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Pagano G, Sastre L, Blasi A, Brugaletta S, Mestres J, Martinez-Ocon J, Ortiz-Pérez JT, Viñals C, Prat-Gonzàlez S, Rivas E, Perea RJ, Rodriguez-Tajes S, Muxí Á, Ortega E, Doltra A, Ruiz P, Vidal B, Martínez-Palli G, Colmenero J, Crespo G. CACS, CCTA and mCAD-LT score in the pre-transplant assessment of coronary artery disease and the prediction of post-transplant cardiovascular events. Liver Int 2024; 44:1912-1923. [PMID: 38591767 DOI: 10.1111/liv.15926] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/22/2024] [Revised: 03/19/2024] [Accepted: 03/24/2024] [Indexed: 04/10/2024]
Abstract
BACKGROUND The optimal cardiovascular assessment of liver transplant (LT) candidates is unclear. We aimed to evaluate the performance of CT-based coronary tests (coronary artery calcium score [CACS] and coronary CT angiography [CCTA]) and a modification of the CAD-LT score (mCAD-LT, excluding family history of CAD) to diagnose significant coronary artery disease (CAD) before LT and predict the incidence of post-LT cardiovascular events (CVE). METHODS We retrospectively analysed a single-centre cohort of LT candidates who underwent non-invasive tests; invasive coronary angiography (ICA) was performed depending on the results of non-invasive tests. mCAD-LT was calculated in all patients. RESULTS Six-hundred-and-thirty-four LT candidates were assessed and 351 of them underwent LT. CACS, CCTA and ICA were performed in 245, 123 and 120 LT candidates, respectively. Significant CAD was found in 30% of patients undergoing ICA. The AUROCs of mCAD-LT (.722) and CCTA (.654) were significantly higher than that of CACS (.502) to predict the presence of significant CAD. Specificity of the tests ranged between 31% for CCTA and 53% for CACS. Among patients who underwent LT, CACS ≥ 400 and mCAD-LT were independently associated with the incidence of CVE; in patients who underwent CCTA before LT, significant CAD at CCTA also predicted post-LT CVE. CONCLUSION In this cohort, mCAD-LT score and CT-based tests detect the presence of significant CAD in LT candidates, although they tend to overestimate it. Both mCAD-LT score and CT-based tests classify LT recipients according to their risk of post-LT CVE and can be used to improve post-LT risk mitigation.
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Affiliation(s)
- Giulia Pagano
- Liver Transplant Unit, Hospital Clínic, Barcelona, Spain
- Department of Hepatology, Hospital Clínic, Barcelona, Spain
| | - Lydia Sastre
- Department of Gastroenterology and Hepatology, Hospital Son Espases, Palma de Mallorca, Spain
| | - Annabel Blasi
- Department of Anesthesiology, Hospital Clínic, Barcelona, Spain
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- CIBER-EHD, Madrid, Spain
| | - Salvatore Brugaletta
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Cardiology, Hospital Clínic, Barcelona, Spain
| | - Judit Mestres
- Department of Radiology, Hospital Clínic, Barcelona, Spain
| | | | - Jose T Ortiz-Pérez
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Cardiology, Hospital Clínic, Barcelona, Spain
| | - Clara Viñals
- Department of Endocrinology and Nutrition, Hospital Clínic, Barcelona, Spain
| | - Susanna Prat-Gonzàlez
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Cardiology, Hospital Clínic, Barcelona, Spain
| | - Eva Rivas
- Department of Anesthesiology, Hospital Clínic, Barcelona, Spain
| | - Rosario J Perea
- IDIBAPS, Barcelona, Spain
- Department of Radiology, Hospital Clínic, Barcelona, Spain
| | - Sergio Rodriguez-Tajes
- Liver Transplant Unit, Hospital Clínic, Barcelona, Spain
- Department of Hepatology, Hospital Clínic, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- CIBER-EHD, Madrid, Spain
| | - África Muxí
- IDIBAPS, Barcelona, Spain
- Department of Nuclear Medicine, Hospital Clínic, Barcelona, Spain
| | - Emilio Ortega
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Endocrinology and Nutrition, Hospital Clínic, Barcelona, Spain
- CIBER-OBN, Madrid, Spain
| | - Ada Doltra
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Cardiology, Hospital Clínic, Barcelona, Spain
| | - Pablo Ruiz
- Liver Transplant Unit, Hospital Clínic, Barcelona, Spain
- Department of Hepatology, Hospital Clínic, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
| | - Bàrbara Vidal
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- Department of Cardiology, Hospital Clínic, Barcelona, Spain
| | - Graciela Martínez-Palli
- Department of Anesthesiology, Hospital Clínic, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- CIBER-RES, Madrid, Spain
| | - Jordi Colmenero
- Liver Transplant Unit, Hospital Clínic, Barcelona, Spain
- Department of Hepatology, Hospital Clínic, Barcelona, Spain
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- CIBER-EHD, Madrid, Spain
| | - Gonzalo Crespo
- Liver Transplant Unit, Hospital Clínic, Barcelona, Spain
- Department of Hepatology, Hospital Clínic, Barcelona, Spain
- University of Barcelona, Barcelona, Spain
- IDIBAPS, Barcelona, Spain
- CIBER-EHD, Madrid, Spain
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Martinez-Perez S, McCluskey SA, Davierwala PM, Kalra S, Nguyen E, Bhat M, Borosz C, Luzzi C, Jaeckel E, Neethling E. Perioperative Cardiovascular Risk Assessment and Management in Liver Transplant Recipients: A Review of the Literature Merging Guidelines and Interventions. J Cardiothorac Vasc Anesth 2024; 38:1015-1030. [PMID: 38185566 DOI: 10.1053/j.jvca.2023.11.039] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/23/2023] [Revised: 11/13/2023] [Accepted: 11/26/2023] [Indexed: 01/09/2024]
Abstract
Liver transplantation (LT) is the second most performed solid organ transplant. Coronary artery disease (CAD) is a critical consideration for LT candidacy, particularly in patients with known CAD or risk factors, including metabolic dysfunction associated with steatotic liver disease. The presence of severe CAD may exclude patients from LT; therefore, precise preoperative evaluation and interventions are necessary to achieve transplant candidacy. Cardiovascular complications represent the earliest nongraft-related cause of death post-transplantation. Timely intervention to reduce cardiovascular events depends on adequate CAD screening. Coronary disease screening in end-stage liver disease is challenging because standard noninvasive CAD screening tests have low sensitivity due to hyperdynamic state and vasodilatation. As a result, there is overuse of invasive coronary angiography to exclude severe CAD. Coronary artery calcium scoring using a computed tomography scan is a tool for the prediction of cardiovascular events, and can be used to achieve risk stratification in LT candidates. Recent literature shows that qualitative assessment on both noncontrast- and contrast-enhanced chest computed tomography can be used instead of calcium score to assess the presence of coronary calcium. With increasing prevalence, protocols to address CAD in LT candidates must be reconsidered. Percutaneous coronary intervention could allow a shorter duration of dual-antiplatelet therapy in simple lesions, with safer perioperative outcomes. Hybrid coronary revascularization is an option for high-risk LT candidates with multivessel disease nonamenable to percutaneous coronary intervention. The objective of this review is to evaluate existing methods for preoperative cardiovascular risk stratification, and to describe interventions before surgery to optimize patient outcomes and reduce cardiovascular event risk.
