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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 17  |  Issue : 2  |  Page : 154-162

Assessment of left ventricular functions and its correlation to the severity of liver cirrhosis caused by hepatitis C virus by different echocardiography modalities (two-dimensional speckle-tracking echocardiography study)


1 Department of Cardiology El Zahraa University Hospital, Cairo, Egypt
2 Department of Tropical Medicine ElZahraa University Hospital, Cairo, Egypt

Date of Submission29-Jan-2019
Date of Decision20-Feb-2019
Date of Acceptance07-Apr-2019
Date of Web Publication23-Oct-2019

Correspondence Address:
Asmaa Ahmed Ali Hassan
MD Cardiology lecturer, MD , Cairo, 11517
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/AZMJ.AZMJ_19_19

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  Abstract 


Background Cardiovascular abnormalities are associated with liver cirrhosis observed especially under conditions of stress, so it is important to evaluate the cardiovascular function in every patient with cirrhosis. The Child–Pugh scoring system is the most commonly used clinical method for classifying liver cirrhosis. Tissue Doppler imaging and Two-dimensional speckle-tracking echocardiography (2D-STE) are newer imaging modalities able to accurately quantify left ventricular (LV) systolic function.
Aim To assess LV functions in patients with chronic liver cirrhosis caused by hepatitis C virus by different echo modalities and correlate the results with the severity of cirrhosis based on Child–Pugh score.
Material and methods A prospective study was done in the Echocardiography Unit, Cardiology Department, Al-Zahraa University Hospital, during a period of one year, including 75 participants, with 45 cirrhotic patients and 30 healthy individuals. For all patients, 2D-STE of the LV was measured. Then the patients with liver cirrhosis were divided into three subgroups according to Child–Pugh score, and LV functions were evaluated with conventional echo, tissue Doppler imaging (TDI), and STE.
Results By conventional echo, the LV systolic function increased in the diseased group (P=0.004) but decreased when using TDI and STE. Then the patient group was divided into three subgroups based on the Child–Pugh score. By conventional echo parameters, there were normal LV dimensions in the three groups but increased in class C with lowered systolic function by using 2D-STE. Conventionally, LV diastolic dysfunction was diagnosed in 30% but in 75% when using TDI. There is a correlation between severity of liver cirrhosis and LV systolic dysfunction when measured only by 2D-speckle tracking.
Conclusion The 2D-STE is considered a useful tool for early detection of LV systolic dysfunction especially in asymptomatic patients with viral liver cirrhosis. The LV diastolic dysfunction occurs earlier in cirrhotic patients. There is correlation between the extent of severity of liver cirrhosis and LV systolic dysfunction.

Keywords: Child–Pugh score, cirrhotic cardiomyopathy, liver cirrhosis, speckle-tracking echocardiography, ventricular functions


How to cite this article:
Hassan AA, Elden NB. Assessment of left ventricular functions and its correlation to the severity of liver cirrhosis caused by hepatitis C virus by different echocardiography modalities (two-dimensional speckle-tracking echocardiography study). Al-Azhar Assiut Med J 2019;17:154-62

How to cite this URL:
Hassan AA, Elden NB. Assessment of left ventricular functions and its correlation to the severity of liver cirrhosis caused by hepatitis C virus by different echocardiography modalities (two-dimensional speckle-tracking echocardiography study). Al-Azhar Assiut Med J [serial online] 2019 [cited 2019 Nov 22];17:154-62. Available from: http://www.azmj.eg.net/text.asp?2019/17/2/154/269760




  Introduction Top


Cirrhotic cardiomyopathy-related heart failure is considered the third leading cause of death, following rejection and infection after transplants [1],[2]. So, it is important to evaluate the cardiovascular function in every patient with cirrhosis. Liver cirrhosis is also associated with normal systolic function at rest, systolic dysfunction under conditions of stress, increased thickness of the left ventricle (LV), and electrophysiological abnormalities [3]. This can be attributed to a blunted heart rate response to stress, reduced myocardial reserve, and impaired muscular oxygen extraction [4]. The pathogenetic mechanisms that are responsible for this include the impairment of beta-adrenergic receptor signaling, cardiomyocyte plasma membrane function, intracellular calcium kinetics, and humoral factors such as endogenous cannabinoids, nitric oxide, and carbon monoxide [4],[5]. All these changes occur in cirrhosis and in the absence of any known causes of cardiac disease [6]. The relationship between the severity of liver disease and cirrhotic cardiomyopathy is controversial. Although some studies have shown no direct relationship between the degree of liver cirrhosis and extent of cardiac dysfunction, others reported cardiac dysfunction in patients with higher model for end-stage liver disease score [7],[8],[9],[10]. The Child–Pugh scoring system is the most commonly used clinical method for classifying liver cirrhosis. So, we used it in our study [11],[12].

