Original Article
Developmental and Neurologic Status of Children after Heart Surgery with Hypothermic Circulatory Arrest or Low-Flow Cardiopulmonary Bypass
N Engl J Med 1995; 332:549-555March 2, 1995
- Abstract
Background
Deep hypothermia with either total circulatory arrest or low-flow cardiopulmonary bypass is used to support vital organs during heart surgery in infants. We compared the developmental and neurologic sequelae of these two strategies one year after surgery.
Methods
Infants with D-transposition of the great arteries who underwent an arterial-switch operation were randomly assigned to a method of support consisting predominantly of circulatory arrest or a method consisting predominantly of low-flow bypass. Developmental and neurologic evaluations and magnetic resonance imaging (MRI) were performed at one year of age.
Results
Of the 171 patients enrolled in the study, 155 were evaluated. After adjustment for the presence or absence of a ventricular septal defect, the infants assigned to circulatory arrest, as compared with those assigned to low-flow bypass, had a lower mean score on the Psychomotor Development Index of the Bayley Scales of Infant Development (a 6.5-point deficit, P = 0.01) and a higher proportion had scores <80 (i.e., 2 SD or more below the population mean) (27 percent vs. 12 percent, P = 0.02). The score on the Psychomotor Development Index was inversely related to the duration of circulatory arrest (P = 0.02). The risk of neurologic abnormalities increased with the duration of circulatory arrest (P = 0.04). The method of support was not associated with the prevalence of abnormalities on MRI scans of the brain, scores on the Mental Development Index of the Bayley Scale, or scores on a test of visual-recognition memory. Perioperative electroencephalographic seizure activity was associated with lower scores on the Psychomotor Development Index (P = 0.002) and an increased likelihood of abnormalities on MRI scans of the brain (P<0.001).
Conclusions
Heart surgery performed with circulatory arrest as the predominant support strategy is associated with a higher risk of delayed motor development and neurologic abnormalities at the age of one year than is surgery with low-flow bypass as the predominant support strategy.
Media in This Article
Figure 1
Score on the Psychomotor Development Index at One Year as a Function of the Duration of Total Circulatory Arrest.Figure 2
Estimated Probability of a Possible or Definite Neurologic Abnormality at One Year as a Function of the Duration of Total Circulatory Arrest.Article Activity
- Article
Deep hypothermia with total circulatory arrest is a method of support for vital organs that is often used during the repair of complex congenital heart abnormalities in infants. The maximal duration of circulatory arrest that will not result in impairment of the central nervous system is uncertain.1,2 Few data are available on the developmental and neurologic sequelae of the most important alternative support strategy, continuous low-flow cardiopulmonary bypass.3
In 1988 we began a randomized clinical trial to compare the incidence of brain injury in children with D-transposition of the great arteries undergoing an arterial-switch operation after assignment to a strategy consisting predominantly of circulatory arrest with that in children assigned to a strategy consisting predominantly of low-flow cardiopulmonary bypass. In the early postoperative period, the infants assigned to circulatory arrest had a higher incidence of neurologic morbidity than those assigned to low-flow bypass, including a higher incidence of seizures and ictal activity on continuous electroencephalographic (EEG) monitoring, a longer time to the reappearance of normal brain EEG activities, and release of greater amounts of the brain isoenzyme of creatine kinase.4 In this report we compare the developmental and neurologic status of the children in the two groups at one year.
Methods
Between April 1988 and February 1992, we enrolled 171 patients in a prospective, randomized, single-center trial. The eligibility criteria included a diagnosis of d-transposition of the great arteries with either an intact ventricular septum or a ventricular septal defect, a scheduled repair to be performed by three months of age, and coronary-artery anatomy considered suitable for the arterial-switch operation. Exclusion criteria included a birth weight below 2.5 kg, a recognizable syndrome of congenital anomalies, associated extracardiac anomalies that were moderate or severe, previous cardiac surgery, or associated cardiovascular anomalies requiring reconstruction of the aortic arch or additional open surgical procedures. Informed consent was obtained from the parents of all the infants. Additional information about the study design, perfusion methods, surgical techniques, and anesthetic management was presented previously.4
Information on family characteristics5,6 was obtained from interviews with the parents. Prenatal and perinatal data were also recorded. Examination of the children at the age of one year was performed by investigators who were unaware of the treatment assignment or clinical course.
Developmental Testing
All assessments were conducted at 8 a.m. Two examiners administered the Bayley Scales of Infant Development,7 which yield scores on two indexes: the Psychomotor Development Index and the Mental Development Index. We also calculated the proportion of children whose scores were less than or equal to 80 (approximately 2 SD below the current mean scores on the 1969 version of this test8). An evaluation of interexaminer reliability (13 infants) showed that the examiners were in agreement for 99 percent of the individual items, and correlations between the raw scores were higher than 0.99.
