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 Table of Contents  
Year : 2020  |  Volume : 4  |  Issue : 1  |  Page : 78-83

Assessment of the left ventricular function in hypertensive pregnant women with or without proteinuria: two-dimensional versus four-dimensional echocardiographic study

1 Department of Cardiology, Faculty of Medicine (for Girls), Al-Azhar University, Cairo, Egypt
2 Department of Obstetrics and Gynecology, ART Unit, International Islamic Institute, Al-Azhar University, Cairo, Egypt

Date of Submission24-Jan-2020
Date of Decision26-Jan-2020
Date of Acceptance06-Feb-2020
Date of Web Publication20-Apr-2020

Correspondence Address:
Shaimaa A Habib
Department of Cardiology, Faculty of Medicine (for Girls), Al-Azhar University, Cairo, 11827
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sjamf.sjamf_9_20

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Background Assessment of left ventricular (LV) function by speckle tracking echocardiography (STE) can detect subtle changes in LV function in preeclampsia. We aimed to assess LV function using two-dimensional (2D) versus four-dimensional (4D) echocardiography in hypertensive (HTN) pregnant women with or without proteinuria.
Patients and methods This study comprised 50 HTN pregnant women with proteinuria as G1 and 50 HTN pregnant women with no proteinuria as G2, who were compared with 50 age-matched healthy pregnant women as G3. All were subjected to abdominal ultrasound and echocardiography. Calculation of cardiac output and total vascular resistance derived from 2D echocardiography was done. Assessment of LV systolic function including 2D and 4D ejection fraction (EF), systolic mitral annular velocity, and global longitudinal strain (GLS) by tissue-Doppler imaging (TDI) and 2D and 4D STE was done. Assessments of LV diastolic function, including mitral early and late diastolic velocities by pulsed-Doppler echocardiography (ME and MA), E/A and E/early diastolic mitral annular velocity (Ea) by TDI, and 2D left atrial volume index (LAVI) was performed.
Results Interventricular septal wall thickness in diastole, LV posterior wall thickness in diastole, and LV mass index were significantly increased in G1 compared with G2 and G3. Cardiac output and total vascular resistance were significantly increased in G1 compared with G2. LV GLS by TDI, 2D, or 4D STE was significantly lower in G1 compared with G3 and G2, despite the insignificant difference in LVEF. E/Em and LAVI were significantly increased in G1 compared with G2 and G3. A positive correlation was found between 2D and 4D measures. A positive correlation was found between proteinuria and LV mass index and LAVI, whereas a negative correlation was found between proteinuria and LV GLS (2D/4D) and 4D EF.
Conclusion Women with HTN associated with proteinuria had significant LV structural and functional changes. Use of newer echocardiographic modalities can detect early subtle changes in cardiac function in those patients.

Keywords: four-dimensional speckle tracking echocardiography, hypertension with proteinuria, preeclampsia

How to cite this article:
Habib SA, Khafagy WE. Assessment of the left ventricular function in hypertensive pregnant women with or without proteinuria: two-dimensional versus four-dimensional echocardiographic study. Sci J Al-Azhar Med Fac Girls 2020;4:78-83

How to cite this URL:
Habib SA, Khafagy WE. Assessment of the left ventricular function in hypertensive pregnant women with or without proteinuria: two-dimensional versus four-dimensional echocardiographic study. Sci J Al-Azhar Med Fac Girls [serial online] 2020 [cited 2020 May 30];4:78-83. Available from: http://www.sjamf.eg.net/text.asp?2020/4/1/78/282868

  Introduction and aim of the work Top

Preeclampsia (PE) is a gestation-associated disorder that is characterized by progressive elevation of blood pressure, proteinuria, and pathological edema, increasing the load on the cardiac function and may be associated with worsening of the left ventricular (LV) function [1]. Asymptomatic patients may also develop subtle echocardiographic changes in the LV [2]; however, conventional echocardiographic indices such as the ejection fraction (EF) are usually normal until advanced stages of the PE [3].