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Affiliation(s)
- Selene Martinez-Perez
- Department of Anesthesia and Pain Management, Toronto General Hospital, University Health Network and Department of Anesthesiology and Pain Medicine, Temetry Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
| | - Stuart A McCluskey
- Department of Anesthesia and Pain Management, Toronto General Hospital, University Health Network and Department of Anesthesiology and Pain Medicine, Temetry Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
| | - Piroze M Davierwala
- Division of Cardiovascular Surgery, Peter Munk Cardiac Centre Toronto, General Hospital, University Health Network, Department of Surgery, University of Toronto, Toronto, Ontario, Canada
| | - Sanjog Kalra
- Division of Cardiology, Interventional Cardiology Section, Peter Munk Cardiac Center Toronto General Hospital, University Health Network and Department of Medicine, Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
| | - Elsie Nguyen
- Department of Medical Imaging, Cardiothoracic Imaging Division Lead, Toronto General Hospital, University of Toronto, Toronto, Ontario, Canada
| | - Mamatha Bhat
- Department of Gastroenterology, Hepatology, Toronto General Hospital, University of Toronto, Toronto, Ontario, Canada
| | - Cheryl Borosz
- Department of Gastroenterology, Toronto General Hospital, Toronto, Ontario, Canada
| | - Carla Luzzi
- Department of Anesthesia and Pain Management, Toronto General Hospital, University Health Network and Department of Anesthesiology and Pain Medicine, Temetry Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
| | - Elmar Jaeckel
- Department of Gastroenterology, Ajmera Transplant Centre, Toronto General Hospital, University of Toronto, Toronto, Ontario, Canada
| | - Elmari Neethling
- Department of Anesthesia and Pain Management, Toronto General Hospital, University Health Network and Department of Anesthesiology and Pain Medicine, Temetry Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada.
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Soldera J, Corso LL, Rech MM, Ballotin VR, Bigarella LG, Tomé F, Moraes N, Balbinot RS, Rodriguez S, Brandão ABDM, Hochhegger B. Predicting major adverse cardiovascular events after orthotopic liver transplantation using a supervised machine learning model: A cohort study. World J Hepatol 2024; 16:193-210. [PMID: 38495288 PMCID: PMC10941741 DOI: 10.4254/wjh.v16.i2.193] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/02/2023] [Revised: 12/27/2023] [Accepted: 02/04/2024] [Indexed: 02/27/2024] Open
Abstract
BACKGROUND Liver transplant (LT) patients have become older and sicker. The rate of post-LT major adverse cardiovascular events (MACE) has increased, and this in turn raises 30-d post-LT mortality. Noninvasive cardiac stress testing loses accuracy when applied to pre-LT cirrhotic patients. AIM To assess the feasibility and accuracy of a machine learning model used to predict post-LT MACE in a regional cohort. METHODS This retrospective cohort study involved 575 LT patients from a Southern Brazilian academic center. We developed a predictive model for post-LT MACE (defined as a composite outcome of stroke, new-onset heart failure, severe arrhythmia, and myocardial infarction) using the extreme gradient boosting (XGBoost) machine learning model. We addressed missing data (below 20%) for relevant variables using the k-nearest neighbor imputation method, calculating the mean from the ten nearest neighbors for each case. The modeling dataset included 83 features, encompassing patient and laboratory data, cirrhosis complications, and pre-LT cardiac assessments. Model performance was assessed using the area under the receiver operating characteristic curve (AUROC). We also employed Shapley additive explanations (SHAP) to interpret feature impacts. The dataset was split into training (75%) and testing (25%) sets. Calibration was evaluated using the Brier score. We followed Transparent Reporting of a Multivariable Prediction Model for Individual Prognosis or Diagnosis guidelines for reporting. Scikit-learn and SHAP in Python 3 were used for all analyses. The supplementary material includes code for model development and a user-friendly online MACE prediction calculator. RESULTS Of the 537 included patients, 23 (4.46%) developed in-hospital MACE, with a mean age at transplantation of 52.9 years. The majority, 66.1%, were male. The XGBoost model achieved an impressive AUROC of 0.89 during the training stage. This model exhibited accuracy, precision, recall, and F1-score values of 0.84, 0.85, 0.80, and 0.79, respectively. Calibration, as assessed by the Brier score, indicated excellent model calibration with a score of 0.07. Furthermore, SHAP values highlighted the significance of certain variables in predicting postoperative MACE, with negative noninvasive cardiac stress testing, use of nonselective beta-blockers, direct bilirubin levels, blood type O, and dynamic alterations on myocardial perfusion scintigraphy being the most influential factors at the cohort-wide level. These results highlight the predictive capability of our XGBoost model in assessing the risk of post-LT MACE, making it a valuable tool for clinical practice. CONCLUSION Our study successfully assessed the feasibility and accuracy of the XGBoost machine learning model in predicting post-LT MACE, using both cardiovascular and hepatic variables. The model demonstrated impressive performance, aligning with literature findings, and exhibited excellent calibration. Notably, our cautious approach to prevent overfitting and data leakage suggests the stability of results when applied to prospective data, reinforcing the model's value as a reliable tool for predicting post-LT MACE in clinical practice.
