Placental ischemia and cardiovascular dysfunction in preeclampsia and beyond: Making the connections

Expert Review of Cardiovascular Therapy

Volumn 6, Issue 10, 2008, Pages 1367-1377

  Gilbert, Jeffrey S ^a   Nijland, Mark J ^b   Knoblich, Penny ^c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c MINNESOTA STATE UNIVERSITY   (United States)

Author keywords

Cardiac; Cytokines; Pregnancy; VEGF

Indexed keywords

2 METHOXYESTRADIOL; ANGIOTENSIN 1 RECEPTOR AUTOANTIBODY; ANGIOTENSIN II; AUTOANTIBODY; C REACTIVE PROTEIN; CATECHOL METHYLTRANSFERASE; ENDOGLIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

CARDIOVASCULAR DISEASE; CLINICAL FEATURE; COMORBIDITY; DISEASE ASSOCIATION; HUMAN; HYPERTENSION; HYPOXIA; INCIDENCE; KIDNEY FAILURE; METABOLIC DISORDER; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PLACENTA DISORDER; PLACENTA ISCHEMIA; PLACENTA PERFUSION; PREECLAMPSIA; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; RISK ASSESSMENT; VASCULAR RESISTANCE; ANIMAL; ANOXIA; DISEASE MODEL; FEMALE; FETUS DISEASE; ISCHEMIA; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; VASCULARIZATION;

ANIMALS; ANOXIA; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; FEMALE; FETAL DISEASES; HUMANS; ISCHEMIA; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATIONS, CARDIOVASCULAR;

EID: 59049092404     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1586/14779072.6.10.1367     Document Type: Review

References (109)

