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Ann Thorac Surg 2000;69:186-192
© 2000 The Society of Thoracic Surgeons


Original Articles

Long-term follow-up of pediatric cardiac patients requiring mechanical circulatory support

Andra E. Ibrahim, MDa, Brian W. Duncan, MDa, Elizabeth D. Blume, MDa, Richard A. Jonas, MDa

a Departments of Cardiology and Cardiac Surgery, Children’s Hospital, Boston, Massachusetts, USA

Address reprint requests to Dr Jonas, Department of Cardiac Surgery, Children’s Hospital, 300 Longwood Ave, Boston, MA 02115


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The present study examines the long-term outcome of pediatric patients with cardiac disease who required mechanical circulatory support with extracorporeal membrane oxygenation or ventricular assist devices.

Methods. Telephone interviews and questionnaires were administered to parents and physicians of pediatric cardiac patients who were in-hospital survivors after requiring mechanical circulatory support, with either extracorporeal membrane oxygenation or ventricular assist devices. Data was collected regarding these patients’ general health, cardiac status, and neurologic outcome, and compared between the two modes of support.

Results. Follow-up was available for 26 patients supported with extracorporeal membrane oxygenation (25 survivors, 96%) and 11 patients supported with ventricular assist devices (10 survivors, 91%); median follow-up 42 months, 11 to 92 months). More than 80% of survivors were in New York Heart Association class I or II. Of 31 patients for whom neurologic assessment data was available, moderate to severe neurologic impairment was more common for extracorporeal membrane oxygenation supported patients [13 of 21, 59%) than for ventricular assist device supported patients (2 of 10, 20% p = 0.03). Neurologic impairment was associated with small patient size and the use of circulatory arrest during cardiac surgical repair, but was not associated with in-hospital neurologic complications, carotid cannulation, or presupport cardiac arrest.

Conclusions. The long-term survival and cardiac functional status of pediatric cardiac patients requiring mechanical circulatory support is favorable. Extracorporeal membrane oxygenation supported patients demonstrate higher rates of neurologic impairment than patients supported with ventricular assist devices. Poor neurologic outcomes are associated with institution of support in younger patients with more complex congenital heart disease.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
We recently reviewed the hospital course of children with cardiac disease requiring mechanical circulatory support with either extracorporeal membrane oxygenation (ECMO) or ventricular support devices (VAD) in our institution. The rates of weaning from support and in-hospital mortality (approximately 66% and 40%, respectively) were nearly identical for patients supported with either modality [1]. Several reports exist detailing the long-term follow-up of children supported with ECMO for respiratory failure, but little information is available regarding the long-term follow-up of children managed with ECMO for heart disease. This report describes the long-term outcome of pediatric cardiac patients who survive to hospital discharge after requiring mechanical circulatory support with ECMO or VAD.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
From November 1987 through March 1996, 96 pediatric patients with cardiac disease required mechanical circulatory support at our institution (67 ECMO, 29 VAD). Twenty-seven ECMO supported patients and 12 VAD supported patients survived to hospital discharge [1]. One ECMO supported patient was lost to follow-up. One survivor received both ECMO and left VAD support during the initial hospitalization. The period of left VAD support lasted only a few hours and required conversion to ECMO due to biventricular failure. This patient was included only in the ECMO supported group for the present study, which resulted in 26 ECMO supported patients and 11 VAD supported patients available for long-term follow-up.

Telephone interviews and written questionnaires
Long-term follow-up was obtained for these surviving children after review and approval from the Committee on Clinical Investigation at Children’s Hospital, Boston. A telephone questionnaire was administered by the same investigator, following a standardized format, to the parents or guardians of young children or the patients themselves, if older than 18 years of age. Data collected included a description of these patients’ current health, cardiovascular status, noncardiac medical problems, and growth. Written questionnaires, which covered a wide range of health issues, and were designed to supplement subjective data supplied from the parents’ questionnaires, were administered to the patient’s pediatricians and cardiologists. Cardiac data obtained included the most recent echocardiogram reports, New York Heart Association (NYHA) classification and the need for further cardiac operations. Questions to physicians also covered ongoing medical problems, noncardiac operations and growth, determined as percentile height and weight using standardized National Center for Health Statistics growth charts. The height and weight of the 1 (ECMO supported) child with trisomy 21 was evaluated using percentile growth curves standardized for children with trisomy 21.

