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Ann Thorac Surg 2012;93:1584-1590. doi:10.1016/j.athoracsur.2012.01.008
© 2012 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

20-Year Experience of Prolonged Extracorporeal Membrane Oxygenation in Critically Ill Children With Cardiac or Pulmonary Failure

Punkaj Gupta, MBBSa,*, Rachel McDonald, BSb, Carl W. Chipman, CRNFAc, Michael Stroud, MDd, Jeffrey M. Gossett, MSe, Michiaki Imamura, MDc, Adnan T. Bhutta, MDa

a Section of Pediatric Cardiology and Critical Care, Department of Pediatrics, University of Arkansas Medical Center, Little Rock, Arkansas
c Section of Pediatric Cardiothoracic Surgery, Department of Pediatrics, University of Arkansas Medical Center, Little Rock, Arkansas
d Section of Pediatric Critical Care, Department of Pediatrics, University of Arkansas Medical Center, Little Rock, Arkansas
e Biostatistics Program, Department of Pediatrics, University of Arkansas Medical Center, Little Rock, Arkansas
b Department of Medical Education, University of Arkansas Medical Center, Little Rock, Arkansas

Accepted for publication January 6, 2012.

* Address correspondence to Dr Gupta, Division of Pediatric Cardiology, Department of Pediatrics, University of Arkansas for Medical Sciences, 1 Children's Way, Slot 512-3, Little Rock, AR 72202-3591 (Email: pgupta2{at}uams.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Extracorporeal membrane oxygenation (ECMO) is a rescue therapy for life-threatening respiratory or circulatory failure. Although outcomes are favorable with short-term ECMO therapy, data on the outcomes of prolonged ECMO therapy in children are very limited. This study aimed to study morbidity and mortality associated with prolonged ECMO therapy (≥28 days) in children with refractory cardiac or pulmonary failure.

Methods: We conducted a retrospective review of all children ≤18 years supported with ECMO for ≥28 days between January 1991 and September 2011 at the Arkansas Children's Hospital. The data collected in our study included patient demographic information; diagnosis; indication for ECMO; ECMO support details; medical and surgical history; laboratory, microbiologic, and radiographic data; information on organ dysfunction; complications; and patient outcomes. The outcome variables evaluated in this report included survival to ECMO decannulation, survival to hospital discharge, and current survival with emphasis on neurologic, renal, pulmonary, and other end organ function.

Results: During the study period, 984 events in 951 patients were supported with ECMO with a 30-day survival of 666 events (68%). Only 22 ECMO runs were ≥28 days and were eligible for inclusion in this report. The longest ECMO run in our series was 1,206 hours (50 days). The average length of ECMO run in this cohort was 855 ± 133 hours, with a mean intensive care unit length of stay of 56 ± 27 days. Ten patients (45%) were successfully decannulated from ECMO. Six patients (27%) were alive 30 days after decannulation, and only 4 patients (19%) survived to hospital discharge. Of the 4 survivors, only 3 patients (14%) are living to date. Of the 3 living children, 2 have significant neurologic issues with brain atrophy and developmental delay, and 1 is awaiting renal transplant; all 3 survivors have chronic lung disease.

Conclusions: This case series highlights that the prolonged use of ECMO in children with refractory cardiac failure, respiratory failure, or both is associated with low survival. Furthermore, it suggests that the survivors of prolonged ECMO runs have significant long-term sequelae.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Mechanical circulatory support in the form of extracorporeal membrane oxygenation (ECMO) is an invaluable tool in the care of children with severe refractory cardiac failure, pulmonary failure, or both [1–3]. ECMO, first introduced clinically in 1972, has been applied as a means of cardiopulmonary support for both neonatal and nonneonatal patients with potentially reversible cardiac failure, respiratory failure, or both in whom conventional medical strategies have been exhausted [4–7]. ECMO has served as rescue therapy for about two decades at our institution. Although there are multiple reports on the successful outcome of children with refractory respiratory and cardiac failure rescued by short-term ECMO therapy [1–7], only a few case reports have been published describing the short-term and long-term outcomes of prolonged ECMO therapy in children [8–14] (Table 1).