1. Sibai B, Dekker G, Kupferminc M. Preeclampsia. Lancet 365(9461), 785-799 (2005).
2. Roberts JM, Pearson G, Cutler J, Lindheimer M. Summary of the NHLBI working group on research on hypertension during pregnancy. Hypertension 41(3), 437-445 (2003).
3. Irgens HU, Reisater L, Irgens LM, Lie RT, Roberts JM. Long term mortality of mothers and fathers after preeclampsia: population based cohort study Preeclampsia and cardiovascular disease later in life: who is at risk? BMJ 323 (7323), 1213-1217 (2001).
4. Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM. Preeclampsia and the risk of end-stage renal disease. N. Engl. J. Med. 359(8), 800-809 (2008).
5. Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS. Association of maternal endothelial dysfunction with preeclampsia. JAMA 285(12), 1607-1612 (2001).
6. Hubel CA, Snaedal S, Ness RB et al. Dyslipoproteinaemia in postmenopausal women with a history of eclampsia. BJOG 107(6), 776-784 (2000).
7. Wikstrom AK, Haglund B, Olovsson M, Lindeberg SN. The risk of maternal ischaemic heart disease after gestational hypertensive disease. BJOG 112(11), 1486-1491 (2005).
8. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Preeclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 335(7627), 974 (2007).
9. Kaaja RJ, Greer IA. Manifestations of chronic disease during pregnancy. JAMA 294(21), 2751-757 (2005).
10. Linke A, Li W, Huang H, Wang Z, Hintze TH. Role of cardiac eNOS expression during pregnancy in the coupling of myocardial oxygen consumption to cardiac work. Am. J. Physiol. Heart Circ. Physiol. 283(3), H1208-H1214 (2002).
11. Gilbert JS, Ryan MJ, LaMarca BB, Sedeek M, Murphy SR, Granger JP. Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. Am. J. Physiol. Heart Circ. Physiol. 294(2), H541-H550 (2008).
12. Bosio P, Mckenna P, Conroy R, O'Herlihy C. Maternal central hemodynamics in hypertensive disorders of pregnancy. Obstet. Gynecol. 94(6), 978-984 (1999).
13. Israel A, Peceno A. Renin - angiotensin - aldosterone system in pregnanty-induced hypertension. J. Hum. Hypertens. 14(Suppl. 1), S36-S39 (2000).
14. Blanco MV, Roisinblit J, Grosso O et al. Left ventricular function impairment in pregnancy-induced hypertension. Am. J. Hypertens. 14(3), 271-275 (2001).
15. Borghi C, Esposti DD, Immordino V et al. Relationship of systemic hemodynamics, left ventricular structure and function, and plasma natriuretic peptide concentrations during pregnancy complicated by preeclampsia. Am. J. Obstet. Gynecol. 183(1), 140-147 (2000).
16. Nishimura MD, Tajik MD. Evaluation of diastolic filling of left ventricle in health and disease: Doppler echocardiography is the clinician's Rosetta stone. J. Am. Coll. Cardiol. 30(1), 8-18 (1997).
17. Yuan L, Duan Y, Cao T. Echocardiographic study of cardiac morphological and functional changes before and after parturition in pregnancy-induced hypertension. Echocardiography. 23(3), 177-182 (2006).
18. Kuwahara F, Kai H, Tokuda K et al. Hypertensive myocardial fibrosis ind diastolic dysfunction: another model of inflammation? Hypertension 43(4), 739-745 (2004).
19. Craici I, Wagner S, Garovic VD. Review: preeclampsia and future cardiovascular risk: formal risk factor or failed stress test? Ther. Adv. Cardiovasc. Dis. 2(4), 249-259 (2008).
20. Freeman DJ, McManus F, Brown EA et al. Short-and long-term changes in plasma inflammatory markers associated with preeclampsia. Hypertension 44(5), 708-714 (2004).
21. Hubel CA, Wallukat G, Wolf M et al. Agonistic angiotensin II type 1 receptor autoantibodies in postpartum women with a history of preeclampsia. Hypertension 49(3), 612-617 (2007).
22. Hubel CA, Powers RW, Snaedal S et al. C-reactive protein is elevated 30 years after eclamptic pregnancy. Hypertension 51(6), 1499-1505 (2008).
23. Alexander BT. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41(3), 457-462 (2003).
24. Alexander BT, Hendon AE, Ferril G, Dwyer TM. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 45(4), 754-758 (2005).
25. Lu F, Bytautiene E, Tamayo E et al. Gender-specific effect of overexpression of sFlt-1 in pregnant mice on fetal programming of blood pressure in the offspring later in life. Am. J. Obstet. Gynecol. 197(4), 418-415 (2007).
26. Lu F, Longo M, Tamayo Eet al. The effect of overexpression of sFlt-1 on blood pressure arfd-he occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am. J. Obstet. Gynecol. 196(4), 396-396 (2007).
27. Gilbert JS, Knoblich PR, Steck S. Effects of regular, voluntary gestational exercise on the development of hypertension in offspring. FASEB J. 16(5), A1141-A1141 (2002).
28. Fisher SJ, Roberts JM. Defects in placentation and placental perfusion. In: Chelsey's Hypertensive Disorders in Pregnancy. Lindheimer MD, Roberts JM, Cunningham FG (Eds). Appleton & Lange, Stanford, CT, USA (1999).
29. Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am. J. Reprod. Immunol. 37(3), 240-249 (1997).
30. Maynard SE, Min JY, Merchan J et al. Excess placental soluble FMS-like tyrosine kinase 1 (sFit1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111(5), 649-658 (2003).
31. Makris A, Thornton C, Thompson J et al. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int. 71(10), 977-984 (2007).
32. Gilbert JS, Babcock SA, Granger JP. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 50, 1142-1147 (2007).
33. Venkatesha S, Toporsian M, Lam C et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 12(6), 642-649 (2006).
34. Wolf Mullah A, Lam C et al. Circulating levels of ihe antiangiogenic marker sFLT-1 are increased in first versus second pregnancies. Am. J. Obstet. Gynecol. 193(1), 16-22 (2005).
35. Thadhani R, Mutter WP, Wolf M et al. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J. Clin. Endecrinol. Metab. 89(2), 770-775 (2004).
36. Shibata E, Rajakumar A, Powers RW et al. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J. Clin. Endocrinol. Metab. 90(8), 4895-4903 (2005).
37. Rajakumar A, Michael HM, Rajakumar PA et al. Extra-placental expression of vascular endothelial growth factor receptor-1, (Flt-1) and soluble Flt-1 (sFlt-1), by peripheral blood mononuclear cells (PBMCs) in normotensive and preeclamptic pregnant women. Placenta 26(7), 563-573 (2005).
38. Levine RJ, Maynard SE, Qian C et al. Circulating angiogenic factors and the risk of preeclampsia. N. Engl. J. Med. 350(7), 672-683 (2004).
39. Levine RJ, Lam C, Qian C et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N. Engl. J. Med. 355(10), 992-1005 (2006).
40. Lam C, Lim KH, Karumanchi SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension 46(5), 1077-1085 (2005).
41. Karumanchi SA, Maynard SE, Stillman IE, Epstein FH, Sukhatme VP. Preeclampsia: a renal perspective. Kidney Int. 67(6), 2101-2113 (2005).
42. Tranquilli AL, Bezzeccheri V, Giannubilo SR, Scagnoli C, Mazzanti L, Garzetti GG. Amniotic vascular endothelial growth factor (VEGF) and nitric oxide (NO) in women with subsequent preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 113(1), 17-20 (2004).
43. Rana S, Karumanchi SA, Levine RJ et al. Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 50(1), 137-142 (2007).
44. Nevo O, Soleymanlou N, Wu Y et al. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291(4), R1085-R1093 (2006).
45. Karumanchi SA, Bdolah Y. Hypoxia and sFlt-1 in preeclampsia: the 'chicken-and-egg' question. Endocrinology 145(11), 4335-4837 (2004).
46. Ianosi-Irimie M, Vu HV, Whitbred JM et al. A rat model of preeclampsia. Clin. Exp. Hypertens. 27(8), 605-617 (2005).
47. Dokras A, Hoffmann DS, Eastvold JS et al. Severe feto-placental abnormalities precede the onset of hypertension and proteinuria in a mouse model of preeclampsia. Biol. Reprod. 75(6), 899-907 (2006).
48. Davisson RL, Hoffmann DS, Butz GM et al. Discovery of a spontaneous genetic mouse model of preeclampsia. Hypertension 39(2 Pt 2), 337-342 (2002).
49. Kanasaki K, Palmsten K, Sugimoto H et al. Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with preeclampsia. Nature 453(7198), 1117-1121 (2008).
50. Sedeek M, Gilbert JS, LaMarca BB et al. Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. Am. J. Hypertens. 21(10), 1152-1156 (2008).
51. Zhou CC, Zhang Y, Irani RA et al. Angiotensin receptor agonistic autoantibodies induce preeclampsia in pregnant mice. Nat. Med. 14(8), 855-862 (2008).
52. Colson D, Gilbert JS, Bridges J et al. Oxidative stress mediates soluble Flt-1 induced vascular dysfunction in pregnant rats. FASEB J. 22(Meeting abstract), 969.7 (2008).
53. Bridges J P, Gilbert JS, Colson D et al. Soluble Flt-1 induces hypertension and vascular dysfunction in pregnant rats. FASEB J. 22(Meeting abstracts), 969.3 (2008).
54. Verlohren S, Niehoff M, Hering L et al. Uterine vascular function in a transgenic preeclampsia rat model. Hypertension 51(2), 547-553 (2008).
55. Gilbert JS, Dukes M, LaMarca BB, 5 Cockrell K, Babcock SA, Granger JP. Effects of reduced uterine perfusion pressure on blood pressure and metabolic factors in pregnant rats. Am. J. Hypertens. 28(6), 686-691 (2007).
56. Schlager G. Genetic hypertension in mice. In: Handbook of Hypertension. Ganten D, DeJong W (Eds). Elsevier, London, UK (1994).
57. Hoffmann DS, Weydert CJ, Lazartigues E et al. Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension 51(4), 1058-1065 (2008).
58. Barnea ER, MacLusky NJ, DeCherney AH, Naftolin F. Catechol-O-methyl transferase activity in the human term placenta. Am. J. Perinatol. 5(2), 121-127 (1988).