Assessment of current neurologic status
The presence of neurologic impairment in these patients was mainly determined by current cognitive functioning, as well as the presence of gross neurologic motor and sensory deficits. Cognitive skills were determined for children placed on support at less than 1 year of age, by determining the age of attaining gross motor and language developmental milestones using established guidelines [2, 3]. Cognitive skills were determined for children that were placed on support at greater than 1 year of age by measuring school performance according to participation at an age-appropriate grade level, requirement for special educational programs, or the inability to attend school altogether because of severe neurologic deficits. Based on present cognitive function, each patient’s neurologic status was placed into one of four groups: normal, mild impairment, moderate impairment, or severe neurologic impairment. In addition to present cognitive function, the presence of significant gross motor abnormalities such as hemiplegia or cerebral palsy, and sensory deficits such as cortical blindness or sensorineural hearing impairment, mandated inclusion into the moderately or severely impaired group. No formal neurologic testing was performed solely for the purposes of this report.

Data management and statistical analysis
Data was collected and analyzed using a statistical program (JMP Software, SAS Institute, Cary, NC). The comparison of neurologic status between ECMO and VAD supported groups was performed with Pearson’s {chi}2. Determining the association of factors present at the time of mechanical circulatory support with neurologic status was performed with the Wilcoxon-rank-sum test for continuous variables or Pearson’s {chi}2 for discrete variables. Variables attaining a p value of 0.05 were reported as statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Of the 26 surviving ECMO supported patients and 11 surviving VAD supported patients, 1 patient in each group died after hospital discharge (long-term ECMO survival 25 of 26 (96.2%); long-term VAD survival 10 of 11 [90.9%]) (Fig 1). Median length of follow-up was 43 months (range 11 to 92 months) for the ECMO supported patients and 41 months (range 17 to 81 months) for the VAD supported patients. Median age at follow-up for patients supported with ECMO was 4.6 years of age (range 1.0 to 18 years of age). Median age at follow-up for the patients supported with VAD was 7.1 years of age (range 2.1 to 24 years of age). Nineteen of the 26 ECMO survivors (73%) and 7 of the 11 survivors (64%) in the VAD supported group were less than 1 year of age at the time of support.



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Fig 1. Survival curves for extracorporeal membrane oxygenation and ventricular support device supported patients.

 
Details of ECMO and VAD support
As described previously [1], ECMO support included a servoregulated flow system driven by a roller-pump with a membrane oxygenator (Avecor ECMO Membrane Oxygenator; Avecor Cardiovascular, Inc, Plymouth, MN). Of the 26 surviving ECMO supported patients, 24 received venoarterial ECMO and 2 received venovenous ECMO. The one nonsurviving ECMO patient received venovenous ECMO support. Activated clotting times (ACT) were maintained within 180 to 220 seconds by a continuous heparin infusion. ACT levels were maintained at lower levels if significant bleeding occurred on support. Antifibrinolytic therapy with aminocaproic acid (AMIKAR; Lederle Parenterals, Carolina, Puerto Rico) was used in essentially all of these patients after 1990. AMIKAR was initiated as an intravenous bolus of 100 mg/kg, maintained as a continuous intravenous infusion of 30 mg/kg/h for the initial 48 hours of support and then discontinued.

