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Almeida F, Sousa A. Cirrhotic cardiomyopathy: Pathogenesis, clinical features, diagnosis, treatment and prognosis. Rev Port Cardiol 2024; 43:203-212. [PMID: 38142819 DOI: 10.1016/j.repc.2023.07.010] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2023] [Revised: 06/09/2023] [Accepted: 07/30/2023] [Indexed: 12/26/2023] Open
Abstract
Cardiac dysfunction among cirrhotic patients has long been recognized in the medical community. While it was originally believed to be a direct result of alcohol toxicity, in the last 30 years cirrhotic cardiomyopathy (CCM) has been described as a syndrome characterized by chronic cardiac dysfunction in cirrhotic patients in the absence of known cardiac disease, regardless of the etiology of cirrhosis. CCM occurs in about 60% of patients with cirrhosis and plays a critical role in disease progression and treatment outcomes. Due to its predominantly asymptomatic course, diagnosing CCM is challenging and requires a high index of suspicion and a multiparametric approach. Patients with CCM usually present with the following triad: impaired myocardial contractile response to exercise, inadequate ventricular relaxation, and electrophysiological abnormalities (notably prolonged QT interval). In recent years, research in this area has grown expeditiously and a new set of diagnostic criteria has been developed by the Cirrhotic Cardiomyopathy Consortium, to properly identify patients with CCM. Nevertheless, CCM is still largely unknown among clinicians, and a major part of its pathophysiology and treatment is yet to be understood. In the present work, we aim to compile and summarize the available data on the pathogenesis, clinical features, diagnosis, treatment, and prognosis of CCM.
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Affiliation(s)
| | - Alexandra Sousa
- Cardiology Department, Unidade Local de Saúde de Entre o Douro e Vouga, Santa Maria da Feira, Portugal; Department of Medicine, Faculty of Medicine, University of Porto, Porto, Portugal; CINTESIS - Centre for Health Technology and Services Research, Porto, Portugal; RISE - Health Research Network, Porto, Portugal
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Impact of Cirrhotic Cardiomyopathy Diagnosed According to Different Criteria on Patients with Cirrhosis Awaiting Liver Transplantation: A Retrospective Cohort Study. Dig Dis Sci 2022; 67:5315-5326. [PMID: 35150344 DOI: 10.1007/s10620-022-07412-z] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/08/2021] [Accepted: 01/23/2022] [Indexed: 01/05/2023]
Abstract
BACKGROUND Recently, the Cirrhotic Cardiomyopathy Consortium (Consortium) proposed criteria to replace the World Congress of Gastroenterology (WGO) criteria for cirrhotic cardiomyopathy (CCM) using contemporary echocardiography parameters. We assessed the impact of substituting WGO by Consortium criteria on the frequency of diagnosis and clinical outcomes in patients with cirrhosis awaiting liver transplantation (LT). METHODS Consecutive adults with cirrhosis approved for LT with echocardiography evaluation from January 2014 to December 2016 were screened. Patients with structural heart diseases were excluded. Two primary outcomes were: (1) frequency of CCM; (2) association of CCM with pre-transplant mortality. The secondary outcomes were pre-LT complications of acute kidney injury (AKI) and/or hepatic encephalopathy (HE), and post-LT mortality. RESULTS Of 386 patients screened, 278 were included. 238 (85.6%) and 208 (74.8%) patients met Consortium and WGO criteria, respectively; 180 (64.7%) patients fulfilled both the criteria, while 12 (4.3%) patients had no evidence of CCM by either criterion. Pre-LT mortality rates in Consortium-CCM group were similar to the other groups (19.3% vs 20.2% vs 25.0%). The patients with advanced diastolic dysfunction (DD) per Consortium-CCM criteria had higher mortality than the other groups. The rates of pre-LT AKI/HE rates and post-LT mortality were similar in Consortium-CCM and WGO-CCM groups. CONCLUSION The Consortium criteria do not impact the prevalence of CCM compared to WGO criteria and have similar predictive accuracy. Presence of advanced DD per the Consortium criteria increases the risk of pre-LT mortality and complications of AKI/HE. The patients with advanced DD could benefit from further monitoring and treatment.
