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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 7  |  Issue : 1  |  Page : 26-30

Echocardiographic abnormalities in patients with cirrhosis and relation to disease severity


Department of Cardiology, Government Medical College, Kottayam, Kerala, India

Date of Web Publication29-Mar-2019

Correspondence Address:
Dr. Narayanapillai Jayaprasad
Department of Cardiology, Government Medical College, Kottayam, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/heartindia.heartindia_37_18

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  Abstract 


Context: Cirrhosis is the leading cause for hepatic transplantation worldwide. Heart is one of the most adversely affected organs in cirrhosis and it increases morbidity and mortality in these patients.
Aims: The objective of this study is to identify the echocardiographic abnormalities in patients with cirrhosis and their relation to severity of cirrhosis.
Subjects and Methods: An observational study was done on patients with cirrhosis (n = 55) and age- and sex-matched controls (n = 30). Detailed echocardiographic examination including 2D, M-mode, pulsed-wave Doppler, tissue Doppler, and 2D speckle-tracking imaging was performed. Severity of cirrhosis was defined by model for end-stage liver disease (MELD) score. Comparison of various echo parameters among cases and controls and among the two groups with MELD score >12 and <12 was made.
Results: The major echocardiographic abnormalities noticed were left ventricular hypertrophy in 47.3%, diastolic dysfunction in 40%, pulmonary artery hypertension in 32.7%, and pericardial effusion in 3.6% of patients. Among the various echocardiographic parameters, mitral annular velocity, deceleration time, isovolumetric relaxation time (IVRT), Sm velocity, e' velocity, E/e' ratio, and average global longitudinal strain (GLS) were significantly different in cirrhosis patients compared to the control population. Mitral annular a velocity and IVRT were significantly more in cirrhotic patients with MELD score >12.
Conclusions: Cirrhosis is associated with increased LV mass and cardiac output. Diastolic dysfunction was present in 40% of patients. Although systolic function by ejection fraction was normal in cirrhotic patients, GLS was less compared to controls.

Keywords: Cirrhotic cardiomyopathy, diastolic dysfunction, global longitudinal strain


How to cite this article:
Anish P G, Jayaprasad N, Madhavan S, George R. Echocardiographic abnormalities in patients with cirrhosis and relation to disease severity. Heart India 2019;7:26-30

How to cite this URL:
Anish P G, Jayaprasad N, Madhavan S, George R. Echocardiographic abnormalities in patients with cirrhosis and relation to disease severity. Heart India [serial online] 2019 [cited 2019 Apr 24];7:26-30. Available from: http://www.heartindia.net/text.asp?2019/7/1/26/255290




  Introduction Top


Cirrhosis is the model for end-stage liver disease (MELD) characterized by hepatocellular necrosis, progressive diffuse hepatocellular fibrosis, and regenerative nodules. It is the leading cause for hepatic transplantation worldwide. It has got a variety of clinical manifestations and complications, some of which are life-threatening. Cirrhosis is associated with an increase in the circulating blood volume, reduction in systemic vascular resistance, and increase in the cardiac output (CO). In cirrhotic patients, cardiac systolic function is usually normal at rest but can develop systolic dysfunction under conditions of pharmacological or physical stress. They often have diastolic dysfunction at rest. These abnormalities collectively constitute what is known as “cirrhotic cardiomyopathy.”[1] This is often an under-recognized clinical entity in these patients. Early recognition carries prognostic importance, especially if the patient is planned for procedures that may stress the heart such as shunt implantation and liver transplantation.[2] Cardiac involvement increases morbidity and mortality in patients with cirrhosis. Cirrhotic cardiomyopathy is an important cause of perioperative morbidity and mortality for liver transplant recipients.[3] Echocardiography with conventional as well as deformation imaging modalities are extremely helpful for the recognition of these abnormalities. The objective of this study is to identify the echocardiographic abnormalities among patients with cirrhosis and their relation to severity of cirrhosis.


  Subjects and Methods Top


We conducted a prospective observational study among patients enrolled in gastroenterology clinic with diagnosis of cirrhosis. Consecutive patients with clinically, biochemically, and sonologically proven cirrhosis liver in the age group of 20 years to 60 years were included in the study. The exclusion criteria were known ischemic and valvular heart disease, hypertension, primary myocardial disease, diabetes mellitus, uremia, severe anemia, and those patients with suboptimal echocardiographic images.

