Maternal hemodynamics: a method to classify hypertensive disorders of pregnancy

Published:November 01, 2017DOI:


      The classification of hypertensive disorders of pregnancy is based on the time at the onset of hypertension, proteinuria, and other associated complications. Maternal hemodynamic interrogation in hypertensive disorders of pregnancy considers not only the peripheral blood pressure but also the entire cardiovascular system, and it might help to classify the different clinical phenotypes of this syndrome.


      This study aimed to examine cardiovascular parameters in a cohort of patients affected by hypertensive disorders of pregnancy according to the clinical phenotypes that prioritize fetoplacental characteristics and not the time at onset of hypertensive disorders of pregnancy.

      Study Design

      At the fetal-maternal medicine unit of Ziekenhuis Oost-Limburg (Genk, Belgium), maternal cardiovascular parameters were obtained through impedance cardiography using a noninvasive continuous cardiac output monitor with the patients placed in a standing position. The patients were classified as pregnant women with hypertensive disorders of pregnancy who delivered appropriate- and small-for-gestational-age fetuses. Normotensive pregnant women with an appropriate-for-gestational-age fetus at delivery were enrolled as the control group. The possible impact of obesity (body mass index ≥30 kg/m2) on maternal hemodynamics was reassessed in the same groups.


      Maternal age, parity, body mass index, and blood pressure were not significantly different between the hypertensive disorders of pregnancy/appropriate-for-gestational-age and hypertensive disorders of pregnancy/small-for-gestational-age groups. The mean uterine artery pulsatility index was significantly higher in the hypertensive disorders of pregnancy/small-for-gestational-age group. The cardiac output and cardiac index were significantly lower in the hypertensive disorders of pregnancy/small-for-gestational-age group (cardiac output 6.5 L/min, cardiac index 3.6) than in the hypertensive disorders of pregnancy/appropriate-for-gestational-age group (cardiac output 7.6 L/min, cardiac index 3.9) but not between the hypertensive disorders of pregnancy/appropriate-for-gestational-age and control groups (cardiac output 7.6 L/min, cardiac index 4.0). Total vascular resistance was significantly higher in the hypertensive disorders of pregnancy/small-for-gestational-age group than in the hypertensive disorders of pregnancy/appropriate-for-gestational-age group and the control group. All women with hypertensive disorders of pregnancy showed signs of central arterial dysfunction. The cardiovascular parameters were not influenced by gestational age at the onset of hypertensive disorders of pregnancy, and no difference was observed between the women with appropriate-for-gestational-age fetuses affected by preeclampsia or by gestational hypertension with appropriate-for-gestational-age fetuses. Women in the obese/hypertensive disorders of pregnancy/appropriate-for-gestational-age and obese/hypertensive disorders of pregnancy/small-for-gestational-age groups showed a significant increase in cardiac output, as well as significant changes in other parameters, compared with the nonobese/hypertensive disorders of pregnancy/appropriate-for-gestational-age and nonobese/hypertensive disorders of pregnancy/small-for-gestational-age groups.


      Significantly low cardiac output and high total vascular resistance characterized the women with hypertensive disorders of pregnancy associated with small for gestational age due to placental insufficiency, independent of the gestational age at the onset of hypertension. The cardiovascular parameters were not significantly different in the women with appropriate-for-gestational-age or small-for-gestational-age fetuses affected by preeclampsia or gestational hypertension. These findings support the view that maternal hemodynamics may be a candidate diagnostic tool to identify hypertensive disorders in pregnancies associated with small-for-gestational-age fetuses. This additional tool matches other reported evidence provided by uterine Doppler velocimetry, low vascular growth factors in the first trimester, and placental pathology. Obesity is associated with a significantly higher cardiac output and outweighs other determinants of hemodynamics in pregnancy; therefore, in future studies on hypertensive disorders, obesity should be studied as an additional disease and not simply as a demographic characteristic.

