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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 15  |  Issue : 1  |  Page : 7-14

Relation of right ventricular dysfunction to the severity of hepatic cirrhosis by different echo modalities using speckle-tracking echocardiography


1 Department of Cardiology, Faculty of Medicine of Girls, Al-Azhar University, Cairo, Egypt
2 Department of Tropical Medicine, Faculty of Medicine of Girls, Al-Azhar University, Cairo, Egypt

Date of Submission24-Jul-2016
Date of Acceptance02-Sep-2016
Date of Web Publication23-Aug-2017

Correspondence Address:
Nessren M Baha El Deen
Tropical Medicine, Faculty of Medicine of Girls, Al-Azhar, University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1687-1693.213588

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  Abstract 


Background
Speckle-tracking echocardiographic (STE) studies have shown the presence of right ventricular (RV) dysfunction before the advent of RV failure in patients with hepatic cirrhosis. We aimed to evaluate RV function in patients with hepatic cirrhosis and assess the relation of RV dysfunction to the severity of hepatic cirrhosis using different echo-Doppler modalities including STE.
Patients and methods
This study included 49 patients with various degrees of hepatic cirrhosis and 34 healthy normal individuals (NL). Patients were classified into group A (11 patients), group B (17 patients), and group C (21 patients) according to disease severity using the Child–Pugh score. Conventional echo-Doppler parameters of RV function together with tissue Doppler imaging-derived RV strain and speckle-tracking echo-derived right ventricular global strain (STE-RVGST) were obtained.

Keywords: hepatic cirrhosis, right ventricular function, speckle tracking echocardiography


How to cite this article:
Zaki ER, Baha El Deen NM. Relation of right ventricular dysfunction to the severity of hepatic cirrhosis by different echo modalities using speckle-tracking echocardiography. Al-Azhar Assiut Med J 2017;15:7-14

How to cite this URL:
Zaki ER, Baha El Deen NM. Relation of right ventricular dysfunction to the severity of hepatic cirrhosis by different echo modalities using speckle-tracking echocardiography. Al-Azhar Assiut Med J [serial online] 2017 [cited 2019 Sep 17];15:7-14. Available from: http://www.azmj.eg.net/text.asp?2017/15/1/7/213588




  Introduction Top


Chronic liver disease (CLD) has high incidence and prevalence worldwide [1]. An association has been found between liver disease and the cardiovascular system [2]. The relation between CLD and the cardiovascular system has been defined as cirrhotic cardiomyopathy (CCM) [3]. Liver function deterioration is associated with structural and functional cardiac abnormalities irrespective of its etiology [4]. This is mediated through increase in nitric oxide and other inflammatory mediators, which leads to splanchnic vasodilatation and reduced arterial compliance, which form part of the pathophysiology of CCM and hepatopulmonary syndrome [4],[5]. In patients with CLD, CCM is underdiagnosed, and most of the time the diagnosis is established only in the terminal phases of CLD [6]. Advanced liver cirrhosis is associated with several cardiovascular and pulmonary abnormalities including hyperdynamic circulation with decreased effective arterial blood volume, CCM, and arterial pulmonary hypertension [3]. The pulmonary consequences of the hyperdynamic circulation and portal hypertension are hepatopulmonary syndrome and portopulmonary hypertension.

Quantification of right ventricular (RV) systolic function has become increasingly important, as detection of subclinical RV dysfunction has a clear correlation with adverse clinical outcomes. Evaluation of RV function has been more challenging than that of left ventricle. The recent introduction of speckle-tracking echocardiography (STE) provides objective measures to quantify segmental and global RV function independently of angle of incidence, chamber translation, cardiac rotation, and ventricular size [6],[7]. STE can be used to detect progressive major cardiac remodeling in cirrhotic patients, which is considered an ominous sign to overt heart failure (HF). We aimed to evaluate RV function in patients with hepatic cirrhosis and to assess the relation of RV dysfunction to the severity of hepatic cirrhosis using different echo-Doppler modalities including STE.


  Patients and methods Top


This study enrolled 49 consecutive hepatic cirrhotic patients referred from the departments of tropical and internal medicine to the echo lab of the Cardiology Department of Al-Zahraa University Hospital between November 2014 and April 2015. The study also included 34 age-matched and sex-matched healthy individuals as a control group. We excluded patients with coronary artery disease, congenital heart disease, organic valvular heart disease, atrial fibrillation, and active hematemesis.

