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J Thorac Cardiovasc Surg 2001;122:440-448
© 2001 The American Association for Thoracic Surgery
Cardiopulmonary Support and Physiology (CPS) |
From the Divisions of Cardiac Surgerya and Cardiology,d Children's Hospital and Regional Medical Center, University of Washington, School of Medicine, Seattle, Wash; the Department of Critical Care Medicine,b Hospital for Sick Children, Toronto, Ontario, Canada; the Division of Pediatric Cardiology,c Medical University of South Carolina, Charleston, SC; and the Department of Cardiology,e Children's Hospital, Harvard Medical School, Boston, Mass.
Received for publication Nov 10, 2000. Revisions requested Dec 18, 2000; revisions received Feb 14, 2001. Accepted for publication Feb 20, 2001. Address for reprints: Brian W. Duncan, MD, Cleveland Clinic Children's Hospital, 9500 Euclid Ave/M-41, Cleveland, OH 44195.
Abstract
Background: Viral myocarditis may follow a rapidly progressive and fatal course in children. Mechanical circulatory support may be a life-saving measure by allowing an interval for return of native ventricular function in the majority of these patients or by providing a bridge to transplantation in the remainder.
Methods: A retrospective chart review of 15 children with viral myocarditis supported with extracorporeal membrane oxygenation (12 patients) or ventricular assist devices (3 patients) was performed.
Results: All patients had histories and clinical findings consistent with acute myocarditis. The median age was 4.6 years (range 1 day–13.6 years) with a median duration of mechanical circulatory support of 140 hours (range 48-400 hours). Myocardial biopsy tissue demonstrated inflammatory infiltrates or necrosis, or both, in 8 (67%) of the 12 patients who had biopsies. Overall survival was 12 (80%) of 15 patients, with 10 (83%) survivors of extracorporeal membrane oxygenation and 2 (67%) survivors of ventricular assist device support. Nine (60%) of the 15 patients were weaned from support, with 7 (78%) survivors; the remaining 6 patients were successfully bridged to transplantation, with 5 (83%) survivors. All survivors not undergoing transplantation are currently alive with normal ventricular function after a median follow-up of 1.1 years (range 0.9-5.3 years).
Conclusion: Eighty-percent of the children who required mechanical circulatory support for acute myocarditis survived in this series. Recovery of native ventricular function to allow weaning from support can be anticipated in many of these patients with excellent prospects for eventual recovery of full myocardial function.
Asubset of patients with acute myocarditis has a rapidly progressive course of fulminant clinical deterioration that results in refractory cardiorespiratory failure despite maximal medical therapy. Because of the reversibility of the ventricular dysfunction observed during the course of this disease in some patients and the option of cardiac transplantation for those whose ventricular function does not recover, aggressive measures to support these patients during the acute phase of their illness are justified.
1-3 This report describes the successful use of mechanical circulatory support with extracorporeal membrane oxygenation (ECMO) or ventricular assist devices (VADs) to support children with clinically fulminant myocarditis and profound ventricular dysfunction. Providing mechanical circulatory support until native ventricular function returns may be a successful strategy in the majority of these patients.
Methods
Patients and institutions
A retrospective chart review of 15 children from 3 institutions (Children's Hospital, Boston; Hospital for Sick Children, Toronto; and Children's Hospital and Regional Medical Center, Seattle) was performed. This represents a consecutive series of children from each institution who required mechanical circulatory support for acute myocarditis over an 8-year period (1990-1997). These 15 patients represent 14.7% of the 102 patients who required admission to the intensive care unit for acute myocarditis at the 3 study institutions during the same period. The mortality for patients with acute myocarditis who did not require mechanical circulatory support was 3 of 87 or 3.4%. Each of these 15 patients had profound, rapidly progressive ventricular dysfunction with a clinical picture compatible with acute fulminant myocarditis and had mechanical circulatory support instituted with ECMO or a VAD because of clinical deterioration accompanied by imminently lethal cardiogenic shock or cardiac arrest. Each patient was intubated and received conventional mechanical ventilation before the institution of mechanical support. The inotropic regimen these patients received at the time support was instituted and 24 hours later is listed inTable 1. The single patient (patient 10,Table 1) who was not receiving continuous infusions of high-dose inotropic agents was in cardiac arrest on admission and was receiving boluses of inotropic drugs while receiving cardiopulmonary resuscitation throughout cannulation.
