clin Obstet Gynecol 1985;28:3–14.CrossRefGoogle Scholar
  66. 66.
    Comp PC, Jacocks RM, Ferrell GL, Esmon CT. Activation of protein C in vivo. J Clin Invest 1982;70:127–34.PubMedCrossRefGoogle Scholar
  67. 67.
    Gonzalez R, Alberca I, Vincente V. Protein C levels in late pregnancy, post partum and in women on oral contraceptives. Thromb Res 1985;39:637–41.PubMedCrossRefGoogle Scholar
  68. 68.
    Dekker GA, de Vries JIP, Doelitzch PM, Huijgens PC, Von Blomberg BME, Jakobs C. Under¬lying disorders associated with severe early onset pre-eclampsia. Am J Obstet Gynecol 1995;173:1042–8.PubMedCrossRefGoogle Scholar
  69. 69.
    Preston FE, Rosendaal FR, Walker ID, Briet E, Berntorp E, Conard J, et al. Increased fetal loss in women with heritable thrombophilia. Lancet 1996;348:913–16.PubMedCrossRefGoogle Scholar
  70. 70.
    De Vries JIP, Dekker GA, Huijgens PC, Jakobs C, Blomberg BME, van Geijn HP. Hyper-homocysteinaemia and protein D deficiency in complicated pregnancies. Br J Obstet Gynecol 1997;104:1248–54.CrossRefGoogle Scholar
  71. 71.
    Cunningham FG, Macdonald PC, Gant NF. Williams obstetrics, 19th edn. East Norwalk, CT: Appleton & Lange, 1993;763–817.Google Scholar
  72. 72.
    Paternoster D, Stella A, Simioni P, Trovo S, Plebani P, Girolami A. Clotting inhibitors and fibronectin as potential markers in pre-eclampsia. Int J Gynaecol Obstet 1994;47:215–21.PubMedCrossRefGoogle Scholar
  73. 73.
    Fernandez JA, Estelles A, Gilabert J. Functional and immunologic protein S in normal pregnant women and in full term neonates. Thromb Haemost 1989;61:474–8.PubMedGoogle Scholar
  74. 74.
    Dahlback B, Carlsson M, Svensson PJ. Familial thrombophilia due to a previously unrecognised mechanism characterised by poor anticoagulant response to activated protein C. Proc Natl Acad Sci USA 1993;90:1004–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Bertina RM, Koeleman BPC, Koster T, Rosendaal FR, Dirven RJ, de Ronde H, et al. Mutation in blood coagulation factor V associated with resistance to activated protein C. Nature 1994;369:64–7.PubMedCrossRefGoogle Scholar
  76. 76.
    Svensson PJ , Dahlback B. Twenty novel families with thrombophilia and inherited resistance to activated protein C. Thromb Haemost 1993;69:1252 [abst]. Google Scholar
  77. 77.
    Koster T, Rosendaal FR, de Ronde H, Briet E, Vandenbroucke JP, Bertina RM. Venous thrombosis due to poor anticoagulant response to activated protein C: Leiden Thrombophilia Study. Lancet 1993;342:1503–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Walker MC, Garner PR, Keely EJ, Rock GA, Reis MD. Changes in activated protein C resistance during normal pregnancy. Am J Obstet Gynecol 1997;177:162–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Lee DH, Henderson PA, Blajchman MA. Prevalence of factor V Leiden in a Canadian blood donor population. Can Med Assoc J 1996;155:285–9.Google Scholar
  80. 80.
    Hellgren M, Svensson PJ, Dahlback B. Resistance to activated protein C as a basis for venous thromboembolism associated with pregnancy and oral contraceptives. Am J Obstet Gynecol 1995;173:210–13.PubMedCrossRefGoogle Scholar
  81. 81.
    Cumming AM, Tait RC, Fildes S, Yoong A, Keeney S, Hay CR. Development of resistance to activated protein C during pregnancy. Br J Haematol 1995;90:725–7.PubMedCrossRefGoogle Scholar
  82. 82.
    Mathonnet F, Demazancourt P, Bastenaire B, Morot M, Benattar N, Beufe X. Activated protein C sensitivity ratio in pregnant women at delivery. Br J Haematol 1996;92:244–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Zoller B, Svensson PJ, He X, Dahlback B. Identification of the same factor V gene mutation in 47 out of 50 thrombosis-prone families with inherited resistance to activated protein C. J Clin Invest 1994;94:2521–4.PubMedCrossRefGoogle Scholar
  84. 84.
    Rotmensch S, Liberati M, Mittelman M, Ben-Rafael Z. Activated protein C resistance and adverse pregnancy outcome. Am J Obstet Gynecol 1997;177:170–3.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2000

Authors and Affiliations

  • Janet R. Ashworth
  • Philip N. Baker

There are no affiliations available

Personalised recommendations