After obtaining informed written consent, 55 patients with cirrhosis who satisfied the inclusion criteria were selected. Thirty individuals who were age and sex matched were selected as controls. The burden of liver disease of the cases was categorized according to their MELD score using the formula:

MELD score = 0.957 × Loge (creatinine mg/dL) +0.378 × Loge(bilirubin mg/dL) +1.120 × Loge (INR) +0.643

Both the cases and the controls were subjected to a thorough clinical examination. Using standard echocardiographic windows, a detailed echocardiographic examination including 2D, M-mode, pulsed-wave Doppler, tissue Doppler, and 2D speckle-tracking imaging for global longitudinal strain (GLS) was performed. All echocardiographic studies were performed with the help of an echocardiography machine (Vivid E9, GE Vingmed Ultrasound AS, Norway) using M5S (1.5–4.6 MHz) transducer. The global longitudinal peak systolic strain average (GLS average) was obtained by averaging peak systolic longitudinal strain values from a 16-segment model from the three apical views using automated function imaging. Echocardiographic examination was done by an experienced operator based on the guidelines set by the American Society of Echocardiography. The echocardiography recordings were analyzed by two independent cardiologists, and the data were recorded in a preset pro forma. Statistical analysis was performed with the help of standard statistical software (IBM SPSS version 18.0, SPSS, Inc. Chicago, IL, USA). For all analysis, a value of P < 0.05 was considered statistically significant.


  Results Top


Comparison of cases with controls

There were 55 cases and 30 age- and sex-matched controls in the study. The average age of the patients in the cirrhosis group was 46.38 and that of the control group was 45.56. Out of the 55 patients in the cirrhosis group, 46 were male and 9 were female. Of the 30 patients in the control group, 25 were male and 5 were female. The average body mass index of the cirrhosis group was 21.8 and that of the control group was 22.1. These differences were statistically not significant.

2D echocardiographic imaging

The most common echocardiographic abnormality noticed was left ventricular (LV) hypertrophy (LVH) in 26 (47.3%) patients. CO in liters/minute) was significantly higher in the cirrhosis group compared to the control population (5.1 and 4.3, respectively). LV ejection fraction (LVEF) was marginally higher in the cirrhosis group, but the values were not statistically significant. The LV mass in end diastole (LVd mass in grams) and LV mass indexed to body surface area (LVD mass/BSA in grams/m2) were also significantly higher in the cirrhosis group (198.26 vs. 144.69 and 128.26 vs. 94.5), respectively. Pericardial effusion occurred in 2 (3.6%) patients.

Doppler echo features

The abnormalities detected were diastolic dysfunction in 22 (40%) patients and pulmonary artery hypertension (PAH) in 18 (32.7%) patients. Among the 22 patients with diastolic dysfunction, 18 patients had Grade 1 diastolic dysfunction, 3 had Grade 2, and 1 patient had Grade 3 diastolic dysfunction. Among the pulsed-wave Doppler parameters, mitral valve (MV) late peak velocity (MV A velocity), MV deceleration time (DT), and MV isovolumetric relaxation time (IVRT) were significantly higher in the cirrhosis group compared to the control population.

Among the tissue Doppler parameters, cirrhosis patients had a significantly higher systolic mitral annular velocity (Sm in meter/sec) compared to the control population (0.118 and 0.109, respectively, P = 0.017). The early diastolic mitral annular velocity (e' in meter/sec) was significantly lower in the cirrhosis group compared to the control population (0.1202 and 0.1403, respectively, P = 0.001). E/e' ratio also showed a significant difference between the two groups. The ratio was higher in the cirrhosis group compared to the control population (7.53 and 5.77, respectively, P = 0.003).

