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Ann Thorac Surg 2007;84:1349-1355
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Clinical and Psychosocial Follow-Up Study of Children Treated With Extracorporeal Membrane Oxygenation

Kari Wagner, MDa,*, Ivar Risnes, MD, PhDb, Torhild Berntsen, PsyDc, Anne-Britt Skarbø, PsyDc, Brith Ramberg, PsyDd, Inger Helene Vandvik, MD, PhDd, Magnhild Rasmussen, MD, PhDc, Terje Nome, MDd, Ketil Berg Olsen, MDd, Jan Ludvig Svennevig, MD, PhDb

a Department of Anaesthesiology, Rikshospitalet-Radiumhospitalet Medical Centre, Oslo, Norway
b Department of Thoracic and Cardiovascular Surgery, Rikshospitalet-Radiumhospitalet Medical Centre, Oslo, Norway
c Department of Pediatrics, Rikshospitalet-Radiumhospitalet Medical Centre, Oslo, Norway
d Division of Child and Adolescent Psychiatry, Radiology, and Neurology, Rikshospitalet-Radiumhospitalet Medical Centre, Oslo, Norway

Accepted for publication May 4, 2007.

* Address correspondence to Dr Wagner, Department of Anaesthesiology, Rikshospitalet-Radiumhospitalet Medical Centre, Oslo, 0027, Norway (Email: kari.wagner{at}rikshospitalet.no).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Conclusion
 References
 
Background: Serious heart and pulmonary failure may be treated with extracorporeal membrane oxygenation (ECMO). The aim of this follow-up study was a multimodal assessment of outcome in children surviving ECMO at our hospital from 1991 to 2004.

Methods: Twenty-two children were, on average, 1.18 years old (SD = 1.92; range, 0.1 to 7.8) when ECMO was initiated. Average age at follow-up was 7.2 years (range, 1.8 to 13.9). Thirteen children were treated for cardiac and nine for pulmonary failure. Venoarterial ECMO was performed in 21 patients and venovenous ECMO in one patient. The protocol included a review of patients records, clinical, neurologic and neuropsychologic, and radiological examinations, electroencephalogram, and interviews with the parents.

Results: Moderate or severe impairment in at least two clinical assessments were found in 16 (72.7%) children. Five (22.7%) children had cerebral palsy and 15 (68.2%) had moderate or severe cognitive impairment. Eight (36%) children had pathological radiologic findings. Pathological electroencephalograms were found in 11 (50%) patients including four (18.2%) with epileptic activity. Children with radiologic findings had a slightly worse cognitive outcome. There was no association between the neurophysiologic findings and the neuropsycohologic performance or the radiologic findings. Based on parental assessment, only four children had pathological scores.

Conclusions: All children, except for two, came walking to the follow-up visit. All parents were positive to the ECMO treatment, and reported a good or slightly reduced quality of life for their child. Cerebral sequelae were frequently found in children treated with ECMO. The need for treatment and support should be assessed in order to optimize their physical and psychosocial functioning.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Conclusion
 References
 
The severity of illness that precipitates the initiation of extracorporeal membrane oxygenation (ECMO), as well as the risks associated with the procedure itself, have raised concerns about morbidity among the survivors. Cerebral complications such as intracerebral hemorrhage, infarction, and hypoxia represent a major cause of the impairments [1–3]. Children surviving ECMO may have severe disabilities related to intracranial complications developed during ECMO treatment [4–7]. Cerebral injury in these patients may also be attributed to events and diseases prior to ECMO treatment. Alteration of cerebral blood flow, and the use of heparin, may also contribute to the high incidence of both hemorrhagic and nonhemorrhagic intracranial lesions [8–10]. These adverse effects place the ECMO survivor at a high risk of acquiring brain injury and subsequent functional deficits [11]. Limited knowledge is available regarding the late status of ECMO-treated children [12]. The aim of the present study was to assess the outcome of the 22 consequtive children, all severely affected either with pulmonary or cardiac failure, but no dysfunction of other organ systems, who survived ECMO treatment at our hospital in the period April 1991 to Feb 2004, and to relate the radiologic and clinical findings to their cognitive functions [13].


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Conclusion
 References
 
Patients and Procedures
Forty-nine children were treated with ECMO from April 1991 to Feb 2004. Twenty-four children died within 30 days (49%), another three patients suffered late mortality. The remaining 22 children were included in the study. The patients and procedures are presented in Table 1.