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  		Table 1 Published Studies on Prolonged Extracorporeal Membrane Oxygenation ≥28 Days in Children
 
The longest duration for any patient maintained by ECMO in published literature is 117 days. This report outlined the rescue of a 26-year-old drowning man with prolonged ECMO and without any permanent sequelae [15]. The longest duration of ECMO support mentioned in the pediatric literature is 48 days [9, 10]. These children were discharged from the hospital with significant neurologic deficits. We report our 20-year experience at Arkansas Children's Hospital with the use of prolonged ECMO in children with refractory cardiac or respiratory failure. The primary aim of this study was to evaluate the morbidity and mortality associated with prolonged ECMO therapy (≥28 days). The secondary aim of this study was to evaluate the end-organ complications associated with prolonged ECMO therapy.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
We conducted a retrospective review of all children 18 years old and younger supported with prolonged ECMO for refractory cardiac or pulmonary failure between January 1991 and September 2011 at the Arkansas Children's Hospital. We defined prolonged ECMO as lasting 28 days or longer (or ≥672 hours). The Institutional Review Board at University of Arkansas Medical Sciences approved review of patient medical records, and need for informed consent was waived. At our institution, the decision to deploy and wean ECMO is made by the attending intensive care unit (ICU) physician, who is responsible for overseeing all aspects of ECMO; the cardiac surgery attending cannulates the patient for ECMO. Patients who are unable to be weaned from ECMO because of persistent myocardial dysfunction, and who have no major end-organ injury, are typically evaluated by our transplantation team to determine their candidacy for heart transplantation. The ECMO team is available 24 hours a day at our institution and is staffed with 10 full-time-equivalent ECMO specialists.

The data collected in our study included patient demographic information; diagnosis; indication for ECMO; ECMO support details; medical and surgical history; laboratory, microbiologic, and radiographic data; information on organ dysfunction; complications; and patient outcomes. The outcome variables evaluated in this report included survival to ECMO decannulation, survival to hospital discharge, and current survival with emphasis on neurologic, renal, pulmonary, and other end-organ function. Bleeding was defined as cannulation site or surgical bleeding requiring surgical exploration [16]. Renal insufficiency was categorized on the basis of peak serum creatinine values exceeding 1.5 mg/dL (for all age groups) after deployment of ECMO or use of renal replacement therapy, including peritoneal dialysis, ultrafiltration, continuous venovenous hemodialysis, hemodialysis, or a combination of these therapies [16]. Patients with hepatic injury were defined as those with a peak aspartate aminotransferase or alanine aminotransferase value exceeding 500 IU/dL, and patients with pancreatic injury were defined as those with serum amylase values exceeding 500 U/L or serum lipase values exceeding 500 U/L that developed in the period after deployment of ECMO [16]. The presence of a positive blood culture and signs and symptoms consistent with sepsis was used to define septicemia during ECMO use. Chronic lung disease was defined as a need for chronic bronchodilator therapy, with a spongelike appearance of lungs on chest radiograph with or without a need for oxygen, mechanical ventilation, or both at home. Recovery of renal function was defined as return of blood urea nitrogen and creatinine levels within the age-appropriate range without any need for dialysis. Developmental delay was defined as inability to perform age-appropriate activity. Mechanical complications evaluated in our study included clots within the circuit, the cannula, or both; issues with the oxygenator, bladder, raceway, arterial cannulas, or venous cannulas; and pump malfunction.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Between 1991 and 2011, 984 events in 951 patients were supported with ECMO at our institution, with a 30-day survival of 666 events (68%). Of these 984 events, only 22 ECMO runs lasted 28 days or more and were deemed eligible for inclusion in this report. The longest ECMO run in our series was 1,206 hours (~50 days). The median age of patients in our cohort was 7 months (range, 1 day to 15 years). There were 8 boys (36%) and 14 girls (64%). The average length of ECMO run was 855 ± 133 hours, and the mean ICU length of stay was 56 ± 27 days. Ten patients (45%) were successfully decannulated from ECMO, with 6 patients (27%) undergoing orthotopic heart transplantation and 1 patient receiving a biventricular assist device. In our cohort, 6 patients (27%) survived 30 days, and 4 patients (19%) survived to hospital discharge. Of the 4 survivors, only 3 patients (14%) are living to date.