Methods

All studied cases were subjected to the following: (a) careful medical history taking with special emphasis on detailed history of liver cirrhosis as regards the etiology and duration of the disease; (b) thorough clinical examination with special emphasis on the presence of clubbing, spider nevi, palmer erythema, Lower limb (LL) edema, ascites, and examination of the liver and spleen; (c) laboratory investigations including complete blood picture, serum liver function tests (Serum glutamic oxaloacetic transaminase (SGOT) and serum glutamate pyruvate transaminase (SGPT)), serum albumin, serum bilirubin levels (direct and total), prothrombin time, prothrombin concentration, and international normalized ratio; (d) assessment of severity of liver cirrhosis using Child–Pugh score with classification into A, B, and C based on bilirubin level, prothrombin time, albumin, the presence and/or severity of ascites, and encephalopathy [8]; (e) abdominal ultrasonography to confirm the diagnosis of hepatic cirrhosis, presence of splenomegaly, and presence of ascites; (f) plain radiograph of the chest and heart in posteroanterior view; and (g) 12-lead surface resting ECG for rate, rhythm, abnormal finding, detection of arrhythmia, and measurement of cQT interval using Bazett formula [9].

Transthoracic echocardiography

Transthoracic echocardiography was performed using a ultrasound machine, the GE-Vingmed Vivd 7 System (GE-Vingmed Ultrasound, Horten, Norway) with an M3S (3.5 MHz) matrix probe and echo Pac version 8.0 GE Healthcare. Images were obtained from parasternal and apical windows and the following parameters were obtained:
  1. Conventional echo-Doppler performed according to the standards of the American Society of Echocardiography [8], which were as follows:
    1. Left ventricular dimensions and ejection fraction (performed as completion of the echo examination).
    2. RV outflow tract dimensions including end-diastolic and end-systolic dimensions (RV end-diastolic dimension and RV end-systolic dimension) obtained from two-dimensional (2D)-guided M-mode of the parasternal short-axis view at the level of the aorta left atrium (Lindqvist et al., 2008) [10].
    3. Tricuspid valve distance measured from 2D apical four-chamber view, which corresponds to the RV minor dimension at the level of the tricuspid annulus (basal RV), its normal reference being less than 42 mm.
    4. Right ventricular fractional shorting percentage (RVFS%) (Rudiski et al., 2010) [11].
    5. Tricuspid annular plane systolic excursion (TAPSE), using a 2D-guided apical four-chamber view. The M-mode cursor was placed through the lateral tricuspid annulus in such a way that the annulus moved along the M-mode cursor. The total systolic displacement was measured from the end-diastole to the highest points of contraction.
    6. Transtricuspid Doppler flow velocities including early (E) and late (A) diastolic peak velocities, E/A ratio, and deceleration time (DT).
    7. RV Tei index by measurement of time interval from the end of one to the onset of the next tricuspid flow pattern, which represents the sum of isovolumic contraction time, isovolumic relaxation time, and ejection time (am interval). Ejection time (bm) was measured from the pulmonary Doppler flow signal (Rudiski et al., 2010) [11]:

  2. Tissue Doppler imaging (TDI) parameters: TDI function was activated at the apical four-chamber for data acquisition. Three complete cardiac cycles were recorded and stored in a cine-loop format. The imaging sector width was set as narrow as possible to allow a frame rate acquisition greater than 100 frames/s with special attention to the color Doppler velocity range setting to avoid any aliasing within the image. Off-line analysis of the digitally stored loops was done by trace profile and placing the sample volume at the free wall of RV at the level of the tricuspid annulus in apical four-chamber view. The trace profile was displayed to measure peak systolic annular velocity (Sa), early diastolic velocity (Ea), late diastolic velocity (Aa), and the ratio between E velocity from pulsed-Doppler echocardiography. Ea was calculated as E/Ea. Tissue Doppler-derived RV strain was obtained from the average of basal, mid, and apical RV segments.
  3. STE-derived RV global strain (STE-RVGST) was obtained with a software package (Echopac, USA) from the apical view, to measure global RVSTE. Standard grayscale 2D images were obtained at a frame rate of 70–90 frames/s. the RV endocardial border was traced manually from an end-systolic frame. Then the epicardial border was automatically detected by the software, and the region of interest was manually adjusted to include the entire RV myocardial wall. The quality tracking was verified and the region of interest was modified, and corrected if necessary to obtain optimal tracking.


