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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 18  |  Issue : 1  |  Page : 1-7

Right ventricular function in pregnant women with or without preeclampsia


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

Date of Submission22-Oct-2019
Date of Decision27-Nov-2019
Date of Acceptance12-Dec-2019
Date of Web Publication26-Mar-2020

Correspondence Address:
Ola H Abd Elaziz
Lecturer of Cardiology Al Azhar University, 29, El Horya Street, Hadayek El Maadi, Cairo 11728
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AZMJ.AZMJ_144_19

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  Abstract 


Background Preeclamsia (PE) is a multisystem disorder that affects maternal and fetal outcomes. We aimed to assess right heart function in PE by echocardiography using conventional, tissue Doppler techniques, and 2D and 4D strain.
Patients and methods This study comprised 100 pregnant women aged between 32 and 41 weeks divided into two groups: group 1 included 50 pregnant women with PE, who were compared with 50 age-matched normotensive pregnant women as a control group (group 2). They were subjected to proteinuria detection, pelviabdominal ultrasound, conventional echo, tissue Doppler imaging, and 2D and 4D speckle tracking echocardiography for measurement of right ventricular (RV) dimensions and RV systolic and diastolic function indices.
Results The higher percentages of cesarean delivery, low birth weight, and need for NICU were present in group 1 compared with group 2. There were significantly increased RV dimensions in group 1 compared with group 2. TAPSE (2D and 4D), RV FAC (2D and 4D), average RV Sa, 4D-RV EF, 2D-RV strain, 4D septal strain, and 4D-RV free wall strain were significantly lower in group 1. RV MPI (PW and TDI) was higher in group 1 patients. Both tricuspid E/A and RV E/Ea were significantly higher in group 1. There was a positive correlation between proteinuria and mean arterial pressure, 2D-TAPSE, RV PW-MPI, and RV TD-MPI, whereas there was a negative correlation with 2D and 4D-RV strain, 4D RVEF, 4D-FAC, and T E/A.
Conclusion Women with PE had significant RV structural and functional changes. Assessment of RV by newer echocardiographic modalities such as speckle tracking echocardiography and 4D-echocardiography can detect subtle cardiac changes that may help in early diagnosis of maternal and fetal complications.

Keywords: 4D-echocardiography, preeclampsia, right ventricular function


How to cite this article:
Abd Elaziz OH, Nassef AH. Right ventricular function in pregnant women with or without preeclampsia. Al-Azhar Assiut Med J 2020;18:1-7

How to cite this URL:
Abd Elaziz OH, Nassef AH. Right ventricular function in pregnant women with or without preeclampsia. Al-Azhar Assiut Med J [serial online] 2020 [cited 2020 Apr 3];18:1-7. Available from: http://www.azmj.eg.net/text.asp?2020/18/1/1/281350




  Introduction Top


Preeclampsia (PE) is a serious complication of pregnancy caused by placenta with acute onset of predominantly cardiovascular (CV) manifestations [1]. Improper placental implantation and related endothelial injury of the uteroplacental and systemic circulation and vasospasm are involved in the fundamental pathophysiology of PE [2]. Decreased placental perfusion owing to abnormality in placenta formation leads to hypoxia, free radical formation, and increased oxidative stress, which results in fetal and maternal morbidity and mortality [3].

Complications of PE include eclampsia, placental abruption, renal and hepatic failure during pregnancy, as well as increased risk of chronic hypertension (HTN), CV disease, stroke, and metabolic syndrome later in life [4].

Neonatal complication of preeclampsia include prematurity and its complications which are compromised motor development and intrauterine fetal growth restriction, with increased risk of diabetes and CV morbidity in adulthood [5].

The functional and structural alterations occurring in the left side of the heart have been focused by many studied, but few published data are present on the structure and function of the right side of the heart in PE.

Our aim was to assess right ventricular (RV) mechanics in PE using different modalities of echocardiography and its correlation with placental and neonatal outcomes.