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  		Table 1 Patients and Procedures
 
The mean age when ECMO was initiated was 1.18 (± 1.92) years. There were eight neonates (0 to 28 days), six infants (28 days to 1 year), and eight pediatric (1 to 8 years) patients. The mean age at follow-up was 7.2 (±4.4) years. The patients were on ECMO a mean of 8.0 (±5.52) days. The diagnoses leading to ECMO are given in Table 1. Two cardiac patients (patients Nos. 12 and 17) were diagnosed with the 22q11 deletion syndrome. One patient was known to be moderate psychomotoric retarded prior to ECMO (patient No. 8). None of the children had Down syndrome. There were two cardiac arrests prior to ECMO treatment (patients Nos. 15 and 18). Thirteen cardiac patients were on ECMO a mean of 6.8 (2 to 14) days, versus a mean of 9.3 (2 to 25) days for nine pulmonary patients. The time on ventilator was a mean of 19.9 (range, 4 to 55) days and a mean of 13.6 (4 to 28) days for cardiac patients, versus a mean of 27.6 (8 to 55) days for pulmonary patients. Four cardiac patients on bypass were continued on ECMO after the operations due to low cardiac output (patients Nos. 2, 4, 19, 20). Eight cardiac patients needed ECMO one to two days after the operation due to low cardiac output (six patients: Nos. 1, 15, 16, 17, 18, 22) and due to oxygenation insufficiency (two patients: Nos. 12, 14). One patient with varicella acute respiratory distress syndrome (patient No. 21) had been operated due to Fallot five years earlier. Fast entry criterion for patients with respiratory failure was partial pressure of oxygen, arterial, less than 50 mm Hg for two hours with fraction of inspired oxygen equal to 1.0. All children below 10 kg were treated with venoarterial (VA) ECMO according to our ECMO protocol. The follow-up study was approved by The Regional Committee for Medical Research Ethics. Patients and (or) parents were informed and gave approval to the study.

Surgical Technique
Details of the ECMO procedure at our hospital using a centrifugal pump have been described by Pedersen and colleagues [14]. Biomedicus wire-reinforced arterial and venous cannulae, sized, respectively, at F8 and F10 or larger according to the childs weight (Medtronics Bio-Medicus Inc, Eden Prairie, MN) were used. The ECMO-cannulas were inserted percutanously into the femoral artery and vein (n = 1), directly by a sternum split (all the cardiac patients except for two patients) (n = 11), or by a cut down technique on the neck with ligation of the right carotid artery (n = 10). In one patient the carotid flow was reestablished after the ECMO treatment. The ECMO circuits were heparin-coated. Hemoglobin was kept above 12 g/dL, platelets kept above 100,000/µL, and antithrombin III (AT III) kept above 60% in children greater than one year of age and greater than 80% in children less than one year. To avoid hemolysis, the negative pressure on the inlet side of the centrifugal pump was not allowed to exceed 80 mm Hg [14].

Data Collection
Data were obtained from our medical database (Datacor), from the Extracorporeal Life Support Organization registry [15], and from the medical records.

Methods
A comprehensive assessment protocol included a medical history, physical examination, neurological and radiologic assessment (cerebral magnetic resonance imaging [MRI], computed tomography [CT] or ultrasound [US]), electroencephalography (EEG), and neuropsychologic assessment. In addition, the parents were interviewed. The type of radiologic assessment depended on what was possible to do without anesthesia. All the examinations were done at follow-up, on average six years after the ECMO run. The only exception was cerebral ultrasound done on four neonates just prior to, during, and the days after ECMO treatment. A functional categorization of the children was made based on general clinical, neurological, neuropsychologic assessments, and assessments by the parents.

Clinical Examination
A general medical history was based on the medical record, parent information, and a general clinical examination. Clinical physical function contained the following: 1 = normal, 2 = moderate impairment, 3 = severe impairment.

Neurological Examination
A standard neurological examination was performed. Muscle tone and power, balance, coordination, involuntary movements, deep tendon reflexes, and cranial nerve function were tested as far as the situation would permit and behavior and gross and fine motor milestones were assessed. The presence of epilepsy, vision, or hearing defects were determined mainly from the parent information or the case notes. The children were given a neurological score where 1 = none or insignificant impairment, 2 = mild-moderate impairment, and 3 = severe impairment. All the neurologic examinations were done at follow-up and by one pediatric neurologist.

