Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-15T15:46:13.724Z Has data issue: false hasContentIssue false
  • English
  • Français

HAEMODYNAMIC CONTRIBUTIONS TO THE PATHOGENESIS OF PREECLAMPSIA AND ECLAMPSIA

Part of: Bespoke shallow archive Weizmann

Published online by Cambridge University Press:  01 February 2008

IRA M BERNSTEIN  and
MARILYN J CIPOLLA
IRA M BERNSTEIN*
Affiliation:
Department of Obstetrics and Gynecology and Reproductive Sciences
MARILYN J CIPOLLA
Affiliation:
Department of Obstetrics and Gynecology and Reproductive Sciences Department of Neurology, University of Vermont College of Medicine.
*
Address for correspondence: Ira M. Bernstein MD, Professor and Vice-Chair for Obstetrics, Director of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, Smith 407, Fletcher Allen Health Care, 111 Colchester Avenue, Burlington, Vermont 05401-1435 University of Vermont College of Medicine
Get access Rights & Permissions [Opens in a new window]

Extract

Current hypotheses regarding the origins of preeclampsia have focused on the “Two stage model”. This model suggests that the primary steps in the pathophysiologic sequence of preeclampsia are initiated by abnormal placentation including the classic finding of abnormal trophoblast invasion of maternal decidual spiral arteries. The second stage of the sequence includes the elaboration of a single or multiple substances from these disordered placentas which contribute to the generalized maternal systemic illness, eventually manifesting as endothelial injury, hypertension and proteinuria. Recent studies have focused on the role of pro and anti-angiogenic peptides as potential placentally derived aetiologic agents in this pathophysiologic sequence, although other placental products have been highlighted in recent research. Despite the fact that this modeling of preeclampsia has widespread support significant limitations to this hypothesis can be identified.

Type
Research Article
Information
Fetal and Maternal Medicine Review , Volume 19 , Issue 1 , February 2008 , pp. 85 - 104
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1Roberts, JR. Preeclampsia: what we know and what we do not know. Seminar Perinatol 2000; 24: 24–28.CrossRefGoogle Scholar
2Maynard, SE, Min, JY, Merchan, J, Lin, KH, Li, J, Mondai, S et al. Excess placental soluble fms-like tyrosine kinase 1 (sflt1) may contribute to endothelial dysfunction, hypertension and proteinuria in preeclampsia. J Clin Invest 2003; 111: 649–58.CrossRefGoogle ScholarPubMed
3Levine, R, Maynardm, SE, Qian, C, Lim, K-H, England, LJ, Yu, KF et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350: 672–83.CrossRefGoogle ScholarPubMed
4Hubel, CA. Oxidative stress and preeeclampsia. Fet Mat Med Rev 1997; 9: 73–101.CrossRefGoogle Scholar
5Roberts, J, Hubel, CA. Is oxidative stress the link in the two-stage model of preeclampsia. Lancet 1999; 354: 788–89.CrossRefGoogle Scholar
6Egbor, M, Ansari, T, Morris, N, Green, CJ, Sibbons, PD. Pre-eclampsia and fetal growth restriction: how morphometrically different is the placenta. Placenta 2006; 27: 727–34.CrossRefGoogle ScholarPubMed
7Meekins, JW, Pijnnenborg, R, Hanssens, M, McFadyen, IR, van Assche, A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994: 101; 669–74.CrossRefGoogle ScholarPubMed
8Zhang, P, Schmidt, M, Cook, L. Maternal vasculopathy and histologic diagnosis of preeclampsia: poor correlation of histological changes and clinical manifestation. Am J Obstet Gynecol 2006; 194: 1050–6.CrossRefGoogle ScholarPubMed
