Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia

American Journal of Obstetrics and Gynecology

Volumn 195, Issue 1, 2006, Pages 40-49

  Ness, Roberta B ^a   Sibai, Baha M ^b  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Cytokines; Fetal growth retardation; Metabolic syndrome x; Placenta; Preeclampsia

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERMEDIATE DENSITY LIPOPROTEIN; TUMOR NECROSIS FACTOR ALPHA; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ANGIOGENESIS; BODY MASS; CARDIOVASCULAR RISK; CLINICAL RESEARCH; DISEASE MARKER; ESSENTIAL HYPERTENSION; GROWTH RETARDATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INTRAUTERINE GROWTH RETARDATION; KIDNEY BLOOD FLOW; MATERNAL HYPERTENSION; METABOLIC SYNDROME X; PATHOPHYSIOLOGY; PLACENTA CIRCULATION; PLACENTA INSUFFICIENCY; PREECLAMPSIA; PREGNANCY COMPLICATION; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; RISK ASSESSMENT; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 CELL; TH2 CELL; UPREGULATION; UTERINE ARTERY;

ANIMALS; CARDIOVASCULAR DISEASES; COMORBIDITY; CYTOKINES; ENDOTHELIUM, VASCULAR; FEMALE; FETAL GROWTH RETARDATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INSULIN RESISTANCE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; TROPHOBLASTS;

EID: 33745272281     PISSN: 00029378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajog.2005.07.049     Document Type: Review

References (175)

1. Kaufmann P., Black S., and Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69 (2003) 1-7
2. Tjoa M.L., Oudejans C.B.M., van Vugt J.M.G., Blankenstein M.A., and van Wijk I.J. Markers for presymptomatic prediction of preeclampsia and intrauterine growth restriction. Hyper Preg 23 (2004) 171-189
3. Sibai B., Dekker G., and Kupferminc M. Pre-eclampsia. Lancet 365 (2005) 785-799
4. Lain K.Y., and Roberts J.M. Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 287 (2002) 3183-3186
5. Baschat A.A. Fetal responses to placental insufficiency: an update. BJOG 111 (2004) 1031-1041
6. Thadhani R., Ecker J.L., Mutter W.P., Wolf M., Smirnakis K.V., Sukhatme V.P., et al. Insulin resistance and alterations in angiogenesis: additive insults that may lead to preeclampsia. Hypertension 43 (2004) 988-992
7. Ness R.B., and Roberts J.M. Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications. Am J Obstet Gynecol 175 (1996) 1365-1370
8. Smith G.C., Pell J.P., and Walsh D. Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 357 (2001) 2002-2006
9. Smith G.C., Harding S., and Rosato M. Relation between infants' birth weight and mothers' mortality: prospective observational study. BMJ 320 (2000) 839-840
10. Davey Smith G., Hart C., Ferrell C., Upton M., Hole D., Hawthorne V., et al. Birth weight of offspring and mortality in the Renfrew and Paisley study: prospective observational study. BMJ 315 (1997) 1189-1193
11. Kramer M.S. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ 65 (1987) 663-737
12. Scott A., Moar V., and Ounsted M. The relative contributions of different maternal factors in small-for-gestational-age pregnancies. Eur J Obstet Gynecol Reprod Biol 12 (1981) 157-165
13. Haelterman E., Bueant G., Paris-Llado J., Dramaix M., and Tchobroutsky C. Effect of uncomplicated chronic hypertension on the risk of small-for-gestational age birth. Am J Epidemiol 145 (1997) 689-695
14. Lawlor D.A., Davey Smith G., and Ebrahim S. Birth weight of offspring and insulin resistance in late adulthood: cross sectional survey. BMJ 325 (2002) 359
15. Herrera J.A., Chaudhuri G., and Lopez-Jaramillo P. Is infection a major risk factor for preeclampsia?. Med Hyotheses 57 (2001) 393-397
16. von Dadelszen P., and Magee L.A. Could an infectious trigger explain the differential maternal response to the shared placental pathology of preeclampsia and normotensive intrauterine growth restriction?. Acta Obstet Gynecol Scand 81 (2002) 642-648
17. Bernstein P.S., and Divon M.Y. Etiologies of fetal growth restriction. Clin Obstet Gynecol 40 (1997) 723-729
18. Xiong X., Demianczuk N.N., Saunders L.D., Wang F., and Fraser W.D. Impact of preeclampsia and gestational hypertension on birth weight by gestational age. Am J Epidemiol 155 (2002) 203-209