Our entire experience with VAD used a centrifugal pump system (Bio-Pump; Bio-Medicus, Minneapolis, MN). For infants and children less than 10 kg the 50 cc Bio-Pump was used. For patients above 10 kg the 80 cc Bio-Pump was used. After September of 1994, we employed Carmeda coated cannulas and Carmeda coated polyvinyl chloride tubing (Medtronic Corporation, Minneapolis, MN). Of the VAD supported patients, 10 patients received left ventricular assist device support (LVAD) and 1 patient received right ventricular assist device support (RVAD). The one nonsurviving VAD patient was supported with LVAD. The ACT was maintained at 180 to 200 seconds and lower ACT levels (160 to 180 seconds) were maintained if Carmeda coated tubing was employed.

The original diagnoses (Table 1) and indications for mechanical support (Table 2) are listed for surviving ECMO and VAD patients. Of special interest were those patients who required mechanical circulatory support for cardiac arrest (17 of the ECMO supported patients and 4 of the VAD supported patients) [1]. Eight of these 17 ECMO supported patients (47%) survived to hospital discharge, all of whom are long-term survivors. Two of the 4 VAD supported patients (50%) survived to hospital discharge with 1 long-term survivor. Survivors of cardiac arrest in both groups received cardiopulmonary resuscitation (CPR) for a mean duration of 53.4 ± 28.3 minutes. In an attempt to lessen the impact of cardiac arrest on neurologic function, patients were maintained mildly hypothermic (34°C) for 24 to 48 hours after cardiac arrest, and hyperthermia (above 37°C) was avoided for 4 to 5 days after arrest [4].


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Table 1. Original Cardiac Diagnosis of Long-Term Survivors of Mechanical Circulatory Support

 

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Table 2. Original Indications for Mechanical Circulatory Support for Long-Term Survivors

 
Current health status
The overall health status for ECMO and VAD supported patients is displayed in Figure 2. Eighty percent of the respondents described their general health as good to excellent for both the ECMO and VAD supported groups.



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Fig 2. Description of surviving children’s overall health status as reported by parents.

 
Cardiac status
The patients’ physicians provided NYHA classifications for 21 ECMO patients and 10 VAD patients (Fig 3). Twenty of 21 ECMO patients (95%) and 9 of 10 VAD patients (90%) were in NYHA class I or class II. The results of the most recent echocardiographic examination for these patients are presented in Table 3. All of the 18 ECMO supported patients, for whom an assessment of left ventricular function was available, were reported to have normal function while 9 of the 10 VAD supported patients had normal ventricular function. One patient with an unbalanced complete atrioventricular canal (CAVC) supported by VAD at the time of a mitral valve replacement had poor left ventricular function and pulmonary hypertension associated with the development of severe subaortic obstruction on follow-up echocardiography. Two patients requiring VAD for perioperative support for repair of anomalous left coronary artery from the pulmonary artery (ALCAPA) had severe postoperative mitral regurgitation. Two ECMO supported patients continued to exhibit poor right ventricular function including a patient with tetralogy of Fallot (TOF) and CAVC who had significant obstruction of the right pulmonary artery, after initial transannular patching, which was treated with stent placement. This patient also demonstrated severe tricuspid regurgitation. The other patient with significant right ventricular dysfunction had obstruction of a right ventricle to pulmonary artery conduit used to repair TOF with pulmonary atresia that was treated with conduit replacement. The patient with combined TOF and CAVC also exhibited free pulmonic regurgitation after transannular patching. The other 3 cases with free pulmonic regurgitation included 1 ECMO supported patient with pulmonary atresia, intact ventricular septum who underwent transannular patching as part of the repair. One ECMO supported patient with free pulmonic regurgitation had progressive deterioration of a right ventricle to pulmonary artery conduit as part of a repair for truncus arteriosus and one ECMO supported patient with transannular patching for TOF also demonstrated free pulmonary regurgitation. Three ECMO supported patients demonstrated a residual VSD. One of these was the previously described patient with combined TOF and CAVC. One patient with double outlet right ventricle repaired with a Rastelli procedure and 1 patient with total anomalous pulmonary venous return and multiple VSDs who underwent repair of total anomalous pulmonary venous return with placement of a pulmonary artery band also demonstrated residual VSDs.