9Moldenhauer, JS, Stanek, J, Warshak, C, Khoury, J, Sibai, B. The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet 2003; 189: 1173–77.CrossRefGoogle ScholarPubMed
10Donker, RB, Molema, G, Faas, MM, Kallenberg, GM, van Pampus, MG, Timmer, A et al. Absence of in vivo generalized pro-inflammatory endothelial activation in severe, early onset preeclampsia. J Soc Gynecol Invest 2005; 12: 518–28.CrossRefGoogle ScholarPubMed
11Xiong, X, Frasier, WD. Impact of pregnancy-induced hypertension on birth weight by gestational age. Paediatr Perinat 2004; 18: 186–91.CrossRefGoogle Scholar
12Vatten, LJ, Skjaerven, R. Is pre-eclampsia more than one disease? BJOG 2004; 111: 298–302.CrossRefGoogle Scholar
13Bernstein, IM, Janowiak, M, Thomas, CS, Badger, GJ. Birth weight shows a bimodal distribution in newborns of near term and term preeclamptic mothers. J Soc Gynecol Invest 2006; 13: 237A.Google Scholar
14Bernstein, IM, Meyer, MC, Osol, G, Ward, K. Intolerance to volume expansion: A theorized mechanism for the development of preeclampsia. Obstet Gynecol 1998; 92: 306–308.Google ScholarPubMed
15Campbell, DM, MacGillivray, I. Preeclampsia in twin pregnancies: incidence and outcome. Hypertension Pregn. 1999; 18: 197–207.CrossRefGoogle Scholar
16Sanchez-Torres, F, Santamaria, A. Histopathologia renal en la gestacion molar. Rev Obstet Ginecol Venezuela 1965; 25: 657–69.Google Scholar
17Rovinsky, JJ, Jaffin, H. Cardiovascular hemodynamics in pregnancy I Blood and plasma volumes in multiple pregnancy. Am J Obstet Gynecol 1965: 93: 1–5CrossRefGoogle Scholar
18Pritchard, JA. Blood volume changes in pregnancy and the puerperium; IV Anemia associated with hydatidiform mole. Am J Obstet Gynecol 1965; 91: 621–29.Google ScholarPubMed
19French, W, Freund, U, Carlson, R, Weil, MH. High output cardiac failure associated with pulmonary edema complicating hydatidiform mole. Arch Int Med 1977; 137: 367–69.CrossRefGoogle ScholarPubMed
20Ward, K, Hata, A, Jeunemaitre, X, Helin, C, Nelson, L, Namikawa, C et al. A molecular variant of angiotensinogen associated with preeclampsia. Nature Genetics 1993; 4: 59–61.CrossRefGoogle Scholar
21Jeunemaitre, X, Soubrier, YV, Kotelevtsev, RP, Lifton, CS, Williams, RR, Charru, A et al. Molecular basis of human hypertension: role of angiotensinogen. Cell 1992; 71: 169–80.CrossRefGoogle ScholarPubMed
22Bernstein, IM, Ziegler, W, Stirewalt, WS, Brumsted, J, Ward, K. Angiotensinogen genotype and plasma volume in nulligravid women. Obstet Gynecol 1998; 92: 171–73.Google ScholarPubMed
23Easterling, TR, Benedetti, TJ, Schmucker, BC, Millard, SP. Maternal hemodynamics in normal and preeclamptic pregnancies: A longitudinal study. Obstet Gynecol 1990; 76: 1061–69.Google ScholarPubMed
24Schobel, HP, Fischer, T, Heuszer, K, Geiger, H, Schmeider, RE. Preeclampsia-a state of sympathetic overactivity. N Engl J Med 1996; 335: 1480–85.CrossRefGoogle ScholarPubMed
25Julius, S, Pascual, AV, Reilly, K, London, R. Abnormalities of plasma volume in borderline hypertension. Arch Intern Med 1971; 127: 116–19.CrossRefGoogle ScholarPubMed
26Ellis, CN, Julius, S. Role of central blood volume in hyperkinetic borderline hypertension. Br Heart J 1973; 35: 450–55.CrossRefGoogle ScholarPubMed
27Clapp, JF, Capeless, EL. Cardiovascular function before, during, and after the first and subsequent pregnancies. Am J Cardiol 1997; 80: 1469–73.CrossRefGoogle ScholarPubMed