The Fagan Test of Infant Intelligence,9 which assesses visual-recognition memory, was also administered. The mean novelty-preference score (percentage of time spent looking at a novel stimulus) was computed, and children with scores lower than 53 percent were considered to have failed the test.9
Neurologic Examination
Neurologic examinations were performed by a pediatric neurologist using the format derived from the National Collaborative Perinatal Project. Findings were classified as normal, possibly abnormal, or definitely abnormal. Abnormalities were subclassified according to type (cerebral palsy, tone alteration, ataxia or dysmetria, focal abnormalities, and abnormalities of the special senses).10-13 Children who had cerebral palsy were excluded from classification in other categories.
Magnetic Resonance Imaging
Patients underwent magnetic resonance imaging (MRI) of the brain with a 1.5-tesla system (General Electric Medical, Milwaukee). We used conventional spin–echo techniques, including sagittal T1-weighted images (repetition time, 600 msec; echo time, 15 msec; number of signals averaged [NSA], 2) and axial proton-density–weighted and T2-weighted images (repetition time, 2000 msec; echo time, 90 msec; NSA, 2). A slice thickness of 5 mm was used with 1.0 to 2.5 mm of spacing between slices and a 24-cm field of view. Gadolinium enhancement was not used.
Two pediatric neuroradiologists independently assessed structural and intensity abnormalities. The findings were classified as normal, possibly abnormal, or definitely abnormal (mild, moderate, or severe). Abnormalities were subclassified as diffuse (ventricular dilatation, delayed myelination or maturation, or periventricular leukomalacia), focal or multifocal (atrophy or intensity abnormality of gray or white matter), or developmental (incidental). In cases of conflicting assessments (14 percent of the studies, with 4 percent frank disagreement), the two examiners reached an agreement.
Statistical Analysis
The two treatment groups were compared in intention-to-treat analyses. Secondary analyses examined the effect of the duration (in minutes) of total circulatory arrest on the outcome. All tests of hypotheses and regression analyses of outcome variables were adjusted for the diagnosis (i.e., intact ventricular septum or ventricular septal defect). Adjustment for the surgeon or for an interaction between the surgeon and the treatment did not alter the results.
The outcomes at one year included both continuous and categorical variables. Multiple linear-regression methods and Wilcoxon rank-sum tests were used to analyze continuous variables. Stratified exact tests14 and multiple logistic-regression methods were used to analyze categorical variables.
Scores on the Bayley Scales were expressed in two ways. First, the standard scores on the Psychomotor Development Index and the Mental Development Index were derived.7 Second, for each scale, the numbers of items passed were totaled and adjusted for age at the time of examination by means of an analysis of covariance. This approach adjusts for imbalances between treatment and diagnostic groups in the assignment of children to the age intervals used to derive standard scores.
For some children, not all outcome scores were available. Analyses were based on scores on the Psychomotor Development Index for 142 children and on scores on the Mental Development Index for 143 children. One child was too distressed for the administration of any developmental tests. Testing of another child had to be terminated before completion of the Psychomotor Development Index. A third child, later found to be autistic, could not be tested because of reduced social relatedness. In addition, before data analysis and without knowledge of the treatment assignments, a decision was made to exclude the developmental scores of the first 10 children who returned for examinations at one year. We had enrolled these 10 children to demonstrate our ability to assign children randomly to treatment groups at the time of surgery. At one year, these infants were evaluated under conditions that were not standardized in terms of time, location, and the children's condition. The National Institutes of Health Data and Safety Monitoring Committee for the trial approved our decision not to include these children in analyses of developmental end points.
Analyses of the Fagan test are based on the scores of 107 children. Twenty children were excluded because they were not within the age range of 11 to 13 months at the time of examination. Seventeen children had incomplete tests because of their inability to cooperate. (The 10 children first enrolled and the autistic child were also not included.)
Neurologic examinations were completed for 154 children, and MRI examinations for 142. The most common reason for the unavailability of MRI scans was parental refusal to grant consent. The percentages of children for whom data were not available for the different end points did not differ significantly according to whether they underwent surgery with circulatory arrest or low-flow bypass.
Results
Of the 171 infants enrolled in the trial, 168 were alive at one year of age, and 155 (92 percent) returned for evaluation. Seventy-six percent were boys, and 89 percent were white. Of the 13 infants who did not return for the one-year evaluation (7 assigned to circulatory arrest and 6 to low-flow bypass), 9 did not return because their parents decided not to participate, 2 could not be located, and 2 were living in other countries. The children who returned for evaluation did not differ significantly from those who did not with respect to sociodemographic factors, intraoperative perfusion variables, or preoperative and postoperative neurologic status. However, the children who did not return had a longer median period of intubation (3.4 vs. 2.9 days, P = 0.02 by the Wilcoxon test) and a longer median hospital stay (11 vs. 9 days, P = 0.08 by the Wilcoxon test).