Tissue Doppler imaging (TDI) and two-dimensional speckle-tracking echocardiography (2D-STE) are newer imaging modalities able to accurately quantify regional and global LV systolic function, especially the recently developed 2D-STE modality, which has a simple and angle-independent evaluation of the LV deformation, which is computed from the spatial gradients of myocardial velocities (using TDI) or from the relative position of ‘speckles’ within a myocardial region, along the cardiac cycle (speckle tracking) [13]. So, this modality is considered more sensitive than conventional echocardiography in detecting even subclinical ventricular dysfunction [14].


  Patients Top


We enrolled a total of 75 individuals, comprising 45 clinically stable (i.e. had not been hospitalized or undergone any interventions owing to cirrhosis or any related complications within the previous 6 months) patients with viral cirrhosis caused by hepatitis C virus between the ages of 20 and 65, who were followed up at the Tropical Department of Al-Zahraa University Hospital, between August 2017 and September 2018 and were referred to the echocardiography laboratory for the assessment of LV structure and functions, as well as 30 age and sex-matched healthy participants, who were recruited as a control group, selected from individuals who had no history of cardiovascular disease and who underwent a routine physical examination with normal ECG and two-dimensional transthoracic echocardiographic imaging (2D-TTE) findings. The following patients were excluded from the study: hypertensive or diabetic patients, pre-existing cardiac disease like rheumatic heart disease, congenital heart disease, other pre-existing cardiovascular disease like myocarditis owing to infective etiology, primary heart muscle diseases like cardiomyopathies, suboptimal echocardiographic images (especially those with poor image quality for the 2D-STE analysis and with obscured endocardial borders on the images), any metabolic or systemic diseases other than liver disease that might disrupt cardiac structure or function, and previous liver transplants that ended with rejection.


  Methods Top


After giving an informed consent, all the individuals included in our study were subjected to the following: full history taking; symptoms related to liver cell failure (jaundice, bleeding tendency, and hepatic encephalopathy); general examination with emphasis on blood pressure, heart rate, and anthropometric measurements; abdominal examination for detection of hepatomegaly or splenomegaly and/or ascites; laboratory investigation including liver profile tests [alanine aminotransferase, aspartate aminotransferase, serum bilirubin, serum albumin, and international normalizing ratio (INR)]; and abdominal ultrasonography, which was recorded for all individuals before the echocardiography. The diagnosis of liver cirrhosis was based on the clinical examination (chronic liver disease stigmata, jaundice, ascites, and esophageal varices), biochemical tests, and abdominal ultrasonographic features in all patients consistent with cirrhosis (diffuse alteration and nodular transformation of liver parenchyma, and signs of portal hypertension). Severity of cirrhosis was evaluated by Child–Pugh score [9]. Moreover, the study analyzed the potential correlation between the disease severity and cirrhosis-related LV remodeling and functional changes.

2D-TTE also was done for all individuals in our study for assessment of LV functions by its different modalities including M-mode, Doppler, TDI, and 2D strain (STE).

Based on the Child–Pugh scoring system which is the most commonly used clinical method for classifying liver cirrhosis, the severity of liver cirrhosis was assessed as follows: the least severe liver disease scored 5–6 points and called class A, the moderately severe liver disease scored 7–9 points and called class B, and the most severe liver disease scored 10–15 points and called class C.

The patient group was classified into three subgroups: 15 patients were in class A, 15 patients were in class B, and 15 patients were in class C.

Informed consent was taken from every individual enrolled, and the study was approved by the local ethics committee of the Al-Azhar University School of Medicine.

Echocardiographic examination

TTE examination was performed for all patients and controls in both supine and left lateral positions. All measurements were made by one staff cardiologist over at least three cardiac cycles, and the average value for each parameter was calculated using GE system Vivid-S3 (GE, Norway), Matrix probe M3S multifrequency 2.5 MHz, with the capability of TDI and gray scale recording for speckle tracking study.