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        • National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy
        Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy.
        Am J Obstet Gynecol. 2000; 183: s1-s22
        • Stevens W.
        • Shih T.
        • Incerti D.
        • et al.
        Short-term costs of preeclampsia to the United States health care system.
        Am J Obstet Gynecol. 2017; 217: 237-248.e16
        • Li R.
        • Tsigas E.Z.
        • Callaghan W.M.
        Health and economic burden of preeclampsia: no time for complacency.
        Am J Obstet Gynecol. 2017; 217: 235-236
        • Bokslag A.
        • Teunissen P.W.
        • Franssen C.
        • et al.
        Effect of early-onset preeclampsia on cardiovascular risk in the fifth decade of life.
        Am J Obstet Gynecol. 2017; 216: 523.e1-523.e7
        • Shields L.E.
        • Wiesner S.
        • Klein C.
        • Pelletreau B.
        • Hedriana H.L.
        Early standardized treatment of critical blood pressure elevations is associated with a reduction in eclampsia and severe maternal morbidity.
        Am J Obstet Gynecol. 2017; 216: 415.e1-415.e5
        • White W.M.
        • Mielke M.M.
        • Araoz P.A.
        • et al.
        A history of preeclampsia is associated with a risk for coronary artery calcification 3 decades later.
        Am J Obstet Gynecol. 2016; 214: 519.e1-519.e8
        • Kilpatrick S.J.
        • Abreo A.
        • Greene N.
        • et al.
        Severe maternal morbidity in a large cohort of women with acute severe intrapartum hypertension.
        Am J Obstet Gynecol. 2016; 215: 91.e1-91.e7
        • Redman C.W.G.
        • Staff A.C.
        Preeclampsia, biomarkers, syncytiotrophoblast stress, and placental capacity.
        Am J Obstet Gynecol. 2015; 213: S9.e1-S9.e4
        • Ness R.B.
        • Roberts J.M.
        Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications.
        Am J Obstet Gynecol. 1996; 175: 1365-1370
        • Borzychowski A.M.
        • Sargent I.L.
        • Redman C.W.G.
        Inflammation and pre-eclampsia.
        Semin Fetal Neonatal Med. 2006; 11: 309-316
        • Redman C.W.
        • Sargent I.L.
        • Staff A.C.
        IFPA Senior Award Lecture: Making sense of pre-eclampsia.
        Placenta. 2014; 35: S20-S25
        • Staff A.C.
        • Redman C.W.G.
        IFPA Award in Placentology Lecture: Preeclampsia, the decidual battleground and future maternal cardiovascular disease.
        Placenta. 2014; 35: S26-S31
        • Valensise H.
        • Vasapollo B.
        • Gagliardi G.
        • Novelli G.P.
        Early and late preeclampsia: two different maternal hemodynamic states in the latent phase of the disease.
        Hypertension. 2008; 52: 873-880
        • Stevens D.U.
        • Al-Nasiry S.
        • Fajta M.M.
        • et al.
        Cardiovascular and thrombogenic risk of decidual vasculopathy in preeclampsia.
        Am J Obstet Gynecol. 2014; 210: 545.e1-545.e6
        • Melchiorre K.
        • Sutherland G.
        • Sharma R.
        • Nanni M.
        • Thilaganathan B.
        Mid-gestational maternal cardiovascular profile in preterm and term pre-eclampsia: a prospective study.
        BJOG. 2012; 120: 496-504
        • Gyselaers W.
        • Staelens A.
        • Mesens T.
        • et al.
        Maternal venous Doppler characteristics are abnormal in pre-eclampsia but not in gestational hypertension.
        Ultrasound Obstet Gynecol. 2015; 45: 421-426
        • Verbraecken J.
        • Van de Heyning P.
        • De Backer W.
        • Van Gaal L.
        Body surface area in normal-weight, overweight, and obese adults. A comparison study.
        Metabolism. 2006; 55: 515-524
        • Kubicek W.G.