  Patients and methods Top


The study was an observational case–control study that enrolled 50 singleton pregnant women between 32 weeks and 41 weeks of pregnancy, with a diagnosis of PE, who were compared with 50 age-matched healthy normotensive pregnant women as a control group. Participants were selected from those admitted to labor and delivery unit on the antepartum floor or during a routine prenatal visit at Al-Zahraa University Hospital during the period from January 2017 till December 2017. Informed oral consent had been obtained from all participants, and the study was approved by Ethical Committee of Faculty of Medicine for Girls, Al-Azhar University.

Gestational age was confirmed by last menstrual period [calculated from the first day of last menstrual period and confirmed by early ultrasonography (using LOGIQ V5 ultrasound with transabdominal probe 3.75 MHz)].

Inclusion criteria

The study included patients diagnosed as having PE based on the National High Blood Pressure Education Program Working Group definition, and also endorsed by the American Congress of Obstetricians and Gynecologists (ACOG) [6].

Systolic blood pressure greater than or equal to 140 mmHg or diastolic blood pressure greater than or equal to 90 mmHg with proteinuria (>300 mg/24 h) or 1+ on dipstick in random urine sample in a previously normotensive woman after 20 weeks of gestation was defined as mild PE. Severe PE was defined by severe HTN (systolic blood pressure greater than or equal to 160 mmHg and diastolic blood pressure greater than or equal to 110 mmHg on two occasions 6 h apart) and proteinuria (≥5 g/24 h) with or without evidence of end organ damage, such as HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome, oliguria (<500 ml in 24 h), pulmonary edema, seizures, and fetal growth restriction. An obstetrician confirmed all diagnoses. Women with gestational or chronic HTN, twin pregnancy, any CVD or medical diseases such as renal, pulmonary, anemia (moderate or severe), or diabetes mellitus were excluded from the study.

All the studied cases were carefully assessed by clinical examination including blood pressure, general examination, and cardiac examination, and anthropometric measures (height and weight) were obtained for BMI and body surface area calculation. Mean arterial pressure (MAP) was calculated using the formula: MAP=2(DBP)+(SBP)/3 [4]. Transabdominal ultrasound was done for all cases for evaluation of the fetal well-being and assessment of fetal biometry, including biparietal diameter (BpD), femur length (FL), abdominal circumference (AC), amniotic fluid index (AFI), and placental localization.

Two-dimensional echocardiography

Two-dimensional echocardiography was performed in Cardiology Department, Al-Zahraa University Hospital using Vivid E9 (GE Ultrasound, Horten, Norway) ultrasound machine with multifrequency (2.5 MHz) matrix probe (M3S). In the left lateral recumbent position, hemodynamic measurement was carried out. Comprehensive TTE M-Mode, 2D, Doppler (pulsed and continuous wave), and color flow mapping in the standard views (parasternal long-axis, parasternal short-axis, and apical four-chamber, three-chamber, and two-chamber views) from all accessible windows were obtained, with ECG physiosignal displayed with all detected echo-Doppler study, with loop recording of 2–3 cycles. All images were digitally stored for later off-line analysis at EchoPAC.GE VERSION 201 (Vivid E9 Horten Norway).

Left ventricular assessment

All parameters were taken according to standards of the American Society of Echocardiography to measure LV dimensions and functions [7] including conventional Doppler [mitral valve early diastolic velocity (MV E vel), mitral valve late diastolic velocity (MV A vel), MV E/A ratio, and deceleration time (DT)]. LV mass was calculated according to the modified Penn formula. LV mass (g): 1.04 [(LVEDD+IVS+LVPW)3-LVEDD3] [6].

The total vascular resistance (TVR) was calculated using the following formula:



where TPR is total peripheral resistance [4].

Right ventricular assessment

Right ventricular (RV) outflow dimensions (RVOTprox and RVOTdist) were measured from left parasternal views, whereas RV inflow diameters [basal (D1), mid (D2) and longitudinal (D3)] were measured from apical four-chamber view.

Right ventricular functional measures were obtained from M-mode tricuspid annular plane systolic excursion (TAPSE), apical four-chamber fractional area change (FAC), calculated as [(end-diastolic area)–(end-systolic area)/end-diastolic area]×100, and RV conventional and tissue Doppler imaging myocardial performance index (RV PW-MPI and TDI-MPI) as an index for global function.

Tricuspid flow velocities were assessed by pulsed-wave Doppler in the apical four-chamber view. The following variables were determined: early diastolic peak flow velocity (ETV), late diastolic flow velocity (ATV), and their ratio (E/A)TV [7].

