A new pathophysiological concept and new classification of pre-eclampsia

  • Ljiljana Mirković Faculty of Medicine, University of Belgrade, Belgrade, Serbia Clinic for Obstetrics and Gynecology, Clinical Centre of Serbia
  • Lazar Nejković University of Belgrade, Faculty of Medicine, Belgrade, Serbia; Clinic for Obstetrics and Gynecology “Narodni front”, Belgrade
  • Jelena Micić Clinical Center of Serbia, Clinic for Obstetrics and Gynecology, Belgrade
Keywords: pre-eclampsia;, diagnosis;, classification

References

Yapijakis C. Hippocrates of Kos, the father of clinical medi-cine, and Asclepiades of Bithynia, the father of molecular medicine. Review. In Vivo 2009; 23(4): 507−14.

Abalos E, Cuesta C, Carroli G, Qureshi Z, Widmer M, Vogel JP, et al. WHO Multicountry Survey on Maternal and Newborn Health Research Network. Pre-eclampsia, eclampsia and ad-verse maternal and perinatal outcomes: a secondary analysis of the World Health Organization Multicountry Survey on Ma-ternal and Newborn Health. BJOG 2014; 121(Suppl 1):14−24.

Cantwell R, Clutton-Brock T, Cooper G, Dawson A, Drife J, Garrod D, et al. Saving Mothers' Lives: Reviewing maternal deaths to make motherhood safer: 2006-2008. The Eighth Report of the Confidential Enquiries into Maternal Deaths in the United Kingdom. BJOG 2011; 118(Suppl1): 1−203.

Lisonkova S, Joseph KS. Incidence of preeclampsia: risk factors and outcomes associated with early- versus late-onset disease. Am J Obstet Gynecol 2013; 209(6): 544.e1−544.e12.

Wallis AB, Saftlas AF, Hsia J, Atrash HK. Secular trends in the rates of preeclampsia, eclampsia, and gestational hyper-tension, United States, 1987-2004. Am J Hypertens 2008; 21(5): 521−6.

Word Health Organisation. The world health report: Make every mother and child count. Geneva: WHO; 2005. Available from: http//www-who.int/whr/2005/whr2005_en.pdf

Duley L. Maternal mortality associated with hypertensive dis-orders of pregnancy in Africa, Asia, Latin America and the Ca-ribbean. Br J Obstet Gynaecol 1992; 99(7): 547−53.

Callaghan WM, Mackay AP, Berg CJ. Identification of severe maternal morbidity during delivery hospitalizations, United States, 1991-2003. Am J Obstet Gynecol 2008; 199(2): 133.e1−8.

Kuklin EV, Ayala C, Callaghan WM. Hypertenesive disorders and severe obstetric morbidity in the United State. Obstet Gynecol 2009; 113(6): 1299−306.

Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: Sys-tematic review and meta-analysis. BMJ 2007; 335(7627): 974.

Armanini D, Sabbadin C, Donà G, Andrisani A, Ambrosini G, Bordin L. Maternal and fetal outcomes in Preeclampsia: Interrelations between Insulin Resistance, Aldosterone, Metabolic Syndrome, and Polycystic Ovary Syndrome. J Clin Hypertens (Greenwich) 2015; 17(10): 783−5.

Burton GJ, Jauniaux E. Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br J Ob-stet Gynaecol 1995; 102(10): 818−25.

Burton GJ, Charnock-Jones DS, Jauniaux E. Regulation of vascu-lar growth and function in the human placenta. Reproduction 2009; 138(6): 895−902.

Hunter W. Anatomia uteri humani gravidi tabulis illustrata. The Anatomy of the Human Gravid Uterus exhibited in Figures. Birmingham: John Baskerville, 1774.

Grosser O. Frühentwicklung, Eihautbildung und placentation des Menschen und der Säugetiere. München: J.F. Bergmann; 1927.

Lyall F, Robson S, Bulmer J. Spiral artery remodeling and tro-phoblast invasion in preeclampsia and fetal growth restriction. Hypertension 2013; 62(6): 1046−54.

Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983; 4(4): 397−413.