The past decade has witnessed significant advances in echocardiographic technology. Speckle tracking echocardiography (STE) analyzes the degree of myocardial deformation [2]. Four-dimensional (4D) echocardiography allows real-time imaging of the myocardium in 4D at a high temporal resolution and relatively low cost [4].

This study was designed to assess LV function in hypertensive (HTN) pregnant women with or without proteinuria, who were compared with normotensive healthy pregnant women using 2D echocardiography versus 4D echocardiography.

  Patients and methods Top

We conducted a case–control study that included 150 women more than 18 years old recruited from outpatient’s clinic with a singleton pregnancy between 28 and 41 weeks, calculated from the first day of last menstrual cycle and confirmed by early ultrasonography during a routine prenatal visit at Assisted Reproduction Technologies Unit, International Islamic Institute, Al-Azhar University, Cairo, during the period from January 2018 till June 2019. The diagnoses of PE with its severity classification and gestational HTN were performed by a maternal-fetal medicine specialist, based on the National High Blood Pressure Education Program Working Group definition [5]. An informed oral consent was provided by all participants, and the study protocol was approved by the ethical committee at the Faculty of Medicine, Al-Azhar University, Cairo, Egypt.

We excluded patients with preexisting cardiovascular, pulmonary, renal diseases, gestational or pregestational diabetes mellitus, congenital fetal malformation, or premature rupture of membranes.

Individuals were divided into three groups: group 1 (G1) included 50 pregnant women with PE (HTN and proteinuria), group 2 (G2) included 50 pregnant women with gestational HTN (without proteinuria), and group 3 (G3) had 50 age-matched healthy normotensive pregnant women.

All the studied cases were subjected to anthropometric measurements including height and weight for body surface area (BSA) and BMI calculation and calculation of mean arterial blood pressure [1]. Transabdominal ultrasound was done for evaluation of fetal well-being, fetal biometry, and placental localization.

2D echocardiography was carried out using Vivid E9 (GE Ultrasound, Horten, Norway) with multifrequency (2.5 MHz) matrix probe (M3S). All images were digitally stored for later off-line analysis at EchoPAC.GE version 201. Comprehensive TTE M-Mode, 2D, Doppler (pulsed and continuous wave), and color flow mapping in the standard views (parasternal long axis, parasternal short axis, apical four, three and two chambers views) were obtained with ECG physiosignal display and loop recording of two to three cycles. All parameters were taken according to the standards of the American Society of Echocardiography [6], including LV dimensions and function: interventricular septal thickness in diastole, LV posterior wall thickness in diastole (PWd), LV end-diastolic diameter, LV end-systolic diameter, LVEF, LV %fraction of shortening, mitral valve early diastolic velocity, mitral valve late diastolic velocity, mitral valve E/A ratio and mitral deceleration time, LV mass, and relative wall thickness (RWT), where LV mass=0.8 [1.04(LVID+PWTd+SWTd)3+0.6 g] and left ventricular mass index (LVMI)=LVM/BSA and LVH was defined by Cornell criteria as the LVMI more than 50 g/m2 in men and more than 47 g/m2 in women, whereas RWT was calculated by dividing the sum of interventricular septal wall thickness in diastole (SWTd) and left ventricular posterior wall thickness in diastole (PWTd) by the left ventricular internal diastolic dimension (LVIDd) as an index of the LV geometric pattern (concentric LVH, RWT≥0.45; eccentric LVH, RWT<0.45) [7].

Total vascular resistance (TVR) was calculated from the equation: TVR (dyn.s/cm5)=mean arterial blood pressure×80/CO where cardiac output (COP)=SV×HR and stroke volume (SV)=π(LVOTd2/2)×velocity time integral of flow signal obtained by PWD [1].

The left atrium (LA) volumes were calculated using a surface algorithm. Maximum and minimum LA volumes were measured using retrospective gating at the end of T wave and at the onset of QRS wave in continuous electrocardiography monitoring and then indexed for BSA to calculate left atrial volume index (LAVI) [6].