Patient Characteristics, Diagnoses, and Complications
Table 2 shows the demographics, baseline characteristics, indications for ECMO, and outcomes in children rescued with prolonged ECMO at our institution. Cardiac failure was the primary indication for ECMO in 15 patients (8 with postoperative low cardiac output syndrome and 7 with myocarditis, cardiomyopathy, or both), respiratory failure in 6 patients (all with acute respiratory distress syndrome), and both respiratory and cardiac failure in 1 patient (patient with pulmonary hypertension due to congenital diaphragmatic hernia). Three patients (14%) received ECMO during active cardiopulmonary resuscitation with chest compressions. Of these 22 patients, 15 patients (69%) had multiple organ system failure (≥4 organ systems). Eight patients (36%) required hemofiltration during the ECMO run, and 7 patients (31%) required dialysis during the ECMO run. After decannulation, 5 patients needed hemofiltration, and 4 patients needed dialysis. All 4 survivors needed dialysis after hospital discharge. Four patients (19%) experienced hepatic insufficiency, and 2 patients (9%) experienced pancreatic insufficiency during ECMO. Nine patients (41%) had documented positive blood cultures with signs and symptoms consistent with septicemia. Three patients had blood cultures positive for enterococci, 2 for Pseudomonas species, 2 for Escherichia coli, 1 for Serratia species, and 1 for Xanthomonas species. One patient had a mixed infection with enterococci and yeast. Another patient had a yeast infection from the site of ECMO cannulation.


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  		Table 2 Collated Patient Data for Patients Receiving Prolonged Extracorporeal Membrane Oxygenation Support
 
Neurologic complications were noted in 13 patients (59%), with 8 patients (37%) having evidence of hemorrhagic complications and 5 patients (23%) having evidence of thromboembolic complications. Bleeding complications varied from punctate hemorrhage to subdural, subarachnoid, and intraparenchymal hemorrhage. Thromboembolic events progressed to ischemic stroke in different portions of the brain, including frontal lobe, occipital lobe, basal ganglia, and parietal lobe. Severe brain atrophy was noted in 6 patients (27%) leading to extraaxial fluid collections in 4 patients (18%), with the need for surgical evacuation in 2 patients (10%). Clinical seizures were observed in 3 patients (13%), with the need for antiepileptic agents in all 3 patients. Although radiographic evidence of cerebral edema was noted in 2 patients (10%), no neurosurgical intervention was performed in these patients. Superior sagittal sinus thrombosis was noted in 1 patient (5%), and cerebral herniation occurred in 1 patient (5%).

Extraneurologic bleeding complications in the form of pericardial tamponade, pulmonary hemorrhage, gastrointestinal bleeding, bleeding from the oral and nasal cavity, and chest tube bleeding that required multiple surgical explorations were noted in 8 patients (36%). Extraneurologic thromboembolic complications such as ischemic bowel, focal infarction of the kidney, and ischemia changes to the extremities were noted in 3 patients (14%). Pulmonary complications, including pulmonary hemorrhage, hemothorax, pleural effusion, and chronic lung disease, were noted in 6 patients (27%). Gastrointestinal complications, including ischemic bowel, necrotizing enterocolitis, and gastrointestinal bleeding, were noted in 5 patients (23%).