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Affiliation(s)
- Jonathan Soldera
- Post Graduate Program at Acute Medicine and Gastroenterology, University of South Wales, Cardiff CF37 1DL, United Kingdom
- Postgraduate Program in Pathology, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre 90050-170, Brazil.
| | - Leandro Luis Corso
- Department of Engineering, Universidade de Caxias do Sul, Caxias do Sul 95070-560, Brazil
| | - Matheus Machado Rech
- School of Medicine, Universidade de Caxias do Sul, Caxias do Sul 95070-560, Brazil
| | | | | | - Fernanda Tomé
- Department of Engineering, Universidade de Caxias do Sul, Caxias do Sul 95070-560, Brazil
| | - Nathalia Moraes
- Department of Engineering, Universidade de Caxias do Sul, Caxias do Sul 95070-560, Brazil
| | | | - Santiago Rodriguez
- Postgraduate Program in Hepatology, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre 90050-170, Brazil
| | - Ajacio Bandeira de Mello Brandão
- Postgraduate Program in Hepatology, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre 90050-170, Brazil
| | - Bruno Hochhegger
- Postgraduate Program in Pathology, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre 90050-170, Brazil
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Kleb C, Sims OT, Fares M, Ruthmann N, Ansari K, Esfeh JM. Screening Modalities for Coronary Artery Disease in Liver Transplant Candidates: A Review of the Literature. J Cardiothorac Vasc Anesth 2023; 37:2611-2620. [PMID: 37690949 DOI: 10.1053/j.jvca.2023.08.126] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/21/2023] [Revised: 07/16/2023] [Accepted: 08/09/2023] [Indexed: 09/12/2023]
Abstract
Patients with cirrhosis undergoing liver transplant (LT) are at high risk of postoperative cardiopulmonary complications. It is known that patients with coronary artery disease (CAD) have greater rates of post-LT morbidity and mortality than patients without CAD. Thus, identifying significant CAD in LT candidates is of the utmost importance to optimize survival posttransplant. Consensus is lacking on the ideal screening test for CAD in LT candidates. Traditional exercise and many pharmacologic stress tests are impractical and inaccurate in patients with cirrhosis due to their unique physiology. The purpose of this review is to describe different screening modalities for CAD among LT candidates. The background, diagnostic accuracy, and limitations of each screening modality are described to achieve this goal.
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Affiliation(s)
- Cerise Kleb
- Department of Gastroenterology, University of Maryland Medical Center, Baltimore, MD.
| | - Omar T Sims
- Department of Gastroenterology, Hepatology and Nutrition, Cleveland Clinic, Cleveland, OH; Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, OH
| | - Maan Fares
- Department of Cardiovascular Medicine, Cleveland Clinic, Cleveland, OH
| | - Nicholas Ruthmann
- Department of Cardiovascular Medicine, Cleveland Clinic, Cleveland, OH
| | - Kianoush Ansari
- Department of Diagnostic Radiology, University Hospital Cleveland Medical Center, Cleveland, OH
| | - Jamak Modaresi Esfeh
- Department of Gastroenterology, Hepatology and Nutrition, Cleveland Clinic, Cleveland, OH
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Kozlik A, Wiseman K, Upadhyaya VD, Sharma A, Chatterjee S. Preoperative Coronary Intervention Before Orthotopic Liver Transplantation (from a Review of Literature). Am J Cardiol 2022; 185:94-99. [DOI: 10.1016/j.amjcard.2022.09.014] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/02/2022] [Revised: 08/30/2022] [Accepted: 09/13/2022] [Indexed: 11/28/2022]
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Kassab K, Doukky R. Cardiac imaging for the assessment of patients being evaluated for liver transplantation. J Nucl Cardiol 2022; 29:1078-1090. [PMID: 33825142 DOI: 10.1007/s12350-021-02591-0] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/09/2021] [Accepted: 02/23/2021] [Indexed: 02/06/2023]
Abstract
Cardiac risk assessment prior to liver transplantation has become widely accepted. With the emergence of nonalcoholic steatohepatitis among the leading causes of end-stage liver disease and the steady rise of the age of liver transplant recipients, the burden of cardiovascular diseases has markedly increased in this population. Selecting appropriate liver transplant candidates is crucial due to the increasing demand for scarce donor organs. The use of noninvasive cardiac imaging for pre-operative assessment of the cardiovascular status of liver transplant recipients has been on the rise, yet the optimal assessment strategy remains an area of active debate. In this review, we examine the relevant literature pertaining to the diagnostic and prognostic applications of noninvasive cardiac imaging in this population. We also propose a simple literature-based evaluation algorithm for CAD surveillance in liver transplant candidates.