28Bernstein, IM, Shapiro, R, Whitsel, A, Schonberg, A. Relationship of plasma volume to sympathetic tone in nulliparous women. Am J Obstet Gynecol 2003; 188: 938–42.CrossRefGoogle ScholarPubMed
29Denq, JC, O'Brien, PC, Low, PA. Normative data on phases of the Valsalva maneuver. J Clinical Neurophys 1998; 15: 535–40.CrossRefGoogle ScholarPubMed
30Sandroni, P, Novak, V, Opfer-Gehrking, TL, Huck, CA, Low, PA. Mechanisms of blood pressure alterations in response to the Valsalva maneuver in postural tachycardia syndrome. Clin Autonomic Res 2000; 10: 1–5.CrossRefGoogle Scholar
31Courtar, DA, Spaanderman, MEA, Aardenburg, R, Janssen, BJA, Peeters, LLH. Low plasma volume coincides with sympathetic hyperactivity and reduced baroreflex sensitivity in formerly preeclamptic patients. J Soc Gynecol Invest 2006; 13: 48–52.CrossRefGoogle ScholarPubMed
32Damron, D, Bouchard, B, Shapiro, R, Schonberg, A, Bernstein, IM. Platelet activation, sympathetic tone and plasma volume in nulligravid women of reproductive age. Obstet Gynecol 2004; 103: 931–36.CrossRefGoogle ScholarPubMed
33Janes, SL, Kyle, PM, Redman, C, Goodall, AH. Flow cytometric detection of activated platelets in pregnant women prior to the development of preeclampsia. Thromb Haemost 1995; 74: 1059–63.Google Scholar
34Konijnenber, A, Van Der Post, JA, Mol, BW, Schaap, MCL, Lazarov, R, Bleker, OP et al. Can flow cytometric detection of platelet activation early in pregnancy predict the occurrence of preeclampsia? A prospective study. Am J Obstet Gynecol 1997; 177: 434–42.CrossRefGoogle Scholar
35McCrae, KR, Samuels, P, Schreiber, AD. Pregnancy-associated thrombocytopenia: pathogenesis and management. Blood 1992; 80: 2697–714.CrossRefGoogle Scholar
36Kupferminc, MJ, Peaceman, AM, Aderka, D, Wallach, D, Socol, ML. Soluble tumor necrosis factor receptors and interleukin-6 levels in patients with severe preeclampsia. Obstet Gynecol 1996; 88: 420–27.CrossRefGoogle ScholarPubMed
37Benyo, DF, Smarason, A, Redman, CWG, Sims, C, Conrad, KP. Expression of inflammatory cytokines in placentas from women with preeclampsia. J Clin Endocrinol Metab 2001; 86: 2505–12.Google ScholarPubMed
38Tjoa, ML, van Vogt, JMG, Blankenstein, MA, Oudejans, CBM, van Wijk, IJ. Elevated C-reactive protein levels during first trimester of pregnancy are indicative of preeclampsia and intrauterine growth restriction. J Reprod Immunol 2003; 59: 29–37.CrossRefGoogle ScholarPubMed
39Damron, D, Sallam, R, Bernstein, IM, Shapiro, R, Schonberg, A. Markers of inflammation and sympathetic tone in nulligravid women. Am J Obstet Gynecol 2003; 89: S85A.CrossRefGoogle Scholar
40Aardenburg, R, Spaanderman, MEA, Ekhart, TH, van Eijndhoven, HW, Van Der Heijden, OWH, Peeters, LLH. Low plasma volume following pregnancy complicated by preeclampsia predisposes for hypertensive disease in a next pregnancy. BJOG 2003; 110: 1001–1006.Google Scholar
41Eguchi, K, Ogun, N, Sawai, T, Yonezawa, M. Comparison of plasma concentrations of arginine vasopressin (AVP) and atrial natriuretic peptide (ANP) in normal and preeclamptic pregnancies. J Perinatal Med 1996; 24: 437–43.CrossRefGoogle ScholarPubMed
42Spaanderman, MEA, Ekhart, THA, de Leeuw, PW, Peeters, LLH. Angiotensin II sensitivity in nonpregnant formerly preeclamptic women and healthy parous controls. J Soc Gynecol Invest 2004; 11: 416–22.CrossRefGoogle ScholarPubMed
43Aardenburg, R, Spaanderman, MEA, van Eijndhoven, HW, de Leeuw, PW, Peeters, LLH. A low plasma volume in formerly preeclamptic women predisposes to the recurrence of hypertensive complications in the next pregnancy. J Soc Gynecol Invest 2006; 13: 598–603.CrossRefGoogle Scholar