Extracorporeal Membrane Oxygenation Cannulation and Complications
Table 3 demonstrates ECMO techniques and circuit complications. All patients in this report were supported by venoarterial ECMO. Before the initiation of ECMO support, 19 patients (86%) were supported by conventional mechanical ventilation, with only 3 patients (14%) receiving high-frequency ventilation. All successful decannulations were followed by transition to conventional mechanical ventilation after the termination of ECMO support. The majority of patients in our cohort were cannulated through the neck vessels (59%). All postsurgical cardiac patients were cannulated through thoracic sites—that is, the right atrium and the aorta (41%). The median number of circuit changes in our cohort was 5 (range, 3 to 8 circuits). One patient had right ventricle perforation during ECMO cannulation, 1 patient had venous cannula fatigue resulting in near fracture, and 1 patient had arterial cannula dislodgement leading to urgent replacement.


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  		Table 3 Collated Equipment Data for Patients Receiving Prolonged Extracorporeal Membrane Oxygenation Support
 
Outcomes
Only 4 patients (18%) survived to hospital discharge. One of these patients expired 23 days after hospital discharge as a result of presumed pulmonary aspiration. Of the 3 living children, 2 children (10%) have significant neurologic issues, with brain atrophy and developmental delay, and 1 patient (5%) is neurologically intact with no focal deficits. Renal function improved in 2 patients with return to nearly normal function, and 1 patient (5%) is awaiting renal transplantation. All 3 survivors (13%) have chronic lung disease, 1 survivor has chronic sinusitis, and 1 survivor has avascular necrosis of the femoral head.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The present case series demonstrates that prolonged ECMO for 28 days or more can be used in children with refractory cardiac or pulmonary failure with variable results; however, the survival rate is low and the rate of complications is very high. To our knowledge, this is the largest study to date reporting survival to decannulation and survival to hospital discharge for a pediatric cohort requiring ECMO for 28 days or more.

Improved survival has been reported with the use of ECMO in children with refractory cardiorespiratory failure. However, some patients may sustain significant cardiorespiratory failure despite prolonged ECMO support as a result of sustained and irreversible myocardial injury, pulmonary injury, or both; progression of underlying disease; failed or inadequate cardiac surgical procedures; or a combination of these. For these patients, the use of ECMO may fail to recover their cardiac function, pulmonary function, or both. In this cohort of children requiring prolonged ECMO for the management of cardiorespiratory dysfunction, we show poor survival to hospital discharge. Although recommendations have been set up for the initiation of ECMO support, indications for weaning and termination in the setting of prolonged refractory cardiorespiratory failure are scarce, and they vary among various centers. Most of the available literature on this topic is in the form of case reports or small case series, with a bias toward publishing only reports of surviving patients [8–14].

At our center, the 30-day survival for children receiving ECMO for fewer than 28 days is 68%. This is in sharp contrast to the 30-day survival rate of 27% in children who received prolonged ECMO for 28 days or more. In another single-center study of pediatric patients, Nehra and associates demonstrated that prolonged ECMO lasting longer than 400 hours was associated with lower survival (42% versus 55%) [1]. The low survival to hospital discharge (18%) in our cohort is comparable to the low survival rate in patients requiring repeated ECMO (25% to 27%) [17, 18]. It is speculated that the early institution of ECMO and a prolonged period of ECMO support can prevent repeated ECMO in patients with refractory cardiorespiratory failure [17, 18]. However, our data demonstrate that in refractory cardiorespiratory failure, even a prolonged run of ECMO may lead to similar results. Waiting for prolonged ECMO to allow healing of potentially recoverable lesions may lead to life-threatening complications and may even increase the risk of death.