Of the children who returned for evaluation, 120 (77 percent) had an intact ventricular septum, and 35 (23 percent) had a ventricular septal defect (Table 1Table 1
Characteristics of Infants with d-Transposition of the Great Arteries, According to Ventricular Septal Status and Treatment Group.). Treatment groups for each diagnosis were similar with respect to preoperative variables, sociodemographic variables, and interim medical history. However, the infants with a diagnosis of ventricular septal defect were older at the time of surgery, making it difficult to distinguish the independent contributions of age at the time of surgery and diagnosis to the status at one year. The treatment groups did not differ in terms of age-adjusted weight or length at one year.During the period between the neonatal arterial-switch operation and the one-year evaluation, 78 children (51 percent of those for whom data were available) underwent cardiac catheterization, and 1 child (who had an intact ventricular septum and was assigned to low-flow bypass) underwent additional cardiac surgery. At the time of the one-year evaluation, 11 children (7 percent) were receiving digoxin, and 2 (1 percent) were receiving diuretics. No child had nonfebrile seizures after hospital discharge. Two children (1 percent) had febrile seizures; neither had seizures detected clinically or by EEG monitoring in the perioperative period.
Developmental Testing
Psychomotor Development Index
The mean (±SD) score on the Psychomotor Development Index for the two treatment groups combined was 95.1±15.5. Scores were significantly lower among the children assigned to circulatory arrest (mean difference between the two groups, 6.5 points; 95 percent confidence interval, 1.6 to 11.5; P = 0.01) (Table 2Table 2
Scores on Developmental Tests, According to Ventricular Septal Status and Treatment Group.). Lower scores were also associated with a longer duration of circulatory arrest (P = 0.02) (Figure 1Figure 1Score on the Psychomotor Development Index at One Year as a Function of the Duration of Total Circulatory Arrest.). None of various nonlinear or piecewise linear models of this association fit the data significantly better than did a linear model. With adjustment for age at the time of examination, the number of scale items passed was lower for children assigned to circulatory arrest (P = 0.003) and was inversely related to the duration of circulatory arrest (P = 0.008). Twenty percent of the children (28 of 142) had a score less than or equal to 80. Lower scores were more prevalent among the children assigned to circulatory arrest (27 percent vs. 12 percent; exact P = 0.02) and those with a longer duration of circulatory arrest (P = 0.03).The effect of the treatment assignment on scores on the Psychomotor Development Index could not be explained by any of the perioperative or sociodemographic variables measured. In multiple-regression models, scores were positively related to birth weight, but adjustment for this variable did not appreciably alter the treatment-group effect. A diagnosis of ventricular septal defect was an independent risk factor for a lower score (mean difference between the two groups, 6.6 points; 95 percent confidence interval, 0.7 to 12.6; P = 0.03).
Mental Development Index
The score on the Mental Development Index for the two treatment groups combined was 105.1±15.0. Scores tended to be lower among children assigned to circulatory arrest (mean difference, 4.1 points; 95 percent confidence interval, -0.7 to 8.8; P = 0.10) (Table 2), although the scores did not decrease significantly with an increased duration of circulatory arrest (P = 0.33). With adjustment for age at the time of examination, the number of scale items passed was lower among children assigned to circulatory arrest (P = 0.04) but was not significantly related to the duration of circulatory arrest (P = 0.16). Of the eight children with scores less than or equal to 80, six were assigned to circulatory arrest (exact P = 0.27). In multiple-regression models, lower scores on the Mental Development Index were significantly associated with a lower level of maternal education, but adjustment for this variable did not appreciably alter the treatment-group effect. A diagnosis of ventricular septal defect was an independent risk factor for a lower score (mean difference, 8.6 points; 95 percent confidence interval, 2.8 to 14.4; P = 0.004).
Fagan Test of Infant Intelligence
The mean novelty-preference score for the two groups combined was 58.8±7.6 percent. Scores were not related to the treatment assignment (Table 2) or the duration of circulatory arrest. A diagnosis of ventricular septal defect was associated with lower scores (mean difference, 3.6 percent; 95 percent confidence interval, 0.2 to 7.0; P = 0.04).
Although 21 percent of the children (23 of 107) had test scores indicating failure (i.e., less than 53 percent), the percentage of such scores did not differ significantly according to the treatment group (circulatory arrest, 25 percent; low-flow bypass, 17 percent) or diagnosis (intact ventricular septum, 19 percent; ventricular septal defect, 29 percent). Inability to complete the test was not associated with the treatment assignment.