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Fig 3. New York Heart Association classification of long-term survivors by patients’ pediatricians and/or cardiologists.

 

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Table 3. Residual Cardiac Lesions by Echocardiography in Long-Term Survivors of Mechanical Circulatory Supporta

 
The list of subsequent cardiac surgical procedures that these children required is listed in Table 4. Cardiac transplantation was performed for a child who suffered progressive biventricular failure during the year after a Ross procedure. This patient required ECMO support for resuscitation after cardiac arrest due to postoperative bleeding. There was no coronary artery problem or other identifiable cause of the progressive ventricular dysfunction in this patient. One ECMO supported patient with TOF required placement of a ventricular pacemaker for complete heart block complicating the original repair. One patient with TOF and pulmonary atresia required ECMO support for a cardiac arrest suffered in the cardiac catheterization laboratory. This patient underwent VSD closure and a right ventricle to pulmonary artery homograft reconstruction of the right ventricular outflow tract during a subsequent hospitalization. The remaining ECMO supported patient who required late operation was the previously described patient with TOF and pulmonary atresia with conduit stenosis that underwent conduit replacement. Three patients in the VAD group required further cardiac operation, including the 2 previously described patients with ALCAPA and persistent postoperative mitral regurgitation. One of these patients was treated with mitral valve replacement while 1 required mitral valve repair. The previously described VAD supported patient with unbalanced CAVC and subaortic obstruction subsequently underwent a successful Konno procedure.


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Table 4. Additional Cardiac Surgical Procedures in Long-Term Survivors of Mechanical Circulatory Support

 
Growth and development
Data was available for 33 patients with a median height in the ECMO supported group at the twenty-eighth percentile (range 10 to 97 percentile) and thirty-second percentile in the VAD supported group (range 1 to 53 percentile). The median weight in the ECMO supported patients was at the thirty-sixth percentile (range 15 to 97 percentile) and forty-fourth percentile (range 1 to 95 percentile) in the VAD supported patients.

Neurologic outcomes
Information on long-term neurologic outcomes was not available for 3 of the 25 ECMO survivors. In addition, 1 ECMO supported patient was excluded from the analysis because he had Down’s syndrome with severe cognitive and developmental delay prior to support. The remaining patients were considered to be neurologically normal prior to their requirement for mechanical circulatory support. This resulted in follow-up data for neurologic outcomes for 21 long-term survivors of ECMO support and all 10 long-term survivors of VAD support. Based on present cognitive functioning and the presence of gross motor or sensory abnormalities, 13 of these 21 ECMO patients (59%) and 2 of the 10 VAD patients (20%) demonstrated moderate to severe neurologic impairment (p = 0.03) (Fig 4). Of the 9 moderately impaired ECMO supported patients, 8 children demonstrated significant delay in attaining developmental milestones. In addition, 3 of these children demonstrated gross motor abnormalities, hemiplegia in 2 cases due to cerebrovascular accidents suffered during ECMO support and 1 child with cerebral palsy. Another moderately impaired child who required ECMO support at the age of 18 months had severe learning disabilities requiring special schooling for learning disabled children. Of the 4 severely impaired ECMO supported children, 3 patients had severe anoxic encephalopathy, and 2 of these patients required 24-hour nursing care. One of these children was quadriplegic with cortical blindness and the other suffered a cerebral vascular accident with residual left-sided hemiplegia. A fourth child, considered severely impaired, had a left-sided hemiplegia and was severely developmentally delayed. Two VAD supported children demonstrated moderate or severe neurologic impairment. The child demonstrating moderate impairment after VAD support had significant delay in attaining developmental milestones and has significant left-sided hemiplegia due to a cerebrovascular accident, suffered during the initial hospitalization. The severely affected child, after VAD support, suffers from severe anoxic encephalopathy and requires 24-hour nursing care.