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Affiliation(s)
- Kameel Kassab
- Division of Cardiology, Cook County Health, Chicago, IL, USA
| | - Rami Doukky
- Division of Cardiology, Cook County Health, Chicago, IL, USA.
- Division of Cardiology, Rush University Medical Center, Chicago, IL, USA.
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Bhatti S, Lizaola-Mayo B, Al-Shoha M, Garcia-Saenz-de-Sicilia M, Habash F, Ayoub K, Karr M, Ahmed Z, Borja-Cacho D, Duarte-Rojo A. Use of Computed Tomography Coronary Calcium Score for Coronary Artery Disease Risk Stratification During Liver Transplant Evaluation. J Clin Exp Hepatol 2022; 12:319-328. [PMID: 35535104 PMCID: PMC9077224 DOI: 10.1016/j.jceh.2021.08.015] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/08/2021] [Accepted: 08/14/2021] [Indexed: 12/12/2022] Open
Abstract
Background End-stage liver disease (ESLD) is not considered a risk factor for atherosclerotic cardiovascular disease (ASCVD). However, lifestyle characteristics commonly associated with increased ASCVD risk are highly prevalent in ESLD. Emerging literature shows a high burden of asymptomatic coronary artery disease (CAD) in patients with ESLD and a high ASCVD risk in liver transplantation (LT) recipients. Coronary artery calcium score (CAC) is a noninvasive test providing reliable CAD risk stratification. We implemented an LT evaluation protocol with CAC playing a central role in triaging and determining the need for further CAD assessment. Here, we inform our results from this early experience. Methods Patients with ESLD referred for LT evaluation were prospectively studied. We compared accuracy of CAC against that of CAD risk factors/scores, troponin I, dobutamine stress echocardiogram (DSE), and single-photon emission computed tomography (SPECT) to detect coronary stenosis ≥70 (CAD ≥ 70) per left heart catheterization (LHC). Thirty-day post-LT cardiac outcomes were also analyzed. Results One hundred twenty-four of 148 (84%) patients underwent CAC, 106 (72%) DSE/SPECT, and 50 (34%) LHC. CAC ≥ 400 was found in 35 (28%), 100 to 399 in 17 (14%), and <100 in 72 (58%). LHC identified CAD ≥ 70% in 8 of 29 (28%), 2 of 9 (22%), and 0 of 4, respectively. Two acute coronary syndromes occurred after LT in a patient with CAC 811 (CAD < 70%), and one with CAC 347 (CAD ≥ 70%). No patients with CAC < 100 presented with acute coronary syndrome after LT. When using CAD ≥ 70% as primary endpoint of LT evaluation, CAC ≥ 346 was the only test showing predictive usefulness (negative predictive value 100%). Conclusions CAC is a promising tool to guide CAD risk stratification and need for LHC during LT evaluation. Patients with a CAC < 100 can safely undergo LT without the need for LHC or cardiac stress testing, whereas a CAC < 346 accurately rules out significant CAD stenosis (≥70%) on LHC, outperforming other CAD risk-stratification strategies.
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Key Words
- ACS, Acute coronary syndromes
- ALD, alcoholic liver disease
- ASCVD, Atherosclerotic cardiovascular disease
- ASCVD, atherosclerosis cardiovascular disease risk
- BMI, Body mass index
- CABG, Coronary angioplasty bypass surgery
- CAC, Coronary calcium score
- CAD, Coronary artery disease
- CKD, chronic kidney disease
- DSE/SPECT, Dobutamine stress echocardiogram or single-photon emission computed tomography
- ESLD, End-stage liver disease
- HCV, hepatitis C virus
- IQR, Interquartile range
- LCx, left circumflex
- LHC, Left heart catheterization
- LT, liver transplantation
- MELD, model for end stage liver disease
- MESA, Multi-Ethnic Study of Atherosclerosis
- METs, Metabolic equivalents
- NPV, negative predictive value
- OM, obtuse marginal
- OPTN, Organ Procurement and Transplantation Network
- PCI, Percutaneous coronary intervention
- PDA, posterior descending artery
- POBA, plain old balloon angioplasty
- PPV, positive predictive value
- RCA, right coronary artery
- RI, ramus intermedius
- ROC, Receiver operating characteristic
- RPL, right posterolateral
- SD, Standard deviation
- VT, Ventricular tachycardia
- agatston score
- angiogram
- cardiac stress test
- cirrhosis
- end-stage liver disease
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Affiliation(s)
- Sabha Bhatti
- Division of Cardiology, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | - Blanca Lizaola-Mayo
- Division of Gastroenterology and Hepatology, Mayo Clinic, 13400 East Shea Blvd, Scottsdale, AZ, 85259, United States
| | - Mohammad Al-Shoha
- Division of Gastroenterology and Hepatology, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | | | - Fuad Habash
- Department of Internal Medicine, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | - Karam Ayoub
- Department of Internal Medicine, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | - Michael Karr