Khong TY. Placental vascular development and neonatal out-come. Semin Neonatol 2004; 9(4): 255−63.

Romero R, Dey SK, Fisher SJ. Preterm labor: One syndrome, many causes. Science 2014; 345(6198): 760−5.

Brosens I, Pijnenborg R, Vercruysset L, Romero R. The Great Ob-stetrical Syndromes are associated with disorders of deep pla-centation. Am J Obstet Gynecol 2011; 204(3): 193−201.

Mistry HD, Wilson V, Ramsay MM, Symonds ME, Broughton Pipkin F. Reduced selenium concentrations and glutathione peroxidase activity in preeclamptic pregnancies. Hypertension 2008; 52(5): 881−8.

Poston L, Raijmakers MT. Trophoblast oxidative stress, antioxidants and pregnancy outcome: A review. Placenta 2004; 25 Suppl A: S72−8.

Zeeman GG, Dekker GA, van Geijn HP, Kraayenbrink AA. Endothelial function in normal and pre-eclamptic pregnancy: a hypothesis. Eur J Obstet Gynecol Reprod Biol 1992; 43(2): 113−22.

Critchley H, MacLean A, Poston L, Walker JJ. Pre-eclampsia. London: RCOG Press; 2004.

Duracková Z. Some current insights into oxidative stress. Phy-siol Res 2010; 59(4): 459−69.

Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human placental development by oxygen tension. Science 1997; 277(5332): 1669−72.

Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signaling. Biochem J 2012; 441(2): 523−40.

Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008; 454(7203): 455−62.

Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS. Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 2009; 30 Suppl A: S43−8.

Redman CW, Sargent IL. Microparticles and immunomodula-tion in pregnancy and pre-eclampsia. J Reprod Immunol 2007; 76(1−2): 61−7.

Wu F, Tian FJ, Lin Y. Oxidative Stress in Placenta: Health and Diseases. Biomed Res Int 2015; 2015: 293271.

Vince GS, Starkey PM, Austgulen R, Kwiatkowski D, Redman CW. Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with pre-eclampsia. Br J Obstet Gynaecol 1995; 102(1): 20−5.

Cackovic M, Buhimschi CS, Zhao G, Funai EF, Norwitz ER, Kuc-zynski E,et al. Fractional excretion of tumor necrosis factor-alpha in women with severe preeclampsia. Obstet Gynecol 2008; 112(1): 93−100.

Sunder-Plassmann G, Derfler K, Wagner L, Stockenhuber F, Endler M, Nowotny C, et al.Increased serum activity of interleukin-2 in patients with pre-eclampsia. J Autoimmun 1989; 2(2): 203−5.

Wang W, Irani RA, Zhang Y, Ramin SM, Blackwell SC, Tao L, et al. Autoantibody-mediated complement C3a receptor activation contributes to the pathogenesis of preeclampsia. Hypertension 2012; 60(3): 712−21.

Ahmad S, Ahmed A. Elevated placental soluble vascular endo-thelial growth factor receptor-1 inhibits angiogenesis in preec-lampsia. Circ Res 2004; 95(9): 884−91.

Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350(7): 672−83.

Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12(6): 642−9.

Gervasi MT, Chaiworapongsa T, Naccasha N, Blackwell S, Yoon BH, Maymon E, et al. Phenotypic and metabolic characteristics of maternal monocytes and granulocytes in preterm labor with intact membranes. Am J Obstet Gynecol 2001; 185(5): 1124−9.

Gervasi MT, Chaiworapongsa T, Naccasha N, Pacora P, Berman S, Maymon E, et al. Maternal intravascular inflammation in pre-term premature rupture of membranes. J Matern Fetal Neo-natal Med 2002; 11(3): 171−5.

Sabatier F, Bretelle F, D'ercole C, Boubli L, Sampol J, Dignat-George F. Neutrophil activation in preeclampsia and isolated intrauterine growth restriction. Am J Obstet Gynecol 2000; 183(6): 1558−63.