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Fig 4. Neurologic impairment for extracorporeal membrane oxygenation and ventricular support device supported pediatric patients with cardiac disease.

 
These 13 ECMO and 2 VAD supported patients, with moderate to severe neurologic impairment, were compared to normal or mildly impaired survivors with respect to factors at the time of their original hospitalization with a potential for adverse influence on neurologic outcomes. Neurologic outcomes in these patients were positively correlated with weight at the time of support (p = 0.01) and negatively correlated with the use of circulatory arrest for those patients that required cardiac operation prior to ECMO or VAD support (p = 0.02) (Table 5). The presence of in-hospital neurologic complications at the time of support, neck cannulation, the performance of carotid reconstruction, and the presence of CPR prior to support did not demonstrate a statistically significant association with poor neurologic outcomes (Table 5).


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Table 5. Clinical Parameters at the Time of ECMO or VAD Support Associated With Long-Term Adverse Neurologic Outcomes

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Mechanical support with ECMO or VAD has become an important tool for the treatment of children with heart disease refractory to maximal medical circulatory and ventilatory support. Reports from our institution, as well as others, have demonstrated that a 40% to 80% in-hospital survival rate is possible for these children [1, 5, 6]. Several reports exist describing the long-term outcome for children requiring ECMO for primary respiratory failure [79]. Despite the increasingly widespread use of mechanical circulatory support in pediatric cardiac patients, little information is available regarding the long-term outlook and quality of life for survivors.

Survival and general health
The significant in-hospital morbidity and mortality associated with mechanical circulatory support for pediatric cardiac patients requires a continual reevaluation of results to ensure that these heroic measures are justified. These results demonstrate excellent long-term survival with more than 90% of these patients alive after an average follow-up of 4 years. Data on the overall condition of survivors is also encouraging, in that more than 80% of the survivors demonstrate good to excellent general health. These results are reassuring and help to justify an aggressive approach in these children.

An interesting subgroup of survivors are those who had a cardiac arrest as the original indication for support. We have previously demonstrated that the in-hospital survival, for this most critically ill subset of patients, is equivalent to the survival for patients requiring mechanical circulatory support for all other indications [1]. These findings formed the basis for our intensified efforts to quickly resuscitate pediatric cardiac patients that suffer cardiac arrest with a rapid response ECMO circuit [4]. The results of the present study support an aggressive stance in these patients as well, because 9 out of 10 patients that survived to hospital discharge, after requiring ECMO or VAD for cardiac arrest, are long-term survivors. The long-term survival data in these cardiac arrest patients further corroborates the observation that many of these patients have reversible causes for cardiac arrest that can be managed successfully with relatively brief periods of circulatory support. These excellent in-hospital and now long-term results for pediatric cardiac patients, contrast with the dismal results after cardiac arrest in children with other medical diseases [10] or adult patients with cardiac disease [11], but appear to be similar to results in infants with respiratory failure who suffer cardiac arrest prior to the initiation of ECMO [12].

Cardiac status of survivors
The cardiac outcomes of surviving children are favorable, with the majority of children currently in NYHA class I or II. The assessment of ventricular function by echocardiographic data demonstrated normal function in all but 1 of the 28 patients for whom data was available. Many of the significant residual cardiac lesions represent the long-term sequellae of primary corrective or palliative procedures such as conduit deterioration and pulmonic regurgitation secondary to transannular patching of the right ventricle. At present 84% of the ECMO supported patients, and 70% of the VAD supported patients remain free of further cardiac procedures.

Neurologic complications
We previously reported that in-hospital neurologic complications occurred in more than 30% of all ECMO supported patients and in nearly 10% of all VAD supported patients, which was a statistically significant difference between the two modalities [1]. This trend persisted during the period of follow-up for survivors. Based on current cognitive function and the presence of motor or sensory deficits, there was a significantly higher rate of neurologic impairment in the ECMO supported group. However, many patients that demonstrated moderate neurologic impairment in either group are doing quite well overall, with only 16% (5 of 31 patients, 4 ECMO, 1 VAD) demonstrating severe disability.