44Naden, RP, Rosenfeld, CR. Modulation of the uteroplacental circulation: renin-angiotensin and adrenergic systems. In: Rosenfeld, CR (ed) Reproductive and Perinatal Medicine, Ithaca, NY: Perinatology Press, 1989, 207–38.Google Scholar
45Magness, RR, Rosenfeld, CR. Systemic and uterine responses to alpha-adrenergic stimulation in pregnant and nonpregnant ewes. Am J Obstet Gynecol 1986; 155: 897–904.CrossRefGoogle ScholarPubMed
46D'Angelo, G, Osol, G. Regional variation in resistance artery diameter responses to alpha-adrenergic stimulation during pregnancy. Am J Physiol 1993; 264: H78–H85.Google Scholar
47Damron, D, Bernstein, IM, Shapiro, R, Schonberg, A. Uterine Blood Flow Response to Alpha-Adrenergic Blockade in Nulligravid Women of Reproductive Age. J Soc Gynecol Invest 2004; 11: 388–92.CrossRefGoogle ScholarPubMed
48Zuspan, FP. Catecholamines: Their role in pregnancy and the development of pregnancy-induced hypertension. J Reprod Med 1979; 23: 143–50.Google ScholarPubMed
49Tunbridge, RDG, Donnai, P. Plasma noradrenaline in normal pregnancy and hypertension of late pregnancy. Br J Obstet Gynecol 1981; 88: 105–108.CrossRefGoogle ScholarPubMed
50Davey, DA, Macnab, MF. Plasma adrenaline, noradrenaline, and dopamine in pregnancy hypertension. Br J Obstet Gynecol 1981; 88: 611–18.CrossRefGoogle Scholar
51Yang, CC, Chao, TC, Kuo, TB, Yin, CS, Chen, HI. Preeclamptic pregnancy is associated with increased sympathetic and decreased parasympathetic control of HR. Am J Physiol Circ Physiol 2000; 278: H1269–73.CrossRefGoogle ScholarPubMed
52Soghomonians, A, Barakat, AI, Thirkill, TL, Douglas, GC. Trophoblast migration under flow is regulated by endothelial cells. Biol Reprod 2005; 73: 14–19.CrossRefGoogle ScholarPubMed
53Magness, RR, Grindle, KM, Balanza, E, Echalar, L, Varags, E, Zamudio, S. Uterine artery shear stress in pregnancy: Altitude, ethnic ancestry and preeclampsia. Reprod Sci 2007; 14: 11A abstract 190.Google Scholar
54Roberts, JM, Redman, CWG. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 1993; 341: 1447–454.CrossRefGoogle ScholarPubMed
55Barron, WM. Hypertension. In: Medical Disorders of Pregnancy. Barron, WM, Lindheimer, M, (eds) Mosby Year Book, St. Louis, 1991; 1–41.Google Scholar
56Villar, MA, Sibai, BM. Eclampsia. In: Arias, F, (ed) Obstetrics and Gynecology clinics of North America. High Risk Pregnancy, vol. 15 Philadelphia: WB Saunders, 1988; 356–77.Google Scholar
57Easton, DJ. Severe preeclampsia/eclampsia hypertensive encephalopathy of pregnancy? Cerebrovasc Dis 1998; 8: 53–58.CrossRefGoogle ScholarPubMed
58Zunker, P, Happe, S. Georgiadis, AL, Louwen, F, Georgiadis, D, Ringelstein, EB et al. Maternal cerebral hemodynamics in pregnancy-related hypertension. A prospective transcranial Doppler study. Ultrasound Obstet Gynecol 2000; 16: 179–87.CrossRefGoogle ScholarPubMed
59Thomas, SV. Neurologic aspects of eclampsia. J Neurol Sci 1998; 155: 37–43.CrossRefGoogle ScholarPubMed
60Donaldson, JO. The brain in eclampsia. Hypertens Pregnancy 1994; 13: 115–33.CrossRefGoogle Scholar
61Cipolla, MJ. Brief review: Cerebrovascular function during pregnancy and eclampsia. Hypertension 2007; 50: 14–24.CrossRefGoogle Scholar
62Williams, KP, Wilson, S. Persistence of cerebral hemodynamic changes in patients with eclampsia: A report of three cases. Am J Obstet Gynecol 1999; 181: 1162–165.CrossRefGoogle ScholarPubMed