Ogge G, Romero R, Chaiworapongsa T, Gervasi MT, Pacora P, Erez O, et al. Leukocytes of pregnant women with small-for-gestational age neonates have a different phenotypic and me-tabolic activity from those of women with preeclampsia. J Ma-tern Fetal Neonatal Med 2010; 23(6): 476−87.

Naccasha N, Gervasi MT, Chaiworapongsa T, Berman S, Yoon BH, Maymon E, et al. Phenotypic and metabolic characteristics of monocytes and granulocytes in normal pregnancy and maternal infection. Am J Obstet Gynecol 2001; 185(5): 1118−23.

Borzychowski AM, Sargent IL, Redman CW. Inflammation and pre-eclampsia. Semin Fetal Neonatal Med 2006; 11(5): 309−16.

Ramma W, Buhimschi IA, Zhao G, Dulay AT, Nayeri UA, Buhimschi CS, et al. The elevation in circulating anti-angiogenic factors is independent of markers of neutrophil activation in preeclampsia. Angiogenesis 2012; 15(3): 333−4.

Shibuya M. Vascular endotelial growth factor and its receptor system: Physiological functions in angiogenesis and pathologi-cal roles in various diseases. J Biochem 2013; 153(1): 13−9.

Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PlGF) and soluble Flt-1 by oxygen: A review. Placenta 2000; 21 Suppl A: S16−24.

Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxiainducible factor 1. Mol Cell Biol 1996; 16(9): 4604−13.

Verlohren S, Galindo A, Schlembach D, Zeisler H, Herraiz I, Moertl MG, et al. An automated method for the determination of the sFlt-1/PlGF ratio in the assessment of preeclampsia. Am J Obstet Gynecol 2010; 202(2): 161.e1−161.e11.

Verlohren S, Herraiz I, Lapaire O, Schlembach D, Moertl M, Zeisler H, et al. The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am J Obstet Gynecol 2012; 206(1): 58.e1−8.

Verlohren S, Herraiz I, Lapaire O, Schlembach D, Zeisler H, Calda P, et al. New gestational phase-specific cutoff values for the use of the soluble fms-like tyrosine kinase-1/placental growth factor ratio as a diagnostic test for preeclampsia. Hy-pertension 2014; 63(2): 346−52.

Álvarez-Fernández I, Prieto B, Rodríguez V, Ruano Y, Escudero AI, Álvarez FV. New biomarkers in diagnosis of early onset preeclampsia and imminent delivery prognosis. Clin Chem Lab Med 2014; 52(8): 1159−68.

Pinheiro CC, Rayol P, Gozzani L, Reis LM, Zampieri G, Dias CB, et al. The relationship of angiogenic factors to maternal and neonatal manifestations of early-onset and late-onset preeclampsia. Prenat Diagn 2014; 34(11): 1084−92.

Chaiworapongsa T, Romero R, Savasan ZA, Kusanovic JP, Ogge G, Soto E, et al. Maternal plasma concentrations of angiogen-ic/anti-angiogenic factors are of prognostic value in patients presenting to the obstetrical triage area with the suspicion of preeclampsia. J Matern Fetal Neonatal Med 2011; 24(10): 1187-207.

Schaarschmidt W, Rana S, Stepan H. The course of angiogenic factors in early- vs. late-onset preeclampsia and HELLP syn-drome. J Perinat Med 2013; 41(5): 511−6.

Chaiworapongsa T, Romero R, Korzeniewski SJ, Kusanovic JP, Soto E, Lam J, et al. Maternal plasma concentrations of angiogen-ic/antiangiogenic factors in the third trimester of pregnancy to identify the patient at risk for stillbirth at or near term and se-vere late preeclampsia. Am J Obstet Gynecol 2013; 208(4): 287.e1−287.e15.

Chaiworapongsa T, Romero R, Korzeniewski SJ, Cortez JM, Pappas A, Tarca AL, et al. Plasma concentrations of angiogenic/anti-angiogenic factors have prognostic value in women presenting with suspected preeclampsia to the obstetrical triage area: a prospective study. J Matern Fetal Neonatal Med 2014; 27(2): 132−44.

German guideline. 2015. Available from: http://www.awmf.org/uploads/tx_szleitlinien/015-018l_S1_Diagnostik_Therapie_hypertensiver_Schwangerschaftserkrankungen_2014-01.pdf [accessed 2015 January].

Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, Mclaughlin MK. Preeclampsia: An endothelial cell disorder. Am J Obstet Gynecol 1989; 161(5): 1200−4.

Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350(7): 672−83.

Maynard SE, Min JY, Merchan J, Lim KH, 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 2003; 111(5): 649−58.

Maharaj AS, Walshe TE, Saint-Geniez M, Venkatesha S, Maldonado AE, Himes NC, et al. VEGF and TGF-beta are re-quired for the maintenance of the choroid plexus and ependyma. J Exp Med 2008; 205(2): 491−501.

Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, Anderson GD, et al. The effect of over-expression of sflt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol 2007; 196(4): 396.e1−7; discussion 396.e7.

Thadhani R, Kisner T, Hagmann H, Bossung V, Noack S, Schaar-schmidt W, et al. Pilot study of extracorporeal removal of so-luble fms-like tyrosine kinase 1 in preeclampsia. Circulation 2011; 124(8): 940−50.

Ramma W, Ahmed A. Is inflammation the cause of pre-eclampsia?. Biochem Soc Trans 2011; 39(6): 1619−27.

Herraiz I, Simón E, Gómez-Arriaga PI, Martínez-Moratalla JM, García-Burguillo A, López JE, et al. Angiogenesis-Related Bio-markers (sFlt-1/PLGF) in the Prediction and Diagnosis of Placental Dysfunction: An Approach for Clinical Integration. Int J Mol Sci 2015; 16(8): 19009−26.

Gant NF, Chand S, Whalley PJ, Macdonald PJ. The nature of pressor responsiveness to angiotensin II in human pregnancy. Obstet Gynecol 1974; 43(6): 854.

Dechend R, Luft FC, Lindheimer MD.. Agonistic autoantibody-mediated disease. In: Lindheimer MD, Roberts JM, Cunningham FG, editors. Chesley's Hypertensive Disorders in Pregnancy. 3rd ed. San Diego: Elsevier; 2009. p. 287−96.

Parrish MR, Murphy SR, Rutland S, Wallace K, Wenzel K, Wallukat G, et al. The effect of immune factors, tumor necro-sis factor-alpha, and agonistic autoantibodies to the angioten-sin II type I receptor on soluble fms-like tyrosine-1 and soluble endoglin production in response to hypertension during pregnancy. Am J Hypertens 2010; 23(8): 911−6.

Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203(9): 2165−75.

Romero R, Vizoso J, Emamian M, Duffy T, Riely C, Halford T, et al. Clinical significance of liver dysfunction in pregnancy-induced hypertension. Am J Perinatol 1988; 5(2): 146−51.

Kenny LC, Baker PN, Cunningham FG. Platelets, coagulation, and the liver. In: Lindheimer MD, Roberts JM, Cunningham GC, editors. Chesley’s hypertensive disorders in pregnancy. San Di-ego: Elsevier; 2009. p. 335–51.

Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: new concepts in an old disease. SeminPerinatol 1988; 12(4): 302−23.

Walsh SW. Preeclampsia: an imbalance in placental prostacyc-lin and thromboxane production. Am J Obstet Gynecol 1985; 152(3): 335−40.

Cadroy Y, Grandjean H, Pichon J, Desprats R, Berrebi A, Fournié A, et al. Evaluation of six markers of haemostatic system in normal pregnancy and pregnancy complicated by hypertension or pre-eclampsia. Br J Obstet Gynaecol 1993; 100(5): 416−20.

Chaiworapongsa T, Yoshimatsu J, Espinoza J, Kim YM, Berman S, Edwin S, et al. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med 2002; 11(6): 362−7.

Kobayashi T, Tokunaga N, Sugimura M, Kanayama N, Terao T. Predictive values of coagulation/fibrinolysis parameters for the termination of pregnancy complicated by severe preeclampsia. Semin Thromb Hemost 2001; 27(2): 137−141.

Ambros V. The functions of animal microRNAs. Nature 2004; 431(7006): 350−5.