Neurologic Examination
Five of the 154 children who underwent neurologic examination (3 percent) had possible abnormalities, and 48 (31 percent) had definite abnormalities, all of which were judged to be mild. Neurologic abnormalities tended to be more common among the children assigned to circulatory arrest than among those assigned to low-flow bypass (41 percent vs. 28 percent; exact P = 0.09) (Table 3Table 3
Neurologic Outcomes According to Ventricular Septal Status and Treatment Group.). Similarly, possible or definite neurologic abnormalities were associated with a longer duration of circulatory arrest (P = 0.04) (Figure 2Figure 2Estimated Probability of a Possible or Definite Neurologic Abnormality at One Year as a Function of the Duration of Total Circulatory Arrest.). A low Apgar score at five minutes and a young gestational age were both independent risk factors for neurologic abnormalities, but adjustment for these factors did not appreciably affect the estimate of the increased risk associated with assignment to circulatory arrest. A total of 28 children (18 percent) had hypotonia, 12 (8 percent) had hypertonia, 7 (5 percent) had cerebral palsy, 4 (3 percent) had focal abnormalities, and 2 (1 percent) had abnormalities of special senses. The occurrence of specific abnormalities was not associated with the treatment assignment or the duration of circulatory arrest.Magnetic Resonance Imaging
Eleven of the 142 children (8 percent) who underwent MRI had possible abnormalities, and 22 (15 percent) had definite abnormalities, which were judged to be mild in 86 percent of these children. The abnormalities were classified as focal or multifocal in 20 children, diffuse in 16, and developmental or incidental in 3 (i.e., left temporal lobar hypoplasia, Chiari type I malformation, or a small arachnoid cyst in the left sylvian fissure).
The prevalence of possible or definite abnormalities was not related to the treatment assignment, the duration of circulatory arrest, or an associated diagnosis of ventricular septal defect. Preoperative acidosis, however, was a significant risk factor for abnormalities detected on MRI scanning.
Relation between Perioperative Seizure Activity and Status at One Year
During the first 48 hours after surgery, the infants assigned to circulatory arrest had a significantly higher risk of seizure activity, detected by continuous EEG monitoring, than the infants assigned to low-flow bypass.4 In regression analyses with adjustment for the treatment group and the presence or absence of a ventricular septal defect, the occurrence of EEG seizure activity in the early postoperative period was associated with a mean reduction of 11.2 points on the Psychomotor Development Index (P = 0.002) and with a significantly higher risk of possible or definite abnormalities on MRI scanning (odds ratio, 9.4; 95 percent confidence interval, 2.7 to 32.3; P<0.001). The children assigned to circulatory arrest also had an increased risk of clinical seizures in the early postoperative period.4 Despite the limited statistical power of the analysis, the occurrence of clinical seizures was associated with an increased risk of possible or definite neurologic abnormalities at one year (P = 0.05).
Discussion
We found that a strategy of support consisting predominantly of circulatory arrest during open-heart surgery in infants, as compared with a strategy consisting predominantly of low-flow cardiopulmonary bypass, was associated with worse performance on tests of developmental and neurologic function at the age of one year. Moreover, longer duration of circulatory arrest was associated with increased risk of delayed psychomotor development and neurologic abnormalities at one year. The magnitude of the effect was modest, since the difference between the scores on the Psychomotor Development Index for the two treatment groups was approximately 0.4 SD. However, trends toward a more favorable outcome for children assigned to low-flow bypass were evident for many of the end points measured. These findings are consistent with the higher risk of neurologic morbidity in the early postoperative period previously reported for the children randomly assigned to circulatory arrest.4 In addition, seizure activity detected on continuous EEG monitoring during the early postoperative period and a diagnosis of ventricular septal defect were independent risk factors for a poor outcome.
The duration of circulatory arrest that is safe (the period during which no irreversible central nervous system damage occurs) is unknown. Studies in animals suggest that periods of arrest that are shorter than 30 minutes at brain temperatures of 15 to 20°C do not result in permanent structural or functional damage.1,15 In follow-up studies of children who had undergone open-heart surgery,3,16-23 developmental impairment was associated with periods of arrest that were longer than 60 minutes (at brain temperatures of 18 to 20°C) and possibly with periods as short as 45 minutes. Modifying factors may include the depth of hypothermia, the nature of the cooling process, cerebral blood flow during cooling and rewarming, and blood pH values and arterial carbon dioxide tension during cooling.3,24
Although we were unable to determine a threshold for the duration of circulatory arrest below which no increase in risk was evident, the data are consistent with the hypothesis that a period shorter than 35 minutes (at 18°C) has a minimal adverse effect on scores on the Psychomotor Development Index at one year. Substantial deficits seemed to be most prevalent among the children with circulatory-arrest periods longer than 45 minutes. Our ability to establish a threshold was limited by the modest effect of the duration of circulatory arrest and the considerable degree of scatter in the data.