Statistical methods

Data were collected, revised, tabulated, and statistically analyzed. Quantitative data were expressed as mean±SD. The unpaired Student t-test was used for testing statistically significant difference between the means of two samples. The χ2-test was used to detect statistically significant relation between different variables (qualitative data). The result was considered significant when P value was less than 0.05 and highly significant when less than 0.01.


  Results Top


The study was conducted on 83 participates, consisting of 49 hepatic cirrhotic patients (11 patients in group A, 17 patients in group B, and 21 patients in group C) according to Child–Pugh classification ([Table 1]), in addition to 34 age-matched and sex-matched normal individuals (NL) as a control group. The mean age of hepatic cirrhosis patients was 45.05±19.26 years, whereas that of the control group was 45.59±13.58 years (P=0.2). The hepatic cirrhosis patients included 34 (70%) men and 15 (30%) women, whereas the control group included 17 (50%) men and 17 (50%) women (χ2=2.42, P=0.12). There was no difference in heart rate between the studied groups.
Table 1 Modified Child–Pugh classification (Friedman and Keeffe, 1998) [24]

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The clinical and demographic data of the study groups are shown in [Table 2].
Table 2 Demographic and clinical characteristics of the patients and controls

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Patients in groups A, B, and C had significantly lower values of serum albumin and platelet count compared with the NL group. Reduction in both albumin and platelet levels was progressive from group A to group C (A vs. B, P=0.001; A vs. C, P=0.0000; and B vs. C, P=0.03). The levels of international normalized ratio, total bilirubin, and aspartate aminotransferase were significantly higher in groups A, B, and C compared with that in the NL group. The increase in the levels of these results was progressive from group A to group C (A vs. B, P=0.001; A vs. C, P=0.002; and B vs. C, P=0.03). The alanine aminotransferase (ALT) level was significantly higher in both group A and group C compared with the NL group, whereas in group B the ALT level showed no significant difference from the NL group; the level of ALT in group C was not significantly different from that in group A.

Comparison between groups A, B, and C and the NL group as regards the conventional echo-Doppler data is shown in [Table 3] and [Table 4].
Table 3 Comparison between group A, group B, group C, and the NL group as regards laboratory investigations

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Table 4 Conventional echo-Doppler measures of right ventricular function in the study groups

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The RV dimensions including RV end-diastolic dimension and RV end-systolic dimension were significantly higher in groups A, B, and C when compared with the NL group.

Likewise, tricuspid valve deceleration time was significantly higher in groups A and C compared with the NL group.

The RVFS% was significantly lower in the three patient groups when compared with the NL group.

Group C had significantly higher tricuspid annular velocity and significantly lower T-E/A ratio when compared with the NL group.

TAPSE and T-E velocity failed to show significant difference in any of the study groups compared with the NL group.

RV Tei index was significantly higher in group C compared with that in the control. It did not show significant difference between groups A and B and the NL group. However, the Tei index between the three study patient groups showed a significant increase in group C compared with groups A and B (C vs. A, P=0.014; C vs. B, P=0.011).

[Table 5] illustrates the comparison of tissue Doppler-derived strain and speckle-tracking-derived strain of the RV between the different study groups.
Table 5 Tissue Doppler and speckle-tracking parameters of right ventricular function in the study groups

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The RV Ea was significantly lower and RV Aa was significant higher in the three study groups (A, B, and C) when compared with the CL group. Both groups B and C had significantly lower RV Sa compared with the NL group with no difference in Sa between group A and the CL group.

Also, the E/Ea ratio was significantly higher in both group A and group C compared with the NL group, with no difference between group B and the NL group.

Analysis of tissue Doppler-derived strain and speckle-tracking echo-derived strain revealed lower values of these two variables in groups A, B, and C when compared with the NL group. RV global ST value showed progressive decrease starting from group A along with disease severity, with highly significant difference between groups A and B compared with group C (P=0.0001). However, the difference between group A and group B was not significant.