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-chamber views) from all accessible windows were obtained with ECG physiosignal displayed with all detected echo-Doppler study with loop recording of two to three cycles. All images were digitally stored for later off-line analysis at echoPac.GE, version 110-1-2. All parameters were taken according to standards of the American Society of Echocardiography to measure LV dimensions and functions including conventional Doppler (mitral valve early diastolic velocity, mitral valve late diastolic velocity, mitral valve E/A ratio, and deceleration time). The relative wall thickness (RWT) [(interventricular septal thickness or PWT)/LV end-diastolic diameter)] was calculated as an index of the LV geometric pattern (concentric LVH, RWT≥0.45; eccentric LVH, RWT <0.45).

The TDI was obtained from apical four-chamber and two-chamber views. For data acquisition, three complete cardiac cycles were collected and stored in a cine loop format. The image sector width was set as narrow as possible to allow a frame rate acquisition greater than 90 frames/s. Special attention was paid to the color Doppler velocity range setting to avoid any aliasing within the image. 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, and then average of these four sites and E/Ea average 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 110.1.2. Images were acquired at 70–90 frames/s at end-expiration in the apical four-chamber, three-chamber, and two-chamber views. Using the Automated Function Imaging software (AFI), a point-and-click approach was used 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 for the six LV walls in the apical four-chamber, two-chamber, and three-chamber views. The averages of these values were used for the comparison of the cirrhotic patients with the control group.

Statistical analysis

The defining statistics were expressed as percentage, mean value, and SD. When a normal distribution hypothesis was present in the analysis of the differences in certain measurements between the control and patient groups, Student’s t test was used, whereas the Mann–Whitney U test was employed when this hypothesis could not be established. Moreover, correlation was done between severity of liver cirrhosis based on Child–Pugh scoring system and LV systolic function by different echocardiographic modalities. Statistical analysis was performed using the Statistical Package for Social Sciences SPSS version 15. P value less than 0.05 was considered to be significant.


  Results Top


We enrolled 75 individuals divided into two groups: group A represented 45 patients with viral liver cirrhosis caused by hepatitis C virus, and group B represented 30 age-matched and sex-matched healthy participants as a control group. When the demographic and clinical data of the groups were compared, the systolic (P=0.03) and diastolic (P=0.03) blood pressures were observed to be lower in the cirrhotic group. When the biochemical values were evaluated, the INR (P<0.001), aspartate aminotransferase (P<0.005), alanine aminotransferase (P=0.00), and total bilirubin (P<0.01) values were higher, whereas the serum albumin (P<0.01) value was lower in the cirrhotic group. The demographic, clinical, and biochemical characteristics of the studied cases are shown in [Table 1].
Table 1 Baseline demographic, clinical, and biochemical characteristics of study population

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By conventional echocardiography, although there was significant increased in EF by M-mode (P=0.004) in cirrhotic group versus control group, there was insignificantly increased LV end-diastolic dimensions, LV end-diastolic volume, and EF by 2D. Regarding diastolic function by conventional parameters, there were statistically higher significant values of E, A, and deceleration time in cirrhotic group versus normal one ([Table 2]).
Table 2 Baseline left ventricular echocardiographic parameters in patient group versus control group

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There was a significant lower TDI systolic velocity and LV global longitudinal strain (GLS) % for assessment of LV systolic function beside LV diastolic dysfunction assessed by TDI in the cirrhotic group versus control.

The LV systolic function increased in the diseased group by M-mode and 2D as the hyperdynamic state but decreased when using TDI systolic velocity, and STE evidenced that it is not load dependent ([Figure 1])
Figure 1 Comparison between cirrhosis group and normal one by LV systolic function indices by different echo modalities.

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In our study, the patient group was divided into three subgroups based on the Child–Pugh score indicating the severity of the disease—group I: Child A consisted of 15 patients and their mean age was 36.7±7.4 years; group II: Child B included 15 patients, and their mean age was 52.4±4 years; and group III: Child C included 15 patients with decompensated cirrhosis, and their mean age was 52.3±4.2 years. All patients had hepatitis C virus, and female sex was more prevalent at approximately 58% of the study population, but there was no significant difference among the three groups (P=0.3). Moreover, there was no statistically significant difference among the three groups regarding risk factors (P=0.5 for smokers).