Tissue-Doppler imaging (TDI) was obtained from apical four-chamber and two-chamber views. The mitral annular systolic velocity (Sa) and mitral annular early diastolic velocity (Ea) by pulsed wave tissue Doppler were obtained at inferoseptal, lateral, inferior, and anterior annular positions then the average E/Ea ratio were calculated. The LV longitudinal strain was also assessed using 2D STE analysis with QRS onset as the reference point, applying a commercially available strain software package to the LV on echoPAC, version 210. Images were acquired at 70–90 frames per second in the apical four-chamber, three-chamber, and two-chamber views. Using the Automated Function Imaging software, a point-and-click approach was utilized to identify three anchor points (two basal and one apical), following which the software tracked the endocardial contour. The LV 2D ST GS% was obtained in all study cases automatically.

Four-dimensional echocardiographic imaging

Six-beat full-volume 4D data sets were imaged during breath-hold using the same model with 4 V transducer. The 12-slice display was employed during acquisition. Then, the data sets were exported to the 4DAutoLVQ package for analysis. A quad view that displayed the end-diastolic frame was used for manual alignment of the axis and the mitral valve leaflet. We set the landmarks corresponding to the aortic annulus diameter in the LV apical long-axis view, and then automated border detection with manual correction if needed. Next, end-diastolic volume, end-systolic volume, SV, CO, and EF were automatically calculated. Thereafter, to calculate LV mass and myocardial strain, the epicardial border was determined for manual adjustment of the region of interest. After 4D speckle tracking was utilized in frame-by-frame analysis, the values of regional and global 4D-derived strain were generated and presented as strain curves and a color-coded 17-segment bull’s eye plot.

Statistical analysis

Results were analyzed using the IBM SPSS software (version 25.0; IBM Inc., Arming, New York, USA). Continuous variables were expressed as mean±SD, whereas categorical variables were expressed as frequencies and percentages. After normality and homogeneity confirmation, comparisons were performed using one-way analysis of variance test with post-hoc analysis using Bonferroni method, whereas Kruskal–Wallis test was used between ordinal variables and c2 test for nominal variables. The associations between variables were assessed by Pearson’s r correlation analysis. P value less than or equal to 0.05 was accepted as statistically significant.

  Results Top

Baseline characteristics

The smallest birth weight (BW) was found in G2 followed by G1 with significant difference between both groups, whereas normal BW was present in G3 with significant difference between groups (P=0.01). Twenty-six (52%) patients of G2 and 20 (40%) patients of G1 needed neonatal intensive care unit (NICU), with significant difference between both groups (P=0.03), whereas none of G3 patients needed it. There was no significant difference between groups regarding maternal age, parity, or BMI ([Table 1]).
Table 1 Baseline demographic and clinical characteristics of the study population

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There was significantly increased interventricular septal wall thickness in diastole, LV posterior wall thickness in diastole, LVMI, and RWT in G1, compared with G2 (P=0.03, P<0.001, P=0.03, and P=0.05, respectively) and G3 (P<0.001, P=0.03, P=0.04, and P<0.001, respectively) whereas no significant difference between G2 and G3. A total of 30 (60%) patients of G1 had eccentric hypertrophy estimated from LVMI and RWT. There was significantly increased COP in G1 compared with G2 (P=0.01), whereas we recorded significantly increased TVR in G1 compared with G2 (P=0.04). No significant difference was found between the studied groups regarding SV. The LV global longitudinal strain (GLS), whether measured by TDI or 2D STE, was significantly lower in G1, compared with G3 (P=0.00 and P<0.001) or G2 (P=0.04 and 0.03) despite the insignificant difference in LVEF ([Table 2]).
Table 2 Echocardiographic parameters of the studied groups

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All pregnant women in G3 had mild LV diastolic dysfunction, whereas 20 (40%) patients in G1 and 10 (20%) patients in G2 had severe LV diastolic dysfunction. We found a significantly higher A wave velocities in G1 compared with G3 (P=0.02), whereas no significant difference was recorded regarding E velocities. G1 had significantly higher E/A compared with G2 (P=0.04). G1 had significantly higher E/Em ratio compared with G2 (P=0.05) and G3 (P=0.01). We found that G1 had significantly higher LAVI compared with G2 (P=0.04) and G3 (P=0.03).