Although this study was designed to compare treatment strategies and did not include a normal control group, the scores of patients in both treatment groups were considerably below average. The mean novelty-preference score was similar to that for other infants at risk for impaired cognitive development.9 The mean scores on the Bayley Scales were approximately 0.5 SD (for the Mental Development Index) to 1 SD (for the Psychomotor Development Index) lower than population norms.25 Apart from the duration of circulatory arrest, these low scores may be associated with preoperative cyanosis or hemodynamic instability, the generally deleterious effects of cardiopulmonary bypass on the central nervous system (e.g., microembolism and hypoperfusion), or the adverse effects of hemodynamic conditions in the postoperative period.
Nearly one quarter of the patients had possible or definite abnormalities on MRI scans, a finding that is relatively common after open-heart surgery in children and adults.26,27 These abnormalities included both diffuse global or watershed (border-zone) injuries related to hypoperfusion or to hypoxia or ischemia and focal or multifocal lesions presumed to be macroembolic. Periventricular leukomalacia, selective neuronal necrosis, focal or multifocal ischemic brain necrosis, and parasagittal cerebral lesions have been reported in infants with congenital heart disease.28-31 White-matter injury, reported in infants after cardiac surgery,28,29 could account for the observed motor deficits. The topography of both neuronal and white-matter injury after heart surgery in infants is consistent with ischemia as an important pathogenetic factor.32
EEG evidence of seizures during the first 48 hours after surgery was common in the study cohort, and infants with seizures had worse outcomes at one year of age than infants without postoperative seizures. Indeed, ictal activity on EEG monitoring in the first 48 hours after surgery was one of the strongest predictors of outcome, which is consistent with the findings in studies of neonates with other conditions.33 At a developmental stage similar to that of the human infant at birth, the infant rat brain is highly vulnerable to postischemic seizures; this epileptic activity is correlated with the degree of neuronal injury and neurologic sequelae.34-36 It is not clear whether the occurrence of seizures reflects an underlying brain injury or contributes independently to the injury.37
Several limitations inherent in the use of infant developmental testing at one year of age warrant comment. Although tests such as the Bayley Scales have satisfactory concurrent validity, the scores of one-year-old children have limited predictive validity.38,39 The relative deficits of the children assigned to circulatory arrest were most prominent in the domain of motor function, but assessments at older ages may reveal treatment effects in other domains, such as language or visual–motor integration, that are not easily tested in very young children.40
In summary, at one year of age the developmental and neurologic status of children randomly assigned to a strategy consisting predominantly of total circulatory arrest as a method of supporting vital organs during heart surgery was worse than that of children randomly assigned to a strategy consisting predominantly of low-flow bypass. Assessments of the children as they approach school age will clarify whether these findings portend clinically important differences in academic functioning. In treating individual infants, cardiovascular surgeons must balance the technical advantages of total circulatory arrest with its potential disadvantages.
Supported by grants (HL41786, RR02172, and P30-HD18655) from the National Institutes of Health.
We are indebted to the members of the Safety and Data Monitoring Committee — Julien I.E. Hoffman, M.D. (chairman), John W. Kirklin, M.D., Barry M. Lester, Ph.D., Robert J. Levine, M.D., Eli M. Mizrahi, M.D., Joseph G. Reves, M.D., George W. Williams, Ph.D., and Joel I. Verter, Ph.D.; to the perfusionists — David M. Farrell, M.A., C.C.P., Willis G. Gieser, C.C.P., Robert A. LaPierre, B.S., C.C.P., Robert J. Howe, B.S., C.C.P., and Bettina Archilla, B.S.; to the electroencephalographers — Lewis Kull, Sheila A. McPeck, Susan M. Hegarty, and Wayne A. Cote; to Ludmila Kyn for data-base and statistical programming; to the nursing staff for assistance with adherence to the protocol; to Donna M. Donati, Donna M. Duva, and Lisa-Jean Buckley for data management; to Kathleen M. O'Brien for project coordination; and to Edward Z. Tronick, Ph.D., for the use of a testing suite in the Child Development Unit, Children's Hospital.
Source Information
From the Departments of Neurology (D.C.B., K.C.K.K., G.L.H., S.L.H., J.E.C., E.J.C.), Cardiovascular Surgery (R.A.J., J.E.M., F.L.H., A.R.C.), Medicine (L.A.R.), Cardiology (G.W., A.Z.W., J.W.N.), Anesthesia (P.R.H.), and Radiology (P.D.B., R.D.S.), Children's Hospital; the Departments of Neurology (D.C.B., K.C.K.K., G.L.H., S.L.H., J.E.C., E.J.C.), Surgery (R.A.J., J.E.M., F.L.H., A.R.C.), Pediatrics (L.A.R., G.W., J.W.N.), and Radiology (P.D.B., R.D.S.), Harvard Medical School; and the Department of Biostatistics, Harvard School of Public Health (D.W., J.H.W.) — all in Boston.
