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Yuzefpolskaya M, Bohn B, Ladanyi A, Pinsino A, Braghieri L, Carey MR, Clerkin K, Sayer GT, Latif F, Koji T, Uriel N, Nandakumar R, Uhlemann AC, Colombo PC, Demmer RT. Alterations in the sarcopenia index are associated with inflammation, gut, and oral microbiota among heart failure, left ventricular assist device, and heart transplant patients. J Heart Lung Transplant 2024; 43:1395-1408. [PMID: 38744352 DOI: 10.1016/j.healun.2024.04.069] [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: 11/09/2023] [Revised: 03/28/2024] [Accepted: 04/27/2024] [Indexed: 05/16/2024] Open
Abstract
BACKGROUND Sarcopenia, characterized by loss of muscle mass and function, is prevalent in heart failure (HF) and predicts poor outcomes. We investigated alterations in sarcopenia index (SI), a surrogate for skeletal muscle mass, in HF, left ventricular assist device (LVAD), and heart transplant (HT), and assessed its relationship with inflammation and digestive tract (gut and oral) microbiota. METHODS We enrolled 460 HF, LVAD, and HT patients. Repeated measures pre/post-procedures were obtained prospectively in a subset of LVAD and HT patients. SI (serum creatinine/cystatin C) and inflammatory biomarkers (C-reactive protein, interleukin-6, tumor necrosis factor-alpha) were measured in 271 and 622 blood samples, respectively. Gut and saliva microbiota were assessed via 16S ribosomal ribonucleic acid sequencing among 335 stool and 341 saliva samples. Multivariable regression assessed the relationship between SI and (1) New York Heart Association class; (2) pre- versus post-LVAD or HT; and (3) biomarkers of inflammation and microbial diversity. RESULTS Median (interquartile range) natural logarithm (ln)-SI was -0.13 (-0.32, 0.05). Ln-SI decreased across worsening HF class, further declined at 1 month after LVAD and HT, and rebounded over time. Ln-SI was correlated with inflammation (r = -0.28, p < 0.01), gut (r = 0.28, p < 0.01), and oral microbial diversity (r = 0.24, p < 0.01). These associations remained significant after multivariable adjustment in the combined cohort but not for all individual cohorts. The presence of the gut taxa Roseburia inulinivorans was associated with increased SI. CONCLUSIONS SI levels decreased in symptomatic HF and remained decreased long-term after LVAD and HT. In the combined cohort, SI levels covaried with inflammation in a similar fashion and were significantly related to overall microbial (gut and oral) diversity, including specific taxa compositional changes.
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Affiliation(s)
- Melana Yuzefpolskaya
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York.
| | - Bruno Bohn
- Division of Epidemiology and Community Health, School of Public Health, University of Minnesota, Minneapolis, Minnesota
| | - Annamaria Ladanyi
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Alberto Pinsino
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Lorenzo Braghieri
- Division of Cardiovascular Medicine, Department of Cardiology, Cleveland Clinic, Cleveland, Ohio
| | - Matthew R Carey
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Kevin Clerkin
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Gabriel T Sayer
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Farhana Latif
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Takeda Koji
- Division of Cardiothoracic Surgery, Department of Surgery, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Nir Uriel
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Renu Nandakumar
- Biomarkers Core Laboratory, Irving Institute for Clinical and Translational Research, Columbia University Irving Medical Center, New York, New York
| | - Anne-Catrin Uhlemann
- Division of Infectious Diseases and Microbiome and Pathogen Genomics Core, Department of Medicine, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Paolo C Colombo
- Division of Cardiovascular Medicine, Department of Cardiology, New York Presbyterian Hospital, Columbia University, New York, New York
| | - Ryan T Demmer
- Division of Epidemiology and Community Health, School of Public Health, University of Minnesota, Minneapolis, Minnesota; Division of Epidemiology, Mailman School of Public Health, Columbia University Irving Medical Center, New York, New York
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Wang AP, Ward K, Griffith G, Gambetta K. Effect of body mass index on exercise capacity following pediatric heart transplantation. Pediatr Transplant 2024; 28:e14772. [PMID: 38702928 DOI: 10.1111/petr.14772] [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: 01/27/2024] [Accepted: 04/15/2024] [Indexed: 05/06/2024]
Abstract
BACKGROUND Obesity and impaired exercise tolerance following heart transplantation increase the risk of post-transplant morbidity and mortality. The aim of this study was to evaluate the effect of body mass index on markers of exercise capacity in pediatric heart transplant recipients and compare this effect with a healthy pediatric cohort. METHODS A retrospective analysis of cardiopulmonary exercise test data between 2004 and 2022 was performed. All patients exercised on a treadmill using the Bruce protocol. Inclusion criteria included patients aged 6-21 years, history of heart transplantation (transplant cohort) or no cardiac diagnosis (control cohort) at the time of testing, and a maximal effort test. Patients were further stratified within these two cohorts as underweight, normal, overweight, and obese based on body mass index groups. Two-way analyses of variance were performed with diagnosis and body mass index category as the independent variables. RESULTS A total of 250 exercise tests following heart transplant and 1963 exercise tests of healthy patients were included. Heart transplant patients across all body mass index groups had higher resting heart rate and lower maximal heart rate, heart rate recovery at 1 min, exercise duration, and peak aerobic capacity (VO2peak). Heart transplant patients in the normal and overweight body mass index categories had higher VO2peak and exercise duration when compared to underweight and obese patients. CONCLUSION Underweight status and obesity are strongly associated with lower VO2peak and exercise duration in heart transplant patients. Normal and overweight heart transplant patients had the best markers of exercise capacity.
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Affiliation(s)
- Alan P Wang
- Division of Pediatric Cardiology, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA
| | - Kendra Ward
- Division of Pediatric Cardiology, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA
| | - Garett Griffith
- Department of Physical Therapy and Human Movement Sciences, Northwestern University, Evanston, IL, USA
| | - Katheryn Gambetta
- Division of Pediatric Cardiology, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA
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Way KL, Thomas HJ, Parker L, Maiorana A, Keske MA, Scott D, Reed JL, Tieng J, Hackett D, Hawkins T, Latella C, Cordina R, Tran DL. Cluster Sets to Prescribe Interval Resistance Training: A Potential Method to Optimise Resistance Training Safety, Feasibility and Efficacy in Cardiac Patients. SPORTS MEDICINE - OPEN 2023; 9:86. [PMID: 37725296 PMCID: PMC10509118 DOI: 10.1186/s40798-023-00634-z] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 02/02/2023] [Accepted: 09/04/2023] [Indexed: 09/21/2023]
Abstract
The integration of resistance training for cardiac patients leads to important health outcomes that are not optimally obtained with aerobic exercise; these include an increase in muscle mass, maintenance of bone mineral density, and improvements in muscular fitness parameters. Despite the proliferation of evidence supporting resistance exercise in recent decades, the implementation of resistance training is underutilised, and prescription is often sub-optimal in cardiac patients. This is frequently associated with safety concerns and inadequate methods of practical exercise prescription. This review discusses the potential application of cluster sets to prescribe interval resistance training in cardiac populations. The addition of planned, regular passive intra-set rest periods (cluster sets) in resistance training (i.e., interval resistance training) may be a practical solution for reducing the magnitude of haemodynamic responses observed with traditional resistance training. This interval resistance training approach may be a more suitable option for cardiac patients. Additionally, many cardiac patients present with impaired exercise tolerance; this model of interval resistance training may be a more suitable option to reduce fatigue, increase patient tolerance and enhance performance to these workloads. Practical strategies to implement interval resistance training for cardiac patients are also discussed. Preliminary evidence suggests that interval resistance training may lead to safer acute haemodynamic responses in cardiac patients. Future research is needed to determine the efficacy and feasibility of interval resistance training for health outcomes in this population.
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Affiliation(s)
- Kimberley L Way
- Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, VIC, 3125, Australia.
- Exercise Physiology and Cardiovascular Health Lab, Division of Cardiac Prevention and Rehabilitation, University of Ottawa Heart Institute, Ottawa, ON, Canada.
| | - Hannah J Thomas
- Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, VIC, 3125, Australia
| | - Lewan Parker
- Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, VIC, 3125, Australia
| | - Andrew Maiorana
- Curtin School of Allied Health, Curtin University, Perth, WA, Australia
- Allied Health Department, Fiona Stanley Hospital, Perth, WA, Australia
| | - Michelle A Keske
- Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, VIC, 3125, Australia
| | - David Scott
- Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, VIC, 3125, Australia
- School of Clinical Sciences at Monash Health, Monash University, Clayton, VIC, Australia
| | - Jennifer L Reed
- Exercise Physiology and Cardiovascular Health Lab, Division of Cardiac Prevention and Rehabilitation, University of Ottawa Heart Institute, Ottawa, ON, Canada
- School of Epidemiology and Public Health, Faculty of Medicine, University of Ottawa, Ottawa, ON, Canada
- School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada
| | - Jessica Tieng
- Epigenetics and RNA Biology Program, Centenary Institute, Camperdown, NSW, Australia
- Central Clinical School, The University of Sydney School of Medicine, Camperdown, NSW, 2006, Australia
| | - Daniel Hackett
- Discipline of Exercise and Sports Science, Sydney School of Health Sciences, Faculty of Medicine and Health, The University of Sydney, Camperdown, Australia
| | - Tess Hawkins
- Concord Centre for STRONG Medicine, Concord Repatriation General Hospital, Concord West, NSW, Australia
| | - Christopher Latella
- School of Health and Medical Sciences, Edith Cowan University, Joondalup, WA, Australia
| | - Rachael Cordina
- Central Clinical School, The University of Sydney School of Medicine, Camperdown, NSW, 2006, Australia
- Department of Cardiology, Royal Prince Alfred Hospital, Camperdown, NSW, Australia
- Charles Perkins Centre, Heart Research Institute, Camperdown, NSW, Australia
| | - Derek L Tran
- Central Clinical School, The University of Sydney School of Medicine, Camperdown, NSW, 2006, Australia.
- Department of Cardiology, Royal Prince Alfred Hospital, Camperdown, NSW, Australia.
- Charles Perkins Centre, Heart Research Institute, Camperdown, NSW, Australia.
- Human Performance Research Centre, School of Sport, Exercise and Rehabilitation, Faculty of Health, University of Technology Sydney, Moore Park, NSW, Australia.