We found that G1 had significantly lower 4D GLS compared with G2 (P=0.02) and G3 (P=0.01). There was significantly lower 4D LVEF (P=0.03) and 4D COP (P=0.03) in G1 compared with G3. Moreover, there was significantly lower GLS in G2 compared with G3 (P<0.001).

Ten (5%) patients of G1 had severe PE, and compared with the mild PE patients of the same group, we found significantly lower 4D LV GLS (P=0.02) and higher LV E/Em (P=0.05) in severe PE patients.

For accuracy, we performed univariate correlation analysis between 2D and 4D measures of LV volumes, EF, and GLS. We found a significant correlation between 2D and 4D measures as shown in [Table 3].
Table 3 Univariate correlation between two-dimensional and four-dimensional parameters

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We found a positive correlation between proteinuria and LVMI and LAVI, whereas negative correlation between proteinuria and LV GLS (2D/4D) and 4D EF ([Figure 1] and [Table 4]). We found a positive association between mean blood pressure and NICU (r=25.053, P<0.001) and a positive association between proteinuria and NICU (r=12.789, P=0.01).
Figure 1 Comparison among the three groups regarding LV global longitudinal strain measured by TDI, 2D STE, and 4D echocardiography. 2D, two dimensional; 4D, four dimensional; LV, left ventricular; STE, speckle tracking echocardiography; TDI, tissue-Doppler imaging.

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Table 4 Correlation between proteinuria and different echocardiographic parameters

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  Discussion Top

PE is a serious condition that may lead to fetal and maternal complications, and various hemodynamic changes occur in the cardiovascular system (CVS). The current study was performed to evaluate the value of 2D versus 4D echocardiography in assessing the LV function in HTN pregnant women with or without proteinuria.

In our study, we found a significant increase in COP and TPR in women with PE compared with G2 or G3 cases, which is in concordance with Tangeda and Shastri [1], who explained this finding by the increased circulating volume leading to significant change in the vascular load in addition to elevated afterload. We found that 60% of G1 cases had LV eccentric hypertrophy with higher LVMI than G2 and G3 cases. This indicated a more advanced degree of LV remodeling in women with PE. Those changes are likely to be an afterload-mediated compensatory mechanism associated with changes in the LV from an ellipsoid to a more spherical shape [8].

There was impaired LV systolic function in G1 (measured by GLS derived from TDI and 2D STE) despite normal EF and fraction of shortening. These significant decreases in GLS are also seen when compared with G2, which suggests that HTN is not the only explanation for the observed changes. Assessment of LV function by strain either TDI or 2D STE helps to detect subtle changes in systolic function before affection of EF. Our results were concordant with Shahul et al. [2] and Vinereanu et al. [9].

Shahul and colleagues explained the subclinical LV dysfunction by the biochemical perturbations on top of the increased end-systolic wall stress, causing subendocardial microvascular ischemia and fibrosis. A major player in these disturbances is sFlt1, which induces vasoconstriction on the systemic and myocardial levels. This explains why the longitudinal strain is most affected because it is a functional measurement of subendocardial longitudinally oriented myocardium. Other possible mechanisms include increased circulating soluble endoglin levels and reduced production of vascular endothelial growth factor and placenta growth factor in addition to endothelial dysfunction, inflammation, coagulopathy, and metabolic abnormalities [2].

G1 patients had significantly higher mitral A velocities compared with G3, which may be explained by the afterload-mediated changes in the hypertrophied LV. We also found a significantly larger LAVI and mitral E/Em in G1 compared with the G2 and G3, reflecting the cumulative effects of increased left-sided chamber filling pressures on ventricular and impaired LV relaxation in the disease. Regarding grading of diastolic dysfunction severity, we found that 40% of G1 had severe LV diastolic dysfunction, compared with 20% of G2.