The causes of adverse neurologic outcomes in the ECMO supported patients is multifactorial, but largely reflects that these are younger patients with more complicated cardiac disease when compared with the VAD supported patients. Sixty percent of the ECMO supported group were neonates, compared with 10% of the VAD supported patients. Small size at the time of support was significantly associated with adverse neurologic outcomes in both ECMO and VAD supported patients. In addition, ECMO supported patients were more likely to have complex cyanotic lesions as opposed to VAD supported patients [1]. The association of neurologic impairment with the use of hypothermic circulatory arrest during cardiac operation in this analysis is consistent with reports that have demonstrated the adverse impact of circulatory arrest on subsequent neurocognitive development [13, 14]. Another important risk factor for poor neurologic outcomes in the ECMO supported patients includes the need for higher levels of anticoagulation that are used, which places these critically ill neonates at risk for intracranial hemorrhage during support. In our previous analysis, intracranial hemorrhage was the most common neurologic complication seen in ECMO supported patients [1]. In addition, the greater complexity of the circuit also predisposes these patients to embolic complications with the oxygenator, and increased tubing lengths required for ECMO, serving as potential sources for thromboemboli. The lack of association with neurologic impairment and carotid cannulation, or reconstruction after ECMO support, is in agreement with the majority of the literature examining the role of carotid reconstruction for children who require ECMO for respiratory failure [15, 16]. In-hospital neurologic complications were not significantly associated with adverse neurologic outcomes in the long-term. The lack of association with in-hospital neurologic complications corroborates the observation that patients suffering neurologic injury may eventually recover without significant sequellae, while poor neurologic outcomes may become apparent in patients without in-hospital neurologic complications as they grow older. Previous reports have demonstrated the inadequacies of imaging studies obtained during ECMO support for respiratory failure in predicting neurologic outcomes [17]. Our results underscore the importance of long-term follow-up in determining the ultimate neurologic status in any survivor of mechanical circulatory support.