- Department of Internal Medicine, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | - Zubair Ahmed
- Division of Cardiology, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
| | - Daniel Borja-Cacho
- Division of Transplant Surgery, Northwestern University, 676 N Saint Clair, Chicago, IL, 60611, United States
| | - Andres Duarte-Rojo
- Division of Cardiology, University of Arkansas for Medical Sciences, 4301 W. Markham Slot #567, Little Rock, AR, 70205, United States
- Thomas E. Starzl Transplantation Institute and Division of Gastroenterology, Hepatology and Nutrition; University of Pittsburgh Medical Center, 3471 Fifth Avenue, Suite 916, Pittsburgh, PA, 15213, United States
- Address for correspondence: Andres Duarte-Rojo, MD, MS, DSc, Starzl Transplantation Institute and Center for Liver Diseases, University of Pittsburgh Medical Center, 3471 Fifth Avenue, Suite 916, Pittsburgh, PA, 15213, United States. Tel.: +1 412 647-1170; fax: +1 412 647 9268
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Villeret F, Dumortier J, Erard-Poinsot D. How will NAFLD change the liver transplant landscape in the 2020s? Clin Res Hepatol Gastroenterol 2022; 46:101759. [PMID: 34311133 DOI: 10.1016/j.clinre.2021.101759] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/04/2021] [Accepted: 06/21/2021] [Indexed: 02/04/2023]
Abstract
Liver steatosis is the hepatic manifestation of the metabolic syndrome, and is now the leading cause of chronic liver disease worldwide. The treatment of metabolic cirrhosis with liver failure and/or hepatocellular carcinoma is liver transplantation (LT). During the past decade, metabolic cirrhosis represented an increasing cause for LT, especially in the United States. At listing, patients with metabolic cirrhosis are older, with numerous cardiovascular (CV) and renal comorbidities, and this requires multidisciplinary pre-transplant assessment. After LT, 5-year survival is similar to other indications. The leading causes of death are infectious, cancers and CV. The recurrence of the initial disease is very frequent, and a significant part of the patients progress towards graft cirrhosis. No specific immunosuppressive regimen is recommended, but the toxicity profiles must probably be taken into account. In these patients, the only etiological treatment is that of obesity, in the absence of specific therapy for non-alcoholic steatohepatitis. The place of bariatric surgery has to be defined, probably sleeve gastrectomy, in a stable patient, 6-12 months after LT.
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Affiliation(s)
- François Villeret
- Hepatology Department, Croix Rousse Hospital, Hospices Civils de Lyon, Lyon, France; University Claude Bernard Lyon 1, Lyon, France
| | - Jérôme Dumortier
- Hepatogastroenterology Department, Edouard Herriot Hospital, Hospices Civils de Lyon, Lyon, France; University Claude Bernard Lyon 1, Lyon, France.
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Prognostic Value of Computed Tomographic Coronary Angiography for Long-Term Major Adverse Cardiac Events after Liver Transplantation. J Clin Med 2021; 10:jcm10143132. [PMID: 34300296 PMCID: PMC8303180 DOI: 10.3390/jcm10143132] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/05/2021] [Revised: 07/09/2021] [Accepted: 07/13/2021] [Indexed: 12/26/2022] Open
Abstract
Computed tomographic coronary angiography (CTCA) has prognostic value for early major adverse cardiac events (MACEs) after liver transplantation. However, the association between CTCA and long-term MACEs in liver transplant (LT) recipients remains unknown. We evaluated the association between CTCA and long-term MACEs within 5 years after living donor liver transplantation (LDLT). A total of 628 LDLT recipients who underwent CTCA were analyzed between 2010 and 2012. MACEs were investigated within 5 years after LDLT. The factors associated with long-term MACEs in transplant recipients were evaluated. Only 48 (7.6%) patients developed MACEs. In the Fine and Gray competing risk regression, a coronary artery calcium score (CACS) of >400 combined with obstructive coronary artery disease (CAD) (subdistribution hazard ratio: 5.01, 95% confidence interval: 2.37–10.58, p < 0.001), age (1.05, 1.01–1.10, p = 0.018), diabetes mellitus (2.43, 1.37–4.29, p = 0.002), dyslipidemia (2.45, 1.23–4.70, p = 0.023), and creatinine (1.19, 1.08–1.30, p < 0.001) were independently associated with long-term MACEs. CACS (>400) combined with obstructive CAD may be associated with MACEs within 5 years after LDLT, suggesting the importance of preoperative noninvasive CTCA in LT recipients. The evaluation of coronary artery stenosis on CTCA combined with CACS may have a prognostic value for long-term MACEs in LT recipients.