Radiological Assessment
The US was done while the patient was on ECMO, and just after ECMO. Nonenhanced CT (NECT) and cerebral MRI were done in connection with the follow-up study. Fourteen patients underwent cerebral MRI examination, four patients cerebral NECT, and four patients cerebral US. The MRI examinations were performed with Siemens Vision 1.5 T or Siemens Harmony 1.0 T (Siemens, Erlangen, Germany). White matter hyperintensities were graded as either within normal range or pathological. Cerebral infarcts were defined as low signal intensity areas measuring more than 10 mm on T1 images, with high signal on T2, and with signal changes consistent with perifocal gliosis and (or) cystic necrosis on fluid attenuation inversion recovery images. The presence of blood products and widening of cerebral fluid spaces were noted. The brain CT examinations were performed on a single slice CT (General Electric Medical Systems, Milwaukee, WI). The CT examinations were evaluated with respect to infarctions, blood products, and cerebral fluid spaces.

The brain US examinations were performed on an ATL HDI 3000/5000 scanner with curved probe 5 to 8 MHz and linear probe 7 to 12 MHz. The US examinations were evaluated with respect to hemorrhage, ventricular size, and infarctions. The MRI and CT images were interpreted retrospectively by one neuroradiologist on either hard copies or on a PACS (picture archive and communication system) workstation (SECTRA AB, Linkoping, Sweden). The neuroradiologist was blinded with regard to the patients’ clinical status and duration of ECMO treatment.

EEG Assessment
Resting scalp EEGs were obtained from all patients. Depending on age, 11 patients were examined with 17-channels-EEG, 11 with 21-channels-EEG (the international 10–20 system). Phototopic stimulation and hyperventilation were not included. The EEGs were interpreted by one neurophysiologist.

Neuropsychologic Assessment
Different neuropsychologic tests were used according to age. The five children under three years of age were assessed with the Bayley Scales of Infant Development, mental scale BSID II [16]. Seven children, aged three to seven years, were tested with the Wechsler Preeschool and Primary Scale of Intelligence Revised, WPSSI-R [17] and the neuropsychologic assessment (NEPSY) [18]. The Wechsler Intelligence Scale for Children III (WISC III) [19] was used for assessment of general cognitive ability in ten children older than seven years. Additional tests for the older children were the following: finger tapping test [20] and a grooved pegboard [21] for assessment of fine motor tempo and coordination. Knox cubes were used for assessment of short-term visual memory-attention span [22], for psychomotor skills, the symbol digits modalities test [23], and for auditory memory, the Rey auditory verbal learning test [24]. Visual memory-organizational abilities were assessed with the Rey complex figure test [25], and verbal fluency with the F-A-S (letters) controlled oral word association test [26]. Individual scores were compared with available, and widely used, age-approriate norms.

Based on the neuropsychologic test results, the children were given a composite score in three categories: no disability, mild-moderate disability, or significant disability. Children given composite score 1 had normal cognitive function; ie, their results on neuropsychologic tests were within normal range. Children given composite score 2 had mild or moderate cognitive disability; ie, their results were between 1 and 2 standard deviation (SD) below average in three or less cognitive domains. Children given composite score 3 had significant cognitive disability; ie, their results were 2 SDs or more below average in three or more cognitive domains.

Parental Assessment
Nineteen mothers and three fathers completed the child behavior checklist (CBCL) version for children 1.5 to 5 years or 6 to 18 years [27]. The checklist provides a total behavior score covering behavior and emotional problems. For 12 children (age, 6 to 13 years) the attention deficit-hyperactivity disorder (AD/HD)-rating scale IV, home version, was completed. The clinical cutoff for CBCL and the AD/HD-rating scale was 1.5 SD above average scores [28]. Based on these questionnaires, the children were categorized in three functional groups: normal or insignificant behavioral difficulties (total score on both tests in the normal range); moderate behavioral difficulties (total score on one test in the clinical range); severe behavioral difficulties (total score in the clinical range on both tests).

The pediatric quality of life inventory (Peds QL TM40) for age 2 to 18 years is a multidimensional scale encompassing physical, emotional, social, and school functioning. The Peds QL was completed by the parents of all children. According to American norms, the clinical cutoff is 1 SD under the average score [29].

Statistical Methods
Comparison of proportions was performed using the {chi}2 test. Continuous nonparametric distributed variables were evaluated using the Mann-Whitney test and the Spearman r correlation coefficient, and continuous parametric data using the Student test. The level of statistical significance was a p value of 0.05 or less. The statistical analysis was performed using the SPSS program version 11 (SPSS, Chicago, IL). The data are presented as mean values ± SD or range.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Conclusion
 References
 
Clinical Findings
All children came walking to the examinations. Pathological respiratory sounds were found in two children with asthma and tracheal stenosis in one. A systolic murmur was found in six children, of which five were on medication for cardiac insufficiency. One patient (patient No. 2) was severely affected because of cardiac impairment and died a few months after the study was finished. No cyanosis or heart arrthymia were found. Hemiparesis was found in five children, all on the right side. One child with left-sided CDH, whose left lung had been removed, showed a serious scoliosis. Five children showed different signs of hyperactivity, mental retardation, concentration problems, and delayed psychomotor development.