Fu G, Brkic J, Hayder H, Peng C. MicroRNAs in human placen-tal development and pregnancy complications. Int J Mol Sci 2013; 14(3): 5519−44.

Wang S, Olson AE. AngiomiR-skey regulators of angiogenesis. Curr Opin Genet 2009; 19(3): 205−11.

Wu F, Yang Z, Li G. Role of specific microRNAs for endo-thelial function and angiogenesis. Biochem Biophys Res Commun 2009; 386(4): 549−53.

Abdelhalim RM, Ramadan DI, Zeyada R, Nasr AS, Mandour IA. Circulating Maternal Total Cell-Free DNA, Cell-Free Fetal DNA and Soluble Endoglin Levels in Preeclampsia: Predictors of Adverse Fetal Outcome?, A Cohort Study. Mol Diagn Ther 2016; 20(2): 135−49.

Report of the National High Blood Pressure Education Pro-gram Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol 2000; 183(1): S1−S22.

Brown MA, Lindheimer MD, de Swiet M, Van Assche A, Moutquin JM. The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society fort he Study of Hypertension in Pregnancy (ISSHP). Hypertens Pregnancy 2001; 20(1): 9−14.

ACOG Committee on Obstetric Practice. ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet 2002; 77(1): 67−75.

Lowe SA, Brown MA, Dekker GA, Gatt S, McLintock CK, McMahon LP, et al. Society of Obstetric Medicine of Australia and New Zealand. Guidelines for the management of hyper-tensive disorders of pregnancy 2008. Aust N Z J Obstet Gynaecol 2009; 49(3): 242−6.

Turner JA. Diagnosis and management of pre-eclampsia: An update. Int J Womens Health 2010; 2: 327−37.

National Collaborating Centre for Women’s and Children’s Health 2011. Commissioned by the National Institute for Health and Clinical Excellence. Available from: http://www.nice.org.uk/nicemedia/live/13098/50475/50475.pdf [accessed 2011 May 31].

American College of Obstetricians and Gynecologists. Task Force on Hypertension in Pregnancy . Hypertension in Pregnancy. Re-port of the American College of Obstetricians and Gynecolo-gists’ Task Force on Hypertension in Pregnancy. Obstet Gy-necol 2013; 122(5): 1122−31.

Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 2005; 365(9461): 785−99.

Lisonkova S, Sabr Y, Mayer C, Young C, Skoll A, Joseph KS. Ma-ternal morbidity associated with early-onset and late-onset preeclampsia. Obstet Gynecol 2014; 124(4): 771−81.

von Dadelszen P, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003; 22(2): 143−8.

Thornton CE, Makris A, Ogle RF, Tooher JM, Hennessy A. Role of proteinuria in defining pre-eclampsia: Clinical outcomes for women and babies. Clin Exp Pharmacol Physiol 2010; 37(4): 466−70.

Homer CS, Brown MA, Mangos G, Davis GK. Non-proteinuric pre-eclampsia: A novel risk indicator in women with gestational hypertension. J Hypertens 2008; 26(2): 295−302.

National Collaborating Centre for Women's and Children's Health (UK). Hypertension in Pregnancy: The Management of Hyper-tensive Disorders During Pregnancy. London: RCOG Press; 2010.

von Dadelszen P, Payne B, Li J, Ansermino JM, Pipkin BF, Cote AM, et al. Prediction of adverse maternal outcomes in pre-eclampsia: Development and valdation of the fullPIERS mod-el. PIERS Study Group. Lancet 2011; 377(9761): 219−27.

Ditisheim A, Boulvain M, Irion O, Pechère-Bertschi A. Atypical presentation of preeclampsia. Rev Med Suisse 2015; 11(485): 1655−8. (French)

Seely EW, Ecker J. Clinical practice. Chronic hypertension in pregnancy. N Engl J Med 2011; 365(5): 439−46.

Fisher KA, Luger A, Spargo BH, Lindheimer MD. Hypertension in pregnancy: clinical- pathological correlations and remote prognosis. Medicine (Baltimore) 1981; 60(4): 267.

Published
2020/10/22
Section
Current Topic