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Shahvaran SA, Menyhárt O, Csedrik L, Patai ÁV. Diagnosis and Prevalence of Cirrhotic Cardiomyopathy: A Systematic Review and Meta-analysis. Curr Probl Cardiol 2021; 46:100821. [PMID: 34016482 DOI: 10.1016/j.cpcardiol.2021.100821] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/16/2021] [Accepted: 02/17/2021] [Indexed: 01/26/2023]
Abstract
The proposed diagnostic criteria for cirrhotic cardiomyopathy (CCM), defines it as documented echocardiographic findings of systolic or diastolic dysfunction (using conventional 2D echocardiogram), with or without electrophysiological abnormalities or elevated biomarkers in cirrhotic patients. In comparison to 2D echocardiogram, tissue Doppler imaging (TDI) has better sensitivity and specificity, when evaluating for cardiac dysfunction. This meta-analysis of 12 selected cohort studies attempted to estimate the pooled prevalence of CCM using either conventional echocardiography or TDI. Using the 2005 criteria, the pooled prevalence of CCM is 61% (P = 0.106). When TDI is used, the prevalence of CCM is at 45% (P = 0.088). Analyzing data of 615 cirrhotic patients, this study estimates the mean population-specific echocardiographic values of cirrhotic patients, including left ventricle ejection fraction (63.52%), deceleration time (229.04 ms), isovolumetric relaxation time (87.71 ms) and E/A ratio (1.04). In comparison to TDI, using standard 2D echocardiography leads to overdiagnosis of CCM.
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Affiliation(s)
| | - Orsolya Menyhárt
- Department of Internal Medicine and Hematology, Semmelweis University, Budapest, Hungary; Buda Health Center
| | | | - Árpád V Patai
- Interdisciplinary Gastroenterology Working Group, Semmelweis University, Budapest, Hungary; Department of Internal Medicine and Hematology, Semmelweis University, Budapest, Hungary.
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Cirrhotic Cardiomyopathy - A Veiled Threat. Cardiol Rev 2020; 30:80-89. [PMID: 33229904 DOI: 10.1097/crd.0000000000000377] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
Abstract
Cirrhotic cardiomyopathy (CCM) is defined as cardiac dysfunction in patients with liver cirrhosis without pre-existing cardiac disease. According to the definition established by the World Congress of Gasteroenterology in 2005, the diagnosis of CCM includes criteria reflecting systolic dysfunction, impaired diastolic relaxation, and electrophysiological disturbances. Because of minimal or even absent clinical symptoms and/or echocardiographic signs at rest according to the 2005 criteria, CCM diagnosis is often missed or delayed in most clinically-stable cirrhotic patients. However, cardiac dysfunction progresses in time and contributes to the pathogenesis of hepatorenal syndrome and increased morbidity and mortality after liver transplantation, surgery or other invasive procedures in cirrhotic patients. Therefore, a comprehensive cardiovascular assessment using newer techniques for echocardiographic evaluation of systolic and diastolic function, allowing the diagnosis of CCM in the early stage of subclinical cardiovascular dysfunction, should be included in the screening process of liver transplant candidates and patients with cirrhosis in general. The present review aims to summarize the most important pathophysiological aspects of CCM, the usefulness of contemporary cardiovascular imaging techniques and parameters in the diagnosis of CCM, the current therapeutic options, and the importance of early diagnosis of cardiovascular impairment in cirrhotic patients.
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Carvalho MVH, Kroll PC, Kroll RTM, Carvalho VN. Cirrhotic cardiomyopathy: the liver affects the heart. ACTA ACUST UNITED AC 2019; 52:e7809. [PMID: 30785477 PMCID: PMC6376321 DOI: 10.1590/1414-431x20187809] [Citation(s) in RCA: 33] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/06/2018] [Accepted: 12/04/2018] [Indexed: 12/14/2022]
Abstract
Cirrhotic cardiomyopathy historically has been confused as alcoholic cardiomyopathy. The key points for diagnosis of cirrhotic cardiomyopathy have been well explained, however this entity was neglected for a long time. Nowadays the diagnosis of this entity has become important because it is a factor that contributes significantly to morbidity-mortality in cirrhotic patients. Characteristics of cirrhotic cardiomyopathy are a hyperdynamic circulatory state, altered diastolic relaxation, impaired contractility, and electrophysiological abnormalities, particularity QT interval prolongation. The pathogenesis includes impaired function of beta-receptors, altered transmembrane currents and overproduction of cardiodepressant factors, such as nitric oxide, cytokines and endogenous cannabinoids. In addition to physical signs of hyperdynamic state and heart failure under stress conditions, the diagnosis can be done with dosage of serum markers, electrocardiography, echocardiography and magnetic resonance. The treatment is mainly supportive, but orthotopic liver transplantation appears to improve this condition although the prognosis of liver transplantation in patients with cirrhotic cardiomyopathy is uncertain.