Speckle-tracking echocardiogram

2D speckle-tracking echocardiogram was done to assess the mean average GLS. The values were significantly lower in the cirrhosis group compared to the control population (−19.52 and −23.66, respectively, P < 0.0001). The echocardiographic details of cases compared to controls are given in [Table 1].
Table 1: Comparison of echocardiographic parameters among cases and controls

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Categorization according to model for end-stage liver disease Score

The average MELD score of the cirrhosis patients was 12. Of the 55 cirrhosis patients, 22 patients had a MELD score >12 and 33 patients had a MELD score <12. Accordingly, the patients were categorized into two groups: MELD score >12 and <12. The echocardiographic features were compared between the two groups. The major abnormalities such as LVH, diastolic dysfunction, PAH, and pericardial effusion were more in those with a MELD score >12. Comparison of different echocardiographic parameters in the two MELD score groups is given in [Table 2].
Table 2: Echocardiographic abnormalities among categories of model for end-stage liver disease score

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LVH was significantly more in those with a MELD score >12. Out of the 22 patients with MELD score >12, 16 patients (72.7%) had LVH. Out of the 33 patients with MELD score <12, only 10 patients (30.3%) had LVH. This difference was statistically significant (P = 0.002). Presence of PAH was significantly more in those with MELD score >12. Among the 22 patients with MELD score >12, 12 patients (54.5%) were having PAH, and among those with MELD score <12, 6 patients (18%) were having PAH (P = 0.005). Both the patients with pericardial effusion in the cirrhosis group had a MELD score >12. The CO, ejection fraction, LV mass, and LV mass indexed to the BSA were comparable between the two groups.

Diastolic dysfunction was significantly more in those with a MELD score >12. Out of the 22 patients with MELD score >12, 14 patients (63.6%) had diastolic dysfunction. Out of the 33 patients with MELD score <12, only 8 patients (24.2%) had diastolic dysfunction. This difference was statistically significant (P = 0.011). Among the pulsed-wave Doppler parameters of the mitral inflow pattern, late peak velocity was higher in those with MELD score >12. The difference was statistically significant (P = 0.035). The IVRT was significantly prolonged in those with a MELD score >12(P = 0.002). Tissue Doppler parameters were not different between the two groups. The mean average GLS was similar in those with a MELD score >12 and those with a MELD score <12 (−19.25 and −19.76, respectively, P = 0.429).


  Discussion Top


Presence of cardiovascular abnormalities in cirrhotic patients was first reported by Kowalski and Abelman in 1953. Advanced liver disease is associated with a hyperkinetic circulatory state characterized by increase in the circulating blood volume, fall in the peripheral vascular resistance, and consequently an increase in the CO.[4] Our study shows that cirrhosis is associated with a variety of echocardiographic abnormalities. Patients with cirrhosis had a significant increase in the CO, LV mass, and LV mass index compared to controls. This is in consensus with previous studies by Wong et al. and De Marco et al.[5],[6] However, there was no statistically significant difference in these parameters between early and advanced stages of cirrhosis. LVH was the most common abnormality observed in this study followed by diastolic dysfunction and PAH. A previous study by Bernal et al. reported high prevalence of LVH in cirrhotic patients.[7]

Diastolic dysfunction is a frequent feature of cirrhotic cardiomyopathy, which is most commonly assessed by studying the diastolic transmitral flow pattern. An increased atrial contribution to late ventricular filling, leading to a reduced E wave to A wave ratio suggests Grade 1 diastolic dysfunction. Other features include prolonged IVRT and DT due to increased resistance to ventricular inflow. In the study by Somani et al., the prevalence of diastolic dysfunction in cirrhosis was 30%; in most cases, it was of mild severity (Grade 1). There was no statistically significant difference in the prevalence of diastolic dysfunction among different grades of severity of cirrhosis assessed by Child–Pugh classes or cirrhosis etiologies. No significant differences were found in survival between patients with or without diastolic dysfunction at 1-year follow-up in this study.[8] Diastolic dysfunction is often linked to increased stiffness of the myocardial wall, due to a combination of myocardial hypertrophy, fibrosis, and subendothelial edema.[9] However, a functional component may also contribute, as improvements in diastolic dysfunction have been reported after paracentesis in patients with tense ascites and transjugular intrahepatic portosystemic shunt insertion in patients with reduced effective circulating volume.[10]