The TDI-derived strain did not show significant correlation with the Child–Pugh score ‘disease severity’ (r=0.047, P=NS), whereas the right ventricular global strain (RVGST) showed highly significant negative correlation with the Child–Pugh score for ‘disease severity’ (r=0.60, P<0.0001).

Also the RVGST showed significant positive correlation with serum albumin (r=0.37, P=0.01), and significant negative correlation with cQT interval (r=−0.48, P=0.001) ([Figure 1] and [Figure 2]).
Figure 1 Distribution of the study groups according to patient classification.

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Figure 2 Comparison of TDI-derived RV strain and STE-derived RV strain among the study groups. TDI-derived RV strain: P=0.000 in groups A, B, or C versus NL. STE-derived RV strain: P=0.0001 in group A, 0.00001 in group B, and 0.000000 in group C. RV, right ventricular; STE, speckle-tracking echocardiography; TDI, tissue Doppler imaging.

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  Discussion Top


Hepatic cirrhosis is associated with morphological and functional heart changes, which is related to the presence of the hyperdynamic circulation, and it is the hallmark of cirrhosis, in addition to peripheral vasodilatation. It also leads to biochemical and mechanical events that result in gross changes in heart geometry, mass, function, and wall stress. Continuous increased wall stress produces further dilatation by stimulation of a number of neurohormonal pathways, resulting in chronic heart failure [9],[12]. CCM is underdiagnosed in CLD patients, and most of the time the diagnosis of CCM is only established in the terminal phases of CLD [7]. Therefore, echocardiography should be a part of the screening of patients with CLD, because patients with systolic and/or diastolic dysfunction and portopulmonary hypertension have higher morbidity and mortality.

The present study aimed to evaluate RV function in patients with hepatic cirrhosis and assess the relation of RV dysfunction with the severity of hepatic cirrhosis using different echo-Doppler modalities including STE.

This study included 34 healthy individuals and 49 patients with various degrees of hepatic cirrhosis. Patients were classified into group A (11 patients), group B (17 patients), and group C (21 patients) according to disease severity on the basis of the Child–Pugh score.

Patients in groups A, B, and C had significantly lower serum albumin levels and platelet count compared with the CL group. Reduction in both albumin and platelet levels was progressive from group A to group C. Our results are concordant with those of Abd-Rabouh (2012) [13], who reported that serum albumin concentration is related to functional reserve of the liver and to the severity of liver disease.

Arnold et al. (2012) [14] reported significant increase in aspartate aminotransferase in hepatic cirrhosis. Others reported significant increase in total bilirubin and significant decrease in albumin level in patients with hepatic cirrhosis.

Our study reported that progressive prolongation of cQT in patients with hepatic cirrhosis from group A to group C was concordant with the findings of Ward et al. (1997) [15], who have shown a decrease in K currents in ventricular cardiomyocytes in cirrhotic patients, which prolong the QT interval.

In our study, parameters of RV functions evaluated with 2D and Doppler echocardiography did not distinguish the severity degrees of liver disease on the basis of the Child–Pugh score. However, the RVFS % was significantly lower in the three patient groups (A, B, and C) when compared with the NL group.

In our study the TAPSE and the tricuspid E velocity values failed to differentiate between study groups and NL patients probably because of the small sample size. Our results in this respect are discordant with those of Kjaergaard and colleagues, who concluded that TAPSE is a reliable, sensitive, and reproducible index for initial diagnosis and for follow-up of RV function and it presents an excellent correlation with the RV EF as calculated with radionuclide ventriculography or MRI.

Our study showed significant increase in DT in groups A, B, and C compared with that in normal participants, with no statistically significant difference between groups A, B, and C. These findings are discordant with those of Soyoral and colleagues, who found no significant increase in DT in cirrhotic patients as compared with controls. In the current study conventional Doppler flow data including T-E velocity and E/A ratio and Tei index were significantly different only in group C compared with the NL group. RV diastolic dysfunction in group C may be due to reduction in cardiac preload and increase in the afterload or impairment in RV relaxation.

RV function provides strong prognostic information in patients having hepatic cirrhosis. Our study showed statistically significant increases in average Aa velocity together with statistically significant reduction in average Ea velocity in the three study groups compared with the normal group, with statistically significant increase in the average E/Ea ratio in both group A and group C compared with normal participants, with no difference between group B and the NL group.