Address reprint requests to Dr. Newburger at the Department of Cardiology, Children's Hospital, 300 Longwood Ave., Boston, MA 02115.
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- Citing Articles (199)
Citing Articles
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Jane W. Newburger. 2012. Central Nervous System Complications. , 753-761.
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Gil Wernovsky. 2012. Neurodevelopmental Outcomes in Children with Congenital Heart Disease. , 801-809.
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Angelo Polito, Zaccaria Ricci, Tiziana Fragasso, Paola E. Cogo. (2011) Balloon atrial septostomy and pre-operative brain injury in neonates with transposition of the great arteries: a systematic review and a meta-analysis. Cardiology in the Young1-7
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Fabrizio De Rita, Gianluca Lucchese, Luca Barozzi, Tiziano Menon, Giuseppe Faggian, Alessandro Mazzucco, Giovanni Battista Luciani. (2011) Selective Cerebro-Myocardial Perfusion in Complex Congenital Aortic Arch Pathology: A Novel Technique. Artificial Organsno-no
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Hannah C. Glass, Chelsea Bowman, Vann Chau, Alisha Moosa, Adam L. Hersh, Andrew Campbell, Kenneth Poskitt, Anthony Azakie, A. James Barkovich, Steven P. Miller, Patrick S. McQuillen. (2011) Infection and white matter injury in infants with congenital cardiac disease. Cardiology in the Young 21:05, 562-571
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H.H. Hövels-Gürich. (2011) Psychomotorische Entwicklung von Kindern mit angeborenem Herzfehler. Monatsschrift Kinderheilkunde
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Alaina K. Kipps, Colin Feuille, Anthony Azakie, Julien I.E. Hoffman, Sarah Tabbutt, Michael M. Brook, Anita J. Moon-Grady. (2011) Prenatal Diagnosis of Hypoplastic Left Heart Syndrome in Current Era. The American Journal of Cardiology 108:3, 421-427
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Jin-Tae Kim, Young-Hee Park, Young-Eun Chang, Hyo-Jin Byon, Hee-Soo Kim, Chong-Sung Kim, Hong-Gook Lim, Woong-Han Kim, Jeong-Ryul Lee, Yong-Jin Kim. (2011) The Effect of Cardioplegic Solution-Induced Sodium Concentration Fluctuation on Postoperative Seizure in Pediatric Cardiac Patients. The Annals of Thoracic Surgery 91:6, 1943-1948
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Lisa Wise-Faberowski, Andreas Loepke. (2011) Anesthesia during surgical repair for congenital heart disease and the developing brain: neurotoxic or neuroprotective?. Pediatric Anesthesia 21:5, 554-559
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Sharon Laing, Karen Walker, Judy Ungerer, Nadia Badawi, Kaye Spence. (2011) Early development of children with major birth defects requiring newborn surgery. Journal of Paediatrics and Child Health 47:3, 140-147
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Joshua W. Lampe, Lance B. Becker. (2011) State of the Art in Therapeutic Hypothermia. Annual Review of Medicine 62:1, 79-93
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Andrew B. Goldstone, David J. Bronster, Anelechi C. Anyanwu, Martin A. Goldstein, Farzan Filsoufi, David H. Adams, Joanna Chikwe. (2011) Predictors and Outcomes of Seizures After Cardiac Surgery: A Multivariable Analysis of 2,578 Patients. The Annals of Thoracic Surgery 91:2, 514-518
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J. I. Berman, S. E. G. Hamrick, P. S. McQuillen, C. Studholme, D. Xu, R. G. Henry, L. K. Hornberger, O. A. Glenn. (2011) Diffusion-Weighted Imaging in Fetuses with Severe Congenital Heart Defects. American Journal of Neuroradiology 32:2, E21-E22
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Marie Schaer, Bronwyn Glaser, Marie-Christine Ottet, Maude Schneider, Meritxell Bach Cuadra, Martin Debbané, Jean-Philippe Thiran, Stephan Eliez. (2010) Regional cortical volumes and congenital heart disease: a MRI study in 22q11.2 deletion syndrome. Journal of Neurodevelopmental Disorders 2:4, 224-234
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George M. Hoffman, Nancy S. Ghanayem. (2010) Perioperative neuromonitoring in pediatric cardiac surgery: Techniques and targets. Progress in Pediatric Cardiology 29:2, 123-130
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Jean A. Ballweg. (2010) Hyperglycemia and neurodevelopmental outcomes in infants with congenital heart disease. Progress in Pediatric Cardiology 29:2, 107-111
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Erin L. Albers, David P. Bichell, BethAnn McLaughlin. (2010) New Approaches To Neuroprotection In Infant Heart Surgery. Pediatric Research1
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Elaine E. Tseng, Malcolm V. Brock, Mary S. Lange, Juan C. Troncoso, Mary E. Blue, Charles J. Lowenstein, Michael V. Johnston, William A. Baumgartner. (2010) Glutamate Excitotoxicity Mediates Neuronal Apoptosis After Hypothermic Circulatory Arrest. The Annals of Thoracic Surgery 89:2, 440-445
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Patrick S. McQuillen, Steven P. Miller. (2010) Congenital heart disease and brain development. Annals of the New York Academy of Sciences 1184:1, 68-86
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Kimberly L. Gandy, George M. Hoffman, Patrick Vanderwal, James S. Tweddell. 2010. Surgical Techniques. , 219-237.