19. Rey E., and Couturier A. The prognosis of pregnancy in women with chronic hypertension. Am J Obstet Gynecol 171 (1994) 410-416
20. Goldenberg R.L., and Cliver S.P. Small for gestational age and intrauterine growth restriction: definitions and standards. Clin Obstet Gynecol 40 (1997) 704-714
21. Moroni G., Quaglini S., Banfi G., Caloni M., Finazzi S., Ambroso G., et al. Pregnancy in lupus nephritis. Am J Kidney Dis 40 (2002) 713-720
22. Cortez-Hernandez J., Ordi-Ros J., Parades F., and Casellas M. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: a prospective study of 103 pregnancies. Rheumatol 41 (2002) 643-650
23. Sibai B., Gordon T., and Thom E. Risk factors for preeclampsia in healthy nulliparous women: a prospective multicenter study. Am J Obstet Gynecol 172 (1995) 642-648
24. Sibai B., Lindheimer M., and Hauth J. Risk factors for preeclampsia, abruptio placentae, and adverse neonatal outcomes among women with chronic hypertension. N Engl J Med 339 (1998) 667-671
25. Kanellis J., Nakagawa T., Herrera-Acosta J., Schreiner G.F., Rodriguez-Iturbe B., and Johnson R.J. A single pathway for the development of essential hypertension. Cardiol Rev 11 (2002) 180-196
26. Savvidou M.D., Hingorani A.D., Tsikas D., Frolich J.C., Vallance P., and Nicolaides K.H. Endothelial dysfunction and raised plasma concentrations of asymmetric dimethylarginine in pregnant women who subsequently develop preeclampsia. Lancet 361 (2003) 1511-1517
27. Ness R.B., Markovic N., Bass D., Harger G., and Roberts J.M. Family history of hypertension, heart disease, and stroke among women who develop hypertension in pregnancy. Obstet Gynecol 102 (2003) 1366-1371
28. Qui C., Williams M.A., Leisenring W.M., Sorensen T.K., Frederick I.O., Dempsey J.C., et al. Family history of hypertension and type 2 diabetes in relation to preeclampsia risk. Hypertension 41 (2003) 408-413
29. Taylor R.N., Crombleholme W.R., Friedman S.A., Jones L.A., Casal D.C., and Roberts J.M. High plasma cellular fibronectin levels correlate with biochemical and clinical features of preeclampsia but cannot be attributed to hypertension alone. Am J Obstet Gynecol 165 (1991) 895-901
30. Kraayenbrink A.A., Dekker G.A., van Kamp G.J., and van Geijn H.P. Endothelial vasoactive mediators in preeclampsia. Am J Obstet Gynecol 169 (1993) 160-165
31. Schiff E., Ben-Baruch G., Peleg E., Rosenthal T., Alcalay M., Devir M., et al. Immunoreactive circulating endothelin-1 in normal and hypertensive pregnancies. Am J Obstet Gynecol 166 (1992) 624-628
32. Higgins J.R., Papayianni A., Brady H.R., Darling M.R.N., and Walshe J.J. Circulating vascular cell adhesion molecule-1 in pre-eclampsia, gestational hypertension, and normal pregnancy-evidence of selective dysregulation of vascular cell adhesion molecule-1 homeostasis in pre-eclampsia. Am J Obstet Gynecol 179 (1998) 464-469
33. Taylor R.N., Musei T.J., Rodgers G.M., and Roberts J.M. Preeclamptic sera stimulate increased platelet-derived growth factor mRNA and protein expression by cultured human endothelial cells. Am J Reprod Immunol 25 (1991) 105-108
34. Bretelle F., Sabatier F., Blann A., D'Ercole C., Boutiere B., Mutin M., et al. Maternal endothelial soluble cell adhesion molecules with isolated small for gestational age fetuses: comparison with pre-eclampsia. BJOG 108 (2001) 1277-1282
35. Chappell L., Seed P., Kelly F., Briley A., Hunt B., and Charnock-Jones S. Vitamin C and E supplementation in women at risk of preeclampsia is associated with changes in indices of oxidative stress and placental function. Am J Obstet Gynecol 187 (2002) 777-784
36. Regnault T.R.H., Galan H.L., Parker T.A., and Anthony R.V. Placental development in normal and compromised pregnancies-a review. Placenta 23 Suppl A (2002) S119-S129
37. Campbell S., Diaz-Recasens J., Griffin D.R., Cohen-Overbeek T.E., Pearce J.M., Wilson K., et al. New Doppler technique for assessing uteroplacental blood flow. Lancet 1 (1983) 675-677
38. Chambers J.C., Fusi L., Malik L., Haskard D., DeSwiet M., and Kooner J. Association of maternal endothelial dysfunction with preeclampsia. JAMA 285 (2001) 1607-1612