59. Alexander BT, Llinas MT, Kruckeberg WC, Granger JP. L-arginine attenuates hypertension in pregnant rats with reduced uterine perfusion pressure. Hypertension 43(4), 832-836 (2004).
60. Sholook MM, Gilbert JS, Sedeek MH, Huang M, Hester RL, Granger JP. Systemic hemodynamic and regional blood flow changes in response to chronic reductions in uterine perfusion pressure in pregnant rats. Am. J. Physiol. Heart Circ. Physiol. 293(4), H2080-H2084 (2007).
61. Gutkowska J, Granger JP, LaMarca B et al. Cardiac hypertrophy and cardiac insulin responsive amino-peptidase (IRAP) in the reduced uterine perfusion (RUPP) model of preeclampsia. Hypertension 46(5), 841-841 (2005).
62. National High Blood Pressure Education Program Working Group Report on High Blood Pressure in Pregnancy. Consensus report. Am. J. Obstet. Gynecol. 163, 1689-1712 (1990).
63. Visser W, Wallenburg HC. Central hemodynamic observations in untreated preedamptic patients. Hypertension 17(6), 1072-1077 (1991).
64. Taylor RN, Roberts JM. Endothelial cell dysfunction. In: Chelsey's Hypertensive Disorder's of Pregnancy. Lindheimer M, Roberts JM, Cunningham FG (Eds). Appleton & Lange, CT, USA (2007).
65. Taylor RN, de Groot CJ, Cho YK, Lim KH. Circulating factors as markers and mediators of endothelial cell dysfunction in preeclampsia. Semin. Reprod. Endocrinol. 16(1), 17-31 (1998).
66. Abid M, Schools I, Spokes K, Wu S, Mawhinney C, Aird W. Vascular endothelial growth factor-mediated induction of manganese superoxide dismutase occurs through redox-dependent regulation of forkhead and IκB/NF-κB. J. Biol. Chem. 279(42), 44030-44038 (2004).
67. Abid M, Tsai J, Spokes K, Deshpande S, Irani K, Aird W. Vascular endothelial growth factor induces manganese-superoxide dismutase expression in endothelial cells by a Rac1-regulated NADPH oxidase-dependent mechanism. FASEB J. 15(13), 2548-2550 (2001).
68. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem. Biophys. Res. Commun. 226(2), 324-328 (1996),
69. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr. Res. 57(5 Pt 2), 1R-7R (2005).
70. Tsatsaris V, Goffin F, Munaut C et al. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J. Clin. Endocrinol. Metab. 88(11), 5555-5563 (2003).
71. Vuorela P, Helske S, Hornig C, Alitalo K, Weich H, Halmesmaki E. Amniotic fluid-soluble vascular endothelial growth factor receptor-1 in preedampsia. Obstet. Gynecol. 95(3), 353-357 (2000).
72. Li Z, Zhang Y, Ying Ma J et al. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 50(4), 686-692 (2007).
73. Masuyama H, Nakatsukasa H, Takamoto N, Hiramatsu Y. Correlation between soluble endoglin, vascular endothelial growth factor receptor-1, and adipocytokines in preeclampsia. J. Clin. Endocrinol. Metab. 92(7), 2672-2679 (2007).
74. Jerkic M, Rivas-Elena JV, Prieto M et al. Endoglin regulates nitric oxide-dependent vasodilatation. FASEB J. 18(3), 609-611 (2004).
75. Li C, Issa R, Kumar P et al. CD105 prevents apoptosis in hypoxic endothelial cells. J. Cell Sci. 116(13), 2677-2685 (2003).
76. Cudmore M, Ahmad S, Al-Ani B et al. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 115(13), 1789-1797 (2007).
77. Walsh SW. Maternal-placental interactions of oxidative stress and antioxidants in preeclampsia. Semin. Reprod. Endocrinol. 16(1), 93-104 (1998).
78. Roberts JM, Taylor RN, Goldfien A. Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am. J. Hypertens. 4(8), 700-708 (1991).
79. Roberts JM, Balk JL, Bodnar LM, Belizan JM, Bergel E, Martinez A. Nutrient involvement in preeclampsia. J. Nutr. 133(5), 1684S-1692S (2003).
80. Rumbold AR, Crowther CA, Haslam RR, Dekker GA, Robinson JS; the ACTS Study Group. Vitamins C and E and the risks of preeclampsia and perinatal complications. N. Engl. J. Med. 354(17), 1796-1806 (2006).
81. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH. Vitamin C and vitamin E in pregnant women at risk for preeclampsia (VIP trial): randomised placebo-controlled trial. Lancet 367(9517), 1145-1154 (2006).
82. Schnackenberg CG, Welch WJ, Wilcox CS. Normalization of blood pressure and renal vascular resistance in shr with a membrane-permeable superoxide dismutase mimetic: role of nitric oxide. Hypertension 32(1), 59-64 (1998).
83. Sedeek MH, Sholook MM, Blazli C, Abram SR, Chandler DL, Granger JP. Tempol, but not vitamin E & C, decreases the blood pressure response to a chronic reduction in uterine perfusion pressure in pregnant rats. FASEB J. 18(4), A740-A740 (2004).
84. Shah DM. Role of the renin-angiotensin system in the pathogenesis of preedampsia. Am. J. Physiol. Renal Physiol. 288(4), F614-F625 (2005).