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4 have previously described the technical aspects of mechanical circulatory support for children with cardiac disease, which is similar for all 3 institutions. The ECMO circuit used a servoregulated flow system driven by a roller pump (Boston, Seattle) or a centrifugal pump (Bio-Pump; Medtronic Bio-Medicus, Minneapolis, Minn) (Toronto) with a membrane oxygenator (Avecor ECMO Membrane Oxygenator; Avecor Cardiovascular, Inc, Plymouth, Minn). VAD support was provided by a centrifugal pump system (Bio-Pump; Medtronic Bio-Medicus). Twelve of the 15 patients were supported with venoarterial ECMO via vessels in the neck (n = 3), groin (n = 3), or chest (n = 6). The remaining 3 patients received VAD support; two were supported with a left VAD and 1 patient required biventricular support. All 6 patients supported with ECMO via chest cannulation required left heart decompression that was performed with direct placement of a left ventricular vent via the sternotomy. One ECMO-supported patient who was cannulated via peripheral vessels required left heart decompression that was accomplished by creation of an interatrial communication by balloon atrial septostomy in the cardiac catheterization laboratory.
Statistical analysis
Multiple clinical parameters were analyzed with respect to their possible impact on recovery of native ventricular function versus the need for transplantation. The same parameters were then analyzed for their possible association with survival (appendix). All variables were analyzed by univariate analysis with the Student t test or the Wilcoxon rank sums for continuous variables and the Fisher exact test for categorical variables. All statistical analyses were performed with a statistical program (JMP Software; SAS Institute, Inc, Cary, NC).
Results
General
The patients included 7 girls and 8 boys with a median age of 4.6 years (range 1 day–13.6 years) and a median weight of 22 kg (range 5.2-55 kg). The median duration of support was 140 hours (range 48-400 hours). The duration of symptoms before presentation was brief with a median duration of 3 days (range 1-14 days).
Indications
The indications for support were hypotension (n = 5), arrhythmia (n = 5), cardiac arrest (n = 4), and hypoxemia (n = 1)(Table 1
). The 4 patients who required support for cardiac arrest underwent cardiopulmonary resuscitation for a median duration of 67 minutes (range 50-90 minutes). Four additional patients who had support instituted primarily for refractory hypotension also required brief periods of cardiopulmonary resuscitation before the institution of mechanical circulatory support.
Virology and histology
Virology titers were positive in 4 (27%) patients and viral cultures were positive in 2 (13%) of the 15 patients. Endomyocardial biopsy samples were submitted for the polymerase chain reaction in 4 patients, with 1 having a positive reaction. With these techniques combined, viral pathogens were isolated from 7 (47%) of the 15 patients and are listed inTable 2. Twelve (80%) of the 15 patients underwent cardiac catheterization with right ventricular endomyocardial biopsy. One half of the patients undergoing biopsy demonstrated unequivocal histologic evidence of myocarditis per the Dallas criteria 5 with both a mononuclear cellular infiltrate and myocyte necrosis, and 4 (33%) of the 12 patients had nondiagnostic biopsy results(Table 3). The presence of myocarditis on endomyocardial biopsy was not associated with the need for subsequent transplantation or survival (P = .58 and P = .91, respectively).
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Complications
Complications were common in this critically ill population of patients. No complication by organ system was significantly associated with outcome (data not shown). Hemorrhage from the cannulation site was the most commonly observed complication, occurring in 9 (60%) of 15 patients, and was statistically associated with transthoracic cannulation (blood loss for chest cannulation 253 ± 55 mL/kg; blood loss for neck or groin cannulation 21 ± 68 mL/kg; P = .02). Seven (78%) of the 9 patients who had hemorrhage from the cannulation site had transthoracic cannulas, and 2 (22%) patients cannulated via the groin had significant cannulation site bleeding. In 1 (6.7%) patient who was cannulated via groin vessels, a pseudoaneurysm of the femoral artery developed and was treated with ultrasound-guided compression and occlusion.