39. Agatisa P.K., Ness R.B., Roberts J.M., Costantino J.P., Kuller L.H., and McLaughlin M.K. Impairment of endothelial function in women with a history of preeclampsia: an indicator of cardiovascular risk. Am J Physiol Heart Circ Physiol 286 (2004) H1389-H1393
40. Sibai B., Sarinoglu C., and Mercer B. Pregnancy outcome after eclampsia and long-term prognosis. Am J Obstet Gynecol 166 (1992) 1757-1761
41. Chesley S.C., Annitto J.E., and Cosgrove R.A. The remote prognosis of eclamptic women. Sixth periodic report. Am J Obstet Gynecol 124 (1976) 446-459
42. Jonsdottir L.S., Arngrimsson R., Geirsson R.T., Sigvaldason H., and Sigfusson N. Death rates from ischemic heart disease in women with a history of hypertension in pregnancy. Acta Obstet Gynecol Scand 74 (1995) 772-776
43. Hannaford P., Ferry S., and Hirsch S. Cardiovascular sequelae of toxaemia of pregnancy. Heart 77 (1997) 154-158
44. Irgens H.U., Reisaeter L., Irgens L.M., and Lie R.T. Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. BMJ 323 (2001) 1213-1217
45. Torry D.S., Hinrichs M., and Torry R.J. Determinants of placental vascularity. Am J Reprod Immunol 51 (2004) 257-268
46. Daayana S., Baker P., and Crocker I. An image analysis technique for the investigation of variations in placental morphology in pregnancies complicated by preeclampsia with and without intrauterine growth restriction. J Soc Gynecol Investig 11 (2004) 545-552
47. Robertson W.B., Brosens I., and Dixon H.G. Uteroplacenta vascular pathology. Eur J Obstet Gynecol Reprod Biol 5 (1975) 47-65
48. Meekins J.W., Pijenborg R., Hanssens M., McFadyen I.R., and VanAsshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclapmtic pregnancies. BJOG 101 (1994) 669-674
49. Redline R.W., and Patterson P. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Human Pathol 26 (1995) 594-600
50. Mayhew T.M., Ohadike C., Baker P.N., Crocker I.P., Mitchell C., and Ong S.S. Stereological investigation of placental morphology in pregnancies complicated by pre-eclampsia with and without intrauterine growth restriction. Placenta 24 (2003) 219-226
51. Bersinger N.A., and Odegard R.A. Second- and third-trimester serum levels of placental proteins in preeclampsia and small-for-gestational age pregnancies. Acta Obstet Gynecol Scand 83 (2004) 37-45
52. Corbacho A.M., Martinez de la Escalera G., and Clapp C. Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 173 (2002) 219-238
53. Achen M.G., Gad J.M., Stacker S.A., and Wilks A.F. Placenta growth factor and vascular endothelial growth factor are co-expressed during early embryonic development. Growth Factors 15 (1997) 69-80
54. Clark D.E., Smith S.K., Licence D., Evans A.L., and Charnock-Jones D.S. Comparison of expression patterns for placenta growth factor, vascular endothelial growth factor (VEGF), VEGF-B and VEGF-C in the human placenta throughout gestation. J Endocrinol 159 (1998) 459-467
55. Shore V.H., Wang T.H., Wang C.L., Torry R.J., Caudle M.R., and Torry D.S. Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 18 (1997) 657-665
56. Odorisio T., Schietroma C., Zaccaria M.L., Cianfarani F., Tiveron C., Tatangelo L., et al. Mice overexpressing placenta growth factor exhibit increased vascularization and vessel permeability. J Cell Sci 115 (2002) 2559-2567
57. Carmeliet P., Moons L., Luttun A., Vincenti V., Compernolle V., De Mol M., et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7 (2001) 575-583
58. Levine R.J., Maynard S.E., Qian C., Lim K., England L.J., Yu K.F., et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350 (2004) 672-683
59. Helske S., Vuorela P., Carpen O., Hornig C., Weich H., and Halmesmaki E. Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol Human Reprod 7 (2001) 205-210
60. Taylor R.N., Grimwood J., Taylor R.S., McMaster M.T., Fisher S.J., and North R.A. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 188 (2003) 177-182
61. Tjoa M.L., van Vugt J.M.G., Mulders M.A.M., Schutgens R.B.H., Oudejans C.B.M., and van Wijk I.J. Plasma placenta growth factor levels in midtrimester pregnancies. Obstet Gynecol 98 (2001) 600-607
62. Tsatsaris V., Goffin F., Munaut C., Brichant J.F., Pignon M.R., Noel A., et al. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 88 (2003) 5555-5563