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Zhan YF, Shi Q, Pan YC, Zheng BS, Ge YP, Luo TG, Xiao ZH, Jiang W. Sufentanil: a risk factor for lactic acidosis in patients after heart valve surgery. J Cardiothorac Surg 2022; 17:233. [PMID: 36085208 PMCID: PMC9461198 DOI: 10.1186/s13019-022-01986-5] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/16/2022] [Accepted: 08/18/2022] [Indexed: 11/11/2022] Open
Abstract
Backgrounds Hyperlactatemia is a common metabolic disorder after cardiac surgery with cardiopulmonary bypass. Epinephrine use has been identified as a potential cause of increased lactate levels after cardiac surgery. Stress can lead to an increase in catecholamines, mainly epinephrine, in the body. Exogenous epinephrine causes hyperlactatemia, whereas endogenous epinephrine released by stress may have the same effect. Opioids are the most effective anesthetics to suppress the stress response in the body. The authors sought to provide evidence through a retrospective data analysis that helps investigate the relationship between intraoperative opioid dosage and postoperative lactic acidosis after cardiac surgery.
Methods The clinical data of 215 patients who underwent valvular heart surgery with cardiopulmonary bypass from July 2016 to July 2019 were analyzed retrospectively. Blood lactate levels were measured at 0.1 h, 2 h, 4 h, and 8 h after surgery. Patients with continuous increases in lactate levels and lactate levels exceeding 5 mmol/L at two or more time points were included in the lactic acidosis group, whereas the other patients were included in the control group. First, univariate correlation analysis was used to identify parameters that were significantly different between the two groups, and then multivariate regression analysis was conducted to elucidate the independent risk factors for lactic acidosis. Fifty-one pairs of patients were screened by propensity score matching analysis (PSM). Then, lactic acid levels at four time points in both groups were analyzed by repeated measures ANOVA. Results he EF (heart ejection fraction) (OR = 0.94, P = 0.003), aortic occlusion time (OR = 10.17, P < 0.001) and relative infusion rate (OR = 2.23, P = 0.01) of sufentanil was an independent risk factor for lactic acidosis after valvular heart surgery. The patients were further divided into two groups with the mean sufentanil infusion rate as the reference point. The data were filtered with PSM (Propensity Score Matching). Lactic acid values in both groups peaked at 4 h after surgery and then declined. The rate of lactic acid decline was significantly faster in the group with a higher sufentanil dosage than in the lower group. The difference was statistically significant (P < 0.05). There was also a significant difference in lactic acid levels at the four time points (0.1 h, 2 h, 4 h and 8 h after surgery) in both groups (P < 0.001). Conclusion The inadequate intraoperative infusion rate of sufentanil is an independent risk factor for lactic acidosis after heart valve surgery. The possibility of lactic acidosis caused by this factor after cardiac surgery should be considered, which is helpful for postoperative patient management.
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Affiliation(s)
- Yu-Fei Zhan
- Department of Cardiothoracic Surgery, The Second Affiliated Hospital of Guilin Medical University, Guilin, 541199, People's Republic of China.,Cardic Centre, 924 Hospital of the Chinese Joint Service Support Force, Guangxi Institute of Metabolic Diseases, Guilin, 541002, People's Republic of China
| | - Quan Shi
- Anesthesiology Department, First Affiliated Hospital of Guilin Medical University, Guilin, 541001, People's Republic of China
| | - Yu-Chen Pan
- Cardic Centre, 924 Hospital of the Chinese Joint Service Support Force, Guangxi Institute of Metabolic Diseases, Guilin, 541002, People's Republic of China
| | - Bao-Shi Zheng
- Department of Cardiothoracic Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, 530213, People's Republic of China
| | - Yi-Peng Ge
- Department of Cardiac Surgery, Anzhen Hospital, Capital Medical University, Beijing, 100029, People's Republic of China
| | - Tian-Ge Luo
- Department of Cardiac Surgery, Anzhen Hospital, Capital Medical University, Beijing, 100029, People's Republic of China
| | - Zhi-Hong Xiao
- Department of Cardiothoracic Surgery, The Second Affiliated Hospital of Guilin Medical University, Guilin, 541199, People's Republic of China
| | - Wei Jiang
- Department of Anatomy and Histology, School of Basic Medical Science, Shenzhen University Health Science Centre, Shenzhen, 518055, People's Republic of China.
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5
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Regamey J, Monney P, Yerly P, Favre L, Kirsch M, Tozzi P, Lamy O, Hullin R. Body composition and maximal exercise capacity after heart transplantation. ESC Heart Fail 2021; 9:122-132. [PMID: 34854252 PMCID: PMC8788057 DOI: 10.1002/ehf2.13642] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/03/2021] [Revised: 09/07/2021] [Accepted: 09/19/2021] [Indexed: 11/13/2022] Open
Abstract
Aims Maximal exercise capacity as measured by peak oxygen consumption (pVO2) in cardiopulmonary exercise testing (CPET) of heart transplant recipients (HTR) is limited to a 50–70% level of healthy age‐matched controls. This study investigated the relationship between body composition and pVO2 during the first decade post‐transplant. Methods and results Body composition was determined by dual‐energy X‐ray absorptiometry (DXA) and pVO2 by CPET in 48 HTR (n = 38 males; mean age 51 ± 12 years). A total of 95 assessments were acquired 1–9 years post‐transplant, and the results of four consecutive periods were compared [Period 1: 1–2 years (n = 25); 2: 3–4 years (n = 23); 3: 5–6 years (n = 23); 4: 7–9 years (n = 24)]. Linear regression analysis analysed the correlation between pVO2 and pairs of appendicular lean mass (ALM) and fat mass (FM). The relation between ALM and daily dose of calcineurin inhibitor (CNI) was explored using partial correlation controlling for age, gender, and height. pVO2 increased from 0.98 (0.34) to 1.35 (0.35) L/min (P < 0.01) between Periods 1 and 4 corresponding to 54.5–63.3% of predicted value. Peak heart rate (HR) raised from 115 ± 19 to 131 ± 23 b.p.m. (P = 0.05), and anaerobic threshold (AT = VO2 achieved at AT) increased from 0.57 (0.18) to 0.83 (0.35) L/min (P < 0.01) between Periods 1 and 3. Median FM normalized to height2 (FMI) always remained elevated (>8.8 kg/m2). ALM normalized to body mass index increased from 0.690 (0.188) to 0.848 (0.204) m2 (P = 0.02) between Periods 1 and 4, explaining 45% of the variance of pVO2 (R2 = 0.455; P < 0.001). Eighty‐one per cent of the variance of pVO2 (R2 = 0.817; P < 0.001) in multiple regression was explained by AT (β = 0.488), ALM (β = 0.396), peak HR (β = 0.366), and FMI (β = −0.181). ALM was negatively correlated with daily CNI dose (partial R = −0.258; P = 0.01). Conclusions After heart transplantation, the beneficial effect of peripheral skeletal muscle gain on pVO2 is opposed by increased FM. Our findings support lifestyle efforts to fight adiposity and CNI dose reduction in the chronic stable phase to favour positive adaptation of peripheral muscle mass.
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Affiliation(s)
- Julien Regamey
- Service de Cardiologie, Département Coeur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Pierre Monney
- Service de Cardiologie, Département Coeur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Patrick Yerly
- Service de Cardiologie, Département Coeur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Lucie Favre
- Service d'Endocrinologie, Diabétologie et Métabolisme, Département de Médecine, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Matthias Kirsch
- Service de Chirurgie Cardiaque, Département Cœur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Piergiorgio Tozzi
- Service de Chirurgie Cardiaque, Département Cœur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Olivier Lamy
- Centre des Maladies osseuses, Département de l'Appareil Locomoteur, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
| | - Roger Hullin
- Service de Cardiologie, Département Coeur-Vaisseaux, Lausanne University Hospital (CHUV) and University of Lausanne (UNIL), Lausanne, Switzerland
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Kourek C, Karatzanos E, Nanas S, Karabinis A, Dimopoulos S. Exercise training in heart transplantation. World J Transplant 2021; 11:466-479. [PMID: 34868897 PMCID: PMC8603635 DOI: 10.5500/wjt.v11.i11.466] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/01/2021] [Revised: 08/12/2021] [Accepted: 10/27/2021] [Indexed: 02/06/2023] Open
Abstract
Heart transplantation remains the gold standard in the treatment of end-stage heart failure (HF). Heart transplantation patients present lower exercise capacity due to cardiovascular and musculoskeletal alterations leading thus to poor quality of life and reduction in the ability of daily self-service. Impaired vascular function and diastolic dysfunction cause lower cardiac output while decreased skeletal muscle oxidative fibers, enzymes and capillarity cause arteriovenous oxygen difference, leading thus to decreased peak oxygen uptake in heart transplant recipients. Exercise training improves exercise capacity, cardiac and vascular endothelial function in heart transplant recipients. Pre-rehabilitation regular aerobic or combined exercise is beneficial for patients with end-stage HF awaiting heart transplantation in order to maintain a higher fitness level and reduce complications afterwards like intensive care unit acquired weakness or cardiac cachexia. All hospitalized patients after heart transplantation should be referred to early mobilization of skeletal muscles through kinesiotherapy of the upper and lower limbs and respiratory physiotherapy in order to prevent infections of the respiratory system prior to hospital discharge. Moreover, all heart transplant recipients after hospital discharge who have not already participated in an early cardiac rehabilitation program should be referred to a rehabilitation center by their health care provider. Although high intensity interval training seems to have more benefits than moderate intensity continuous training, especially in stable transplant patients, individualized training based on the abilities and needs of each patient still remains the most appropriate approach. Cardiac rehabilitation appears to be safe in heart transplant patients. However, long-term follow-up data is incomplete and, therefore, further high quality and adequately-powered studies are needed to demonstrate the long-term benefits of exercise training in this population.