        • Karnegis J.N.
        • Patterson R.P.
        • Witsoe D.A.
        • Mattson R.H.
        Development and evaluation of an impedance cardiac output system.
        Aerosp Med. 1966; 37: 1208-1212
        • Tomsin K.
        • Mesens T.
        • Molenberghs G.
        • Gyselaers W.
        Diurnal and position-induced variability of impedance cardiography measurements in healthy subjects.
        Clin Physiol Funct Imaging. 2011; 31: 145-150
        • Tomsin K.
        • Mesens T.
        • Molenberghs G.
        • Gyselaers W.
        Impedance cardiography in uncomplicated pregnancy and pre-eclampsia: a reliability study.
        J Obstet Gynaecol. 2012; 32: 630-634
        • Gyselaers W.
        • Mullens W.
        • Tomsin K.
        • Mesens T.
        • Peeters L.
        Role of dysfunctional maternal venous hemodynamics in the pathophysiology of pre-eclampsia: a review.
        Ultrasound Obstet Gynecol. 2011; 38: 123-129
        • Vonck S.
        • Staelens A.S.
        • Mesens T.
        • Tomsin K.
        • Gyselaers W.
        Hepatic hemodynamics and fetal growth: a relationship of interest for further research.
        PLoS One. 2014; 9 (e115594–10)
        • Thilaganathan B.
        Placental syndromes: getting to the heart of the matter.
        Ultrasound Obstet Gynecol. 2017; 49: 7-9
        • Easterling T.R.
        • Benedetti T.J.
        • Carlson K.C.
        • Brateng D.A.
        • Wilson J.
        • Schmucker B.S.
        The effect of maternal hemodynamics on fetal growth in hypertensive pregnancies.
        Am J Obstet Gynecol. 1991; 165: 902-906
        • Vasapollo B.
        • Valensise H.
        • Novelli G.P.
        • et al.
        Abnormal maternal cardiac function and morphology in pregnancies complicated by intrauterine fetal growth restriction.
        Ultrasound Obstet Gynecol. 2002; 20: 452-457
        • Tomsin K.
        • Mesens T.
        • Molenberghs G.
        • Peeters L.
        • Gyselaers W.
        Characteristics of heart, arteries, and veins in low and high cardiac output preeclampsia.
        Eur J Obstet Gynecol Reprod Biol. 2013; 169: 218-222
        • Khalil A.
        • Sodre D.
        • Syngelaki A.
        • Akolekar R.
        • Nicolaides K.H.
        Maternal hemodynamics at 11-13 weeks of gestation in pregnancies delivering small for gestational age neonates.
        Fetal Diagn Ther. 2012; 32: 231-238
        • Salas S.P.
        • Marshall G.
        • Gutierrez B.L.
        • Rosso P.
        Time course of maternal plasma volume and hormonal changes in women with preeclampsia or fetal growth restriction.
        Hypertension. 2006; 47: 203-208
        • Melchiorre K.
        • Sutherland G.R.
        • Baltabaeva A.
        • Liberati M.
        • Thilaganathan B.
        Maternal cardiac dysfunction and remodeling in women with preeclampsia at term.
        Hypertension. 2010; 57: 85-93
        • Egbor M.
        • Ansari T.
        • Morris N.
        • Green C.J.
        • Sibbons P.D.
        Maternal medicine: morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction.
        BJOG. 2006; 113: 580-589
        • Frohlich E.D.
        • Susic D.
        Mechanisms underlying obesity associated with systemic and renal hemodynamics in essential hypertension.
        Curr Hypertens Rep. 2008; 10: 151-155
        • Hall J.E.
        • do Carmo J.M.
        • da Silva A.A.
        • Wang Z.
        • Hall M.E.
        Obesity-induced hypertension: interaction of neurohumoral and renal mechanisms.
        Circ Res. 2015; 116: 991-1006
        • Kawarazaki W.
        • Fujita T.
        The role of aldosterone in obesity-related hypertension.
        Am J Hypertens. 2016; 29: 415-423
        • Xie D.
        • Bollag W.B.