TDI was used to obtain RV myocardial velocities in the apical four-chamber view, with a sample volume placed at the lateral segment of the tricuspid annulus to obtain peak tricuspid annular systolic velocity (RV Sa), early diastolic velocity (RV Ea), and late diastolic velocity (RV Aa) and then calculation of E/Ea for RV diastolic function.

Two-dimensional RV strain imaging was performed by using three consecutive cardiac cycles of 2D images in the apical four-chamber view to assess RV-GLS [7].

3D echocardiographic imaging of the right ventricle

3D echocardiographic imaging six-beat full-volume 3D data sets (≥30 vol/s) were obtained during breath-hold using Vivid E9 (GE Vingmed Ultrasound, Horten, Norway) equipped with 4 V probe. The 12-slice display was used during acquisition to ensure a complete inclusion of the RV in the data set. The 3D data set was aligned by setting the RV longitudinal axes in the reference end-diastolic frame. On the LV apical long-axis view, the operator sets the landmarks corresponding to the aortic annulus diameter, and on the RV short-axis view, the anterior and posterior junctions of the RV free wall with the interventricular septum, and the septum-to-RV free wall distance are set. Then, the RV contours are automatically tracked over the entire cardiac cycle using the speckle-tracking technology, and automated measurements of RV volumes, EF, and strain are provided. Manual corrections on end-systolic and end-diastolic frames are continuously updated on the RV 3D model and then propagated to all the other frames of the cardiac cycle using the derived tracking. RV volumes over time are computed from the dynamic surface model, and maximal and minimal volumes are used to calculate EDV, ESV, and EF ([Figure 1])
Figure 1 Alignment of 3D data set and identification of landmarks.

Click here to view


Statistical analysis

Results were analyzed using the SPSS for Windows software (version 25; IBM SPSS Inc., Armonk, New York, USA). Continuous variables were presented as means and SD, whereas categorical variables were presented as percentages and frequencies. Normality was confirmed by central limit theorem. Univariate analysis for group comparisons was performed using the unpaired Student’s t-test. The associations between variables were assessed by Pearson r correlation analysis. P less than or equal to 0.05 was accepted as statistically significant, and P less than or equal to 0.001 was considered highly significant.


  Results Top


Demographic and clinical characteristics of the studied cases are shown in [Table 1].
Table 1 Baseline demographic and clinical characteristics of study population

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There was no significant difference between both groups regarding maternal age, gravidity, parity, or BMI.

There was a significant difference between both groups regarding fetal age whether gestational or by ultrasound (P=0.002 and 0.05, respectively).

A significantly higher percent of CS was seen in women with PE (82%, P<0.001), with significantly lower birth weight (P<0.001) and a higher need for NICU admission in 44% of PE women.

The data of LV evaluation in [Table 2] showed no significant difference between both groups regarding LVEDD, LVESD, EF, COP, or M E/A ratio.
Table 2 Echocardiographic assessment of the left ventricle

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IVSd, LVPWd, LVMI, RWT, TPR, LV MPI, and LV E/Ea were significantly higher in PE, whereas LV strain whether measured by 2D or 4D echocardiography was significantly lower in PE group.

RV dimensions (D1, D2, and D3) and RVOT diameters (proximal and distal) were significantly higher in women with PE (P=0.02, 0.02, and 0.002, and <0.001 for both, respectively). TAPSE (2D or 4D), RV FAC (2D or 4D), avg RV Sa, 4D-RV EF, 2D-RV strain, 4D septal strain, and 4D-RV free wall strain were significantly lower in women with PE compared with control group [P<0.001 for both, <0.001 for both, and 0.01, <0.001, <0.001, <0.001 and <0.001, respectively].

RV MPI was significantly higher in PE group whether measured by PWD or TDI (P<0.001 for both).

Tricuspid E velocity, T E/A, RV Ea, and RV E/Ea were significantly higher in PE group compared with the control group (P=0.02, 0.01, 0.02, and 0.03, respectively).