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Affiliation(s)
- Christos Kourek
- Clinical Ergospirometry, Exercise & Rehabilitation Laboratory, Evaggelismos Hospital, Athens 10676, Attica, Greece
| | - Eleftherios Karatzanos
- Clinical Ergospirometry, Exercise & Rehabilitation Laboratory, Evaggelismos Hospital, Athens 10676, Attica, Greece
| | - Serafim Nanas
- Clinical Ergospirometry, Exercise & Rehabilitation Laboratory, Evaggelismos Hospital, Athens 10676, Attica, Greece
| | - Andreas Karabinis
- Cardiac Surgery Intensive Care Unit, Onassis Cardiac Surgery Center, Athens 17674, Greece
| | - Stavros Dimopoulos
- Clinical Ergospirometry, Exercise & Rehabilitation Laboratory, Evaggelismos Hospital, Athens 10676, Attica, Greece
- Cardiac Surgery Intensive Care Unit, Onassis Cardiac Surgery Center, Athens 17674, Greece
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Hornikx M, Van Aelst L, Claessen G, Droogne W, Vörös G, Janssens S, Van Cleemput J. Exercise capacity, muscle strength and objectively measured physical activity in patients after heart transplantation. Transpl Int 2021; 34:2589-2596. [PMID: 34644421 DOI: 10.1111/tri.14139] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/25/2021] [Revised: 09/10/2021] [Accepted: 10/11/2021] [Indexed: 11/28/2022]
Abstract
Maximal exercise capacity of patients after heart transplantation (HTX) remains limited, affecting their quality of life. Evidence on the evolution of muscle strength and physical activity (PA) post-HTX is lacking, but a prerequisite to tailor cardiac rehabilitation programmes. Forty-five consecutive patients were evaluated every 3 months during the first year post-HTX. Functional exercise capacity (Six minutes walking distance test (6MWD)), peripheral (Quadriceps strength (QF)) and respiratory (Maximal inspiratory strength (MIP)) muscle strength were evaluated. PA (number of steps (PAsteps), active time (PAactive) and sedentary time (PAsed)) was objectively measured. 6MWD, QF, MIP, PAsteps and PAactive significantly improved over time (P < 0.001). No change in PAsed was noticed (P = 0.129). Despite improvements in 6MWD and QF, results remained substantially below those of age-and gender-matched healthy subjects. One year post-HTX, 30% of patients presented with peripheral muscle weakness. Baseline levels of 6MWD and QF were significantly higher in patients with pretransplant LVAD-implantation and this difference was maintained during follow-up. cardiac rehabilitation, combining aerobic exercise training and peripheral muscle strength training, is mandatory in patients post-HTX. Inspiratory muscle training should be implemented when respiratory muscle weakness is present. Programmes improving physical activity and reducing sedentary time post-HTX are essential.
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Affiliation(s)
- Miek Hornikx
- Department of Rehabilitation Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Lucas Van Aelst
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Guido Claessen
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Walter Droogne
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Gabor Vörös
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Stefan Janssens
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
| | - Johan Van Cleemput
- Department of Cardiovascular Sciences, University Hospitals Leuven, KU Leuven-University of Leuven, Leuven, Belgium
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8
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Whitsett M, Serper M. Exercise Interventions for Transplant Recipients. CURRENT TRANSPLANTATION REPORTS 2021. [DOI: 10.1007/s40472-021-00324-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
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Beltrami M, Fumagalli C, Milli M. Frailty, sarcopenia and cachexia in heart failure patients: Different clinical entities of the same painting. World J Cardiol 2021; 13:1-10. [PMID: 33552398 PMCID: PMC7821009 DOI: 10.4330/wjc.v13.i1.1] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/20/2020] [Revised: 11/25/2020] [Accepted: 12/28/2020] [Indexed: 02/06/2023] Open
Abstract
Heart Failure (HF) in elderly patients is a systemic syndrome where advanced age, comorbidities with organ system deterioration, frailty and impaired cognition significantly impact outcome. Cardiac cachexia, sarcopenia and frailty despite overlap in definitions are different clinical entities that frequently coexist in HF patients. However, these co-factors often remain unaddressed, resulting in poor quality-of-life, prolonged physical disability and exercise intolerance and finally with higher rehospitalization rates and mortality. Strategy aim to increase muscle mass and muscle strength and delay the occurrence of frailty state appear essential in this regard. Common HF drugs therapy (b-blockers, angiotensin-converting enzyme inhibitors) and prescription of physical exercise program remain the cornerstone of therapeutic approach in HF patients with new promising data regarding nutritional supplementation. However, the treatment of all these conditions still remain debated and only a profound knowledge of the specific mechanisms and patterns of disease progression will allow to use the appropriate therapy in a given clinical setting. For all these reasons we briefly review current knowledge on frailty, sarcopenia and cachexia in HF patients with the attempt to define clinically significant degrees of multiorgan dysfunction, specific "red alert" thresholds in clinical practice and therapeutic approach.
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Affiliation(s)
- Matteo Beltrami
- Cardiology Unit, San Giovanni di Dio Hospital, Florence 50142, Italy
| | - Carlo Fumagalli
- Cardiomyopathy Unit, Careggi University Hospital, Florence 50139, Italy
| | - Massimo Milli
- Cardiology Unit, San Giovanni di Dio Hospital, Florence 50142, Italy
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10
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Masarone D, Melillo E, Petraio A, Valente F, Gravino R, Verrengia M, Pacileo G. Exercise-based rehabilitation strategies in heart transplant recipients: Focus on high-intensity interval training. Clin Transplant 2020; 35:e14143. [PMID: 33150597 DOI: 10.1111/ctr.14143] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/12/2020] [Revised: 10/26/2020] [Accepted: 10/30/2020] [Indexed: 11/29/2022]
Abstract
Despite progressive improvement in medical therapy and standard care, the exercise capacity of heart transplant recipients is reduced compared with age-matched healthy individuals. Exercise-based rehabilitation programs have been shown to improve the exercise capacity of transplant patients through a multifactorial effect. In this context, high-intensity interval exercise is a growing field of research, with current evidence suggesting a major benefit in heart transplant recipients compared with a conventional training protocol. Therefore, this study aimed to provide an overview of the mechanisms involved in the reduced exercise capacity of heart transplant patients and a review of current rehabilitation strategies with a special focus on the mechanisms and clinical effects of high-intensity interval training exercise.
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Affiliation(s)
- Daniele Masarone
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Enrico Melillo
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Andrea Petraio
- Department of Cardiovascular Surgery and Transplants, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Fabio Valente
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Rita Gravino
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Marina Verrengia
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
| | - Giuseppe Pacileo
- Heart Failure and Rehabilitative Cardiology Unit, AO dei Colli, Monaldi Hospital, Naples, Italy
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11
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Venado A, Kolaitis NA, Huang CY, Gao Y, Glidden DV, Soong A, Sutter N, Katz PP, Greenland JR, Calabrese DR, Hays SR, Golden JA, Shah RJ, Leard LE, Kukreja J, Deuse T, Wolters PJ, Covinsky K, Blanc PD, Singer JP. Frailty after lung transplantation is associated with impaired health-related quality of life and mortality. Thorax 2020; 75:669-678. [PMID: 32376733 DOI: 10.1136/thoraxjnl-2019-213988] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/20/2019] [Revised: 04/01/2020] [Accepted: 04/15/2020] [Indexed: 12/13/2022]
Abstract
BACKGROUND Lung transplantation and related medications are associated with pathobiological changes that can induce frailty, a state of decreased physiological reserve. Causes of persistent or emergent frailty after lung transplantation, and whether such transplant-related frailty is associated with key outcomes, are unknown. METHODS Frailty and health-related quality of life (HRQL) were prospectively measured repeatedly for up to 3 years after lung transplantation. Frailty, quantified by the Short Physical Performance Battery (SPPB), was tested as a time-dependent binary and continuous predictor. The association of transplant-related frailty with HRQL and mortality was evaluated using mixed effects and Cox regression models, respectively, adjusting for age, sex, ethnicity, diagnosis, and for body mass index and lung function as time-dependent covariates. We tested the association between measures of body composition, malnutrition, renal dysfunction and immunosuppressants on the development of frailty using mixed effects models with time-dependent predictors and lagged frailty outcomes. RESULTS Among 259 adults (56% male; mean age 55.9±12.3 years), transplant-related frailty was associated with lower HRQL. Frailty was also associated with a 2.5-fold higher mortality risk (HR 2.51; 95% CI 1.21 to 5.23). Further, each 1-point worsening in SPPB was associated, on average, with a 13% higher mortality risk (HR 1.13; 95% CI 1.04 to 1.23). Secondarily, we found that sarcopenia, underweight and obesity, malnutrition, and renal dysfunction were associated with the development of frailty after transplant. CONCLUSIONS Transplant-related frailty is associated with lower HRQL and higher mortality in lung recipients. Abnormal body composition, malnutrition and renal dysfunction may contribute to the development of frailty after transplant. Confirming the role of these potential contributors and developing interventions to mitigate frailty may improve lung transplant success.
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Affiliation(s)
- Aida Venado
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Nicholas A Kolaitis
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Chiung-Yu Huang
- Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA
| | - Ying Gao
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - David V Glidden
- Epidemiology and Biostatistics, University of California San Francisco, San Francisco, California, USA
| | - Allison Soong
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Nicole Sutter
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Patricia P Katz
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - John R Greenland
- Medicine, University of California San Francisco, San Francisco, California, USA.,Medicine, VA Medical Center, San Francisco, California, USA
| | - Daniel R Calabrese
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Steven R Hays
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Jeffrey A Golden
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Rupal J Shah
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Lorriana E Leard
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Jasleen Kukreja
- Surgery, University of California San Francisco, San Francisco, California, USA
| | - Tobias Deuse
- Surgery, University of California San Francisco, San Francisco, California, USA
| | - Paul J Wolters
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Kenneth Covinsky
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Paul D Blanc
- Medicine, University of California San Francisco, San Francisco, California, USA
| | - Jonathan P Singer
- Medicine, University of California San Francisco, San Francisco, California, USA
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12
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Impaired Exercise Tolerance Early After Heart Transplantation Is Associated With Development of Cardiac Allograft Vasculopathy. Transplantation 2020; 104:2196-2203. [DOI: 10.1097/tp.0000000000003110] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
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13
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Exercise for Solid Organ Transplant Candidates and Recipients: A Joint Position Statement of the Canadian Society of Transplantation and CAN-RESTORE. Transplantation 2019; 103:e220-e238. [DOI: 10.1097/tp.0000000000002806] [Citation(s) in RCA: 29] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
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14
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15
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Fernandes LCBC, de Oliveira IM, Fernandes PFCBC, de Souza Neto JD, Farias MDSQ, de Freitas NA, Magalhães NC, Bacal F. Impact of Heart Transplantation on the Recovery of Peripheral and Respiratory Muscle Mass and Strength in Patients With Chronic Heart Failure. Transplant Direct 2018; 4:e395. [PMID: 30534588 PMCID: PMC6233658 DOI: 10.1097/txd.0000000000000837] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/15/2018] [Accepted: 08/28/2018] [Indexed: 01/05/2023] Open
Abstract
BACKGROUND To assess the impact of heart transplantation (HT) on the recovery of peripheral and respiratory muscle mass and strength in patients with congestive heart failure. METHODS The study included 23 patients with an indication for HT (patients in the waiting list [WL] group). These patients were monitored for 1.5 to 3 years after HT; 8 died before 6 months of follow-up, 15 patients completed the early follow-up period of 6 months after HT (FU6m group), 4 died between 6 months and 3 years after HT, and 11 patients completed the late follow-up period 1.5 to 3 years after HT (FU1.5-3y group). Twenty-three healthy subjects were included in the control group. The study variables included inspiratory muscle strength, expressed as the maximum inspiratory pressure (MIP); expiratory muscle strength, expressed as the maximum expiratory pressure (MEP); peripheral muscle strength, expressed as bilateral handgrip strength (bHGS); and the cross-sectional area of the bilateral psoas major muscle (CSAbPm). RESULTS The results showed a reduction in the CSAbPm (1238.9 ± 312.3 mm2), a reduction in the bHGS (27.0 ± 5.7 kg/f), a reduction in the MIP (60.2 ± 29.8 cmH2O), and a reduction in the MEP (75.2 ± 33.4 cmH2O) in patients in the WL group compared with the healthy controls. In the time series comparison, for patients in the WL, FU6m, and FU1.5-3y groups, increases were found in the CSAbPm (1305.4 vs 1458.1 vs 1431.3 mm2, respectively), bHGS (27.3 vs 30.2 vs 34.7 kg/f, respectively), MIP (59.5 vs 85.5 vs 90.9 cmH2O, respectively), and MEP (79.5 vs 93.2 vs 101.8 cmH2O, respectively) (P < 0.00). CONCLUSIONS Sarcopenia was observed in patients in the WL group. Patients recovered peripheral and respiratory muscle mass and strength at 3 years after HT.