In our study, assessment of diastolic function using PW Doppler showed an increase in the mitral annular velocity, DT, and IVRT. There was significant increase in the prevalence with increasing severity of cirrhosis as assessed by MELD score. In this study, among patients with cirrhosis, those with a higher MELD score had a statistically significant increase in the MV late peak velocity and IVRT. This has been previously observed in other studies.[11],[12] However, the study of diastolic dysfunction using transmitral flow pattern has got many limitations as it is load dependent. Grade 2 diastolic dysfunction is associated with a pseudonormal pattern (normal E/A) which may be mistakenly included as normal if transmitral flow alone is studied.[13] Hence, tissue Doppler parameters are widely used to study diastolic dysfunction.[14] Tissue Doppler imaging revealed an increase in Sm velocity and e' velocity in patients with cirrhosis. The increase in Sm velocity in the present study is in consensus with a previous study by Altekin et al.[15] The increase in Sm velocity may be due to increased contractility from hyperdynamic circulation. In our study, the LV filling pressures were significantly higher in patients with cirrhosis compared to the control population, as evidenced by a statistically significant increase in the E/e' ratio. The tissue Doppler parameters were not significantly different between the two categories of MELD score in our study.

Although most patients with cirrhosis have normal systolic function and high CO at rest, an impaired hemodynamic responsiveness to physiological and pharmacological stresses has been documented in studies.[16] Similar results were seen when cirrhotic patients were subjected to exercise challenge. Ejection fraction in cirrhotic patients increased by 6% only compared with a 14% increase in healthy participants despite similar values at baseline.[17] In our study, none of the patients had systolic dysfunction measured by ejection fraction. Even when the LV systolic function is normal at rest, cirrhosis patients are susceptible for cardiac failure under conditions of stress.[18] This is due to the presence of under-recognized subclinical LV systolic dysfunction. The presence of subclinical LV dysfunction carries prognostic significance, especially if the patient is a prospective candidate for hepatic transplantation.[2] After liver transplantation, rapid hemodynamic changes may worsen preexisting congestive heart failure and almost 25% of patients undergoing liver transplant have high risk for postoperative pulmonary edema.[19],[20]

Previous studies have shown that 2D speckle-tracking is more sensitive than conventional echocardiography in detecting subclinical ventricular dysfunction in various clinical disorders.[21] Longitudinal contractile forces of the LV myocardium are carried out by the subendocardial region of the heart. Studies have shown that longitudinal function deteriorates early under pathological cardiac conditions, and longitudinal strain and longitudinal strain rate have been shown to be sensitive indicators of subclinical ventricular dysfunction and to correlate with myocardial fibrosis. Our study showed significantly reduced GLS in the cirrhotic patients compared to the control group. This indicates that there is a subclinical impairment in the longitudinal LV systolic function in cirrhotic patients with preserved LVEF. This observation was previously made by Altekin et al. in patients with nonalcoholic cirrhosis.[15] In our study, although GLS was less in cirrhotic patients compared to controls, among the two categories of MELD score, it was similar.

Our study had a small sample size which was an important limitation. Other limitations include the lack of follow-up data regarding clinical outcomes and lack of stress testing.


  Conclusions Top


Detailed echocardiographic assessment is helpful for the early identification of cardiac dysfunction in patients with cirrhosis. The important echocardiographic abnormalities are increase in LV mass and CO in cirrhotic patients. Abnormalities of diastolic function are common in cirrhosis patients. Although systolic function is normal in cirrhosis, GLS is significantly less compared to healthy controls, and it may be a marker of subclinical LV systolic dysfunction.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Zardi EM, Abbate A, Zardi DM, Dobrina A, Margiotta D, Van Tassell BW, et al. Cirrhotic cardiomyopathy. J Am Coll Cardiol 2010;56:539-49.  Back to cited text no. 1
    
2.
Zardi EM, Zardi DM, Chin D, Sonnino C, Dobrina A, Abbate A, et al. Cirrhotic cardiomyopathy in the pre- and post-liver transplantation phase. J Cardiol 2016;67:125-30.  Back to cited text no. 2
    
3.
Myers RP, Lee SS. Cirrhotic cardiomyopathy and liver transplantation. Liver Transpl 2000;6:S44-52.  Back to cited text no. 3
    
4.
Abelmann WH, Kowalski HJ, McNeely WF. The circulation of the blood in alcohol addicts; the cardiac output at rest and during moderate exercise. Q J Stud Alcohol 1954;15:1-8.  Back to cited text no. 4
    