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Robertson M, Chung W, Liu D, Seagar R, O'Halloran T, Koshy AN, Horrigan M, Farouque O, Gow P, Angus P. Cardiac Risk Stratification in Liver Transplantation: Results of a Tiered Assessment Protocol Based on Traditional Cardiovascular Risk Factors. Liver Transpl 2021; 27:1007-1018. [PMID: 33606328 DOI: 10.1002/lt.26025] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/15/2020] [Revised: 12/14/2020] [Accepted: 12/17/2020] [Indexed: 01/13/2023]
Abstract
Coronary artery disease (CAD) confers increased perioperative risk in patients undergoing liver transplantation (LT). Although routine screening for CAD is recommended, there are limited data on the effectiveness of screening strategies. We evaluated the safety and efficacy of a 3-tiered cardiac risk-assessment protocol that stratifies patients based on age and traditional cardiac risk factors. We peformed a single-center, prospective, observational study of consecutive adult patients undergoing LT assessment (2010-2017). Patients were stratified into low-risk (LR), intermediate-risk (IR), or high-risk (HR) cardiac groups and received standardized investigations with selective use of transthoracic echocardiography (TTE), dobutamine stress echocardiography (DSE), computed tomography coronary angiography (CTCA), and coronary angiography (CA). Primary outcomes were cardiac events (CEs) and cardiovascular death up to 30 days after LT. Overall, 569 patients were included, with 76 patients identified as LR, 256 as IR, and 237 as HR. Cardiac risk factors included diabetes mellitus (26.0%), smoking history (47.3%), hypertension (17.8%), hypercholesterolemia (7.2%), family (17.0%) or prior history of heart disease (6.0%), and obesity (27.6%). Of the patients, 42.0% had ≥2 risk factors. Overall compliance with the protocol was 90.3%. Abnormal findings on TTE, DSE, and CTCA were documented in 3, 23, and 44 patients, respectively, and 12 patients were not listed for transplantation following cardiac assessment (1 LR, 2 IR, and 9 HR). Moderate or severe CAD was identified in 25.4% of HR patients on CTCA following a normal DSE. CEs were recorded in 7 patients (1.2%), with 2 cardiovascular deaths (0.4%). Cardiac risk stratification based on traditional cardiac risk factors with the selective use of DSE, CTCA, and CA is a safe and feasible approach that results in a low perioperative cardiac event rate.
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Affiliation(s)
- Marcus Robertson
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia.,Department of Medicine, University of Melbourne, Heidelberg, Victoria, Australia
| | - William Chung
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia
| | - Dorothy Liu
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia
| | - Rosemary Seagar
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia
| | - Tess O'Halloran
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia
| | - Anoop N Koshy
- Department of Medicine, University of Melbourne, Heidelberg, Victoria, Australia.,Department of Cardiology, Austin Hospital, Heidelberg, Victoria, Australia
| | - Mark Horrigan
- Department of Cardiology, Austin Hospital, Heidelberg, Victoria, Australia
| | - Omar Farouque
- Department of Cardiology, Austin Hospital, Heidelberg, Victoria, Australia
| | - Paul Gow
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia.,Department of Medicine, University of Melbourne, Heidelberg, Victoria, Australia
| | - Peter Angus
- Liver Transplant Unit, Austin Hospital, Heidelberg, Victoria, Australia.,Department of Medicine, University of Melbourne, Heidelberg, Victoria, Australia
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11
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Abstract
Increased life expectancy and advances in the care of chronic liver disease has increased the number of elderly patients needing liver transplant. Organ donation policies prioritize transplant to the sickest. There is an ongoing debate with regard to balancing the principles of equity and utility. Several hospitals have adopted center-specific policies and there has been an increased trend of transplant in elderly patients since 2002. Appropriate patient selection and long-term outcomes in the setting of limited organ availability pose several challenges. This article reviews the data and discusses the pros and cons of transplants in the elderly.
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Affiliation(s)
- Claudia Cottone
- Department of Internal Medicine at Northwestern Medicine McHenry Hospital, Rosalind Franklin University of Medicine and Science, 4309 West Medical Center Drive, McHenry, IL 60050, USA.
| | - Nathalie A Pena Polanco
- Division of Digestive Health and Liver Diseases, University of Miami Miller School of Medicine, 1120 Northwest 14th Street, Suite 1105, Miami, FL 33136, USA
| | - Kalyan Ram Bhamidimarri
- Division of Digestive Health and Liver Diseases, University of Miami Miller School of Medicine, 1120 Northwest 14th Street, Suite 1144, Miami, FL 33136, USA
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12
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Bonou M, Mavrogeni S, Kapelios CJ, Skouloudi M, Aggeli C, Cholongitas E, Papatheodoridis G, Barbetseas J. Preoperative Evaluation of Coronary Artery Disease in Liver Transplant Candidates: Many Unanswered Questions in Clinical Practice. Diagnostics (Basel) 2021; 11:diagnostics11010075. [PMID: 33466478 PMCID: PMC7824885 DOI: 10.3390/diagnostics11010075] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/21/2020] [Revised: 12/31/2020] [Accepted: 12/31/2020] [Indexed: 12/29/2022] Open
Abstract
Cardiovascular (CV) complications represent the first non-graft-related cause of death and the third overall cause of death among patients undergoing liver transplantation (LT). History of coronary artery disease is related to increased CV mortality following LT. Although it is of paramount importance to stratify CV risk in pre-LT patients, there is no consensus regarding the choice of the optimal non-invasive cardiac imaging test. Algorithms proposed by scientific associations include non-traditional risk factors, which are associated with increased cardiac risk profiles. Thus, an individualized pre-LT evaluation protocol should be followed. As the average age of patients undergoing LT and the number of candidates continue to rise, the “3 W” questions still remain unanswered, Who, Which and When? Who should be screened for coronary artery disease (CAD), which screening modality should be used and when should the asymptomatic waitlisted patients repeat cardiac evaluation? Prospective studies with large sample sizes are warranted to define an algorithm that can provide better risk stratification and more reliable survival prediction.
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Affiliation(s)
- Maria Bonou
- Department of Cardiology, Laiko General Hospital, 11527 Athens, Greece; (M.B.); (M.S.); (J.B.)
| | - Sophie Mavrogeni
- Department of Cardiology, Onassis Cardiac Surgery Center, 17674 Athens, Greece;
| | - Chris J. Kapelios
- Department of Cardiology, Laiko General Hospital, 11527 Athens, Greece; (M.B.); (M.S.); (J.B.)