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Affiliation(s)
- M V H Carvalho
- Departamento de Cirurgia, Faculdade de Medicina de Jundiaí, Jundiaí, SP, Brasil
| | - P C Kroll
- Hospital de Transplante E.J. Zerbini, São Paulo, SP, Brasil
| | - R T M Kroll
- Instituto Dante Pazzanese de Cardiologia, São Paulo, SP, Brasil
| | - V N Carvalho
- Hospital Municipal Dr. Mario Gatti, Campinas, SP, Brasil
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Total bile acid levels are associated with left atrial volume and cardiac output in patients with cirrhosis. Eur J Gastroenterol Hepatol 2018; 30:392-397. [PMID: 29227330 DOI: 10.1097/meg.0000000000001043] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/18/2022]
Abstract
BACKGROUND AND AIMS Bile acids (BAs) are potent signaling molecules involved in the regulation of several metabolic and functional aspects of cardiovascular homeostasis. BA pool alteration in cirrhosis may contribute toward the development of hemodynamic and cardiac disturbances. We aimed to investigate the association between total BA levels and echocardiographic and biochemical markers of cardiac dysfunction in cirrhotic patients. METHODS Cirrhotic patients were enrolled prospectively in this hypothesis-generating study and evaluated for cardiac and hemodynamic dysfunction through clinical, echocardiographic, and biochemical means. Associations between total serum BA concentrations and markers of systolic or diastolic dysfunction and the presence of cirrhotic cardiomyopathy were tested through univariate and multivariate analyses. RESULTS Fifty-eight patients with cirrhosis were assessed in this monocentric study. 49 (85%) patients had decompensated cirrhosis according to the Child class. The median total BA level was 45 µmol/l. There was no correlation between BA levels and the etiology of cirrhosis (P=0.2), current alcohol use (P=0.8), sex (P=0.1), smoking status (P=0.2), age, or BMI. Systolic and diastolic dysfunction were rare in the cohort. Total BA levels associated with several echocardiographic parameters of the hyperdynamic syndrome in univariate analysis but only with left atrial volume in multivariate analysis (P=0.007). BA concentrations did not differ according to the presence of echocardiographically diagnosed cirrhotic cardiomyopathy in the two models tested. CONCLUSION Total serum BA levels are associated with enlarged left atrial volume and markers of the hyperdynamic circulation in patients with cirrhosis irrespective of the etiology or the severity of liver disease.
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Rehm J, Hasan OSM, Imtiaz S, Neufeld M. Quantifying the contribution of alcohol to cardiomyopathy: A systematic review. Alcohol 2017; 61:9-15. [PMID: 28599715 DOI: 10.1016/j.alcohol.2017.01.011] [Citation(s) in RCA: 53] [Impact Index Per Article: 6.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/26/2016] [Revised: 12/21/2016] [Accepted: 01/20/2017] [Indexed: 02/07/2023]
Abstract
Alcohol has a direct toxic impact on the heart, and while there is an ICD code for alcoholic cardiomyopathy, the burden of alcohol-attributable cardiomyopathy is not clear. For the usual estimation of this burden via population-attributable fractions, one would need to determine the risk relationships, i.e., average risk associated with different dimensions of alcohol exposure. The most important among these risk relationships is the dose-response relationship with different levels of average alcohol consumption. To establish risk relationships, we systematically searched for all studies on dose-response relationships, directly and indirectly, via reviews. The results did not permit computation of pooled estimates through meta-analyses. There were clear indications that heavy drinking (≥80 g per day) over several years was linked to high risk of cardiomyopathy, with greater lifetime exposure of alcohol linked to higher risks. Some studies indicated potential effects of patterns of drinking as well. As such, the global quantification of alcohol-attributable cardiomyopathy will have to rely on other methods than those used conventionally.