Our finding is concordant with Sengodan et al. [10] who reported that all parameter of diastolic dysfunction including increased E wave velocity, E/A ratio, and LAVI were higher in PE patients compared with normal pregnant women and explained their findings by the increased TPR in PE and increased afterload that led to stiff LV even independent from LVH.

In the present study, 4D-derived LV GLS decreased significantly in G1. We found a good correlation between 2D and 4D echocardiography studies regarding LV volumes, LVEF, and GLS. Our findings were in concordance with Cong and colleagues who reported a significant LV remodeling and dramatic changes in the systolic and diastolic function of LV using 2D and 4D echocardiography. In our study, we demonstrated a positive correlation between proteinuria and LVMI and LAVI, whereas a negative correlation between proteinuria and LV GLS (2D/4D) and 4D EF, which indicate more advanced LV and LA remolding with increased severity of PE [5].We found a significant difference between groups in neonatal BW, where it was higher in the G3 than among newborn in G2 or G3, which is in agreement with Xiong et al. [11], who found that the overall mean BW was lower markedly in babies born to mothers with PE than in those babies born to normotensive mothers.

In the current study, 50% of infants of mothers with PE and HTN were admitted to NICU owing to different causes including prematurity, respiratory distress, transient tachypnea of the newborn, or intrauterine growth restriction.

Our study has some limitations. We could not follow the cases after labor to study the changes in LV strain. We did not measure serum biomarkers such as endoglin and sFlt1, which may explain the hemodynamic changes.

We conclude that HTN women with proteinuria had significant subclinical LV remodeling, including structural and functional changes. Using 2D and 4D echocardiography can detect early subtle changes in cardiac function.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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Melchiorre K, Sutherland GR, Baltabaeva A, Liberati M, Thilaganathan B. Maternal cardiac dysfunction and remodeling in women with preeclampsia at term. Hypertension 2011; 57:85–93.  Back to cited text no. 3
Tyldum EV, Backe B, Støylen A, Slørdahl SA. Maternal left ventricular and endothelial functions in preeclampsia. Acta Obstet Gynecol Scand 2012; 91:566–573.  Back to cited text no. 4
Lenfant C. Report of the National High Blood Pressure Education Program Working Group on high blood pressure in pregnancy. J Clin Hypertens (Greenwich) 2001; 3:75–88.  Back to cited text no. 5
Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 2015; 16:233–271.  Back to cited text no. 6
Ogunlade O, Akintomide AO. Assessment of voltage criteria for left ventricular hypertrophy in adult hypertensives in south-western Nigeria. J Cardiovasc Dis Res 2013; 4:44–46.  Back to cited text no. 7
Cong J, Fan T, Yang X, Shen J, Cheng G, Zhang Z. Maternal cardiac remodeling and dysfunction in preeclampsia: a three-dimensional speckle-tracking echocardiography study. Int J Cardiovasc Imaging 2015; 31:1361–1368.  Back to cited text no. 8
Vinereanu D, Bruja R, Lungeanu Juravle L, Cirstoiu M, Trasca LF, Patrascu N et al. p3256 pregnant women with gestational hypertension or preeclampsia had lower global and regional left ventricular systolic function by comparison with normotensive pregnant women. Eur Heart J 2017; 38:8–10.  Back to cited text no. 9
Sengodan SS, Dhanapal M, Pandian A. Left ventricular dysfunction in preeclampsia: an echocardiographic study. IJRCOG 2017; 6:4895–4898.  Back to cited text no. 10
Xiong X, Demianczuk NN, Saunders LD, Wang F-L, Fraser WD. Impact of preeclampsia and gestational hypertension on birth weight by gestational age. Am J Epidemiol 2002; 155:203–209.  Back to cited text no. 11


  [Figure 1]

  [Table 1], [Table 2], [Table 3], [Table 4]


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