63. Maynard S.E., Min J.Y., Merchan J., Lim K.H., Li J., Mondal 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 111 (2003) 649-658
64. Tidwell S.C., Ho H.N., Chiu W.H., Torry R.J., and Torry D.S. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 184 (2001) 1267-1272
65. Su Y.N., Lee C.N., Cheng W.F., Shau W.Y., Chow S.N., and Hsieh F.J. Decreased maternal serum placenta growth factor in early second trimester and preeclampsia. Obstet Gynecol 97 (2001) 898-904
66. 3. J Clin Invest 105 (2000) 577-587
67. 3 restores the invasive capability of extravillous trophoblast in preeclamptic pregnancies. J Clin Invest 103 (1999) 1641-1650
68. Pijnenborg R., McLaughlin P.J., Vercruysse L., Hanssens M., Johnson P.M., Keith J.C., et al. Immunolocalization of tumour necrosis factor-α (TNF-α) in the placental bed of normotensive and hypertensive human pregnancies. Placenta 19 (1998) 231-239
69. Zhou Y., Damsky C.H., Chiu K., Roberts J.M., and Fisher S.J. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 91 (1993) 950-960
70. Caniggia I., and Winter J.L. Adriana and Luisa Castellucci Award Lecture 2001. Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies-a review. Placenta 23 Suppl A (2002) S47-S57
71. Tazuke S.I., Mazure N.M., Sugawara J., Carland G., Faessen G.H., Suen L.F., et al. Hypoxia stimulates insulin-like growth factor binding protein 1 (IGFBP-1) gene expression in HepG2 cells: a possible model for IGFBP-1 expression in fetal hypoxia. Natl Acad Sci 95 (1998) 10188-10193
72. Rajakumar A., Whitelock K.A., Weissfeld L.A., Daftary A.R., Markovic N., and Conrad K.P. Selective overexpression of the hypoxia-inducible transcription factor, HIF-2alpha, in placentas from women with preeclampsia. Biol Reprod 64 (2001) 499-506
73. Genbacev O., Zhou Y., Ludlow J.W., and Fisher S.J. Regulation of human placental development by oxygen tension. Science 277 (1997) 1669-1672
74. Genbacev O., Joslin R., Damsky C.H., Polliotti B.M., and Fisher S.J. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 97 (1996) 540-550
75. Ukamura K., Watanabe T., Tanigawara S., Shintaku Y., Endo H., Iwamoto M., et al. Biochemical evaluation of fetus with hypoxia caused by severe preeclampsia using cordocentesis. J Perinat Med 18 (1990) 441-447
76. Salafia C.M., Minior V.K., Lopez-Zeno J.A., Whittington S.S., Pezzullo J.C., and Vintzileos A.M. Relationship between placental histologic features and umbilical cord blood gases in preterm gestations. Am J Obstet Gynecol 173 (1995) 1058-1064
77. Kingdom J.C., and Kaufmann P. Oxygen and placental vascular development. Adv Exp Med Biol 474 (1999) 259-275
78. Lash G.E., Taylor C.M., Trew A.J., Cooper S., Anthony F.W., Wheeler T., et al. Vascular endothelial growth factor and placental growth factor release in cultured trophoblast cells under different oxygen tensions. Growth Factors 20 (2002) 189-196
79. Shih S.C., and Claffey K.P. Regulation of human vascular endothelial growth factor mRNA stability in hypoxia by heterogeneous nuclear ribonucleoprotein L. J Biol Chem 274 (1999) 1359-1365
80. Wang G.L., and Semenza G.L. General involvement of hypoxia inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90 (1993) 4304-4308
81. Wang G.L., Jiang B.H., Rue E.A., and Semenza G.L. Hypoxia inducible factor 1 is a basic helix-loop-helix PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92 (1995) 5510-5514
82. Semenza G.L. Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol 59 (2000) 47-53
83. Hodgkinson C.P., Hodari A., and Bumpus F.M. Experimental hypertensive disease of pregnancy. Obstet Gynecol 30 (1967) 371-380
84. Combs C.A., Katz M.A., Kitzmiller J.L., and Brescia R.J. Experimental preeclampsia produced by chronic constriction of the lower aorta: validation with longitudinal blood pressure measurements in conscious rhesus monkeys. Am J Obstet Gynecol 169 (1993) 215-223
85. Lin J., and August P. Genetic thrombophilias and preeclampsia: a meta-analysis. Obstet Gynecol 105 (2005) 182-192
86. Rajakumar A., and Conrad K.P. Expression, ontogeny, and regulation of hypoxia-inducible transcription factors in the human placenta. Biol Reprod 63 (2000) 559-569