The results from the present study are reassuring in that children with heart disease who survive to hospital discharge, after requiring ECMO or VAD support, demonstrate favorable long-term survival, overall general health, and cardiac outcomes. The relatively higher rates of neurologic complications in the ECMO supported group are a cause for concern, and appear to be due to multiple causes in critically ill neonates. Results may be improved by modifications in ECMO that utilize simpler circuits requiring less anticoagulation. These results further underscore the difficulties in predicting the extent of neurologic injury during the acute phases of care in these children, and the necessity of long-term follow-up to assess ultimate neurologic status.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Duncan B.W., Hraska V., Jonas R.A., et al. Mechanical circulatory support in children with cardiac disease. J Thorac Cardiovasc Surg 1999;117:529-542.[Abstract/Free Full Text]
  2. Simeonsson R.J., Simeonsson N.E. Developmental surveillance and intervention. In: Hoekelman R.A., Friedman S.B., eds. Primary pediatric care, 3rd ed. St. Louis: Mosby-Year Book, 1997:236-243.
  3. First L.R., Palfrey J.S. The infant or young child with developmental delay. N Engl J Med 1994;330:478-483.[Free Full Text]
  4. Duncan B.W., Ibrahim A.E., Hraska V., et al. Use of a rapid deployment extracorporeal membrane oxygenation circuit for the resuscitation of pediatric cardiac patients. J Thorac Cardiovasc Surg 1998;116:305-311.[Abstract/Free Full Text]
  5. Walters H.L., Hakimi M., Rice M.D., Lyons J.M., Whittlesey G.C., Klein M.D. Pediatric cardiac surgical ECMO. Ann Thorac Surg 1995;60:329-337.[Abstract/Free Full Text]
  6. Black M.D., Coles J.G., Williams W.G., et al. Determinants of success in pediatric cardiac patients undergoing extracorporeal membrane oxygenation. Ann Thorac Surg 1995;60:133-138.[Abstract/Free Full Text]
  7. Glass P., Wagner A.E., Papero P.H., et al. Neurodevelopmental status at age five years of neonates treated with extracorporeal membrane oxygenation. J Pediatr 1995;127:447-457.[Medline]
  8. Towne B.H., Lott I.T., Hicks D.A., Healey T. Long-term follow-up of infants and children treated with extracorporeal membrane oxygenation (ECMO). J Pediatr Surg 1985;20:410-414.[Medline]
  9. Andrews A.F., Nixon C.A., Cilley R.E., Roloff D.W., Bartlett R.H. One- to three-year outcome for 14 neonatal survivors of extracorporeal membrane oxygenation. Pediatrics 1986;78:692-698.[Abstract/Free Full Text]
  10. Slonim A.D., Patel K.M., Ruttimann U.E., Pollack M.M. Cardiopulmonary resuscitation in pediatric intensive care units. Crit Care Med 1997;25:1951-1955.[Medline]
  11. Dembitsky W.P., Moreno-Cabral R., Adamson R.M., Daily P.O. Emergency resuscitation using portable extracorporeal membrane oxygenation. Ann Thorac Surg 1993;55:304-309.[Abstract]
  12. Doski J.J., Butler T.J., Louder D.S., Dickey L.A., Cheu H.W. Outcome of infants requiring cardiopulmonary resuscitation before extracorporeal membrane oxygenation. J Pediatr Surg 1997;32:1318-1321.[Medline]
  13. Newburger J.W., Jonas R.A., Wernovsky G., et al. Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. N Engl J Med 1995;332:549-555.[Abstract/Free Full Text]
  14. Bellinger D.C., Jonas R.A., Rappaport L.A., et al. Developmental and neurologic status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass. N Engl J Med 1995;332:349-355.
  15. Baumgart S., Streletz L.J., Needleman L., et al. Right common carotid artery reconstruction after extracorporeal membrane oxygenation. J Pediatr 1994;125:295-304.[Medline]
  16. McGahren E.D., Mallik K., Rodgers B.M. Neurological outcome is diminished in survivors of congenital diaphragmatic hernia requiring extracorporeal membrane oxygenation. J Pediatr Surg 1997;32:1216-1220.[Medline]
  17. Lazar E.L., Abramson S.J., Weinstein S., Stolar C.G.H. Neuroimaging of brain injury in neonates treated with extracorporeal membrane oxygenation. J Pediatr Surg 1994;29:186-191.[Medline]
Accepted for publication June 30, 1999.




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S. E. G. Hamrick, D. B. Gremmels, C. A. Keet, C. H. Leonard, J. K. Connell, S. Hawgood, and R. E. Piecuch
Neurodevelopmental Outcome of Infants Supported With Extracorporeal Membrane Oxygenation After Cardiac Surgery
Pediatrics, June 1, 2003; 111(6): e671 - 675.
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Ann. Thorac. Surg.Home page
B. W. Duncan
Mechanical circulatory support for infants and children with cardiac disease
Ann. Thorac. Surg., May 1, 2002; 73(5): 1670 - 1677.
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Ann. Thorac. Surg.Home page
A. S. Aharon, D. C. Drinkwater Jr, K. B. Churchwell, S. V. Quisling, V. S. Reddy, M. Taylor, S. Hix, K. G. Christian, J. B. Pietsch, J. K. Deshpande, et al.
Extracorporeal membrane oxygenation in children after repair of congenital cardiac lesions
Ann. Thorac. Surg., December 1, 2001; 72(6): 2095 - 2102.
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SEMIN CARDIOTHORAC VASC ANESTHHome page
E. B. Mossad
Introduction
Seminars in Cardiothoracic and Vascular Anesthesia, September 1, 2001; 5(3): 185 - 186.
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