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Affiliation(s)
- Lenise C B C Fernandes
- Heart Institute University of São Paulo School of Medicine and Heart and Lung Messejana's Hospital, Fortaleza, CE, Brazil
| | | | | | | | | | | | | | - Fernando Bacal
- Heart Institute University of São Paulo School of Medicine and Heart and Lung Messejana's Hospital, Fortaleza, CE, Brazil
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16
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Tucker WJ, Beaudry RI, Samuel TJ, Nelson MD, Halle M, Baggish AL, Haykowsky MJ. Performance Limitations in Heart Transplant Recipients. Exerc Sport Sci Rev 2018; 46:144-151. [DOI: 10.1249/jes.0000000000000149] [Citation(s) in RCA: 32] [Impact Index Per Article: 4.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/06/2023]
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17
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Peled Y, Varnado S, Lowes BD, Zolty R, Lyden ER, Moulton MJ, Um JY, Raichlin E. Sinus tachycardia is associated with impaired exercise tolerance following heart transplantation. Clin Transplant 2017; 31. [DOI: 10.1111/ctr.12946] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/23/2017] [Indexed: 12/14/2022]
Affiliation(s)
- Yael Peled
- Heart Center; Sheba Medical Center; Ramat Gan and Sackler School of Medicine; Tel Aviv University; Tel Aviv Israel
| | - Sara Varnado
- Division of Cardiology; University of Nebraska Medical Center; Omaha NE USA
| | - Brian D. Lowes
- Division of Cardiology; University of Nebraska Medical Center; Omaha NE USA
| | - Ronald Zolty
- Division of Cardiology; University of Nebraska Medical Center; Omaha NE USA
| | - Elizabeth R. Lyden
- Department of Biostatistics; College of Public Health; University of Nebraska Medical Center; Omaha NE USA
| | - Michael J. Moulton
- Department of Cardiothoracic Surgery; University of Nebraska Medical Center; Omaha NE USA
| | - John Y. Um
- Department of Cardiothoracic Surgery; University of Nebraska Medical Center; Omaha NE USA
| | - Eugenia Raichlin
- Division of Cardiology; University of Nebraska Medical Center; Omaha NE USA
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18
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Saitoh M, dos Santos MR, Anker M, Anker SD, von Haehling S, Springer J. Neuromuscular electrical stimulation for muscle wasting in heart failure patients. Int J Cardiol 2016; 225:200-205. [DOI: 10.1016/j.ijcard.2016.09.127] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/31/2016] [Accepted: 09/30/2016] [Indexed: 12/12/2022]
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Ericsson A, Bremell T, Cider Å, Mannerkorpi K. Effects of exercise on fatigue and physical capacity in men with chronic widespread pain - a pilot study. BMC Sports Sci Med Rehabil 2016; 8:29. [PMID: 27602228 PMCID: PMC5011845 DOI: 10.1186/s13102-016-0054-9] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/25/2015] [Accepted: 08/23/2016] [Indexed: 12/19/2022]
Abstract
Background There is very limited knowledge about the effects of exercise on men with Chronic Widespread Pain (CWP), especially regarding fatigue. We wanted to investigate the effects of resistance exercise compared with pool exercise on multidimensional fatigue, psychological distress and physical capacity in men with CWP. Methods Thirty-four men with CWP, with a mean age of 49 (SD 8, range 26–59) years, were randomised to 12 weeks of standardised pool exercise (PE) or resistance exercise (RE). The primary outcome was the Multidimensional Fatigue Inventory (MFI-20). Depression, anxiety, isometric force, pain and health-related quality of life were also assessed. Results No significant differences were found for changes in MFI-20 between the exercise groups. The RE group improved the isometric forces of right shoulder abduction (RE: ∆2.2 SD 1.5 N, PE: ∆0.6 SD 1.2 N, p = 0.009), right knee flexion (RE: ∆50, SD 50 N, PE: ∆-17, SD 71 N, p = 0.003) and left knee flexion (RE: ∆33 SD 39, PE: ∆-9 SD 52 N, p = 0.017) compared with the PE group. The drop-out rate was 29 % in the RE group and 18 % in the PE group. Conclusions Both a resistance exercise programme and a pool exercise programme improved different dimensions of fatigue in men with CWP. There were no differences in the change in fatigue over time between the exercise groups. Resistance exercise improved isometric strength compared with pool exercise. Because different types of exercise appear to improve different aspects of health, the goals could guide the choice of treatment. Further exercise studies with larger groups are needed to gain more knowledge about the effect of exercise on fatigue in men with CWP. Trial registration ClinicalTrials.gov Identifier NCT01278641. Registration date April 2008.
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Affiliation(s)
- Anna Ericsson
- Institute of Neuroscience and Physiology, Department of Health and Rehabilitation/Physiotherapy, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Tomas Bremell
- Institute of Medicine, Department of Rheumatology and Inflammation Research, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Åsa Cider
- Institute of Neuroscience and Physiology, Department of Health and Rehabilitation/Physiotherapy, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Kaisa Mannerkorpi
- Institute of Neuroscience and Physiology, Department of Health and Rehabilitation/Physiotherapy, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
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20
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Abstract
Heart failure (HF) patients suffer from exercise intolerance that diminishes their ability to perform normal activities of daily living and hence compromises their quality of life. This is due largely to detrimental changes in skeletal muscle mass, structure, metabolism, and function. This includes an impairment of muscle contractile performance, i.e., a decline in the maximal force, speed, and power of muscle shortening. Although numerous mechanisms underlie this reduction in contractility, one contributing factor may be a decrease in nitric oxide (NO) bioavailability. Consistent with this, recent data demonstrate that acute ingestion of NO3 (-)-rich beetroot juice, a source of NO via the NO synthase-independent enterosalivary pathway, markedly increases maximal muscle speed and power in HF patients. This review discusses the role of muscle contractile dysfunction in the exercise intolerance characteristic of HF, and the evidence that dietary NO3 (-) supplementation may represent a novel and simple therapy for this currently underappreciated problem.
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Affiliation(s)
- Andrew R Coggan
- Cardiovascular Imaging Laboratory, Mallinckrodt Institute of Radiology, Department of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd. - Campus Box 8225, St. Louis, MO, 63110, USA.
| | - Linda R Peterson
- Cardiovascular Imaging Laboratory, Mallinckrodt Institute of Radiology, Department of Radiology, Washington University School of Medicine, 510 S. Kingshighway Blvd. - Campus Box 8225, St. Louis, MO, 63110, USA
- Cardiovascular Division, Department of Internal Medicine, Washington University School of Medicine, 660 S. Euclid Ave. - Campus Box 8086, St. Louis, MO, 63110, USA
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21
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Brosig C, Pai A, Fairey E, Krempien J, McBride M, Lefkowitz DS. Child and family adjustment following pediatric solid organ transplantation: factors to consider during the early years post-transplant. Pediatr Transplant 2014; 18:559-67. [PMID: 24923434 DOI: 10.1111/petr.12286] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 04/14/2014] [Indexed: 11/29/2022]
Abstract
Adjusting to life after transplant can be challenging to pediatric solid organ transplant recipients and their families. In this review, we discuss a number of important factors to consider during the first 2-3 yr after transplant (defined as the "early years"), including transitioning from hospital to home, returning to physical activity, feeding and nutrition, school reentry, potential cognitive effects of transplant, family functioning, and QOL. We highlight steps that providers can take to optimize child and family adjustment during this period.
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Affiliation(s)
- Cheryl Brosig
- Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI, USA; Herma Heart Center, Children's Hospital of Wisconsin, Milwaukee, WI, USA
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22
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Comparisons of Dyspnea, Fatigue, and Exercise Intolerance Between Individuals with Heart Failure with High Versus Low Knee Extensor Muscle Strength. Cardiopulm Phys Ther J 2014. [DOI: 10.1097/01823246-201403000-00004] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
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Abstract
Organ transplantation is one of the medical miracles or the 20th century. It has the capacity to substantially improve exercise performance and quality of life in patients who are severely limited with chronic organ failure. We focus on the most commonly performed solid-organ transplants and describe peak exercise performance following recovery from transplantation. Across all of the common transplants, evaluated significant reduction in VO2peak is seen (typically renal and liver 65%-80% with heart and/or lung 50%-60% of predicted). Those with the lowest VO2peak pretransplant have the lowest VO2peak posttransplant. Overall very few patients have a VO2peak in the normal range. Investigation of the cause of the reduction of VO2peak has identified many factors pre- and posttransplant that may contribute. These include organ-specific factors in the otherwise well-functioning allograft (e.g., chronotropic incompetence in heart transplantation) as well as allograft dysfunction itself (e.g., chronic lung allograft dysfunction). However, looking across all transplants, a pattern emerges. A low muscle mass with qualitative change in large exercising skeletal muscle groups is seen pretransplant. Many factor posttransplant aggravate these changes or prevent them recovering, especially calcineurin antagonist drugs which are key immunosuppressing agents. This results in the reduction of VO2peak despite restoration of near normal function of the initially failing organ system. As such organ transplantation has provided an experiment of nature that has focused our attention on an important confounder of chronic organ failure-skeletal muscle dysfunction.