- Correspondence: or ; Tel.: +30-213-2061032; Fax: +30-213-2061761
| | - Marina Skouloudi
- Department of Cardiology, Laiko General Hospital, 11527 Athens, Greece; (M.B.); (M.S.); (J.B.)
| | - Constantina Aggeli
- First Department of Cardiology, Hippokration General Hospital, Medical School of National & Kapodistrian University, 11527 Athens, Greece;
| | - Evangelos Cholongitas
- First Department of Internal Medicine, Medical School of National & Kapodistrian University, 11527 Athens, Greece;
| | - George Papatheodoridis
- Department of Gastroenterology, Laiko General Hospital, Medical School of National & Kapodistrian University, 11527 Athens, Greece;
| | - John Barbetseas
- Department of Cardiology, Laiko General Hospital, 11527 Athens, Greece; (M.B.); (M.S.); (J.B.)
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13
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Buggs J, Aslam S, Walker C, Hook M, M. Matyja T, Rogers E, Nyce S, Patiño D, Kumar A, Kemmer N. Pre-Liver Transplant Coronary Artery Disease Workup for Low-Risk Patients. Am Surg 2020; 86:976-980. [DOI: 10.1177/0003134820942169] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
Background Coronary artery disease (CAD) is a leading cause of mortality following orthotopic liver transplant, yet there is no standardized protocol for pre-liver-transplant coronary artery disease assessment. The main objective of this study was to determine the agreement between 2 methods of cardiac risk assessment: dobutamine stress echocardiogram (DSE) and coronary calcium score (CCS) and to determine which test was best able to predict coronary calcification in low-risk patients. Methods A retrospective study was performed using the medical records of 436 patients who received cardiac clearance for a liver transplant. A total of 152 patients’ medical records were included based on the inclusion of patients who had received both DSE and CCS. A kappa coefficient was calculated to determine the agreement between the DSE and CCS results. In addition, the positive predictive values (PPVs) of both the CCS and DSE along with cardiac catheterization indicating abdominal occlusion were analyzed to compare the accuracy of the 2 tests. Results It was determined that there was a 12% agreement between DSE results and CCS. It was found that the DSE had a PPV of 56% and the CCS had a PPV of 80%. Conclusion From this data, it was concluded that there was no agreement between the results of the CCS and the DSE. While neither the CCS nor the DSE presents an optimal method of risk assessment, the CCS had a much higher PPV and was therefore determined to be the more accurate test.
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Affiliation(s)
- Jacentha Buggs
- Department of Transplant Surgery, Tampa General Medical Group, Tampa, FL, USA
| | - Sadaf Aslam
- Morsani College of Medicine, University of South Florida, Tampa, FL, USA
| | - Chelsea Walker
- Morsani College of Medicine, University of South Florida, Tampa, FL, USA
| | - Madison Hook
- Pre-medical Studies, University of Tampa, Tampa, FL, USA
| | | | - Ebonie Rogers
- Office of Clinical Research, Tampa General Hospital, Tampa, FL, USA
| | - Samantha Nyce
- Pre-medical Studies, University of Tampa, Tampa, FL, USA
| | - Diego Patiño
- Pre-medical Studies, University of Tampa, Tampa, FL, USA
| | - Ambuj Kumar
- Morsani College of Medicine, University of South Florida, Tampa, FL, USA
| | - Nyingi Kemmer
- Department of Transplant Hepatology, Tampa General Medical Group, Tampa, FL, USA
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14
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Soldera J, Camazzola F, Rodríguez S, Brandão A. Dobutamine stress echocardiography, myocardial perfusion scintigraphy, invasive coronary angiography, and post-liver transplantation events: Systematic review and meta-analysis. Clin Transplant 2018; 32:e13222. [PMID: 29436036 DOI: 10.1111/ctr.13222] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/04/2018] [Indexed: 12/15/2022]
Abstract
The impact of coronary artery disease on the clinical course of patients enrolled for liver transplantation (LT) has changed over the years as these patients become older and sicker. The purpose of this systematic review and meta-analysis was to investigate the value of dobutamine stress echocardiography (DSE), myocardial perfusion scintigraphy (MPS), and invasive coronary angiography (ICA) in predicting cardiac events post-LT in cirrhotic patients. A literature search was conducted using Scopus, Web of Science, EMBASE, MEDLINE (via PubMed), BIREME (regional medical library of the Pan American Health Organization), LILACS (Latin American and Caribbean Health Sciences Literature), Cochrane Library for Systematic Reviews, and OpenGrey Repository (www.opengrey.eu) electronic databases. A total of 322 records were retrieved for DSE, 90 for MPS, and 149 for ICA. In the final analysis, 11 records for DSE, 7 for MPS, and 8 for ICA were included. The relative risk and confidence interval for major adverse cardiac events were 30.2 (2.8-325.4) for DSE, 2.6 (1.09-6.1) for MPS, and 2.1 (1.0-2.3) for ICA, while the relative risk and confidence interval for all-cause mortality was 4.7 for DSE (1.8-12.0), 2.7 (1.25-5.9) for MPS, and 1.5 (0.89-3.2) for ICA. In conclusion, this meta-analysis found that DSE, MPS, and ICA do not satisfactorily predict increased risk of perioperative MACE or all-cause mortality among cirrhotic patients listed for LT, among small and heterogenous studies.