The clinical function scoring was based on signs of heart and lung failure, growth impairment, and reduced physical activity. Neurological impairment was not included in the clinical scoring, but assessed separately. Seven (32%) children had normal clinical functions. Eleven (50%) patients had moderate clinical impairment and four patients were severely affected (18%).

Neurological Findings
Normal motor function was found in six children (27.3%), mild or moderate neurological affection in ten children (45.4%), and severe impairment in six children (27.3%). Five (23%) children had cerebral palsy. They had a right-sided hemiplegia, and three of them were severely affected. Three children (13.6%) (patients Nos. 4, 8, 11) were on antiepileptic medication. All had a severe motor disturbance as well. One of the patients with cerebral palsy, prematurely born (26th week), suffered a large left-sided infarct during ECMO treatment, and later developed severe epilepsy and was hemispherectomized. Five children were microcephalic, with head circumference below the 2.5th percentile. Visual problems, mostly strabismus or refraction failure, were reported in 11 (50%) patients. Two of them had temporary blindness. Chronic hearing loss was not reported in any of the children.

Radiological Findings
All US (n = 4) and NECT (n = 4) examinations were normal. The MRI examinations (n = 14) revealed findings consistent with cerebral ischemic injury in eight (36%) patients. One patient with a 22q11 deletion syndrome (patient No. 17), had abnormal neuronal migration and cortical organization, but no sign of ischemic injury. Cerebral infarctions were documented in five paients (Fig 1). Extensive white matter hyperintensities consistent with ischemic injury were found in two patients. One patient demonstrated atrophy and extensive signal abnormalities in the basal ganglia after global ischemia (Fig 2).


Figure 1
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  		Fig 1. Axial T2 weighted image from follow-up MRI shows a complete infarction of the left middle cerebral artery territory.

 

Figure 2
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  		Fig 2. Axial T2 weighted image shows atrophy and extensive signal abnormalities in the basal ganglia due to global ischemia.

 
EEG Findings
Pathological changes were seen in 11 (50%) patients, with epileptic activity in four children (18.2%). Epileptic activity in the left hemisphere was found in three patients. Epileptic activity in the right hemisphere was found in one patient after hemispherectomy.

Neuropsychologic Findings
Normal cognitive function was found in seven (31.8%) children and mild cognitive disability in five (22.7%) children, while significant cognitive disability was found in ten (45.5%). A mean IQ/MDI (mental developmental index)-score for the whole group was 74.7 (SD 26.7, range 39 to 114); data were missing for one child. For the five children below three years, the mean MDI-score as estimated by BSID II was 58.8 (SD 11.9; range, 49 to 78). The youngest children were tested with Bayley scales only.

For six children with scores in the normal range, the mean IQ-score was 107.8 (SD 6.6; range, 99 to 114). No significant difference was found between performance IQ (mean 103.5; SD 9.1; range, 94 to 117) and verbal IQ (mean 108.8; SD 7.6; range, 101 to 123).

Clinical Severity Score
Clinical severity score (CSS) was defined as the average of the three evaluations: clinical-physical, neurological, and cognitive function tests. Cognitive functions were the following: 1 = normal, 2 = moderate cognitive disability, 3 = severe cognitive disability. Ten children (45.5%) obtained CSS greater than 2.0.

Parental Scoring
Four (18%) children (mean age 9.9 years; range, 6 to 13) with pathological scores were assessed by the parents as having behavioral difficulties. Eight (36%) parents rated their child as having a reduced quality of life, which included both physical and psychosocial functioning. None of the parents regretted that their child had been treated with ECMO. In general the parents were positive to the follow-up study. Comparing the parents’ scores with the neuropsychologic-developmental assessment (cognitive.func), revealed full agreement in eight (36%) cases. Fourteen (64%) children were assessed as more disabled by the psychologists than by the parents. Comparison of the parents’ scores with the CSS revealed full agreement in nine (41%) cases, whereas 12 (55%) children were assessed as more disabled by the psychologists than by the parents. One child (4%) was assessed as more disabled by the parents than the neuropsychologic evaluation indicated. In spite of the good parental evaluations, 19 of the families received basic economic support, which is intended for parents of children who need more help and support than healthy children. Thirteen children received supplementary support in kindergarten or school. Four children were referred for further evaluation interventions.