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Affiliation(s)
- Trevor J Williams
- Department of Allergy, Immunology, and Respiratory Medicine Alfred Hospital and Monash University, Melbourne, Australia.
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Metabolism and the heart: An overview of muscle, fat, and bone metabolism in heart failure. Int J Cardiol 2013; 162:77-85. [DOI: 10.1016/j.ijcard.2011.09.079] [Citation(s) in RCA: 54] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/08/2011] [Revised: 09/14/2011] [Accepted: 09/17/2011] [Indexed: 12/20/2022]
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N'Guessan BB, Sanchez H, Zoll J, Ribera F, Dufour S, Lampert E, Kindo M, Geny B, Ventura-Clapier R, Mettauer B. Oxidative capacities of cardiac and skeletal muscles of heart transplant recipients: mitochondrial effects of cyclosporin-A and its vehicle Cremophor-EL. Fundam Clin Pharmacol 2012; 28:151-60. [DOI: 10.1111/fcp.12002] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/02/2011] [Revised: 08/31/2012] [Accepted: 09/11/2012] [Indexed: 01/24/2023]
Affiliation(s)
- Benoit Banga N'Guessan
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
- Laboratoire de Physiologie, Pharmacologie et Phytothérapie; UFR SN, Université d'Abobo-Adjamé; 02 BP 801 Abidjan 02 Abidjan Côte d'Ivoire
- Department of Pharmacology and Toxicology; School of Pharmacy; College of Health Sciences; University of Ghana; PO Box KB 52 Korle Bu Accra Ghana
| | - Hervé Sanchez
- Département des facteurs humains; CRSSA; BP 87, 38702 La-Tronche Cedex France
| | - Joffrey Zoll
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Florence Ribera
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Stéphane Dufour
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Eliane Lampert
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Michel Kindo
- Service de chirurgie cardiaque Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Bernard Geny
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
| | - Renée Ventura-Clapier
- Signalisation et Physiopathologie Cardiaque U-769 INSERM; Université Paris-Sud; Châtenay-Malabry F-92296 France
| | - Bertrand Mettauer
- Service de Physiologie Clinique et des Explorations Fonctionnelles; équipe d'accueil EA3072 Hôpitaux Universitaires de Strasbourg; 67091 Strasbourg Cedex France
- Service de Cardiologie; Hôpitaux Civils de Colmar; 68024 Colmar Cedex France
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Fanzani A, Conraads VM, Penna F, Martinet W. Molecular and cellular mechanisms of skeletal muscle atrophy: an update. J Cachexia Sarcopenia Muscle 2012; 3:163-79. [PMID: 22673968 PMCID: PMC3424188 DOI: 10.1007/s13539-012-0074-6] [Citation(s) in RCA: 252] [Impact Index Per Article: 19.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/09/2012] [Accepted: 05/13/2012] [Indexed: 02/06/2023] Open
Abstract
Skeletal muscle atrophy is defined as a decrease in muscle mass and it occurs when protein degradation exceeds protein synthesis. Potential triggers of muscle wasting are long-term immobilization, malnutrition, severe burns, aging as well as various serious and often chronic diseases, such as chronic heart failure, obstructive lung disease, renal failure, AIDS, sepsis, immune disorders, cancer, and dystrophies. Interestingly, a cooperation between several pathophysiological factors, including inappropriately adapted anabolic (e.g., growth hormone, insulin-like growth factor 1) and catabolic proteins (e.g., tumor necrosis factor alpha, myostatin), may tip the balance towards muscle-specific protein degradation through activation of the proteasomal and autophagic systems or the apoptotic pathway. Based on the current literature, we present an overview of the molecular and cellular mechanisms that contribute to muscle wasting. We also focus on the multifacetted therapeutic approach that is currently employed to prevent the development of muscle wasting and to counteract its progression. This approach includes adequate nutritional support, implementation of exercise training, and possible pharmacological compounds.
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Affiliation(s)
- Alessandro Fanzani
- Department of Biomedical Sciences and Biotechnologies and Interuniversitary Institute of Myology (IIM), University of Brescia, viale Europa 11, 25123, Brescia, Italy,
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Estenne M, Fessler HE, DeCamp MM. Lung transplantation and lung volume reduction surgery. Compr Physiol 2011; 1:1437-71. [PMID: 23733648 DOI: 10.1002/cphy.c100044] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/06/2022]
Abstract
Since the publication of the last edition of the Handbook of Physiology, lung transplantation has become widely available, via specialized centers, for a variety of end-stage lung diseases. Lung volume reduction surgery, a procedure for emphysema first conceptualized in the 1950s, electrified the pulmonary medicine community when it was rediscovered in the 1990s. In parallel with their technical and clinical refinement, extensive investigation has explored the unique physiology of these procedures. In the case of lung transplantation, relevant issues include the discrepant mechanical function of the donor lungs and recipient thorax, the effects of surgical denervation, acute and chronic rejection, respiratory, chest wall, and limb muscle function, and response to exercise. For lung volume reduction surgery, there have been new insights into the counterintuitive observation that lung function in severe emphysema can be improved by resecting the most diseased portions of the lungs. For both procedures, insights from physiology have fed back to clinicians to refine patient selection and to scientists to design clinical trials. This section will first provide an overview of the clinical aspects of these procedures, including patient selection, surgical techniques, complications, and outcomes. It then reviews the extensive data on lung and muscle function following transplantation and its complications. Finally, it reviews the insights from the last 15 years on the mechanisms whereby removal of lung from an emphysema patient can improve the function of the lung left behind.
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Affiliation(s)
- Marc Estenne
- Chest Service and Thoracic Transplantation Unit, Erasme University Hospital, Brussels, Belgium
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Cardiac allograft hypertrophy is associated with impaired exercise tolerance after heart transplantation. J Heart Lung Transplant 2011; 30:1153-60. [PMID: 21621424 DOI: 10.1016/j.healun.2011.04.012] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/04/2011] [Revised: 03/23/2011] [Accepted: 04/10/2011] [Indexed: 01/19/2023] Open
Abstract
BACKGROUND Exercise performance, an important aspect of quality of life, remains limited after heart transplantation (HTx). This study examines the effect of cardiac allograft remodeling on functional capacity after HTx. METHODS The total cohort of 117 HTx recipients, based on echocardiographic determination of left ventricle mass and relative wall thickness at 1 year after HTx, was divided into 3 groups: (1) NG, normal geometry; (2) CR, concentric remodeling; and (3) CH, concentric hypertrophy. Cardiopulmonary exercise testing was performed 5.03 ± 3.08 years after HTx in all patients. Patients with acute rejection or significant graft vasculopathy were excluded. RESULTS At 1 year post-HTx, 30% of patients had CH, 55% had CR and 15% had NG. Exercise tolerance, measured by maximum achieved metabolic equivalents (4.62 ± 1.44 vs 5.52 ± 0.96 kcal/kg/h), normalized peak Vo(2) (52 ± 14% vs 63 ± 12%) and Ve/Vco(2) (41 ± 17 vs 34 ± 6), was impaired in the CH group compared with the NG group. A peak Vo(2) ≤14 ml/kg/min was found in 6%, 22% and 48% of patients in the NG, CR and CH groups, respectively (p = 0.01). The CH pattern was associated with a 7.4-fold increase in relative risk for a peak Vo(2) ≤14 ml/kg/min compared with NG patients (95% confidence interval 1.1 to 51.9, p = 0.001). After multivariate analysis, a 1-year CH pattern was independently associated with a reduced normalized peak Vo(2) (p = 0.018) and an elevated Ve/Vco(2) (p = 0.035). CONCLUSIONS The presence of CH at 1 year after HTx is independently associated with decreased normalized peak Vo(2) and increased ventilatory response in stable heart transplant recipients. The identification of CH, a potentially reversible mechanism of impairment in exercise capacity after HTx, may have major clinical implications.
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Lizak M, Zakliczyński M, Jarosz A, Zembala M. The Influence of Chronic Heart Failure on Pulmonary Function Tests in Patients Undergoing Orthotopic Heart Transplantation. Transplant Proc 2009; 41:3194-7. [DOI: 10.1016/j.transproceed.2009.07.072] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/20/2022]
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Miller MS, Vanburen P, Lewinter MM, Lecker SH, Selby DE, Palmer BM, Maughan DW, Ades PA, Toth MJ. Mechanisms underlying skeletal muscle weakness in human heart failure: alterations in single fiber myosin protein content and function. Circ Heart Fail 2009; 2:700-6. [PMID: 19919996 DOI: 10.1161/circheartfailure.109.876433] [Citation(s) in RCA: 69] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/25/2022]
Abstract
BACKGROUND Patients with chronic heart failure (HF) frequently experience skeletal muscle weakness that limits physical function. The mechanisms underlying muscle weakness, however, have not been clearly defined. METHODS AND RESULTS This study examined the hypothesis that HF promotes a loss of myosin protein from single skeletal muscle fibers, which in turn reduces contractile performance. Ten patients with chronic HF and 10 controls were studied. Muscle atrophy was not evident in patients, and groups displayed similar physical activity levels, suggesting that observed differences reflect the effects of HF and not muscle atrophy or disuse. In single muscle fibers, patients with HF showed reduced myosin heavy chain protein content (P<0.05) that manifested as a reduction in functional myosin-actin cross-bridges (P<0.05). No evidence was found for a generalized loss of myofilament protein, suggesting a selective loss of myosin. Accordingly, single muscle fiber maximal Ca(2+)-activated tension was reduced in myosin heavy chain I fibers in patients (P<0.05). However, tension was maintained in myosin heavy chain IIA fibers in patients because a greater proportion of available myosin heads were bound to actin during Ca(2+) activation (P<0.01). CONCLUSIONS Collectively, our results show that HF alters the quantity and functionality of the myosin molecule in skeletal muscle, leading to reduced tension in myosin heavy chain I fibers. Loss of single fiber myosin protein content represents a potential molecular mechanism underlying muscle weakness and exercise limitation in patients with HF.