87. Feldser D., Agani F., Iyer N.V., Pak B., Ferreira G., and Semenza G.L. Reciprocal positive regulation of hypoxia-inducible factor 1a and insulin-like growth factor 2. Cancer Research 59 (1999) 3915-3918
88. Carmeliet P., Dor Y., Herbert J.-M., Fukumuras D., Brusselmans K., Dewerchin M., et al. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394 (1998) 485-490
89. Richard D.E., Berra E., and Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1a in vascular smooth muscle cells. J Biol Chem 275 (2000) 26765-26771
90. Scharte M., Han X., Bertges D.J., Fink M.P., and Delude R.L. Cytokines induce HIF-1 DNA binding and the expression of HIF-1 dependent genes in cultured rat enterocytes. Am J Physiol 284 (2003) G373-G384
91. Benyo D.F., Miles T.M., and Conrad K.P. Hypoxia stimulates cytokine production by villous explants from the human placenta. J Clin Endocrinol Metab 82 (1997) 1582-1588
92. Holcberg G., Huleihel M., Sapir O., Katz M., Tsadkin M., Furman B., et al. Increase production of tumor necrosis factor-alpha TNF-alpha by IUGR human placentae. Eur J Obstet Gynecol Reprod Biol 94 (2001) 69-72
93. Redman C.W., Sacks G.P., and Sargent I.L. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 180 (1999) 499-506
94. Bartha J.L., Romero-Carmona R., and Comino-Delgado R. Inflammatory cytokines in intrauterine growth retardation. Acta Obstet Gynecol Scand 82 (2003) 1099-1102
95. Tjoa M.L., van Vugt J.M.G., Go A.T.J.J., Blankenstein M.A., Oudejans C.B.M., and van Wijk I.J. Elevated C-reactive protein levels during first trimester of pregnancy are indicative of preeclampsia and intrauterine growth restriction. J Reprod Immunol 59 (2003) 29-37
96. Wolf M., Kettyle E., Sandler L., Ecker J.L., Roberts J., and Thadhani R. Obesity and preeclampsia: the potential role of inflammation. Obstet Gynecol 98 (2001) 757-762
97. Vince G.S., Starkey P.M., Austgulen R., Kwiatkowski D., and Redman C.W. Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with pre-eclampsia. BJOG 102 (1995) 20-25
98. Williams M.A., Farrand A., Mittendorf R., Sorensen T.K., Zingheim R.W., O'Reilly G.C., et al. Maternal second trimester serum tumor necrosis factor-alpha-soluble receptor p55 (sTNFp55) and subsequent risk of preeclampsia. Am J Epidemiol 149 (1999) 323-329
99. Savvidou M.D., Lees C.C., Parra M., Hingorani A.D., and Nicolaides K.H. Levels of c-reactive protein in pregnant women who subsequently developed preeclampsia. BJOG 109 (2002) 297-301
100. Sacks G.P., Studena K., Sargent K., and Redman C.W. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 179 (1998) 80-86
101. Benyo D.F., Smarason A., Redman C.W., Sims C., and Conrad K.P. Expression of inflammatory cytokines in placentas from women with preeclampsia. J Clin Endocrinol Metab 86 (2001) 2505-2512
102. Saito S., Umekage H., Sakamoto Y., Sakai M., Tanebe K., Sasaki Y., et al. Increased T-helper-1-type immunity and decreased T-helper-2-type immunity in patients with preeclampsia. Am J Reprod Immunol 41 (1999) 297-306
103. Kupferminc M.J., Peaceman A.M., Wigton T.R., Rehnberg K.A., and Socol M.L. Tumor necrosis factor-alpha is elevated in plasma and amniotic fluid of patients with severe preeclampsia. Am J Obstet Gynecol 170 (1994) 1752-1757
104. Schiff E., Friedman S.A., Baumann P., Sibai B.M., and Romero R. Tumor necrosis factor-alpha in pregnancies associated with preeclampsia or small-for-gestational-age newborns. Am J Obstet Gynecol 170 (1994) 1224-1229
105. Wang Y.P., and Walsh S.W. TNF-alpha concentrations and mRNA expression are increased in preeclamptic placentas. J Reprod Immunol 32 (1996) 157-169
106. Hara N., Fujii T., Okai T., and Taketani Y. Histochemical demonstration of interleukin-2 in deciduas cells of patients with preeclampsia. Am J Reprod Immunol 34 (1995) 44-51
107. Hennesy A., Pilmore H.L., Simmons L.A., and Painter D.M. A deficiency of placental IL-10 in preeclampsia. J Immunol 163 (1999) 3491-3495
108. Agarwal R., Loganath A., Roy A.C., Wong Y.C., and Ng S.C. Expression profiles of interleukin-15 in early and later gestational human placenta and in pre-eclamptic placenta. Mol Hum Reprod 7 (2001) 97-101