85. AbdAlla S, Lother H, Quitterer U. AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature 407(6800), 94-98 (2000).
86. AbdAlla S, Lother H, el Massiery A, Quitterer U. Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat. Med. 7(9), 1003-1009 (2001).
87. Wallukat G, Homuth V, Fischer T et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J. Clin. Invest. 103(7), 945-952 (1999).
88. Wallukat G, Neichel D, Nissen E, Homuth V, Luft FC. Agonistic autoantibodies directed against the angiotensin II AT1 receptor in patients with preeclampsia. Can. J. Physiol. Pharmacol. 81(2), 79-83 (2003).
89. Stepan H, Faber R, Wessel N, Wallukat G, Schultheiss HP, Walther T. Relation between circulating angiotensin II type 1 receptor agonistic autoantibodies and soluble fms-like tyrosine kinase 1 in the pathogenesis of preeclampsia. J. Clin. Endocrinol. Metab. 91(6), 2424-2427 (2006).
90. Walther T, Wallukat G, Jank A et al. Angiotensin II Type 1 receptor agonistic antibodies reflect fundamental alterations in the uteroplacental vasculature. Hypertension 46(6), 1275-1279 (2005).
91. Bobst SM, Day MC, Gilstrap LC 3rd, Xia Y, Kellems RE. Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human mesangial cells and induce interleukin-6 and plasminogen activator inhibitor-1 secretion. Am. J. Hypertens. 18(3), 330-336 (2005).
92. Xia Y, Wen H, Bobst S, Day MC, Kellems RE. Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human trophoblast cells. J. Soc. Gynecol. Investig. 10(2), 82-93 (2003).
93. Zhou CC, Ahmad S, Mi T et al. Angiotensin II induces soluble fms-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ. Res. 100(1), 88-95 (2006).
94. Llinas M, Wallukat G, Dechend R et al. Agonistic autoantibodies to the At1 receptor in a rat model of preeclampsia induced by chronic reductions in uterine perfusion pressure (RUPP). Hypertension 46(5), 884-884 (2005).
95. Magnussen EB, Vatten LJ, Lund-Nilsen TI, Salvesen KA, Smith GD, Romundstad PR. Prepregnancy cardiovascular risk factors as predictors of preeclampsia: population based cohort study. BMJ 335(7627), 978 (2007).
96. Kaaja R, Tikkanen MJ, Viinikka L, Ylikorkala O. Serum lipoproteins, insulin, and urinary prostanoid metabolites in normal and hypertensive pregnant women. Obstet. Gynecol. 85(3), 353-356 (1995).
97. Lorentzen B, Drevon CA, Endresen MJ, Henriksen T. Fatty acid pattern of esterified and free fatty acids in sera of women with normal and preeclamptic pregnancy. Br. J. Obstet. Gynaecol. 102(7), 530-537 (1995).
98. Martinez Abundis E, Gonzalez Ortiz M, Quiones Galvan A, Ferrannini E. Hyperinsulinemia in glucose-tolerant women with preeclampsia A controlled study. Am. J. Hypertens. 9(6), 610-614 (1996).
99. Bartha J, Romero-Carmona R, Torrejon-Cardoso R, Comino--Delgado R. Insulin, insulin-like growth factor-1, and insulin resistance in women with pregnancy-induced hypertension. Am. J. Obstet. Gynecol. 1870), 735-740 (2002).
100. Seely EW, Solomon CG. Insulin resistance and its potential role in pregnancy-induced hypertension. J. Clin. Endocrinol. Metab. 88(6), 2393-2398 (2003).
101. Wolf M, Sandier L, Munoz K, Hsu K, Ecker JL, Thadhani R. First trimester insulin resistance and subsequent preeclampsia: a prospective study. J. Clin. Endocrinol. Metab. 87(4), 1563-1568 (2002).
102. Innes KE, Wimsatt JH, McDuffie R. Relative glucose tolerance and subsequent development of hypertension in pregnancy. Obstet. Gynecol. 97(6), 905-910 (2001).
103. Solomon CG, Graves SW, Greene MF, Seely EW. Glucose intolerance as a predictor of hypertension in pregnancy. Hypertension 23(6), 717-721 (1994).
104. Joffe G, Esterlitz J, Levine R et al. The relationship between abnormal glucose tolerance and hypertensive disorders of pregnancy in healthy nulliparous women. Am. J. Obstet. Gynecol. 179(4), 1032-1037 (1998).
105. Thadhani R, Ecker JL, Mutter WP et al. Insulin resistance and alterations in angiogenesis: additive insults that may lead to preeclampsia. Hypertension 43(5), 988-992 (2004).
106. Murai JT, Muzykanskiy E, Taylor RN. Maternal and fetal modulators of lipid metabolism correlate with the development of preeclampsia. Metabolism 46(8), 963-967 (1997).
107. Lorentzen B, Henriksen T. Plasma lipids and vascular dysfunction in preeclampsia. Semin. Reprod. Endocrinol. 16(1), 33-39 (1998).
108. Sattar N, Greer IA, Louden J et al. Lipoprotein subtraction changes in normal pregnancy: threshold effect of plasma triglyceride on appearance of small, dense low density lipoprotein. J. Clin. Endocrinol. Metab. 82(8), 2483-2491 (1997).
109. Elahi MM, Cagampang FR, Anthony FW, Curzen N, Ohri SK, Hanson MA. Statin treatment in hypercholesterolemic pregnant mice reduces cardiovascular risk factors in their offspring. Hypertension 51(4), 939-944 (2008).