Seven (47%) patients had renal failure including 5 patients who required temporary dialysis and 2 patients who demonstrated an increase in serum creatinine above 3 mg/dL. All surviving patients have recovered normal renal function. Serious infection occurred in 4 (27%) patients and directly contributed to 1 patient's death from overwhelming fungemia. Neurologic complications developed in 4 (27%) patients, with 2 survivors. Each of these patients has experienced substantial recovery, demonstrating grossly normal neurologic function at present. Only 1 of the 4 patients who demonstrated neurologic impairment at some point during the hospitalization required cardiopulmonary resuscitation before the institution of ECMO. All of the other 10 survivors had a neurologically benign course during hospitalization and remain in neurologically normal condition during follow-up, despite the need for cardiopulmonary resuscitation before ECMO in 5 of these patients.
Outcome
The outcome for these 15 patients is shown inFigure 1, which demonstrates 12 (80%) survivors. There was no significant difference in survival between the two modalities (ECMO 10/12 survivors, 83%; VAD 2/3 survivors, 67%; P = .5). Mechanical circulatory support was used to manage patients along two different pathways: expectantly (until return of native ventricular function) and as a bridge to transplantation. Nine (60%) of 15 patients had return of native ventricular function allowing weaning from support, with 7 (78%) survivors, and 6 (40%) patients were successfully bridged to cardiac transplantation, with 5 (83%) survivors. Patients bridged to transplantation were generally encountered early in the series when it was believed that this degree of ventricular dysfunction was likely to be irreversible and the decision to transplant was made early after admission. Patients who received a heart transplant were listed for transplantation the second day of support on average (range 1-4 days) and received a donor organ a median of 6 days later (range 2-13 days). No patient died on support while awaiting a donor organ. Four other patients were listed for transplantation but had return of ventricular function sufficient for weaning from mechanical circulatory support(Table 1). There was no difference in duration of support, days intubated, intensive care unit stay, or length of hospitalization between patients who underwent transplantation and those who did not(Table 4).
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Despite profound ventricular dysfunction at the time of presentation, all survivors who did not undergo transplantation now have normal ventricular function(Figure 2) after a median follow-up of 1.1 years (range 0.9-5.3 years). Interestingly, several of these patients still had significantly reduced left ventricular fractional shortening at the time of weaning from support. As indicators of recovery of end-organ function, the serum creatinine(Figure 3) and aspartate aminotransferase(Figure 4) are plotted throughout the clinical course for 9 of the 12 survivors for whom this information is available and for the 3 nonsurvivors. Despite significant elevations of serum creatinine or aspartate aminotransferase in several of the surviving patients, all survivors currently have normal renal and hepatic function.
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In its fulminant form, acute myocarditis has a rapidly progressive course quickly resulting in death due to profound ventricular dysfunction. 1,6 The present series is composed of 15 children with clinically fulminant myocarditis whose condition continued to deteriorate despite maximal medical therapy. The favorable outcomes for these critically ill children support aggressive measures during the acute phase of this disease. Of special importance is the observation that native ventricular function recovered to allow weaning from support in the majority of these patients, with all of the survivors who did not undergo transplantation currently demonstrating normal ventricular function.
Decision to institute support
Indications
Determining the need for mechanical circulation to support children with fulminant myocarditis is a clinical decision. The rapid progression of the disease is an immediate clue that medical therapy alone may be insufficient; all of the patients in this series had the onset of mild constitutional symptoms precede cardiovascular collapse by only hours to days. Diagnostic tests such as chest x-ray films and electrocardiograms provide supportive evidence for the diagnosis but are nonspecific. The demonstration of profound ventricular dysfunction on echocardiography identifies patients at risk, but the clinical status of the patient remains the critical determinant of whether to institute ECMO or VAD support.
The most important factor leading to the decision to institute mechanical circulatory support is the observation that medical treatment is failing. Increasing inotropic requirements, accompanied by evidence of inadequate cardiac output such as poor cutaneous perfusion, oliguria, and systemic acidosis are unlikely to be reversed by further medical management in this condition. The need for excessive inotropic doses accompanied by significant ventricular ectopy is a particularly dangerous combination for which mechanical circulatory support should be strongly considered. Cardiac arrest, even of brief duration, is an ominous sign indicating that circulatory support should be considered. Overall, an aggressive stance toward the institution of mechanical circulatory support should be taken in these patients because of their tendency toward unpredictable and rapid deterioration.