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Affiliation(s)
- Jonathan Soldera
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, RS, Brazil
- School of Medicine, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil
| | - Fábio Camazzola
- School of Medicine, Universidade de Caxias do Sul (UCS), Caxias do Sul, RS, Brazil
| | - Santiago Rodríguez
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, RS, Brazil
| | - Ajacio Brandão
- Graduate Program in Medicine: Hepatology, School of Medicine, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, RS, Brazil
- Liver Transplantation Group, Santa Casa de Misericórdia de Porto Alegre, Porto Alegre, RS, Brazil
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15
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VanWagner LB, Harinstein ME, Runo JR, Darling C, Serper M, Hall S, Kobashigawa JA, Hammel LL. Multidisciplinary approach to cardiac and pulmonary vascular disease risk assessment in liver transplantation: An evaluation of the evidence and consensus recommendations. Am J Transplant 2018; 18:30-42. [PMID: 28985025 PMCID: PMC5840800 DOI: 10.1111/ajt.14531] [Citation(s) in RCA: 111] [Impact Index Per Article: 15.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/23/2017] [Revised: 09/12/2017] [Accepted: 09/28/2017] [Indexed: 01/25/2023]
Abstract
Liver transplant (LT) candidates today are older, have greater medical severity of illness, and have more cardiovascular comorbidities than ever before. In addition, there are specific cardiovascular responses in cirrhosis that can be detrimental to the LT candidate. Cirrhotic cardiomyopathy, a condition characterized by increased cardiac output and a reduced ventricular response to stress, is present in up to 30% of patients with cirrhosis, thus challenging perioperative management. Current noninvasive tests that assess for subclinical coronary and myocardial disease have low sensitivity, and altered hemodynamics during the LT surgery can unmask latent cardiovascular disease either intraoperatively or in the immediate postoperative period. Therefore, this review, assembled by a group of multidisciplinary experts in the field and endorsed by the American Society of Transplantation Liver and Intestine and Thoracic and Critical Care Communities of Practice, provides a critical assessment of the diagnosis of cardiac and pulmonary vascular disease and interventions aimed at managing these conditions in LT candidates. Key points and practice-based recommendations for the diagnosis and management of cardiac and pulmonary vascular disease in this population are provided to offer guidance for clinicians and identify gaps in knowledge for future investigations.
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Affiliation(s)
- Lisa B. VanWagner
- Division of Gastroenterology and Hepatology, Department of Medicine and Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL USA
| | - Matthew E. Harinstein
- Heart and Vascular Institute, Division of Cardiology, University of Pittsburgh Medical Center, Pittsburgh, PA USA
| | - James R. Runo
- Division of Pulmonary and Critical Care Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI USA
| | - Christopher Darling
- Department of Anesthesiology, University of Wisconsin School of Medicine and Public Health, Madison, WI USA
| | - Marina Serper
- Division of Gastroenterology, Department of Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA USA
| | - Shelley Hall
- Division of Transplant Cardiology, Baylor University Medical Center, Dallas, TX USA
| | - Jon A. Kobashigawa
- Division of Cardiology, Cedars-Sinai Medical Center, Los Angeles, CA USA
| | - Laura L. Hammel
- Department of Anesthesiology, University of Wisconsin School of Medicine and Public Health, Madison, WI USA
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16
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Kwon JH, Yoon YI, Song GW, Kim KH, Moon DB, Jung DH, Park GC, Tak EY, Kirchner VA, Lee SG. Living Donor Liver Transplantation for Patients Older Than Age 70 Years: A Single-Center Experience. Am J Transplant 2017; 17:2890-2900. [PMID: 28510341 DOI: 10.1111/ajt.14355] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/22/2016] [Revised: 05/01/2017] [Accepted: 05/04/2017] [Indexed: 01/25/2023]
Abstract
Over the past two decades, the age of liver transplantation (LT) recipients has been increasing. We reviewed our experience with LT for patients aged ≥70 years (range: 70-78 years) and investigated the feasibility of performing LT, especially living donor LT (LDLT), for older patients. We retrospectively reviewed the medical records of 25 patients (15 LDLT recipients, 10 deceased donor LT recipients) aged ≥70 years who underwent LT from January 2000 to April 2016. Their perioperative morbidity rate was 28.0%, and the in-hospital mortality rate was 16.0%; these results were comparable to those of matched patients in their 60s (n = 73; morbidity, p = 0.726; mortality, p = 0.816). For patients in their 70s, the 1- and 5-year patient survival rates were 84.0% and 69.8%, and the 1- and 5-year graft survival rates were 83.5% and 75.1%, respectively. Comparisons of patient and graft survival rates between matched patients in their 60s and 70s showed no statistically significant differences (patient survival, p = 0.372; graft survival, p = 0.183). Our experience suggests that patients aged ≥70 years should not be excluded from LT, or even LDLT, based solely on age and implies that careful selection of recipients and donors as well as meticulous surgical technique are necessary for successful results.
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Affiliation(s)
- J H Kwon
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Y I Yoon
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Korea University Medical Center, University of Korea College of Medicine, Seoul, Korea
| | - G W Song
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - K H Kim
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - D B Moon
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - D H Jung
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - G C Park
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - E Y Tak
- Asan Institute for Life Sciences and Asan-Minnesota Institute for Innovating Transplantation, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - V A Kirchner
- Division of Transplantation, Department of Surgery and Asan-Minnesota Institute for Innovating Transplantation, University of Minnesota, Minneapolis, MN
| | - S G Lee
- Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
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