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Mary T. Donofrio, An N. Massaro. (2010) Impact of Congenital Heart Disease on Brain Development and Neurodevelopmental Outcome. International Journal of Pediatrics 2010, 1-13
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Amanda J. Shillingford, Gil Wernovsky. 2010. The Central Nervous System in Children and Young Adults with Congenital Cardiac Disease. , 1267-1278.
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C. Berg, O. Gembruch, U. Gembruch, A. Geipel. (2009) Doppler indices of the middle cerebral artery in fetuses with cardiac defects theoretically associated with impaired cerebral oxygen delivery in utero: is there a brain-sparing effect?. Ultrasound in Obstetrics and Gynecology 34:6, 666-672
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Matthew C. Scanlon, Nancy S. Ghanayem, Andrew M. Atz, David S. Cooper. (2009) Innovation in Congenital and Paediatric Cardiac Critical Care. Cardiology in the Young 19:S2, 85
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Chloe A. Joynt, Charlene M.T. Robertson, Po-Yin Cheung, Alberto Nettel-Aguirre, Ari R. Joffe, Reg S. Sauve, Wayne S.G. Biggs, Norma J. Leonard, David B. Ross, Ivan M. Rebeyka. (2009) Two-year neurodevelopmental outcomes of infants undergoing neonatal cardiac surgery for interrupted aortic arch: A descriptive analysis. The Journal of Thoracic and Cardiovascular Surgery 138:4, 924-932
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Estella M Alonso, Lisa G Sorensen. (2009) Cognitive development following pediatric solid organ transplantation. Current Opinion in Organ Transplantation 14:5, 522-525
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Jodi Chen, Robert A. Zimmerman, Gail P. Jarvik, Alex S. Nord, Robert R. Clancy, Gil Wernovsky, Lisa M. Montenegro, Diane M. Hartman, Susan C. Nicolson, Thomas L. Spray, J. William Gaynor, Rebecca Ichord. (2009) Perioperative Stroke in Infants Undergoing Open Heart Operations for Congenital Heart Disease. The Annals of Thoracic Surgery 88:3, 823-829
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Mary Ellen McCann, David C. Bellinger, Andrew J. Davidson, Sulpicio G. Soriano. (2009) Clinical research approaches to studying pediatric anesthetic neurotoxicity. NeuroToxicology 30:5, 766-771
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Eric S. Weiss, Kevin K.W. Wang, Jeremiah G. Allen, Mary E. Blue, Lois U. Nwakanma, Ming Cheng Liu, Mary S. Lange, Jennifer Berrong, Mary Ann Wilson, Vincent L. Gott, Juan C. Troncoso, Ronald L. Hayes, Michael V. Johnston, William A. Baumgartner. (2009) Alpha II-Spectrin Breakdown Products Serve as Novel Markers of Brain Injury Severity in a Canine Model of Hypothermic Circulatory Arrest. The Annals of Thoracic Surgery 88:2, 543-550
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Janet S. Soul, Richard L. Robertson, David Wypij, David C. Bellinger, Karen J. Visconti, Adré J. du Plessis, Barry D. Kussman, Lisa A. Scoppettuolo, Frank Pigula, Richard A. Jonas, Jane W. Newburger. (2009) Subtle hemorrhagic brain injury is associated with neurodevelopmental impairment in infants with repaired congenital heart disease. The Journal of Thoracic and Cardiovascular Surgery 138:2, 374-381
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Jorge D. Salazar, Ryan D. Coleman, Stephen Griffith, Jeffrey D. McNeil, Megan Steigelman, Haven Young, Bart Hensler, Patricia Dixon, John Calhoon, Faridis Serrano, Robert DiGeronimo. (2009) Selective Cerebral Perfusion: Real-Time Evidence of Brain Oxygen and Energy Metabolism Preservation. The Annals of Thoracic Surgery 88:1, 162-169
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G. Burkhard Mackensen, David L. McDonagh, David S. Warner. (2009) Perioperative Hypothermia: Use and Therapeutic Implications. Journal of Neurotrauma 26:3, 342-358
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David C. Bellinger, Jane W. Newburger, David Wypij, Karl C. K. Kuban, Adre J. duPlesssis, Leonard A. Rappaport. (2009) Behaviour at eight years in children with surgically corrected transposition: The Boston Circulatory Arrest Trial. Cardiology in the Young 19:01, 86
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Lisa R. Bomgaars, Stacey L. Berg, Ann R. Stark. 2009. Pediatrics. , 497-507.