Management issues during support
Choice of device and site of cannulation
We have previously reported that either ECMO or a VAD may be used to successfully support children with a wide range of cardiac diseases. 4 In terms of the site of cannulation, ECMO provides greater flexibility because vessels in the neck, groin, or chest are used, whereas the use of a VAD necessitates transthoracic cannulation. In the present study, the institution of ECMO or VAD support via transthoracic cannulation led to significantly more bleeding complications and introduced an additional source of infection. With these factors in mind, we prefer ECMO for children who require support for myocarditis because of its ability to be instituted via peripheral cannulation and the presence of an oxygenator for use in patients with hypoxemia. For the institution of ECMO, we prefer neck cannulation for neonates and infants. For older children and adolescents, we prefer femoral cannulation to avoid cerebral ischemia that may result from carotid cannulation.
For ECMO-supported patients, the development of left-sided cardiac distention must be assiduously avoided by monitoring left-sided filling pressures and the echocardiographic appearance of the left ventricle. If left ventricular distention is documented, decompression should be aggressively performed. For patients who are cannulated via the transthoracic route, direct venting of the left ventricle by placement of a drainage cannula via the left atrial appendage or right superior pulmonary vein can be easily performed. For ECMO-supported patients cannulated via peripheral vessels, balloon atrial septostomy, performed in the cardiac catheterization laboratory or at the bedside under echocardiographic guidance, is an effective means of left-sided decompression for patients without an existing sternotomy. 7,8 In the present series, 7 (58%) of the 12 patients supported with ECMO required some form of left-sided cardiac decompression.
Optimization of end-organ function
In the present study, elevations of markers of end-organ function such as creatinine, liver enzymes, and serum lactate before support and early after support was instituted were predictive of increased mortality. Early elevations of these markers identify children with an aggressive disease process, as well as reflecting the effectiveness of resuscitative efforts. The best approach to optimize end-organ function in patients who require mechanical circulatory support is to institute support early, before extended periods of low cardiac output or cardiac arrest. Measurement of markers of end-organ function may provide prognostic information in these children as well as reflecting the timeliness of the establishment of circulatory support.
Endomyocardial biopsy
Two thirds of the patients in this study had unequivocal or borderline evidence of lymphocytic myocarditis according to the Dallas criteria, similar to the 20% to 60% of patients with positive biopsy results reported in other series. 5,9-11 Factors leading to negative biopsy results in these children have been previously described and include sampling error and the possibility that humoral rather than cellular mediators are responsible for the clinical condition. 10,12 All 3 reporting centers advocate performing endomyocardial biopsy during the course of acute myocarditis to rule out other causes of profound ventricular dysfunction such as metabolic causes of dilated cardiomyopathy. This is especially important in the pediatric population because metabolic causes of cardiomyopathy may require specific treatment and may be inherited, with implications for family planning. Currently, children who require mechanical circulatory support with histologic findings of acute myocarditis would be managed expectantly with hope for the eventual return of native ventricular function, whereas patients with histologic findings of cardiomyopathy who require ECMO or VAD would be urgently listed for transplantation.
Immunotherapy
Fourteen (93%) of the 15 patients in this series received some form of immunotherapy, with the majority (12 patients) receiving intravenous gamma globulin. We believe that the use of intravenous gamma globulin is of potential benefit in patients with acute myocarditis and is associated with relatively few risks. 13 The benefit of this therapy cannot be clearly demonstrated in this small population; however, the low overall mortality and the return of native ventricular function in a significant number of patients in this series suggests that gamma globulin administration may have contributed positively. On the basis of the existing data, we do not advocate the routine use of steroids in the treatment of this condition. 14,15 In fact, steroid administration during the acute phase of the disease has been shown experimentally to impair viral clearance and decrease survival. 16,17 The merits of any immunotherapeutic regimen in patients with acute myocarditis will be best addressed by prospective randomized trials in larger numbers of patients.
Outlook for pediatric patients with clinically fulminant myocarditis
Return of native ventricular function versus bridge to transplantation
The importance of the present study lies chiefly in demonstrating excellent survival in even the most severely affected children with few chronic complications. An equally significant finding from the present study is the reversibility of myocardial dysfunction demonstrated by these patients. Historically, studies have suggested that dilated cardiomyopathy would be expected to develop in a significant percentage of children with acute myocarditis with the ultimate need for cardiac transplantation. 6 Our findings suggest that the present pediatric population with acute, fulminant myocarditis behaves differently, with an overall favorable outcome and a significant degree of disease reversibility if successfully supported during the acute phase of illness.