By conventional echo parameters, there were normal LV dimensions in the three groups (left ventricular internal dimension in diastole and left ventricular internal dimension in systole) but increased (especially LV end-diastolic dimension and EF by M-mode) in class C (group III), indicating hyperdynamic function especially in group III, and by TDI, there was an increase in Sa in group III but lowered systolic function in STE ([Table 3] and [Table 4]).
Table 3 Comparison of left ventricular tissue Doppler imaging echocardiographic parameters and speckle-tracking echocardiography in patient group versus control group

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Table 4 Baseline echocardiographic parameters in the patient groups according to Child–Pugh class

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Regarding diastolic function, by conventional PW Doppler, LV diastolic dysfunction was diagnosed in 30% (15% in Child A, 3% in Child B, and 12% in Child C), but with TDI, LV diastolic dysfunction was diagnosed in 75% (22% in Child A, 23% in Child B, and 30% in Child C) ([Figure 2] and [Figure 3]).
Figure 2 Percentage of diastolic dysfunction by conventional echo versus TDI in all patient group.

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Figure 3 Percentage of LV diastolic dysfunction in 3 groups by conventional echo and TDI.

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When we compared laboratory investigation for liver function among the three patient groups, we found that there was a significant difference between group I versus group II regarding aspartate aminotransferase, serum albumin, total bilirubin, and INR, and also, serum bilirubin and INR in group I versus group III, but no significant difference in laboratory investigation was seen in group II versus group III ([Table 5] and [Table 6]).
Table 5 Tissue Doppler imaging and speckle-tracking echo parameters in the patient groups according to Child–Pugh class

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Table 6 Comparison among the three patient groups by laboratory investigations representing liver function

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Moreover, we did not find any significant difference between groups I and II regarding parameters measured by either conventional Doppler echocardiography, TDI, or 2D-STE. However, there were significant differences between group II versus group III in LVESV, EF, and STE, and between group I versus group III regarding LV volumes, EF by 2D, and LV GLS%. So, in the Child C group, when the 2D-STE values were compared, values were observed to be significantly lower in the Child C group ([Table 7] and [Table 8]).
Table 7 Comparison among the patient subgroups according to Child–Pugh classification in left ventricular systolic function by different echocardiographic modalities

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Table 8 Comparison between patient groups according to Child–Pugh classification in left ventricular diastolic function by different echocardiographic parameters

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Regarding LV diastolic function, there were no statistically significant differences between the three groups regarding conventional Doppler, except deceleration time in group I versus group II and E velocity in group II versus group III, but by TDI, there was a significant difference in E velocity only in group I versus group III ([Table 9]).
Table 9 Correlation between Child–Pugh score and left ventricular systolic function by different echo modalities

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By correlation between severity of liver cirrhosis based on Child–Pugh scoring system and LV systolic function by different echocardiographic modalities, we found that there is a significant correlation with LV systolic function when measured by GLS (2D-speckle tracking) and 2D-EF and not by M-mode EF or EF measured by TVI.


  Discussion Top


Patients with liver cirrhosis are proved to have a hyperdynamic circulation, which is manifested as high cardiac output, decreased systemic vascular resistance, and widespread arterial vasodilatation, resulting in cardiovascular abnormalities as proved in the previous studies [15],[16]. Cirrhotic cardiomyopathy is used to describe a collection of characters expressive of abnormal heart structure and function in patients with cirrhosis. So, our study was conducted to evaluate LV systolic and diastolic functions in patients with liver cirrhosis caused by hepatitis C virus by conventional Doppler echocardiography, TDI, and STE and correlate the results with severity of cirrhosis based on Child–Pugh scoring system of the cirrhotic patients.

In our study by conventional echo assessment, there was a significant increase in LV systolic function (EF) and volumes especially end-diastolic volume by conventional echo-Doppler study found in the patients with cirrhosis. A probable reason for this could be the facilitation of LV performance because of decreased peripheral vascular resistance and increased cardiac output as a result of hyperdynamic circulation. So recent echocardiographic modalities, especially which are not load dependent, are needed to detect early changes in the LV before its clinical manifestation of dysfunction. These results are present in a number of previous animal and human studies on cirrhosis which have shown that systolic function is apparently normal or even increased at rest [17].