63Richards, AM, Moodley, J, Graham, DI, Bullock, MR. Active management of the unconscious eclamptic patient. Br J Obstet Gynecol 1986; 93: 554–62.CrossRefGoogle ScholarPubMed
64Richards, AM, Graham, DI, Bullock, MR. Clinical pathological study of neurological complications due to hypertensive disorders of pregnancy. J Neurol Neurosurg Psychiatr 1988; 51: 416–21.CrossRefGoogle ScholarPubMed
65Schwartz, RB, Jones, KM, Kalina, P, Gajakian, RL, Mantello, MT, Garada, B et al. Hypertensive encephalopathy: findings on CT, MR-Imaging, and SPECT-Imaging in 14 cases. Am J Radiol 1992; 159: 379–83.Google Scholar
66Kanki, T, Tsukimori, K, Mihara, F, Nakano, H. Diffusion-weighted images and vasogenic edema in eclampsia. Obstet Gynecol 1999; 93: 821–23.Google Scholar
67Manfredi, M, Beltramello, A, Bongiovanni, LG, Polo, A, Pistoia, L, Rizzuto, N. Eclamptic encephalopathy: imaging and pathogenetic considerations. Acta Neurol Scand 1997; 96: 277–82.CrossRefGoogle ScholarPubMed
68Koch, S, Rabinstein, A, Falcone, S, Forteza, A. Diffusion-weighted imaging shows cytotoxic and vasogenic edema in eclampsia. Am J Neurorad 2001; 22: 1068–1070.Google ScholarPubMed
69Mas, J-L, Lamy, C. Stroke in pregnancy and the postpartum period. In: Ginsberg MD, MD, Bogousslavsky, J (eds) Cerebrovascular Disease: Pathophysiology, Diagnosis and Management. Blackwell Science, Malden, MA, 2004, Vol. II, Ch. 119.Google Scholar
70Port, JD, Beauchamp, NJ. Reversible intracerebral pathologic entities mediated by vascular autoregulatory dysfunction. Radiographics 1998; 18: 253–67.CrossRefGoogle ScholarPubMed
71Digre, KB, Varner, MW, Osborn, AG, Crawford, S. Cranial magnetic resonance imaging in severe preeclapmsia vs. eclampsia. Arch Neurol 1993; 50: 399–406.CrossRefGoogle Scholar
72Schafer, PW, Buonnano, FS, Gonzalez, RG, Schwamm, LH. Diffusion-weighted imaging discriminates between cytotoxic and vasogenic edema in patients with eclampsia. Stroke 1997; 28: 1082–1085.CrossRefGoogle Scholar
73Schwartz, RB, Mulern, RV, Grudbjartsson, H, Jolesz, F. Diffusion-weighted imaging in hypertensive encephalopathy: clues to pathogenesis. Am J Neuroradiol 1998; 19: 859–62.Google ScholarPubMed
74Shah, AK, Whitty, JE. Brain MRI in periperum seizures: usefulness of combined T2 and diffusion-weighted MR imaging. J Neurol Sci 1999; 166: 122–25.CrossRefGoogle ScholarPubMed
75Pizon, AF, Wolfson, AB. Postpartum focal neurologic deficits: Posterior leukoencephalopathy syndrome. J Emergency Med 2005; 29: 163–66.CrossRefGoogle ScholarPubMed
76Servillo, G, Striano, P, Striano, S. Posterior reversible encephalopathy syndrome (PRES) in obstetric critically ill patients. Intensive Care Med 2003; 29: 2323–326.CrossRefGoogle Scholar
77Rapoport, SI. Brain edema and the blood-brain barrier. In: Welch, KMA, Caplan, LR, Reis, DJ, Siesjo, BK, Weir, B (eds) Primer on Cerebrovascular Disease. Academic Press, San Diego, 1997; 25–28.CrossRefGoogle Scholar
78Ishii, S, Koike, J, Hatashita, . In: Mizukami, M et al. (eds) Hypertensive Intracranial Hemorrhage. Brain edema in hypertensive intracranial hemorrhage. Raven Press, New York, 1983; 118–35.Google Scholar
79Johansson, B, Li, C-L, Olsson, Y, Klatzo, I. Effect of acute arterial hypertension on the blood-brain barrier to protein tracers. Acta Neuropath 1970; 16: 117–24.CrossRefGoogle ScholarPubMed
80Hinchey, J, Chaves, C, Appignani, B, Breen, J, Pao, L, Wang, A et al. A reversible posterior encephalopathy syndrome. N Engl J Med 1996; 334: 494–500.CrossRefGoogle Scholar