These results support those in a recent study by McCarthy and coworkers, 18 who described the superior long-term outcome of a group of adult patients with fulminant myocarditis compared with patients who had acute, nonfulminant myocarditis. Patients with fulminant disease presented with severe hemodynamic compromise, distinct onset of heart failure symptoms, and the presence of a viral illness within 2 weeks of hospitalization. All patients with fulminant myocarditis were receiving high doses of intravenous inotropic agents, but only 2 of 15 patients required mechanical circulatory support. Patients classified with acute, nonfulminant myocarditis had a clinical picture that was less severe with an indistinct onset. Despite being more critically ill acutely, the patients with fulminant myocarditis had a better long-term outcome, with 93% of these patients being alive without transplantation after 11 years of follow-up, compared with only 45% of patients with acute, nonfulminant myocarditis.
The reasons for better long-term outcomes and a decreased incidence of progression to dilated cardiomyopathy in patients who are the most severely affected with myocarditis remain unexplained. Proposed mechanisms for this clinical paradox include differences in viral agents leading to fulminant versus nonfulminant forms of myocarditis, differences in host response to viral infection between the two entities, and the possibility that fulminant myocarditis is due to an autoimmune disorder. 18-20 In the present study, salutary effects of mechanical circulatory support may have contributed to the improved long-term outcomes in these children. In patients with dilated cardiomyopathy, prolonged mechanical circulatory support may result in ultimate recovery of ventricular function because of favorable influences on the neurohormonal cardiovascular milieu and unloading of the left ventricle resulting in normalization of ventricular geometry—a process termed reversible remodeling. 21 We believe that the institution of mechanical circulatory support in patients with acute fulminant myocarditis can favorably affect these same factors, resulting in ventricular recovery over a much shorter time course—a process that we have termed rapid reversible remodeling. In these most severe cases of myocarditis, mechanical circulatory support provides the ultimate form of physiologic rest, similar to simple bed rest and oxygen used to support less severe cases. It is compelling to speculate that normalization of ventricular geometry and function by the early institution of support in the present study may have helped to prevent the development of dilated cardiomyopathy.
We agree with the conclusion of McCarthy and coworkers 18 that native ventricular function may ultimately be expected to return in most patients with fulminant myocarditis. This raises questions as to the role of transplantation in the fulminant form of this disease. The present study was not a randomized trial of expectant management versus bridge to transplantation in these patients. In the present series, patients were listed for transplantation according to the preferences and practices of the physicians in each institution; they were generally listed early (median of 2 days) and received a donor organ quickly (median of 6 days after listing). Currently, all 3 of the participating centers would adopt a more expectant course of management to give these patients a greater chance for return of native ventricular function.
On the basis of these results, the optimal approach for children with acute fulminant myocarditis may be to provide mechanical circulatory support, even if required for prolonged periods, in anticipation of eventual ventricular recovery. Previous reports have documented full return of ventricular function in young adults with myocarditis after weeks or months of mechanical support. 22,23 A limitation of this approach for children is that ECMO and centrifugal VAD systems, which are currently available in the United States for pediatric patients, are not suitable for such extended periods of support. Pulsatile paracorporeal or implantable systems that allow extended periods of support have been used successfully in pediatric patients in Europe and have demonstrated the feasibility of this approach. 24,25 Prolonged mechanical circulatory support in a larger number of pediatric patients with fulminant myocarditis may reveal that the capability of supporting these children for weeks or months will allow return of native ventricular function, thereby avoiding transplantation in the majority of these children.
Appendix
Clinical parameters tested for their possible association with (1) Return of native ventricular function versus the need for transplantation and (2) Survival
Acknowledgments
We appreciate the statistical consultation of Geoffrey L. Rosenthal, MD, PhD.