Correlations
There was no correlation between the neurological sequelae or the CSS and the duration of ECMO. Further, there was no correlation between the neuropsychologic performance or the radiologic findings and the EEG (Table 2).


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  		Table 2 Neuroradiologic, Neurophysiologic, Clinical, Neuropsychologic, and Parental Scoring
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Conclusion
 References
 
We found various degrees of neurological impairment in 72.7% of the patients, whereas Ibrahim and colleagues [13] found 59% neurologic impairment in pediatric patients after cardiac ECMO. The patient material is small; however, all patients underwent extended clinical and psychosocial testing. Our follow-up study revealed a normal neuropsychologic function in seven (31.8%) children, mildly impaired function in five (22.7%), and severe impairment in ten (45.4%). The outcome status of our children revealed more serious functional deficits than reported by the UK Collaborative Randomized Trial [2] which reported 76% normal cognitive function in survivors after neonatal ECMO followed up at seven years of age. Regarding cognitive function there was agreement between parents and psychologists on the evaluation of only eight children. The reason for this discrepancy could be that most of the children were preschoolers and their psychosocial problems were not yet very evident. The child with the poorest outcome in the neuropsychologic and cognitive testing suffered severe cardiac insufficiency and died after the study was completed. The five children below three years, tested with Bayley scales, had significantly lower scores of general cognitive ability than the group as a whole. Because the number of children younger than three years is low, and because BSID ll was the sole instrument for assessing these children, the reliability of this test is thus uncertain.

In contrast to Ikle and colleagues [30], we did not find significant differences between results on performance IQ and verbal IQ, or areas of unusual strength or weakness on IQ subtest scores. Impaired psychosocial functioning has also been seen in children with congenital heart disease after open heart surgery without ECMO [31]. Our follow-up disclosed that four children and their families needed more support and they were referred for further evaluation. This is in accordance with the UK Collaborative Trial Group underlining the need for professional support to children treated with ECMO [2]. None of the parents regretted the ECMO treatment, even if the outcome was poor [12]. However, other ethical aspects [32] were not discussed in the present work.

Eight patients (36%) had MRI findings consistent with cerebral ischemic injury. These results correspond with the results in adult patients, where radiologic lesions were seen in 50% [33]. Other ECMO centers perform radiologic tests to evaluate possible intracerebral lesions. Lidegran and colleagues [6] reported 31% significant CNS findings on cerebral CT scans. Abnormal EEGs were recorded in 11 (50%) of our patients; of these, three were on antiepileptic treatment. Epileptic activity was seen in four (18.2%) children.

Our findings indicate the importance of neurophysiologic testing of children after ECMO. Other studies confirm pathological EEG findings in ECMO-treated patients [33]. All children in the study, except one, were treated with VA ECMO. In adult ECMO patients, cerebral injuries were reported more frequently after VA ECMO (75%) than after VV ECMO (7%) [33].

Cerebral lesions after ECMO treatment may be found on either side [9, 10]. Despite the right-sided carotid artery ligation in ten patients, in all patients with cerebral palsy the hemiplegia was found on the right side. A left-sided cerebral infarction was found in four of these patients. Mendoza and colleagues [10] found most of the hemorrhagic lesions on the side opposite to the carotid ligation. Microcephaly was found in five children, three were diagnosed with complex CHD. It is uncertain to which extent the impaired clinical and psychosocial functioning are due to the disease or to the ECMO treatment per se. Wernovsky [34] found that chronic fetal cerebral hypoxemia and abnormal cerebral flow patterns in complex CHD may have an implication for cerebral development and preoperative neurological morbidity, seen in neonates with CHD. Thirteen patients with complex CHD had been treated with open heart surgery prior to ECMO and the original diagnoses may have contributed to the poor cerebral development.


   Conclusion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Conclusion
References
 
The parents considered 12 (54%) of the children to have no, or insignificant, difficulties and a good quality of life. At follow-up we found clinical impairment in 15 (68%) children. Neurological tests revealed impairment in 16 (72.7%) patients. Cerebral radiologic findings were seen in eight (36%) children. The EEG revealed abnormal findings in 11 (50%) patients. Fifteen (68%) children had cognitive disabilities that may affect their everyday life negatively. Many patients will need special education and training programs. It is essential to identify these patients as early as possible and refer them to specialized neuropsychologic assessment. Although most of the younger children behave normally and their language and conversational skills may seem within normal limits, a closer scrutiny of their cognitive abilities detected serious problems. After successful surgical treatment it is important that the development of the children is closely monitored. The parents’ judgment is not sufficient. Specialists are needed to uncover sequelae.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Conclusion
 References
 

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Kirk R. Kanter
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