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Falletta C, Filì D, Nugara C, Di Gesaro G, Minà C, Baravoglia CMH, Romano G, Scardulla C, Tuzzolino F, Vizzini G, Clemenza F. Diastolic dysfunction diagnosed by tissue Doppler imaging in cirrhotic patients: Prevalence and its possible relationship with clinical outcome. Eur J Intern Med 2015; 26:830-4. [PMID: 26525531 DOI: 10.1016/j.ejim.2015.10.009] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/16/2015] [Revised: 08/25/2015] [Accepted: 10/14/2015] [Indexed: 02/06/2023]
Abstract
BACKGROUND Cirrhotic cardiomyopathy has been characterized by impaired contractile response to stress and/or altered diastolic relaxation, with electrophysiological abnormalities in the absence of known cardiac disease. However, the clinical significance of diastolic dysfunction (DDF) in cirrhotic patients has not been clarified. METHODS We studied 84 cirrhotic patients with normal systolic function to evaluate the prevalence of DDF using tissue Doppler imaging, and to investigate the possible correlation of DDF with outcomes (hospitalization, death) and with the specific causes of death. RESULTS The mean follow-up was 10±8months. DDF was diagnosed in 22 patients (26.2%). Patients with DDF more frequently had ascites (90.9% vs. 64.5 %; p=0.026), lower levels of albumin (OR: 5.39; p=0.004), higher NT-proBNP levels, and longer QTc interval (464±23ms vs. 452±30ms; p=0.039). At follow-up, patients with DDF did not have a higher incidence of adverse events in terms of hospitalization and death. CONCLUSIONS The presence of diastolic dysfunction has not been found to be clearly associated with outcome, and prognosis has been determined primarily by the severity of liver disease.
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Affiliation(s)
- Calogero Falletta
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Daniela Filì
- Hepatology Unit, Department for the Treatment and Study of Abdominal Diseases and Abdominal Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Cinzia Nugara
- Division of Cardiology A.O.U.P. Paolo Giaccone, Palermo, Italy
| | - Gabriele Di Gesaro
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Chiara Minà
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Cesar Mario Hernandez Baravoglia
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Giuseppe Romano
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Cesare Scardulla
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Fabio Tuzzolino
- Research Office, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Giovanni Vizzini
- Hepatology Unit, Department for the Treatment and Study of Abdominal Diseases and Abdominal Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
| | - Francesco Clemenza
- Cardiology Unit, Department for the Treatment and Study of Cardiothoracic Diseases and Cardiothoracic Transplantation, Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT), Palermo, Italy
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Ruiz-del-Árbol L, Serradilla R. Cirrhotic cardiomyopathy. World J Gastroenterol 2015; 21:11502-11521. [PMID: 26556983 PMCID: PMC4631957 DOI: 10.3748/wjg.v21.i41.11502] [Citation(s) in RCA: 91] [Impact Index Per Article: 9.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/15/2015] [Revised: 06/17/2015] [Accepted: 09/14/2015] [Indexed: 02/06/2023] Open
Abstract
During the course of cirrhosis, there is a progressive deterioration of cardiac function manifested by the disappearance of the hyperdynamic circulation due to a failure in heart function with decreased cardiac output. This is due to a deterioration in inotropic and chronotropic function which takes place in parallel with a diastolic dysfunction and cardiac hypertrophy in the absence of other known cardiac disease. Other findings of this specific cardiomyopathy include impaired contractile responsiveness to stress stimuli and electrophysiological abnormalities with prolonged QT interval. The pathogenic mechanisms of cirrhotic cardiomyopathy include impairment of the b-adrenergic receptor signalling, abnormal cardiomyocyte membrane lipid composition and biophysical properties, ion channel defects and overactivity of humoral cardiodepressant factors. Cirrhotic cardiomyopathy may be difficult to determine due to the lack of a specific diagnosis test. However, an echocardiogram allows the detection of the diastolic dysfunction and the E/e′ ratio may be used in the follow-up progression of the illness. Cirrhotic cardiomyopathy plays an important role in the pathogenesis of the impairment of effective arterial blood volume and correlates with the degree of liver failure. A clinical consequence of cardiac dysfunction is an inadequate cardiac response in the setting of vascular stress that may result in renal hypoperfusion leading to renal failure. The prognosis is difficult to establish but the severity of diastolic dysfunction may be a marker of mortality risk. Treatment is non-specific and liver transplantation may normalize the cardiac function.