81Iannotti, F, Hoff, JT, Schielke, GP. Brain tissue pressure in focal cerebral ischemia. J Neurosurg 1985; 62: 83–89.CrossRefGoogle ScholarPubMed
82Zeeman, GG, Fleckenstein, J, Twickler, DM, Cunningham, FG. Cerebral infarction in eclampsia. Am J Obstet Gynecol 2004; 190: 714–20.CrossRefGoogle Scholar
83Rapoport, SI. In: Welch, KMA, Caplan, LR, Reis, DJ, Siesjo, BK, Weir, B (eds) Brain edema and the blood-brain barrier. Primer on cerebrovascular disease. Academic Press, San Diego, 1997; 25–28.CrossRefGoogle Scholar
84Donaldson, JO. In: Donaldson, JO (ed.) Eclampsia. Neurology of pregnancy. London: WB Saunders, 1989; 269–310.Google Scholar
85Mackey, K, Meyer, MC, Stirewalt, WS, Starcher, BC, McLaughlin, MK. Composition and mechanics of mesenteric resistance arteries from pregnant rats. Am J Physiol 1992; 263: R2–8.Google ScholarPubMed
86Hermsteiner, M, Zoltan, DR, Kunzel, W. The vasoconstrictor response of uterine and mesenteric resistance arteries is differentially altered in the course of pregnancy. Eur J Obstet Gynecol Reprod Biol 2001; 100: 29–35.CrossRefGoogle Scholar
87Cipolla, M, Osol, G. Hypertrophic and hyperplastic effects of pregnancy on the uterine arterial wall. Am J Obstet Gynecol 1994; 171: 805–11.CrossRefGoogle ScholarPubMed
88Gilson, GJ, Mosher, MD, Conrad, KP. Systemic hemodynamics and oxygen transport during pregnancy in chronically instrumented, conscious rats. Am J Physiol 1992; 263: H1911–H1918.Google ScholarPubMed
89Euser, AG, Cipolla, MJ. Cerebral blood flow autoregulation and edema formation during pregnancy in anesthetized rats. Hypertension 2007; 49: 334–40.CrossRefGoogle ScholarPubMed
90Cipolla, MJ, Vitullo, L, McKinnon, J. Cerebral artery reactivity changes during pregnancy and postpartum: a role in eclampsia? Am J Physiol 2004; 286: H2127–H2132.Google ScholarPubMed
91Sabai, BM. Eclampsia. VI. Maternal-perinatal outcome in 254 consecutive cases. Am J Obstet Gynecol 1990; 163: 1049–55.Google Scholar
92Mattar, F, Sabai, BM. Eclampsia. VIII. Risk factors for maternal mortality. Am J Obstet Gynecol 2000; 182: 307–12.CrossRefGoogle Scholar
93Douglas, KA, Redman, CWG. Eclampsia in the United Kingdom. Br Med J 1994; 309: 1395–1400.CrossRefGoogle ScholarPubMed
94Sadoshima, S, Busija, DW, Heistad, DD. Mechanisms of protection against stroke in stroke-prone spontaneously hypertensive rats. Am J Physiol 1983; 244: H406–H412.Google ScholarPubMed
95Cipolla, MJ, Bullinger, LV. Pregnancy decreases cerebrovascular resistance and increases blood-brain barrier permeability during acute hypertension: Role in eclampsia? Reprod Sci 2008; (In press).Google Scholar
96Baumbach, GL, Dobrin, PB, Hart, MN, Heistad, DD. Mechanics of cerebral arterioles in hypertensive rats. Circ Res 1988; 62: 56–64.CrossRefGoogle ScholarPubMed
97Heistad, DD, Baumbach, GL. Cerebral vascular changes during chronic hypertension: good guys and bad guys. J Hypertens 1992; 10: S71–S75.CrossRefGoogle ScholarPubMed
98Baumbach, GL, Heistad, DD. Cerebral circulation in chronic arterial hypertension. Hypertension 1988; 12: 89–95.CrossRefGoogle ScholarPubMed
99Chillon, J-M, Ghoniem, S, Baumbach, GL. Effects of chronic nitric oxide synthase inhibition on cerebral arterioles in rats. Hypertension 1997; 30: 1097–104.CrossRefGoogle ScholarPubMed
100Morreau, P, Takase, H, Kung, CF, van Rooijen, M, Schaffner, T, Luscher, TF. Structure and function of the rat basilar artery during chronic nitric oxide synthase inhibition. Stroke 1995; 26: 1922–929.CrossRefGoogle Scholar