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Affiliation(s)
- Mark S Miller
- Departments of Molecular Physiology and Biophysics and Medicine, University of Vermont, College of Medicine, Burlington, Vt, USA
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Standards for the use of cardiopulmonary exercise testing for the functional evaluation of cardiac patients: a report from the Exercise Physiology Section of the European Association for Cardiovascular Prevention and Rehabilitation. ACTA ACUST UNITED AC 2009; 16:249-67. [PMID: 19440156 DOI: 10.1097/hjr.0b013e32832914c8] [Citation(s) in RCA: 261] [Impact Index Per Article: 16.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
Cardiopulmonary exercise testing (CPET) is a methodology that has profoundly affected the approach to patients' functional evaluation, linking performance and physiological parameters to the underlying metabolic substratum and providing highly reproducible exercise capacity descriptors. This study provides professionals with an up-to-date review of the rationale sustaining the use of CPET for functional evaluation of cardiac patients in both the clinical and research settings, describing parameters obtainable either from ramp incremental or step constant-power CPET and illustrating the wealth of information obtainable through an experienced use of this powerful tool. The choice of parameters to be measured will depend on the specific goals of functional evaluation in the individual patient, namely, exercise tolerance assessment, training prescription, treatment efficacy evaluation, and/or investigation of exercise-induced adaptations of the oxygen transport/utilization system. The full potentialities of CPET in the clinical and research setting still remain largely underused and strong efforts are recommended to promote a more widespread use of CPET in the functional evaluation of cardiac patients.
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Richard R, Zoll J, Mettauer B, Piquard F, Geny B. Counterpoint: Cardiac denervation does not play a major role in exercise limitation after heart transplantation. J Appl Physiol (1985) 2008; 104:560-2, discussion 562-4. [DOI: 10.1152/japplphysiol.00694.2007a] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
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Tomczak CR, Warburton DE, Riess KJ, Jendzjowsky NG, Esch BT, Liang Y, Haennel RG, Haykowsky MJ. Pulmonary Oxygen Uptake and Heart Rate Kinetics During the Six-Minute Walk Test in Transplant Recipients. Transplantation 2008; 85:29-35. [DOI: 10.1097/01.tp.0000296056.00863.f0] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
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Braith RW, Beck DT. Resistance exercise: training adaptations and developing a safe exercise prescription. Heart Fail Rev 2007; 13:69-79. [DOI: 10.1007/s10741-007-9055-9] [Citation(s) in RCA: 66] [Impact Index Per Article: 3.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
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Jendzjowsky NG, Tomczak CR, Lawrance R, Taylor DA, Tymchak WJ, Riess KJ, Warburton DER, Haykowsky MJ. Impaired pulmonary oxygen uptake kinetics and reduced peak aerobic power during small muscle mass exercise in heart transplant recipients. J Appl Physiol (1985) 2007; 103:1722-7. [PMID: 17717113 DOI: 10.1152/japplphysiol.00725.2007] [Citation(s) in RCA: 23] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
We examined peak and reserve cardiovascular function and skeletal muscle oxygenation during unilateral knee extension (ULKE) exercise in five heart transplant recipients (HTR, mean +/- SE; age: 53 +/- 3 years; years posttransplant: 6 +/- 4) and five age- and body mass-matched healthy controls (CON). Pulmonary oxygen uptake (Vo(2)(p)), heart rate (HR), stroke volume (SV), cardiac output (Q), and skeletal muscle deoxygenation (HHb) kinetics were assessed during moderate-intensity ULKE exercise. Peak exercise and reserve Vo(2)(p), Q, and systemic arterial-venous oxygen difference (a-vO(2diff)) were 23-52% lower (P < 0.05) in HTR. The reduced Q and a-vO(2diff) reserves were associated with lower HR and HHb reserves, respectively. The phase II Vo(2)(p) time delay was greater (HTR: 38 +/- 2 vs. CON: 25 +/- 1 s, P < 0.05), while time constants for phase II Vo(2)(p) (HTR: 54 +/- 8 vs. CON: 31 +/- 3 s), Q (HTR: 66 +/- 8 vs. CON: 28 +/- 4 s), and HHb (HTR: 27 +/- 5 vs. CON: 13 +/- 3 s) were significantly slower in HTR. The HR half-time was slower in HTR (113 +/- 21 s) vs. CON (21 +/- 2 s, P < 0.05); however, no significant difference was found between groups for SV kinetics (HTR: 39 +/- 8 s vs. CON 31 +/- 6 s). The lower peak Vo(2)(p) and prolonged Vo(2)(p) kinetics in HTR were secondary to impairments in both cardiovascular and skeletal muscle function that result in reduced oxygen delivery and utilization by the active muscles.
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Affiliation(s)
- Nicholas G Jendzjowsky
- Cardiovascular Therapeutic Exercise Laboratory, 1-30 Corbett Hall, Faculty of Rehabilitation Medicine, Univ. of Alberta, Edmonton AB, Canada, T6G 2G4
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Warburton DER, Taylor A, Bredin SSD, Esch BTA, Scott JM, Haykowsky MJ. Central haemodynamics and peripheral muscle function during exercise in patients with chronic heart failure. Appl Physiol Nutr Metab 2007; 32:318-31. [PMID: 17486176 DOI: 10.1139/h06-085] [Citation(s) in RCA: 26] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
In this narrative review of the current literature, we examine the central and peripheral mechanisms responsible for the exercise intolerance of chronic heart failure and highlight briefly the benefits of exercise training in the treatment of this debilitating disorder. Specifically, we identify the common finding of reduced cardiac output reserve during exercise conditions leading to decreased exercise tolerance. We also reveal that the stroke volume response to exercise varies depending on the individual patient, the presence of mitral regurgitation, and the aetiology of heart failure. Chronic heart failure patients with left ventricular systolic dysfunction appear able to use the Frank-Starling mechanism to compensate (in part) for their decreased contractile reserve. Patients with left ventricular diastolic dysfunction have normal contractile function; however, they are unable to make use of the Frank-Starling mechanism during exercise conditions. We also reveal that pericardial constraint may limit diastolic filling and exercise capacity in patients with chronic heart failure. It appears that interventions that reduce pericardial constraint and mitral regurgitation enhance diastolic filling and increase exercise tolerance. A series of peripheral muscle changes also occur, including changes in muscle mass, cellular structure, energy metabolism, and blood flow. Each of these factors is associated with decreased exercise capacity and the symptoms of chronic heart failure. Exercise training has been shown to improve both central haemodynamics and peripheral muscle function leading to improvements in exercise capacity, functional status, and overall quality of life in patients with chronic heart failure.
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Affiliation(s)
- Darren E R Warburton
- Cardiovascular Physiology and Rehabilitation Laboratory, 6108 Thunderbird Blvd., University of British Columbia, Vancouver, BC V6T 1Z3, Canada.
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Tomczak CR, Jendzjowsky NG, Riess KJ, Tymchak W, Kim D, Haennel R, Haykowsky MJ. Relation of etiology of heart failure (ischemic versus nonischemic) before transplantation to delayed pulmonary oxygen uptake kinetics after heart transplantation. Am J Cardiol 2007; 99:1745-9. [PMID: 17560887 DOI: 10.1016/j.amjcard.2007.01.058] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/22/2006] [Revised: 01/17/2007] [Accepted: 01/17/2007] [Indexed: 01/05/2023]
Abstract
The effect that pretransplantation heart failure cause has on pulmonary oxygen uptake (VO2p) kinetics and peak aerobic power (VO2peak) in heart transplant recipients (HTRs) has not been studied. We examined VO2p kinetics and VO2peak in HTRs with previous ischemic heart failure (I-HTRs; n=16, mean age 64+/-6 years) or nonischemic heart failure (NI-HTRs; n=13, mean age 50+/-12 years). HTRs performed an incremental exercise (VO2peak) test and a constant work rate submaximal exercise (VO2p kinetics) test. A monoexponential model was used to determine the phase II VO2p time constant (tau). Phase II VO2p tau was slower in I-HTRs (49+/-10 seconds) than in NI-HTRs (34+/-10 seconds) (p<0.001). No significant difference was found between I-HTRs and NI-HTRs for VO2peak (19.0+/-6.4 vs 23.0+/-8.2 ml.kg-1.min-1, respectively), change in heart rate from rest to steady-state exercise (11+/-8 vs 9+/-9 beats.min-1, respectively), or peak exercise heart rate (140+/-22 vs 144+/-22 beats.min-1, respectively). In conclusion, the prolonged phase II VO2p tau in I-HTRs compared with NI-HTRs suggests that the magnitude of alteration in VO2p kinetics after heart transplantation may be dependent on previous heart failure cause.
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Affiliation(s)
- Corey R Tomczak
- Cardiovascular Therapeutic Exercise Laboratory, Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, Alberta, Canada
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Bhatnagar D, Hussain F. Omega-3 fatty acid ethyl esters (Omacor®) for the treatment of hypertriglyceridemia. ACTA ACUST UNITED AC 2007. [DOI: 10.2217/17460875.2.3.263] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/21/2022]
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Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, Lecarpentier Y. Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 2007; 292:H1009-17. [PMID: 17040975 DOI: 10.1152/ajpheart.00438.2006] [Citation(s) in RCA: 90] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/22/2022]
Abstract
Intrinsic muscle abnormalities affecting skeletal muscle are often reported during chronic heart failure (CHF). Because myosin is the molecular motor of force generation, we sought to determine whether its dysfunction contributes to skeletal muscle weakness in CHF and, if so, to identify the underlying causative factors. Severe CHF was induced in rats by aortic stenosis. In diaphragm and soleus muscles, we investigated in vitro mechanical performance, myosin-based actin filament motility, myosin heavy (MHC) and light (MLC) chain isoform compositions, MLC integrity, caspase-3 activation, and oxidative damage. Diaphragm and soleus muscles from CHF exhibited depressed mechanical performance. Myosin sliding velocities were 16 and 20% slower in CHF than in sham in diaphragm (1.9 ± 0.1 vs. 1.6 ± 0.1 μm/s) and soleus (0.6 ± 0.1 vs. 0.5 ± 0.1 μm/s), respectively (each P < 0.05). The ratio of slow-to-fast myosin isoform did not differ between sham and CHF. Immunoblots with anti-MLC antibodies did not detect the presence of protein fragments, and no activation of caspase-3 was evidenced. Immunolabeling revealed oxidative damage in CHF muscles, and MHC was the main oxidized protein. Lipid peroxidation and expression of oxidized MHC were significantly higher in CHF than in shams. In vitro myosin exposure to increasing ONOO−concentrations was associated with an increasing amount of oxidized MHC and a reduced myosin velocity. These data provide experimental evidence that intrinsic myosin dysfunction occurs in CHF and may be related to oxidative damage to myosin.
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Affiliation(s)
- Catherine Coirault
- INSERM U689, Centre de Recherche Cardiovasculaire INSERM, Hôpital Lariboisière, 41 Bd de la Chapelle, 75475 Paris Cedex 10, France.