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Abstract
Patients with cirrhosis and portal hypertension are at an increased risk of the development of circulatory dysfunction that may potentially result in multiple organ failure. Apart from the liver, this may involve the heart, lungs, kidneys, the immune system, the adrenal glands, and other organ systems. As the disease progresses, the circulation becomes hyperdynamic, and signs of cardiac, pulmonary, and renal dysfunction are observed, in addition to reduced survival. Infections and an altered cardiac function known as cirrhotic cardiomyopathy may be precipitators for the development of other complications such as hepatorenal syndrome. In patients with chronic organ dysfunction, various precipitating events may induce an acute-on-chronic renal failure and acute-on-chronic liver failure that negatively affect the prognosis. Future research on the pathophysiologic mechanisms of the complications and the precipitating factors is essential to understand the basics of the treatment of these challenging conditions. The aim of the present review is to focus on the development and precipitating factors of various organ failures in patients with decompensated cirrhosis.
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Farr M, Schulze PC. Recent advances in the diagnosis and management of cirrhosis-associated cardiomyopathy in liver transplant candidates: advanced echo imaging, cardiac biomarkers, and advanced heart failure therapies. CLINICAL MEDICINE INSIGHTS-CARDIOLOGY 2015; 8:67-74. [PMID: 25657603 PMCID: PMC4310615 DOI: 10.4137/cmc.s15722] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/01/2014] [Revised: 11/09/2014] [Accepted: 11/09/2014] [Indexed: 12/15/2022]
Abstract
Patients with end-stage liver disease in need of liver transplantation increasingly are older with a greater burden of cardiac disease and other co-morbidities, which may increase perioperative risk and adversely affect long-term prognosis. Cirrhosis of any etiology manifests hemodynamically as a state of low systemic vascular resistance, with high peripheral, but low central blood volume, leading to a state of neurohormonal activation and high cardiac output, which may adversely affect cardiac reserve under extreme perioperative stress, aptly termed cirrhosis-associated or cirrhotic cardiomyopathy. Evidence of asymptomatic cirrhotic cardiomyopathy may be found in subtle electrocardiographic and echocardiographic changes, but may progress to severe heart failure under the demands of bleeding and transfusions, vasopressors, rebounding peripheral vascular resistance, withdrawal of cardioprotective beta-blockers and mineralocorticoid antagonists, exacerbated by sepsis or systemic inflammatory response syndrome. This review will add to the current body of literature on cirrhotic cardiomyopathy by focusing on the role of advanced echocardiographic imaging techniques, cardiac biomarkers, and advanced heart failure therapies available to manage patients with cirrhotic cardiomyopathy while waiting for liver transplant and during the perioperative period.
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Affiliation(s)
- Maryjane Farr
- Center for Advanced Cardiac Care, Division of Cardiology, Columbia University Medical Center, New York, NY, USA
| | - Paul Christian Schulze
- Center for Advanced Cardiac Care, Division of Cardiology, Columbia University Medical Center, New York, NY, USA
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DellaVolpe JD, Garavaglia JM, Huang DT. Management of Complications of End-Stage Liver Disease in the Intensive Care Unit. J Intensive Care Med 2014; 31:94-103. [PMID: 25223828 DOI: 10.1177/0885066614551144] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2014] [Accepted: 07/14/2014] [Indexed: 12/19/2022]
Abstract
The management of critically ill patients with end-stage liver disease can be challenging due to the vulnerability of this population and the wide-ranging complications of the disease. This review proposes an approach based on the major organ systems affected, to provide a framework for managing the most common complications. Although considerable practice variation exists, a focus on the evidence behind the most common practices will ensure the development of the optimal skillset to appropriately manage this disease.
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Affiliation(s)
- Jeffrey D DellaVolpe
- Department of Critical Care Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA, USA
| | - Jeffrey M Garavaglia
- Department of Pharmacy & Therapeutics, Transplant Intensive Care Unit, UPMC Presbyterian Shadyside, Pittsburgh, PA, USA
| | - David T Huang
- Department of Critical Care Medicine, Director Multidisciplinary Acute Care Research Organization, University of Pittsburgh Medical Center, Pittsburgh, PA, USA
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