There was significantly higher RVSP in patients with PE compared with control group (P<0.001), as shown in [Table 3].
Table 3 Echocardiographic assessment of the right ventricle

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We found a significant positive correlation between MAP and 2D-TAPSE (r=0.661, P<0.001), PW-RVMPI (r=0.421, P<0.001), and TD-RVMPI (r=0.399, P<0.001), whereas a negative correlation with 4D-RV septal strain (r=−0.550, P<0.001), 4D-RV free wall strain (r=−0.511, P<0.001), 2D-RVGLS (r=−0.479, P<0.001), 4D RVEF (r=−0.455, P<0.001), 4D-FAC (r=−0.349, P<0.001), and T E/A (r=−0.236, P=0.02), as shown in [Table 4] and [Figure 2].
Table 4 Correlation between mean arterial pressure and different echocardiographic parameters

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Figure 2 Correlation between MAP and (a) TAPSE, (b) TD-RVMPI, and (c) 4D RVEF.

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We found a significant association between NICU admission and RV dysfunction measured by 2D and 4D-RV strain and RV-MPI (PW and TD), as shown in [Table 5].
Table 5 Association between NICU and different echocardiographic right ventricular parameters

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Proteinuria was significantly associated with RV systolic dysfunction measured by TAPSE (R2=15.326, P=0.002), average RV Sa (R2=35.998, P<0.001), 2D-RVGLS (R2=27.565, P<0.001), and 4D-RV free wall strain (R2=57.604, P<0.001).

There was a significant association between proteinuria and RV diastolic dysfunction measured by RV E/Ea (R2=27.388, P<0.001).


  Discussion Top


Dramatic CV changes occur during pregnancy to meet the maternal and growing fetal metabolic needs. Blood volume increases, and PVR decreases along with progressive placental growth. Increase also in heart rate and cardiac output during pregnancy. Cardiac remodeling, including progressive mild dilation of all cardiac chambers and increase in LV mass, occurs as a compensatory response for such changes [8].

To the best of our knowledge, our research is one of the earliest studies for RV structure and function in women with PE. We found that RV dimensions (D1, D2, and D3) and RVOT (proximal and distal) were higher in PE group compared with normotensive group, which is concordant with the study by Çağlar et al. [2].

PVR during normal pregnancy keeps low despite elevated renin and angiotensin II blood concentrations [9]. This lack of vascular response to activated renin-angiotensin system may be related to the humoral factors such as prostaglandin and progesterone [10].

Abnormal pressure overloading in pregnancy complicated by HTN would lead to different cardiac remodeling compared with that of normal pregnancy [8].

In severe PE and eclampsia, decreased circulatory volume and low central venous pressure in addition to elevated systemic vascular resistance result in hyperdynamic LV function, elevated LV filling pressure, decreased COP, and decreased peripheral perfusion [10]. The abnormalities in uteroplacental vascular bed and endothelial dysfunction are thought to play critical roles in pathogenesis of GH .

All of these findings explained our results regarding higher IVSd, LVPWd, LVMI, RWT, and TPR in PE compared with normotensive group.

This study showed that TAPSE (2D or 4D), RV FAC (2D or 4D), avg RV Sa, 4D-RV EF, 2D-RV strain, 4D septal strain, and 4D-RV free wall strain were significantly lower in women with PE compared with control group, which is in agreement with Çağlar et al. [2] who were the first authors to conduct a study to evaluate the right side of the heart in PE in details, and they confirmed that echocardiography was a useful technique for evaluating the right side of the heart in PE.

Moreover, our results regarding RV strain were concordant with Vaught et al. [11] who studied acute cardiac complication in PE and found that preeclamptic women had higher RVSP levels, diminished RVLSS, abnormal LV cardiac relaxation, increased LV wall thickness, and increased LV filling pressures. In addition, they explain a reduction in RVLSS, likely owing to a combination of intrinsic subclinical RV dysfunction and increased RV afterload, and increased pulmonary artery pressures (i.e.elevated RVSP).

We found a significant positive correlation between MAP and 2D-TAPSE, PW-RVMPI, and TD-RVMPI, whereas a negative correlation with 4D-RV septal strain, 4D-RV free wall strain, 2D-RVGLS, 4D RVEF, 4D-FAC, and T E/A. These findings may be explained by increased PVR, leading to increased LV diastolic filling pressures and increased pulmonary resistance that finally reflected on RV function.Most of group I patients were delivered by cesarean section, which is in agreement with Bramham et al. [12] who concluded that women with PE were more likely to have a cesarean section.