5.
Wong F, Liu P, Lilly L, Bomzon A, Blendis L. Role of cardiac structural and functional abnormalities in the pathogenesis of hyperdynamic circulation and renal sodium retention in cirrhosis. Clin Sci (Lond) 1999;97:259-67.  Back to cited text no. 5
    
6.
De Marco M, Chinali M, Romano C, Benincasa M, D'Addeo G, D'Agostino L, et al. Increased left ventricular mass in pre-liver transplantation cirrhotic patients. J Cardiovasc Med (Hagerstown) 2008;9:142-6.  Back to cited text no. 6
    
7.
Bernal V, Pascual I, Lanas A, Esquivias P, Piazuelo E, Garcia-Gil FA, et al. Cardiac function and aminoterminal pro-brain natriuretic peptide levels in liver-transplanted cirrhotic patients. Clin Transplant 2012;26:111-6.  Back to cited text no. 7
    
8.
Somani PO, Contractor Q, Chaurasia AS, Rathi PM. Diastolic dysfunction characterizes cirrhotic cardiomyopathy. Indian Heart J 2014;66:649-55.  Back to cited text no. 8
    
9.
Ma Z, Lee SS. Cirrhotic cardiomyopathy: Getting to the heart of the matter. Hepatology 1996;24:451-9.  Back to cited text no. 9
    
10.
Cazzaniga M, Salerno F, Pagnozzi G, Dionigi E, Visentin S, Cirello I, et al. Diastolic dysfunction is associated with poor survival in patients with cirrhosis with transjugular intrahepatic portosystemic shunt. Gut 2007;56:869-75.  Back to cited text no. 10
    
11.
Saleh A, Matsumori A, Negm H, Fouad H, Onsy A, Shalaby M, et al. Assessment of cardiac involvement of hepatitis C virus; tissue Doppler imaging and NTproBNP study. J Saudi Heart Assoc 2011;23:217-23.  Back to cited text no. 11
    
12.
Pozzi M, Carugo S, Boari G, Pecci V, de Ceglia S, Maggiolini S, et al. Evidence of functional and structural cardiac abnormalities in cirrhotic patients with and without ascites. Hepatology 1997;26:1131-7.  Back to cited text no. 12
    
13.
Galderisi M, Dini FL, Temporelli PL, Colonna P, de Simone G. Doppler echocardiography for the assessment of left ventricular diastolic function: Methodology, clinical and prognostic value. Ital Heart J Suppl 2004;5:86-97.  Back to cited text no. 13
    
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Merli M, Calicchia A, Ruffa A, Pellicori P, Riggio O, Giusto M, et al. Cardiac dysfunction in cirrhosis is not associated with the severity of liver disease. Eur J Intern Med 2013;24:172-6.  Back to cited text no. 14
    
15.
Altekin RE, Caglar B, Karakas MS, Ozel D, Deger N, Demir I, et al. Evaluation of subclinical left ventricular systolic dysfunction using two-dimensional speckle-tracking echocardiography in patients with non-alcoholic cirrhosis. Hellenic J Cardiol 2014;55:402-10.  Back to cited text no. 15
    
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Gould L, Shariff M, Zahir M, Di Lieto M. Cardiac hemodynamics in alcoholic patients with chronic liver disease and a presystolic gallop. J Clin Invest 1969;48:860-8.  Back to cited text no. 16
    
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Wong F, Girgrah N, Graba J, Allidina Y, Liu P, Blendis L, et al. The cardiac response to exercise in cirrhosis. Gut 2001;49:268-75.  Back to cited text no. 17
    
18.
Gaskari SA, Honar H, Lee SS. Therapy insight: Cirrhotic cardiomyopathy. Nat Clin Pract Gastroenterol Hepatol 2006;3:329-37.  Back to cited text no. 18
    
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20.
Tiukinhoy-Laing SD, Rossi JS, Bayram M, De Luca L, Gafoor S, Blei A, et al. Cardiac hemodynamic and coronary angiographic characteristics of patients being evaluated for liver transplantation. Am J Cardiol 2006;98:178-81.  Back to cited text no. 20
    
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