For patients supported by ECMO, cardiac patients are known to have worse outcomes than respiratory patients. In a recent query from the International Registry for Extracorporeal Life Support Organization (ELSO), survival to hospital discharge was 75% in neonates with respiratory failure and 39% with cardiac failure. Similarly, the survival to hospital discharge in children was 56% for respiratory failure and 48% for cardiac failure [19, 20]. Similar trends are noted in published reports on prolonged ECMO in surviving children wherein the majority of children had illnesses caused by respiratory conditions (Table 1) [8–14]. However, our results demonstrate that cardiac patients supported with prolonged ECMO had better outcomes. In our cohort, 60% (9/15) of the patients supported by ECMO for cardiac failure were successfully decannulated, in contrast to no decannulation for patients supported for respiratory failure. Cardiac transplantation with ventricular assist device support remains the mainstay for successful decannulation in patients after prolonged ECMO. In our cohort, 60% (6/10) of patients undergoing successful decannulation received heart transplantation, and 10% (1/10) of the patients received support by a ventricular assist device. Therefore, in refractory cardiorespiratory failure, these modalities should be discussed earlier to prevent complications and end-organ damage.

As in other studies, the most common complications in this study were related to bleeding, thromboembolic events, and nosocomial infections [21–24]. Cerebral or other organ hemorrhage (pulmonary or gastrointestinal) forces the medical team to withdraw ECMO support in an effort to stop anticoagulation. This limits the time for myocardial recovery, pulmonary recovery, or both and eventually for withdrawal of care. In fact, prolonged ECMO use is known to increase the chance of nosocomial infection, which in turn is known to increase the duration of ECMO [25, 26]. In our study, 41% of patients had positive blood cultures, most of them after the first 2 weeks of ECMO. Although all the blood cultures cleared at the time of either withdrawal of care or decannulation, it is possible that the ECMO course in these patients was prolonged because of infection.

The three most common neurologic complications of ECMO in children include central nervous system hemorrhage, central nervous system infarction, and seizures. In a recent study from the ELSO registry, intracranial hemorrhage occurred in 7.4% of patients, cerebral infarction occurred in 5.7% of patients and clinically diagnosed seizures occurred in 8.4% of all ECMO-treated patients [27]. In our cohort receiving prolonged ECMO, the incidence of these complications was higher, with hemorrhage occurring in 37% of patients, cerebral infarction in 23% of patients, and clinical seizures in 13% of patients. Unremitting cardiorespiratory failure, multiple organ system failure, and a higher rate of complications were the most frequent causes of death in our patients. It has been suggested that the development of end-organ damage during ECMO support is associated with poor outcomes [28–31]. The increased mortality in our report may have been due to the fact that most of the end-organ system failure and complications happened during ECMO. Dialysis was used in one form or other in about 70% of our cohort. Given the small sample size in our report, it is difficult to predict an association of renal failure warranting dialysis with mortality. However, the available literature on this topic suggests that renal injury severe enough to require dialysis is strongly associated with increased mortality [28, 32–34]. Careful attention should be paid to maintaining good end-organ perfusion during ECMO, minimizing patient exposure to nephrotoxic medications, avoiding the induction of severe prerenal azotemia, and promptly recognizing and relieving abdominal compartment syndrome in the effort to help preserve renal function and improve outcomes [34].

Survivors after prolonged ECMO experience long-term sequelae such as developmental delay, neurologic deficits, chronic lung disease, renal insufficiency, and other end-organ dysfunction [8–14]. The data from this report have all the limitations of case series, but they may be viewed as a proof-of-concept study demonstrating the complications and outcomes of prolonged ECMO in pediatric patients. Despite the potential for improved survival with prolonged ECMO, one should candidly discuss the potential long-term sequelae in these children with their families.

This case series highlights that the prolonged use of ECMO in children with refractory cardiac failure, respiratory failure, or both is associated with low survival and a high complication rate. Furthermore, it demonstrates the long-term sequelae in survivors with prolonged ECMO. Careful selection of the patient population, a multidisciplinary team approach, and candid discussions with families regarding long-term sequelae are crucial for successful outcomes in children receiving prolonged ECMO for 28 days or longer.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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Invited Commentary
Ryan Davies and Mark Priest
Ann. Thorac. Surg. 2012 93: 1590-1591. [Extract] [Full Text] [PDF]



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Ann. Thorac. Surg., May 1, 2012; 93(5): 1590 - 1591.
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