109. Munno I., Chiechi L.M., Lacedra G., Putignano G., Patimo C., Lobascio A., et al. Spontaneous and induced release of prostaglandins, interleukin (IL)-1beta, IL-6, and tumor necrosis factor-alpha by placental tissue from normal and preeclamptic pregnancies. Am J Reprod Immunol 42 (1999) 369-374
110. Rinehart B.K., Terrone D.A., Lagoo-Deenadayalan S., Barber W.H., Hale E.A., Martin Jr. J.N., et al. Expression of the placental cytokines tumor necrosis factor alpha, interleukin 1 beta, and interleukin 10 is increased in preeclampsia. Am J Obstet Gynecol 181 (1999) 915-920
111. Faas M.M., Schuiling G.A., Baller J.F., Visscher C.A., and Bakker W.W. A new animal model for human preeclampsia: ultra-low-dose endotoxin infusion in pregnant rats. Am J Obstet Gynecol 171 (1994) 158-164
112. Heine R.P., Ness R.B., and Roberts J.M. Seroprevalence of antibodies to Chlamydia pneumoniae in women with preeclampsia. Obstet Gynecol 101 (2003) 221-226
113. Sartelet H., Rogier C., Milko-Sartelet I., Angel G., and Michel G. Malaria associated pre-eclampsia in Senegal. Lancet 347 (1996) 1121
114. Hsu C.D., and Witter F.R. Urogenital infection in preeclampsia. Int J Gynaecol Obstet 49 (1995) 271-275
115. Mittendorf R., Lain K.Y., Williams M.A., and Walker C.K. Preeclampsia. A nested, case-control study of risk factors and their interactions. J Reprod Med 41 (1996) 491-496
116. Hill J.A., Devoe L.D., and Bryans Jr. C.I. Frequency of asymptomatic bacteriuria in preeclampsia. Obstet Gynecol 67 (1986) 529-532
117. Trogstad L.I., Eskild A., Bruu A.L., Jeansson S., and Jenum P.A. Is preeclampsia an infectious disease?. Acta Obstet Gynecol Scand 80 (2001) 1036-1038
118. Carreiras M., Montagnani S., and Layrisse Z. Preeclampsia: a multifactorial disease resulting from the interaction of the feto-maternal HLA genotype and HCMV infection. Am J Reprod Immunol 48 (2002) 176-183
119. von Dadelszen P., Magee L.A., Krajden M., Alasaly K., Popovska V., Devarakonda R.M., et al. Levels of antibodies against cytomegalovirus and Chlamydophila pneumoniae are increased in early onset pre-eclampsia. BJOG 110 (2003) 725-730
120. Wimalasundera R.C., Larbalestier N., Smith J.H., de Ruiter A., McG Thorn S.A., Hughes A.D., et al. Pre-eclampsia, antiretroviral therapy, and immune reconstitution. Lancet 360 (2002) 1152-1154
121. Sabatier F., Bretelle F., D'ercole C., Boubli L., Sampol J., and Dignat-George F. Neutrophil activation in preeclampsia and isolated intrauterine growth restriction. Am J Obstet Gynecol 183 (2000) 1558-1563
122. von Dadelszen P., Watson R.W., Noorwali F., Marshall J.C., Parodo J., Farine D., et al. Maternal neutrophil apoptosis in normal pregnancy, preeclampsia, and normotensive intrauterine growth restriction. Am J Obstet Gynecol 181 (1999) 408-414
123. Heinig J., Wilhelm S., Muller H., Briese V., Bittorf T., and Brock J. Determination of cytokine mRNA-expression in term human placenta of patients with gestational hypertension, intrauterine growth retardation and gestational diabetes mellitus using polymerase chain reaction. Zentralblatt Gynakologie 122 (2000) 413-418
124. Hahn-Zoric M., Hagberg H., Kjellmer I., Ellis J., Wennergren M., and Hanson L.A. Aberrations in placental cytokine mRNA related to intrauterine growth retardation. Pediatr Res 51 (2002) 201-206
125. Jacques S.M., and Qureshi F. Chronic chorioamnionitis: a clinicopathologic and immunohistochemical study. Human Pathol 29 (1998) 1457-1461
126. Moormann A.M., Sullivan A.D., Rochford R.A., Chensue S.W., Bock P.J., Nyirenda T., et al. Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J Infect Dis 180 (1999) 1987-1993
127. Matteelli A., Caligaris S., Castelli F., and Carosi G. The placenta and malaria. Ann Trop Med Parasitol 91 (1997) 803-810
128. Sattar N., and Greer I.A. Pregnancy complications and maternal cardiovascular risk: opportunities for intervention and screening?. BMJ 325 (2002) 157-160
129. Martin U., Davies C., Hayavi S., Hartland A., and Bunne F. Is normal pregnancy atherogenic?. Clin Sci 96 (1999) 421-425
130. Montes A., Walden C.E., Knopp R.H., Cheung M., Chapman M.B., and Albers J.J. Physiologic and supraphysiologic increases in lipoprotein lipids and apoproteins in late pregnancy and postpartum. Possible markers for the diagnosis of "prelipemia". Arterioscl 4 (1984) 407-417