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Pierce GL, Magyari PM, Aranda JM, Edwards DG, Hamlin SA, Hill JA, Braith RW. Effect of heart transplantation on skeletal muscle metabolic enzyme reserve and fiber type in end-stage heart failure patients. Clin Transplant 2007; 21:94-100. [PMID: 17302597 DOI: 10.1111/j.1399-0012.2006.00589.x] [Citation(s) in RCA: 11] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/15/2023]
Abstract
BACKGROUND Skeletal muscle myopathy is a hallmark of chronic heart failure (HF). Phenotypic changes involve shift in myosin heavy chain (MHC) fiber type from oxidative, MHC type I, towards more glycolytic MHC IIx fibers, reductions in oxidative enzyme activity, and increase in glycolytic enzyme activity. However, it is unknown if muscle myopathy is reversed following heart transplantation. The purpose of this study was to determine the effect of heart transplantation on skeletal muscle metabolic enzyme reserve and MHC fiber type in end-stage HF patients. METHODS Thirteen HF subjects were prospectively studied before and two months after heart transplantation and a subgroup (n = 6) at eight months after transplantation. Skeletal muscle biopsy of the vastus lateralis was performed and relative MHC composition was determined using sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Lactate dehydrogenase (LDH), citrate synthase (CS), and 3-hydroxyacyl-CoA-dehydrogenase (HACoA) enzyme activity assays were performed to assess glycolytic, oxidative, and beta-oxidative metabolic enzyme reserves, respectively. RESULTS Lactate dehydrogenase activity (130.5 +/- 13.3 vs. 106.1 +/- 13.2 micromol/g wet wt/min, p < 0.05), CS activity (14.0 +/- 1.2 vs. 9 +/- 0.9 micromol/g wet wt/min, p < 0.05), and HACoA activity (4.5 +/- 0.48 vs. 3.6 +/- 0.3 micromol/g wet wt/min, p < 0.05) decreased two months after heart transplantation. At eight months, LDH activity was restored (139.0 +/- 11 micromol/g wet wt/min), but not CS or HACoA activity compared with before transplantation. There was no significant change in muscle %MHC type I (28.7 +/- 3.5% vs. 25.3 +/- 3.0%, p = NS), %MHC type IIa (33.2 +/- 2.0% vs. 34.6 +/- 1.9%, p = NS), or %MHC type IIx (38.1 +/- 2.8% vs. 40.1 +/- 3.7%, p = NS) fiber type two months after heart transplantation. However, %MHC type I (19.3 +/- 6.6%) was decreased and %MHC type IIx (51.0 +/- 6.5%) was increased at eight months after (p < 0.05) compared with before transplantation. CONCLUSIONS Skeletal muscle glycolytic, oxidative, and beta-oxidative enzymatic reserves are diminished early after heart transplantation, with reduced oxidative capacity persisting late in the first year. The myopathic MHC phenotype present in end-stage HF persists early in the post-operative state and declines further by eight months.
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Affiliation(s)
- Gary L Pierce
- Department of Applied Physiology and Kinesiology, Center for Exercise Science, College of Health and Human Performance, University of Florida, Gainesville, FL, USA.
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Abstract
The study of patient healthcare outcomes after cardiothoracic transplantation has increased substantially over the last 2 decades. Physical function after heart, lung, and heart-lung transplantation has been studied using both subjective and objective measures. The majority of reports in the literature on physical function after cardiothoracic transplantation are descriptive and observational. The purposes of the article are to review and critique the existing literature on cardiothoracic recipients' subjective and objective physical function, including respiratory function for heart-lung and lung transplant recipients. In addition, the literature on sexual function in cardiothoracic recipients is examined, the gaps in the literature are identified, and recommendations are given for future research.
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Affiliation(s)
- Kathleen L Grady
- Center for Heart Failure, and Division of Cardiac Surgery, Bluhm Cardiovascular Institute, Feinberg School of Medicine, 201 E. Huron Street, Chicago, IL 60611, USA.
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Richard R, Verdier JC, Doutreleau S, Piquard F, Gény B, Rieu M. Exercise limitation in trained heart and kidney transplant recipients: central and peripheral limitations. J Heart Lung Transplant 2005; 24:1774-80. [PMID: 16297781 DOI: 10.1016/j.healun.2005.03.017] [Citation(s) in RCA: 17] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/22/2004] [Revised: 03/17/2005] [Accepted: 03/17/2005] [Indexed: 12/25/2022] Open
Abstract
BACKGROUND To evaluate the role of central and peripheral contributions to exercise limitation after transplantation, we compared, during exercise, 2 groups of very well-trained heart transplants recipients (HTRs) and kidney transplant recipients (KTRs) with a group of control subjects (CSs), matched for physical level. METHODS Nineteen male subjects, 7 HTRs, 6 KTRs and 6 CSs, participated in the study. All transplant patients were in sinus rhythm and were matched for immunosuppressive therapy, none of whom had therapy with chronotropic effects. Exercise capacities were evaluated using a symptom-limited treadmill test. Oxygen consumption (VO2) and heart rate (HR) were measured continuously. Heart rate reserve (HRR) was defined as peak HR minus resting HR; resting HR was the stabilized HR measured in the supine position before the treadmill test. RESULTS Functional capacities were evaluated for all HTRs, KTRs and CSs, according to maximal VO2 (41.5 +/- 4.0, 52.0 +/- 8.7 and 50.6 +/- 9.0 ml/kg per min, respectively), maximal treadmill speed (9.9 +/- 1.2, 12.7 +/- 1.9 and 15.5 +/- 1.5 km/h) and HRR (65 +/- 17, 101 +/- 12 and 110 +/- 11 beats per minute [bpm]), which were significantly lower in the HTR group (p < 0.05). Regardless of type of organ transplant, both HTR and KTR patients had a similar VO2/treadmill speed relationship, significantly higher than in the CS group. HRR correlated with maximal VO2 for HTRs (r = 0.72, p < 0.05). CONCLUSIONS Despite regular training, the decreased mechanical efficiency reflected by an increased VO2/treadmill speed relationship suggests a peripheral limitation in both heart and kidney transplant patients. Furthermore, exercise limitations in HTRs likely arose from both central and peripheral factors, in view of their specific HRR reduction. These factors probably contributed to the decreased speed and VO2 observed in the HTR group.
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Affiliation(s)
- Ruddy Richard
- Service de Physiologie et des Explorations Fonctionnelles, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.
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Braith RW, Magyari PM, Pierce GL, Edwards DG, Hill JA, White LJ, Aranda JM. Effect of resistance exercise on skeletal muscle myopathy in heart transplant recipients. Am J Cardiol 2005; 95:1192-8. [PMID: 15877992 DOI: 10.1016/j.amjcard.2005.01.048] [Citation(s) in RCA: 54] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/13/2004] [Revised: 01/10/2005] [Accepted: 01/10/2005] [Indexed: 12/17/2022]
Abstract
The purpose of this study was to determine the efficacy of resistance exercise in reversing skeletal muscle myopathy in heart transplant recipients. Myopathy, engendered by both heart failure and immunosuppression with glucocorticoids, is a post-transplant complication. The sequelae of myopathic disease includes fiber-type shifts and deficits in aerobic metabolic capability. We randomly assigned patients to either 6 months of resistance exercise (training group; n = 8) or a control (control group; n = 7) group. Exercise was initiated at 2 months after transplant. Biopsy of the right vastus lateralis was performed before and after the 6-month intervention. Myosin heavy chain (MHC) composition was assessed using sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Biochemical assays were performed to determine citrate synthase, 3-hydroxyacyl-CoA-dehydrogenase, and lactate dehydrogenase activity. There were no group differences (p >or=0.05) in MHC composition and enzymatic reserve at baseline. Improvements in the training group for citrate cynthase (+40%), 3-hydroxyacyl-CoA-dehydrogenase (+10%), and lactate dehydrogenase activity (+48%) were significantly greater (p <or=0.05) than in the control group (+10%, -15%, and +20%, respectively). Oxidative type 1 MHC isoform concentration increased significantly in the training group (+73%, p <or=0.05) but decreased in the control group (-28%; p <or=0.05). Glycolytic type 2x MHC isoform increased significantly (17%; p <or=0.05) in the control group but decreased (-33%; p <or=0.05) in the training group. This is the first study to demonstrate that resistance training elicits myofibrillar shifts from less oxidative type II fibers to more oxidative fatigue-resistant type I fibers in heart transplant recipients. Resistance exercise initiated early in the post-transplant period is efficacious in changing skeletal muscle phenotype through increases in enzymatic reserve and shifts in fiber morphology.
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Williams AD, Selig S, Hare DL, Hayes A, Krum H, Patterson J, Geerling RH, Toia D, Carey MF. Reduced exercise tolerance in CHF may be related to factors other than impaired skeletal muscle oxidative capacity. J Card Fail 2004; 10:141-8. [PMID: 15101026 DOI: 10.1016/j.cardfail.2003.09.004] [Citation(s) in RCA: 52] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/23/2022]
Abstract
BACKGROUND We sought to determine whether skeletal muscle oxidative capacity, fiber type proportions, and fiber size, capillary density or muscle mass might explain the impaired exercise tolerance in chronic heart failure (CHF). Previous studies are equivocal regarding the maladaptations that occur in the skeletal muscle of patients with CHF and their role in the observed exercise intolerance. Methods and results Total body O(2) uptake (VO(2peak)) was determined in 14 CHF patients and 8 healthy sedentary similar-age controls. Muscle samples were analyzed for mitochondrial adenosine triphosphate (ATP) production rate (MAPR), oxidative and glycolytic enzyme activity, fiber size and type, and capillary density. CHF patients demonstrated a lower VO(2peak) (15.1+/-1.1 versus 28.1+/-2.3 mL.kg(-1).min(-1), P<.001) and capillary to fiber ratio (1.09+/-0.05 versus 1.40+/-0.04; P<.001) when compared with controls. However, there was no difference in capillary density (capillaries per square millimeter) across any of the fiber types. Measurements of MAPR and oxidative enzyme activity suggested no difference in muscle oxidative capacity between the groups. CONCLUSIONS Neither reductions in muscle oxidative capacity nor capillary density appear to be the cause of exercise limitation in this cohort of patients. Therefore, we hypothesize that the low VO(2peak) observed in CHF patients may be the result of fiber atrophy and possibly impaired activation of oxidative phosphorylation.