In the current study, follow-up of all cases was done till delivery. We found a significant difference between groups in neonatal birth weight, where it was higher in the control group than among newborn of the mothers with PE. These results were in agreement with Xiong et al. [13], who found that the mean birth weight was lower markedly in babies born to preeclamptic mothers than in those babies born to normotensive mothers.

In the current study, 44% of infants of mothers with PE were admitted to NICU owing to different causes including prematurity, respiratory distress (RDS), transient tachypnea of the newborn (TTN), or intrauterine growth restriction (IUGR).

Marconi et al. [14], stated that the high risk of morbidity related to preterm, in addition to the effect of mild PE on fetal growth and maternal health, is important for deciding the optimal time of delivery in pregnancies complicated by IUGR.

Limitation of the study

We did not study RV function separately from LV function. It was also better to follow-up the patients after delivery to study the recovery of RV function.


  Conclusion Top


RV systolic and diastolic dysfunction may occur in PE reflecting the hemodynamic abnormalities. Newer echocardiographic modalities can detect RV dysfunction that may help in early diagnosis of maternal and fetal complications.

Financial support and sponsorship

Nil.

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 201; 57:85–93.  Back to cited text no. 1
    
2.
Çağlar FNT, Ozde C, Bostancı E, Çağlar İM, Çiftçi S, Unğan İ et al. Assessment of right heart function in preeclampsia by echocardiography. Pregnancy Hypertens 2016; 6:89–94.  Back to cited text no. 2
    
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Lenfant C. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. 2000. Am J Obstet Gynecol 183: S1– S22. J Clin Hypertens 2001; 3:75–88.  Back to cited text no. 3
    
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Tangeda P, Shastri N. Maternal left ventricular systolic and diastolic function during second trimester of pregnancy with preeclampsia. J Dr NTR Univ Heal Sci 2015; 4:224–228.  Back to cited text no. 4
    
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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. 5
    
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Yl NR, Kanakamahalakshmi A, Vani I, Rama P. Assessment of cardiovascular hemodynamics in gestational hypertension and preeclampsia. Int Arch Integ Med 2015; 2:17–23.  Back to cited text no. 6
    
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Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K et al. Guidelines for the Echocardiographic Assessment of the Right Heart in Adults: A Report from the American Society of Echocardiography. Endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and. J Am Soc Echocardiogr 2010; 23:685–713.  Back to cited text no. 7
    
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Kim M, Seo J, Cho K, Yoon S. Echocardiographic assessment of structural and hemodynamic changes in hypertension-related pregnancy. J Cardiovasc Ultrasound 2016; 24:28–34.  Back to cited text no. 8
    
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Gant NF, Worley RJ, Everett RB, Macdonald PC. Control of vascular responsiveness during human pregnancy. Kidney Int 1980; 18:253–258.  Back to cited text no. 9
    
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Easterling TR, Benedetti TJ, Schmucker B, Millard S. Maternal hemodynamic in normal and preeclamptic pregnancies: a longitudinal study. Obstet Gynecol 1990; 76:1061–1069.  Back to cited text no. 10
    
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Vaught AJ, Kovell LC, Szymanski LM, Mayer SA, Seifert SM, Vaydia D et al. Acute cardiac effects of severe pre-eclampsia. J Am Coll Cardiol 2018; 72:1–11.  Back to cited text no. 11
    
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Bramham K, Poli-de-figueiredo CE, Seed PT, Briley AL, Poston L, Shennan AH et al. Association of proteinuria threshold in pre-eclampsia with maternal and perinatal outcomes: a nested case control cohort of high risk women. PLoS One 2013; 8:1–8.  Back to cited text no. 12
    
13.
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. 13
    
14.
Marconi AM, Ronzoni S, Vailati S, Bozzetti P, Morabito A, Battaglia FC. Neonatal morbidity and mortality in intrauterine growth restricted (IUGR) pregnancies is predicated upon prenatal diagnosis of clinical severity. Reprod Sci 2009; 16:373–379.  Back to cited text no. 14
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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