Although the small numbers of our patients group, we found that GLS was significantly lower in cirrhotic patients than control (P=0.04) despite having an apparently normal EF finding by conventional echo measurement (a subclinical impairment in the longitudinal LV systolic function in cirrhotic patients with preserved LV pump function). Our finding is in concordance with Altekin et al. [18], who examined 38 cirrhotic patients and 37 healthy persons and revealed that in the cirrhotic group, the GLS was lower than healthy persons (20.57±2.1 vs.28.7±43.1, P<0.001), and also with Sampaio et al. [19], who examined 109 hospitalized and ambulatory patients with cirrhosis and 18 healthy controls and showed that peak systolic longitudinal strain was lower in patients than control, but ejection fraction was similar in patients and controls. This may be interpreted by changes in LV mechanics and geometry that during systole the radial muscle fiber thickening is preserved, with an increase in the circumferential shortening and a decrease in the longitudinal muscle fiber shortening. This results in the maintenance of the LV global ejection fraction. These changes have been considered to represent an underlying ‘pump dysfunction.’ So, volume-derived measurements of LV systolic function have important limitations in assessing myocardial contractile function, though a number of compensatory mechanisms, including an increase in LV end-diastolic volume and hypertrophy, can mask the underlying changes in myocardial force development [20],[21]. So, in our study we prefer LV GLS in early detection of the LV systolic dysfunction as it deteriorates early. These results have been proven in the recent studies which showed that the longitudinal function deteriorates early (i.e. before the onset of the clinical symptoms and the reduction in the global ventricular function) under pathological cardiac conditions.

Many patients with cirrhosis have various degrees of diastolic dysfunction, which affects ventricular filling. Diastolic relaxation is impaired early because of the stiffening, leading to decreased compliance and higher diastolic pressures compared with the control. Diastolic dysfunction occurs before systolic dysfunction and may progress to systolic dysfunction [22],[23]. In addition, we found in our study significant increase in the deceleration time and the E wave (P=0.02) than the normal group by conventional Doppler in a higher percentage of our cirrhotic patients. These percentages increased when diastolic function is assessed by TDI. This is considered in agreement with some previous studies which proved that diastolic dysfunction by simple echocardiography is not sufficient to differentiate patients with true cirrhotic cardiomyopathy from general cirrhotic patients [24].

In our study, when the cirrhosis group was divided into three subgroups according to the Child–Pugh scoring system, the longitudinal global strain in assessing LV systolic function in particular was observed to be reduced in the group III (Child–Pugh C). Moreover, we found in our study, the conventional echo parameters were within normal range in the three groups and were hyperdynamic in Child C. Regarding diastolic parameters, there was no significant difference among three groups for conventional Doppler parameters, and diastolic dysfunction was diagnosed only in 30% of cases. These results are in agreement with a recent study by Piyush et al. [25] who compared cardiac status in patients with liver cirrhosis and healthy controls by conventional echo parameters; it was found that echocardiographic parameters of systolic and diastolic functions were not different in cirrhosis etiologies or different Child–Pugh classes. Although the diastolic dysfunction is a frequent event in cirrhosis [26], in our study, systolic and diastolic dysfunction was evident especially in Child B and C, and by TDI, we can diagnose diastolic dysfunction in 75% of all patient groups, indicating that TDI is more accurate in detecting early LV diastolic dysfunction. In concordant with a study that was conducted on 60 patients with liver cirrhosis by TDI, it was found that LV diastolic dysfunction is commonly associated with advancement of hepatic dysfunction whereas systolic function is maintained till advanced hepatic failure [27]. When we correlate severity of liver cirrhosis based on Child–Pugh scoring system and LV systolic function by different echocardiographic modalities, we found that there is a significant correlation with LV systolic function only when measured by GLS (2D-speckle tracking) and 2D-EF and not by M-mode EF or EF measured by TVI, which is discordant to a study in 2017 which proved that in cirrhotic cardiomyopathy, there was no correlation between the stage of cirrhosis and any of the systolic function parameters (LVEF, S wave, Tei index, GLS, and basal strain). This may be owing to small number of patients in our study or may be owing to that they correlated LV systolic function with compensated and decompensated liver cirrhosis in scoring system [28].

Limitations of the study

Although the efficiency of the 2D-STE method was proved in our study, the small number of patients may represent a limitation to the validation of the efficiency of this recent method.


  Conclusion Top


The noninvasive recent 2D-STE technique appears to be a useful tool for early detection of LV systolic dysfunction especially in asymptomatic patients with viral liver cirrhosis. The LV diastolic dysfunction occurs earlier in cirrhotic patients even with preserved LV systolic function.

Based on Child–Pugh scoring system, there is correlation between the extent of severity of liver cirrhosis and LV systolic dysfunction that was detected by 2D-STE.

Recommendation

We recommend a future study on a large number of patients and examining patients with liver cirrhosis with STE, which is considered a recent echocardiographic modality whatever the stage of the disease routinely and especially before any invasive procedure.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]



 

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