131. Khan K.S., Hashmi F.A., and Rizvi J.H. Are non-diabetic women with abnormal glucose screening test at increased risk of pre-eclampsia, macrosomia and caesarean birth?. J Pakistan Med Assoc 45 (1995) 176-179
132. Joffe G.M., Esterlitz J.R., Levine R.J., Clemens J.D., Ewell M.G., Sibai B.M., et al. The relationship between abnormal glucose tolerance and hypertensive disorders of pregnancy in healthy nulliparous women. Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 179 (1998) 1032-1037
133. Wolf M., Sandler L., Munoz K., Hsu K., Ecker J.L., and Thadhani R. First trimester insulin resistance and subsequent preeclampsia: a prospective study. J Clin Endocrinol Metab 87 (2002) 1563-1568
134. Arbogast B., Leeper S., Merrick R., Olive K., and Taylor R. Which plasma factors bring about disturbance of endothelial function in pre-eclampsia?. Lancet 343 (1994) 340-341
135. Lorentzen B., Endresen M.J., Clausen T., and Henriksen T. Fasting serum free ftty acids and triglycerides are increased before 20 weeks of gestation in women who later develop preeclampsia. Hypertens Preg 13 (1994) 103-109
136. Lorentzen B., Drevon C.A., Endresen M.J., and Henriksen T. Fatty acid pattern of esterified and free fatty acids in sera of women with normal and pre-eclamptic pregnancy. BJOG 102 (1995) 530-537
137. Gratacos E., Casals E., Sanllehy C., Cararach V., Alonso P.L., and Fortuny A. Variation in lipid levels during pregnancy in women with different types of hypertension. Acta Obstet Gynecol Scand 75 (1996) 896-901
138. Eskenazi B., Fenster L., and Sidney S. A multivariate analysis of risk factors for preeclampsia. JAMA 266 (1991) 237-241
139. Sibai B.M., Ewell M., Levine R.J., Klebanoff M.A., Esterlitz J., Catalano P.M., et al. Risk factors associated with preeclampsia in healthy nulliparous women. Am J Obstet Gynecol 177 (1997) 1003-1010
140. Stone J.L., Lockwood C.J., Berkowitz G.S., Alvarez M., Lapinski R., and Berkowitz R.L. Risk factors for severe preeclampsia. Obstet Gynecol 83 (1994) 357-361
141. Bianco A.T., Smilen S.W., Davis Y., Lopez S., Lapinski R., and Lockwood C.J. Pregnancy outcome and weight gain recommendations for the morbidly obese woman. Obstet Gynecol 91 (1998) 97-102
142. Thadhani R., Stampfer M., Chasan-Taber L., Willett W., and Curhan G. A prospective study of pregravid oral contraceptive use and risk of hypertensive disorders of pregnancy. Contraception 60 (1999) 145-150
143. Ogunyemi D., Hullett S., Leeper J., and Risk A. Prepregnancy body mass index, weight gain during pregnancy, and perinatal outcome in a rural black population. J Matern Fetal Med 7 (1998) 190-193
144. Cedergren M.I. Maternal morbid obesity and the risk of adverse pregnancy outcome. Obstet Gynecol 103 (2004) 219-224
145. Han T.S., Williams K., Sattar N., Hunt K.J., Lean M.E., and Haffner S.M. Analysis of obesity and hyperinsulinemia in the development of metabolic syndrome: San Antonio Heart Study. Obesity Res 10 (2002) 923-931
146. Sattar N., Clark P., Holmes A., Lean M.E., Walker I., and Greer I.A. Antenatal waist circumference and hypertension risk. Obstet Gynecol 97 (2001) 268-271
147. Astedt B., Lindoff C., and Lecander I. Significance of the plasminogen activator inhibitor of placental type (PAI-2) in pregnancy. Semin Thromb Hemost 24 (1998) 431-435
148. Chappell L.C., Seed P.T., Briley A., Kelly F.J., Hunt B.J., Charnock-Jones D.S., et al. A longitudinal study of biochemical variables in women at risk of preeclampsia. Am J Obstet Gynecol 187 (2002) 127-136
149. Redman W.G., and Bonnar J. Plasma urate changes in pre-eclampsia. BMJ 1 (1978) 1484-1485
150. Stubbs T.M., Lazarchick J., Van Dorsten J.P., Cox J., and Loadholt C.B. Evidence of accelerated platelet production and consumption in nonthrombocytopenic preeclampsia. Am J Obstet Gynecol 155 (1986) 263-265
151. Davidge S.T., Signorella A.P., Lykins D.L., Gilmour C.H., and Roberts J.M. Evidence of endothelial activation and endothelial activators in cord blood of infants of preeclamptic women. Am J Obstet Gynecol 175 (1996) 1301-1306