        Obesity, hypertension and aldosterone: is leptin the link?.
        J Endocrinol. 2016; 230: F7-F11
        • Stelfox H.T.
        • Ahmed S.B.
        • Ribeiro R.A.
        • Gettings E.M.
        • Pomerantsev E.
        • Schmidt U.
        Hemodynamic monitoring in obese patients: the impact of body mass index on cardiac output and stroke volume.
        Crit Care Med. 2006; 34: 1243-1246
        • Rigano S.
        • Ferrazzi E.
        • Boito S.
        • Pennati G.
        • Padoan A.
        • Galan H.
        Blood flow volume of uterine arteries in human pregnancies determined using 3D and bi-dimensional imaging, angio-Doppler, and fluid-dynamic modeling.
        Placenta. 2010; 31: 37-43
        • Konje J.
        Longitudinal quantification of uterine artery blood volume flow changes during gestation in pregnancies complicated by intrauterine growth restriction.
        BJOG. 2003; 110: 301-305
        • Flo K.
        • Wilsgaard T.
        • Vårtun A.
        • Acharya G.
        A longitudinal study of the relationship between maternal cardiac output measured by impedance cardiography and uterine artery blood flow in the second half of pregnancy.
        BJOG. 2010; 117: 837-844
        • Lees C.
        • Ferrazzi E.
        Relevance of hemodynamics in treating pre-eclampsia.
        Curr Hypertens Rep. 2017; 19: 1-5
        • Ray J.G.
        • Vermeulen M.J.
        • Schull M.J.
        • Redelmeier D.A.
        Cardiovascular health after maternal placental syndromes (CHAMPS): population-based retrospective cohort study.
        Lancet. 2005; 366: 1797-1803
        • Staff A.C.
        • Redman C.W.
        • Williams D.
        • et al.
        Pregnancy and long-term maternal cardiovascular health.
        Hypertension. 2016; 67: 251-260
        • Scholten R.R.
        • Sep S.
        • Peeters L.
        • Hopman M.T.E.
        • Lotgering F.K.
        • Spaanderman M.E.A.
        Prepregnancy low-plasma volume and predisposition to preeclampsia and fetal growth restriction.
        Obstet Gynecol. 2011; 117: 1085-1093
        • Scholten R.R.
        • Thijssen D.J.H.
        • Lotgering F.K.
        • Hopman M.T.E.
        • Spaanderman M.E.A.
        Cardiovascular effects of aerobic exercise training in formerly preeclamptic women and healthy parous control subjects.
        Am J Obstet Gynecol. 2014; 211: 516.e1-516.e11
        • Marconi A.M.
        • Ronzoni S.
        • Bozzetti P.
        • Vailati S.
        • Morabito A.
        • Battaglia F.C.
        Comparison of fetal and neonatal growth curves in detecting growth restriction.
        Obstet Gynecol. 2008; 112: 1227-1234
        • Ferrazzi E.
        • Zullino S.
        • Stampalija T.
        • et al.
        Bedside diagnosis of two major clinical phenotypes of hypertensive disorders of pregnancy.
        Ultrasound Obstet Gynecol. 2016; 48: 224-231
        • Levine R.J.
        • Maynard S.E.
        • Qian C.
        • et al.
        Circulating angiogenic factors and the risk of preeclampsia.
        N Engl J Med. 2004; 350: 672-683
        • Meah V.L.
        • Cockcroft J.R.
        • Backx K.
        • Shave R.
        • Stöhr E.J.
        Cardiac output and related hemodynamics during pregnancy: a series of meta-analyses.
        Heart. 2016; 102: 518-526
        • Burton G.J.
        • Woods A.W.
        • Jauniaux E.
        • Kingdom J.C.P.
        Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy.
        Placenta. 2010; 30: 473-482
        • de Haas S.
        • Ghossein-Doha C.
        • van Kuijk S.M.J.
        • van Drongelen J.
        • Spaanderman M.E.A.
        Physiological adaptation of maternal plasma volume during pregnancy: a systematic review and meta-analysis.
        Ultrasound Obstet Gynecol. 2017; 49: 177-187