Our result revealed statistically insignificant increase in Sa wave velocity in group A, with statistically significant increase in group C and statistically highly significant reduction in group B compared with that in normal individuals. There was a statistically significant reduction in Sa wave velocity in group B compared with group A and group C. In a previous study, observation of the correlation between the E/Ea value and the invasively measured right atrial pressure indicated a correlation between the increasing RV filling pressure and the related parameter [5] in hepatic cirrhosis patients. The increased E/Ea value in groups B and C indicates the presence of increased RV filling pressure and subclinical myocardial dysfunction. Our result is discordant with that of Dadhich et al. [16] They revealed a statistically insignificant increase in systolic wave velocity in preascetic and ascetic hepatic cirrhosis patients compared with controls. However, they did not measure the E/Ea ratio. Sa wave velocity has been reported to be significantly correlated with RV ejection fraction and to reflect longitudinal RV movement [17],[18]. The RV contracts predominantly along the longitudinal plane rather than along the short-axis plane in healthy individuals [19]. Therefore, the significantly increased Sa wave in group C indicates that the RV contractility in group C is not only preserved but is also increased, which may be due to hyperdynamic circulation and increased preload. Sa wave velocity is load dependent and may be pseudonormal under conditions of increased volume loading as in group C.

Our results revealed that hepatic cirrhosis in groups A, B, and C disrupts the diastolic function of the RV. The significant increase in E/Ea ratio reflects significant increase in RV end-diastolic pressure in hepatic cirrhosis patients (groups A, B, and C). Sade et al. [20] confirmed that measurement of E/Ea is a useful noninvasive method for estimation RV filling pressure in a wide range of clinical conditions. They found that E/Ea of at least four correlates with right atrial pressure of at least 10 mmHg with sensitivity 88% and specificity 85% (but not in status postcardiac surgery). Our result is in concordance with that of Utsunomiya et al. [21] They found that tricuspid E/Ea ratio provides a reliable estimation of RV filling pressure and predicts cardiac events in patients with pulmonary arterial hypertension. Increased right atrial pressure in cirrhosis especially in decompensated patients. Paracentesis has been shown to lower right atrial pressure. Karabulut et al. [22] reported that RV diastolic dysfunction is more common in cirrhotic patients with hepatopulmonary syndrome than in those without. In our study we did not measure oxygen saturation to diagnose hepatopulmonary syndrome.

The new echocardiographic method of speckle tracking assesses myocardial strain and strain rate by tracking speckles in the myocardium on grayscale (B-mode imaging) and can be used to evaluate both global and regional myocardial strain without being limited by Doppler beam angle, tethering effect, and load dependency [6]. Our study showed significantly lower values of both TD-derived strain and speckle-tracking echo-derived strain in groups A, B, and C compared with the NL group. The RV global strain value showed progressive decrease starting from group A along with disease severity, with highly significant reduction between groups A and B compared with C, whereas the difference between A and B was not significant. TDI did not show significant correlation with Child–Pugh score. In contrast, STE effectively quantified and characterized the RV systolic function and its association with severity of hepatic cirrhosis.

Meris et al. (2010) [23],[24] showed a high degree of interobserver and intraobserver compatibility in their study indicating the reliability of 2D-STE values in the evaluation of RV function. In our study global RV speckle-tracking-derived strain values related to RV systolic functions were found to be decreased along with the severity of the disease. The stronger positive correlation of RV global strain with serum albumin and negative correlation with corrected QT interval would suggest that the RV dysfunction can be determined using the 2D-STE method in the subclinical phase.

It was reported that STE effectively quantifies and characterizes the RV systolic function. Our data showed that global RV longitudinal strain was reduced in hepatic cirrhosis patients and the reduction was progressive from group A to group C.

Our study revealed that the TDI-derived strain did not show significant correlation with the Child–Pugh score for ‘disease severity’ (r=0.047, P=NS), whereas the RVGST showed highly significant negative correlation with the Child–Pugh score for ‘disease severity’ (r=0.60, P<0.0001), indicating the superiority of STE-derived RV strain over TDI-derived strain in characterizing the disease severity.


  Conclusion Top


Patients with hepatic cirrhosis have RV dysfunction that is related to the severity of hepatic affection. STE-RVGST is superior to other parameters of RV function in assessing the severity of RV dysfunction in those patients with different hepatic cirrhosis grades.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

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


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