101Werber, AH, Heistad, DD. Effects of chronic hypertension and sympathetic nerves on the cerebral microvasculature of stroke-prone spontaneously hypertensive rats. Circ Res 1984; 55: 268–94.CrossRefGoogle ScholarPubMed
102Cipolla, MJ, DeLance, N, Vitullo, L. Pregnancy prevents hypertensive remodeling of cerebral arteries: A potential role in the development of eclampsia. Hypertension 2006; 47: 619–26.CrossRefGoogle ScholarPubMed
103Aukes, AM, Vitullo, L, Zeeman, GG, Cipolla, MJ. Pregnancy prevents hypertensive remodeling and decreases myogenic reactivity in posterior cerebral arteries from Dahl salt-sensitive rats: A role in eclampsia? Am J Physiol 2007; 292: H1071–1076.Google ScholarPubMed
104Cipolla, MJ, Smith, J, Bishop, N, Bullinger, LV, Godfrey, JA. Pregnancy reverses hypertensive remodeling of cerebral arteries. Hypertension 2008; 51: 1–6.CrossRefGoogle ScholarPubMed
105Cipolla, MJ, Vitullo, L, DeLance, N, Hammer, E. The cerebral endothelium during pregnancy: A potential role in the development of eclampsia. Endothelium 2005; 12: 1–5.CrossRefGoogle ScholarPubMed
106Witlin, AG, Sibai, BM. Magnesium sulfate therapy in preeclampsia and eclampsia. Obstet Gynecol 1998; 92: 883–89.Google Scholar
107Belfort, MA, Moise, KJ Jr.. Effect of magnesium sulfate on maternal brain blood flow in preeclampsia: a randomized, placebo-controlled study. Am J Obstet Gynecol 1992; 167: 661–66.CrossRefGoogle ScholarPubMed
108Euser, AG, Bullinger, LV, Cipolla, MJ. Magnesium sulfate decreases blood-brain barrier permeability during acute hypertension in pregnant rats. Exp Physiol 2008; 93: 254–61.CrossRefGoogle ScholarPubMed
109Bernstein, IM, Thibault, A, Mongeon, J, Badger, GJ. The effect of pregnancy on arterial compliance. Obstet Gynecol 2005; 105: 621–25.CrossRefGoogle Scholar
110Skhaerven, R, Wilcox, AJ, Lie, RT. The interval between pregnancies and the risk of preeclampsia. N Engl J Med 2002; 346: 33–38.CrossRefGoogle Scholar
111Basso, O, Christensen, K, Olsen, J. Higher risk of preeclampsia after change of partner. An effect of longer interpregnancy intervals. Epidemiology 2001; 12: 624–29.CrossRefGoogle Scholar
112Li, DK, Wi, S. Changing paternity and the risk of preeclampisa/eclampsia in the subsequent pregnancy. Am J Epidemiol 2000; 151: 57–62.CrossRefGoogle Scholar
113Sibai, B, Dekker, G, Kupferminc, M. Pre-eclampsia. Lancet 2005; 353: 785–99.CrossRefGoogle Scholar
114Jonsdottir, LS, Arngrimsson, R, Geirsson, RT, Sigvaldason, H, Sigfusson, N. Death rates from ischemic heart disease in women with a history of hypertension in pregnancy. Acta Obstet Gynecol Scand 1995; 74: 772–76.CrossRefGoogle ScholarPubMed
115Irgens, HU, Reisaeter, L, Irgens, LM, Rie, RT. Long-term mortality of mothers and father after pre-eclampsia:populations based cohort study. BMJ 2001; 323: 1213–217.CrossRefGoogle ScholarPubMed
116Funai, EF, Friedlander, Y, Paltiel, O, Tiram, E, Xue, X, Deutsch, L et al. Long-term mortality after preeclampsia. Epidemiology 2005; 16: 206–15.CrossRefGoogle ScholarPubMed
117Danesh, J, Collins, R, Appleby, P, Peto, R. Association of fibrinogen, c-reactive protein, albumin, or leukocyte count with coronary artery disease: Meta-analyses of prospective studies. JAMA 1998; 279; 18: 1477–482.CrossRefGoogle Scholar
118Kamat, SG, Kleiman, NS. Platelets and platelet inhibitors in acute myocardial infarction. Cardiology Clin 1995; 13: 435–47.CrossRefGoogle ScholarPubMed
119Julius, S, Majahalme, S. The changing face of sympathetic overactivity in hypertension. Ann Med 2000; 32: 365–70.CrossRefGoogle Scholar