References
This article has been cited by other articles:
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  T. Chan, R. R. Thiagarajan, D. Frank, and S. L. Bratton Survival after extracorporeal cardiopulmonary resuscitation in infants and children with heart disease. J. Thorac. Cardiovasc. Surg., October 1, 2008; 136(4): 984 - 992. [Abstract] [Full Text] [PDF]
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 P. Monagle, E. Chalmers, A. Chan, G. deVeber, F. Kirkham, P. Massicotte, and A. D. Michelson Antithrombotic Therapy in Neonates and Children: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition) Chest, June 1, 2008; 133(6_suppl): 887S - 968S. [Abstract] [Full Text] [PDF]
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 S. Paul Collison and K. Singh Dagar The role of the Intra-aortic balloon pump in supporting children with acute cardiac failure Postgrad. Med. J., May 1, 2007; 83(979): 308 - 311. [Abstract] [Full Text] [PDF]
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 C. E. Canter, R. E. Shaddy, D. Bernstein, D. T. Hsu, M. R.K. Chrisant, J. K. Kirklin, K. R. Kanter, R. S.D. Higgins, E. D. Blume, D. N. Rosenthal, et al. Indications for Heart Transplantation in Pediatric Heart Disease: A Scientific Statement From the American Heart Association Council on Cardiovascular Disease in the Young; the Councils on Clinical Cardiology, Cardiovascular Nursing, and Cardiovascular Surgery and Anesthesia; and the Quality of Care and Outcomes Research Interdisciplinary Working Group Circulation, February 6, 2007; 115(5): 658 - 676. [Abstract] [Full Text] [PDF]
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 E-T Wu, S-C Huang, Y-S Chen, J-K Wang, M-H Wu, and W-J Ko Children with fulminant myocarditis rescued with extracorporeal membrane oxygenation. Heart, September 1, 2006; 92(9): 1325 - 1326. [Full Text] [PDF]
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N Amabile, A Fraisse, J Bouvenot, P Chetaille, and C Ovaert Outcome of acute fulminant myocarditis in children Heart, September 1, 2006; 92(9): 1269 - 1273. [Abstract] [Full Text] [PDF]
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 V. H. Thourani, P. M. Kirshbom, K. R. Kanter, J. Simsic, B. E. Kogon, S. Wagoner, F. Dykes, J. Fortenberry, and J. M. Forbess Venoarterial extracorporeal membrane oxygenation (VA-ECMO) in pediatric cardiac support. Ann. Thorac. Surg., July 1, 2006; 82(1): 138 - 144. [Abstract] [Full Text] [PDF]
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V. K. Topkara, N. C. Dang, F. Barili, T. P. Martens, I. George, F. H. Cheema, H. Bardakci, A. V. Ozcan, and Y. Naka Ventricular assist device use for the treatment of acute viral myocarditis J. Thorac. Cardiovasc. Surg., May 1, 2006; 131(5): 1190 - 1191. [Full Text] [PDF]
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J. T. Baldwin, H. S. Borovetz, B. W. Duncan, M. J. Gartner, R. K. Jarvik, W. J. Weiss, and T. R. Hoke The National Heart, Lung, and Blood Institute Pediatric Circulatory Support Program Circulation, January 3, 2006; 113(1): 147 - 155. [Abstract] [Full Text] [PDF]
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 Y. Asaumi, S. Yasuda, I. Morii, H. Kakuchi, Y. Otsuka, A. Kawamura, Y. Sasako, T. Nakatani, H. Nonogi, and S. Miyazaki Favourable clinical outcome in patients with cardiogenic shock due to fulminant myocarditis supported by percutaneous extracorporeal membrane oxygenation Eur. Heart J., October 2, 2005; 26(20): 2185 - 2192. [Abstract] [Full Text] [PDF]
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B. Alsoufi, I. Shen, T. Karamlou, C. Giacomuzzi, G. Burch, M. Silberbach, and R. Ungerleider Extracorporeal Life Support in Neonates, Infants, and Children After Repair of Congenital Heart Disease: Modern Era Results in a Single Institution Ann. Thorac. Surg., July 1, 2005; 80(1): 15 - 21. [Abstract] [Full Text] [PDF]
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B. W. Duncan INVITED COMMENTARY Ann. Thorac. Surg., January 1, 2005; 79(1): 183 - 184. [Full Text] [PDF]
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R R Chaturvedi, D Macrae, K L Brown, M Schindler, E C Smith, K B Davis, G Cohen, V Tsang, M Elliott, M de Leval, et al. Cardiac ECMO for biventricular hearts after paediatric open heart surgery Heart, May 1, 2004; 90(5): 545 - 551. [Abstract] [Full Text] [PDF]
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S. L.C. Reddy, A. Hasan, L. R.J. Hamilton, J. Dark, S. W. Schueler, D. T. Bolton, S. R. Haynes, and J. H. Smith Mechanical versus medical bridge to transplantation in children. What is the best timing for mechanical bridge? Eur. J. Cardiothorac. Surg., April 1, 2004; 25(4): 605 - 609. [Abstract] [Full Text] [PDF]
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