152. Ramsey J.E., Ferrell W.R., Crawford L., Wallace A.M., Greer I.A., and Sattar N. Maternal obesity is associated with dysregulation of metabolic, vascular, and inflammatory pathways. J Clin Endocrinol Metab 87 (2002) 4231-4237
153. Nisell H., Erikssen C., Persson B., and Carlstrom K. Is carbohydrate metabolism altered among women who have undergone a preeclamptic pregnancy?. Gynecol Obstet Invest 48 (1999) 241-246
154. He S., Silveira A., Hamsten A., Blomback M., and Bremme K. Haemostatic, endothelial and lipoprotein parameters and blood pressure levels in women with a history of preeclampsia. Thromb Haemost 81 (1999) 538-542
155. Laivuori H., Tikkanen M.J., and Ylikorkala O. Hyperinsulinemia 17 years after preeclamptic first pregnancy. J Clin Endocrinol Metab 81 (1996) 2908-2911
156. Hubel C.A., Shaedal S., Ness R.B., Weissfeld L.A., Geirsson R.T., Roberts J.M., et al. Dyslipoproteinaemia in postmenopausal women with a history of eclampsia. BJOG 107 (2000) 776-784
157. Ramsay J.E., Stewart F., Greer I.A., and Sattar N. Microvascular dysfunction: a link between pre-eclampsia and maternal coronary heart disease. BJOG 110 (2003) 1029-1031
158. Moretti M., Phillips A., Abouzeid A., Catanco R.N., and Greenberg J. Increased birth markers of oxidative stress in normal pregnancy and in preeclampsia. Am J Obstet Gynecol 190 (2004) 1184-1190
159. Hubel C.A., Roberts J.M., Linheimer M.D., Roberts J.M., and Cunningham F.G. Lipid metabolism and oxidative stress. In: Lindheimer, Roberts, and Cunningham (Eds). Chesley's hypertensive disorders in pregnancy. 2nd ed. (1999), Appleton and Lange, Stanford (CT)
160. Stark J.M. Pre-eclampsia and cytokine induced oxidative stress. BJOG 100 (1993) 105-109
161. Vinatier D., and Monnier J.C. Pre-eclampsia: physiology and immunological aspects. Eur J Obstet Gynecol Reprod 61 (1995) 85-97
162. Renard C.B., Kramer F., Johansson F., Lamharzi N., Tannock L.R., von Herrath M.G., et al. Diabetes and diabetes-associated lipid abnormalitites have distinct effects on initiation and progression of atherosclerotic lesions. J Clin Invest 114 (2004) 659-668
163. Anonymous. Effect of intensive diabetes management on macrovascular events and risk factors in the Diabetes Control and Complications Trial. Am J Cardiol 75 (1995) 894-903
164. UK Prospective Study (UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352 (1998) 837-853
165. Sattar N., Greer I., Galloway P.J., Packard C.H., Shepherd J., Kelly T., et al. Lipid and lipoprotein concentrations in pregnancies complicated by intrauterine growth restriction. J Clin Endocrinol Metab 84 (1999) 128-130
166. Zeitlin J.A., Ancel P.Y., Saurel-Cubizokes M.J., and Papiernik E. Are risk factors the same for small for gestational age versus other preterm births?. Am J Obstet Gynecol 185 (2001) 208-215
167. Holmes R.P., Holly J.M., and Soothill P.W. Maternal insulin-like growth factor binding protein-1, body mass index, and fetal growth. Arch Dis Child Fetal Neonatal Ed 82 (2000) F113-F117
168. Bradley R.J., Nicolaides K.H., and Brudenell J.M. Are all infants of diabetic mothers "macrosomic"?. BMJ 297 (1988) 1583-1584
169. Coustan D.R., and Imarah J. Prophylactic insulin treatment of gestational diabetes reduces the incidence of macrosomia, operative delivery, and birth trauma. Am J Obstet Gynecol 150 (1984) 836-842
170. Coustan D.R., and Lewis S.B. Insulin therapy for gestational diabetes. Obstet Gynecol 51 (1978) 306-310
171. Rotter V., Nagaev I., and Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-α, overexpressed in human fat cells from insulin-resistant subjects. J Biol Chem 278 (2003) 45777-45784
172. Kirwan J.P., Hauguel-De Mouzon S., Lepercq J., Challier J., Huston-Presley L., Friedman J.E., et al. TNF-α is a predictor of insulin resistance in human pregnancy. Diabetes 51 (2002) 2207-2213
173. McDonald A.D., Armstrong B.G., and Sloan M. Cigarette, alcohol, and coffee consumption and prematurity. Am J Public Health 82 (1992) 87-90
174. Conde-Agudelo A., Althabe F., Belizan J., and Kafury-Goeta A. Cigarette smoking during pregnancy and risk of preeclampsia: a systematic review. Am J Obstet Gynecol 181 (1999) 1026-1035
175. Salafia C., and Shiverick K. Cigarette smoking and pregnancy. II Vascular effects. Placenta 20 (1999) 273-279