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Affiliation(s)
- Andrew D Williams
- Centre for Rehabilitation, Exercise and Sport Science, Victoria University of Technology, Melbourne, Australia
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Crevenna R, Mayr W, Keilani M, Pleiner J, Nuhr M, Quittan M, Pacher R, Fialka-Moser V, Wolzt M. Safety of a combined strength and endurance training using neuromuscular electrical stimulation of thighs muscles in patients with heart failure and bipolar sensing cardiac pacemakers. Wien Klin Wochenschr 2003; 115:710-4. [PMID: 14650946 DOI: 10.1007/bf03040887] [Citation(s) in RCA: 17] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/01/2022]
Abstract
Neuromuscular electrical stimulation (NMES) is an effective and non-strenuous therapy to enhance the strength and endurance capacity of the skeletal muscles in patients with severe chronic heart failure. NMES in patients with pacemakers is controversial because potential electromagnetic interference may result in pacemaker malfunction. Therefore, such patients are in general excluded from NMES. The aim of this pilot study was to evaluate the safety of a combined NMES protocol to increase strength and endurance capacity of the skeletal muscles in patients with heart failure and implanted pacemakers. Seven patients with chronic heart failure and implanted cardiac pacemakers with bipolar sensing leads received NMES treatment of thigh muscles, using a combined protocol comprising biphasic, symmetric, rectangular constant current impulses at different frequencies (8-50 Hz), pulse width up to 60 s (8 Hz), 4 s (15 Hz), 4 s (30 Hz), and 6 s (50 Hz), and amplitudes up to +/- 100 mA (all frequencies) applied to both knee extensor and flexor muscles via surface electrodes (8 x 13 cm each). Acute electromagnetic interference during a safety procedure (telemetric monitoring) before therapeutic NMES application was not observed in any of the patients. The 7 patients received during 20 therapeutic NMES sessions a total of 23,380 on-phases, comprising 2194.08 x 10(3) biphasic electrical pulses, without adverse events. Heart rate monitoring during stimulation and pacemaker interrogation revealed no abnormalities. NMES treatment of thigh muscles using a combined NMES protocol to enhance strength and endurance capacity appears to be safe in patients with heart failure and implanted pacemakers with bipolar sensing, as far as the described electrode configuration and parameter range is applied.
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Affiliation(s)
- Richard Crevenna
- Universitätsklinik für Physikalische Medizin und Rehabilitation, Universität Wien, Vienna, Austria.
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Abstract
Exercise intolerance in heart transplant recipients (HTR) has a multifactorial origin, involving complex interactions among cardiac, neurohormonal, vascular, skeletal muscle and pulmonary abnormalities. However, the role of these abnormalities may differ as a function of time after transplantation and of many other variables. The present review is aimed at evaluating the role of cardiac, pulmonary and muscular factors in limiting maximal aerobic performance of HTR, and the benefits of chronic exercise. Whereas pulmonary function does not seem to affect gas exchange until a critical value of diffusing lung capacity is attained, cardiac and skeletal muscle function deterioration may represent relevant factors limiting maximal and submaximal aerobic performance. Cardiac function is mainly limited by chronotropic incompetence and diastolic dysfunction, whereas muscle activity seems to be limited by impaired oxygen supply as a consequence of the reduced capillary network. The latter may be due to either immunosuppressive regimen or deconditioning. Endurance and strength training may greatly improve muscle function and maximal aerobic performance of HTR, and may also reduce side effects of immunosuppressive therapy and control risk factors for cardiac allograft vasculopathy. For the above reasons exercise should be considered an important therapeutic tool in the long-term treatment of heart transplant recipients.
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Affiliation(s)
- Claudio Marconi
- Muscle Physiology and Proteome Section, IBFM-Consiglio Nazionale delle Ricerche, LITA, v Flli Cervi 93, Segrate, 20090 Milan, Italy.
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Zoll J, N'Guessan B, Ribera F, Lampert E, Fortin D, Veksler V, Bigard X, Geny B, Lonsdorfer J, Ventura-Clapier R, Mettauer B. Preserved response of mitochondrial function to short-term endurance training in skeletal muscle of heart transplant recipients. J Am Coll Cardiol 2003; 42:126-32. [PMID: 12849672 DOI: 10.1016/s0735-1097(03)00499-6] [Citation(s) in RCA: 51] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
Abstract
OBJECTIVES We sought to determine whether intrinsic mitochondrial function and regulation were altered in heart transplant recipients (HTRs) and to investigate the response of mitochondrial function to six-week endurance training in these patients. BACKGROUND Despite the normalization of central oxygen transport during exercise, HTRs are still characterized by limited exercise capacity, which is thought to result from skeletal muscle metabolic abnormalities. METHODS Twenty HTRS agreed to have vastus lateralis biopsies and exercise testing: before and after training for 12 of them and before and after the same control period for eight subjects unwilling to train. Mitochondrial respiration was evaluated on saponin-permeabilized muscle fibers in the absence or presence (maximum respiration rate [V(max)]) of saturating adenosine diphosphate. RESULTS Mitochondrial function was preserved at the level of sedentary subjects in untrained HTRs, although they showed 28 +/- 5% functional aerobic impairment (FAI). After training, V(max), citrate synthase, cytochrome c oxidase, and mitochondrial creatine kinase (CK) activities were significantly increased by 48%, 40%, 67%, and 53%, respectively (p < 0.05), whereas FAI decreased to 12 +/- 5% (p < 0.01). The control of mitochondrial respiration by creatine and mitochondrial CK was also improved (p < 0.01), suggesting that phosphocreatine synthesis and transfer by the mitochondrial CK become coupled to oxidative phosphorylation, as shown in trained, healthy subjects. CONCLUSIONS In HTRs, the mitochondrial properties of skeletal muscle were preserved and responded well to training, reaching values of physically active, healthy subjects. This suggests that, in HTRs, immunosuppressive drugs do not alter the intrinsic muscle oxidative capacities and that the patients' physical handicap results from nonmitochondrial mechanisms.
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Affiliation(s)
- Joffrey Zoll
- Service de Physiologie Clinique et des Explorations Fonctionnelles, Département de Physiologie, Faculté de Médecine, 11 rue Humann, 67000 Strasbourg, France.
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Squires RW, Leung TC, Cyr NS, Allison TG, Johnson BD, Ballman KV, Wagner JA, Olson LJ, Frantz RP, Edwards BS, Kushwaha SS, Dearani JA, Daly RC, McGregor CGA, Rodeheffer RJ. Partial normalization of the heart rate response to exercise after cardiac transplantation: frequency and relationship to exercise capacity. Mayo Clin Proc 2002; 77:1295-300. [PMID: 12479515 DOI: 10.4065/77.12.1295] [Citation(s) in RCA: 30] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/16/2022]
Abstract
OBJECTIVE To determine the frequency of partial normalization of the heart rate response to graded exercise and its relationship to exercise capacity in cardiac transplant recipients. SUBJECTS AND METHODS The study subjects were 95 adults (77 men, 18 women) who were available to perform a cardiopulmonary exercise test 1 year after orthotopic cardiac transplantation, which occurred between June 1988 and September 1998. All subjects received standard immunosuppressant medications. At the time of the exercise tests, the mean +/- SD age of the subjects was 49+/-14 years. The mean +/- SD resting left ventricular ejection fraction was 62%+/-8%. All subjects participated in a 6- to 8-week supervised exercise program, starting no later than 1 month after surgery. Subjects were given an exercise prescription for independent exercise training after finishing the supervised program. Self-reported weekly exercise training had a median value of 90 minutes (interquartile range, 0-210 minutes). Symptom-limited graded exercise was performed on a treadmill, with breath-by-breath analysis of expired air. RESULTS For the entire cohort, peak exercise oxygen uptake was 19.9+/-4.8 mL x kg(-1) x min(-1) (61%+/-15% of age and sex predicted). Thirty-two subjects (34%) had a partially normalized heart rate response to graded exercise. The frequency was similar for men (25/77 [33%]) and for women (7/18 [39%]) and was independent of recipient or donor age. Peak exercise heart rate (147+/-18 vs 134+/-21 beats/min; P=.008) and heart rate reserve (46+/-15 vs 33+/-15 beats/min; P<.001) were greater for subjects with a partial normalization of heart rate response. Peak exercise oxygen uptake was similar for subjects with or without partial normalization of the heart rate response (20.9+/-5.8 vs 19.4+/-4.2 mL x kg(-1) x min(-1); P=.22). Submaximal exercise oxygen uptake during the first few minutes of exercise was also not affected by normalization of the heart rate response. CONCLUSION At 1 year after cardiac transplantation, approximately one third of subjects had partial normalization of the heart rate response to graded exercise. However, a higher peak exercise heart rate and a larger heart rate reserve did not result in better aerobic exercise capacity.
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Affiliation(s)
- Ray W Squires
- Division of Cardiovascular Diseases and Internal Medicine, Mayo Clinic, Rochester, Minn 55905, USA.
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Mohacsi P, Pedrazzinia G, Tanner H, Tschanz HU, Hullin R, Carrel T. Lactic acidosis following heart transplantation: a common phenomenon? Eur J Heart Fail 2002; 4:175-9. [PMID: 11959046 DOI: 10.1016/s1388-9842(02)00007-7] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 10/27/2022] Open
Abstract
BACKGROUND Lactic acidosis (LAc) is a common form of metabolic acidosis early after heart transplantation (HTX). The mechanism remains unclear. This study analyzed 13 patients who developed severe LAc after HTX. METHODS From a series of 60 consecutive heart transplant patients, we identified 13 patients with LAc in the first hours following HTX. Nine patients with normal or mildly elevated lactate levels (<5.0 mmol/l) were investigated as controls. RESULTS Thirteen patients developed a moderate or severe LAc (up to 14.6 mmol/l) after HTX. Serum lactate levels increased immediately following surgery with a peak after 6.3+/-1.4 h, spontaneously returning to normal values within 24 h. In contrast to the control group, a significant correlation was found between the maximal serum lactate level and the maximal dosage of inotropic drugs (r=0.93, P<0.02), administered during the reperfusion phase and continued for 12-24 h postoperatively. No correlation was found between LAc and blood gas analysis during extracorporeal perfusion period. CONCLUSION LAc can occur after HTX and seems to be related to the inotropic support of the graft. In contrast to other forms, LAc after HTX has an excellent prognosis and resolves rapidly and spontaneously without treatment. The fact that inotropic support during and immediately after cardiac transplantation can enhance preexisting severe peripheral metabolic cellular dysfunction remains hypothetical.
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Affiliation(s)
- Paul Mohacsi
- Cardiology, Swiss Cardiovascular Center Bern, University Hospital (Inselspital), CH-3010, Bern, Switzerland.
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