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Robert Ryan Clancy. (2008) Neuroprotection in Infant Heart Surgery. Clinics in Perinatology 35:4, 809-821
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Amanda Shillingford, Jack Rychik. 2008. Congenital heart disease and the central nervous system: a perinatal perspective. , 749-757.
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Lena S. Sun, Guohua Li, Charles DiMaggio, Mary Byrne, Virginia Rauh, Jeanne Brooks-Gunn, Athina Kakavouli, Alastair Wood. (2008) Anesthesia and Neurodevelopment in Children. Anesthesiology 109:5, 757-761
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Hedwig H. Hövels-Gürich, Sebastian B. Bauer, Ralph Schnitker, Klaus Willmes-von Hinckeldey, Bruno J. Messmer, Marie-Christine Seghaye, Walter Huber. (2008) Long-term outcome of speech and language in children after corrective surgery for cyanotic or acyanotic cardiac defects in infancy. European Journal of Paediatric Neurology 12:5, 378-386
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R. van der Rijken, G. Hulstijn-Dirkmaat, F. Kraaimaat, L. Nabuurs-Kohrman, A. Nijveld, B. Maassen, O. Daniels. (2008) Open-heart surgery at school age does not affect neurocognitive functioning. European Heart Journal 29:21, 2681-2688
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Gil Wernovsky. (2008) Improving neurologic and quality-of-life outcomes in children with congenital heart disease: Past, present, and future. The Journal of Thoracic and Cardiovascular Surgery 135:2, 240-242.e2
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David C. Bellinger. (2008) Are children with congenital cardiac malformations at increased risk of deficits in social cognition?. Cardiology in the Young 18:01,
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Rabih S. Talhouk, Michele P. Zeinieh, Mohamad A. Mikati, Marwan E. El-Sabban. (2008) Gap junctional intercellular communication in hypoxia–ischemia-induced neuronal injury. Progress in Neurobiology 84:1, 57-76
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Jia Li, Gencheng Zhang, Helen Holtby, Anne-Marie Guerguerian, Sally Cai, Tilman Humpl, Christopher A. Caldarone, Andrew N. Redington, Glen S. Van Arsdell. (2008) The influence of systemic hemodynamics and oxygen transport on cerebral oxygen saturation in neonates after the Norwood procedure. The Journal of Thoracic and Cardiovascular Surgery 135:1, 83-90.e2
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Fahad Shuja, José Pedro Almeida, Hasan B. Alam. (2008) Role of hypothermia in hemorrhagic shock. Journal of Organ Dysfunction 4:3, 151-160
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Lori A Aronson, James P Spaeth. (2007) Frontiers in Pediatric Anesthesia. International Anesthesiology Clinics 44:1, 33-49
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Jean A. Ballweg, Gil Wernovsky, Richard F. Ittenbach, Judy Bernbaum, Marsha Gerdes, Paul R. Gallagher, Troy E. Dominguez, Elaine Zackai, Robert R. Clancy, Susan C. Nicolson, Thomas L. Spray, J. William Gaynor. (2007) Hyperglycemia After Infant Cardiac Surgery Does Not Adversely Impact Neurodevelopmental Outcome. The Annals of Thoracic Surgery 84:6, 2052-2058
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Miller, Steven P., McQuillen, Patrick S., Hamrick, Shannon, Xu, Duan, Glidden, David V., Charlton, Natalie, Karl, Tom, Azakie, Anthony, Ferriero, Donna M., Barkovich, A. James, Vigneron, Daniel B., . (2007) Abnormal Brain Development in Newborns with Congenital Heart Disease. New England Journal of Medicine 357:19, 1928-1938
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Xudong Pan, Lizhong Sun, Weiguo Ma, Yue Tang, Cun Long, Liangxin Tian, Ningning Liu, Zhengyi Feng, Jun Zheng. (2007) Overactivation of poly(adenosine phosphate–ribose) polymerase 1 and molecular events in neuronal injury after deep hypothermic circulatory arrest: Study in a rabbit model. The Journal of Thoracic and Cardiovascular Surgery 134:5, 1227-1233.e5
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H. H. Hövels-Gürich, K. Konrad, D. Skorzenski, R. Minkenberg, B. Herpertz-Dahlmann, B. J. Messmer, M.-C. Seghaye. (2007) Long-Term Behavior and Quality of Life After Corrective Cardiac Surgery in Infancy for Tetralogy of Fallot or Ventricular Septal Defect. Pediatric Cardiology 28:5, 346-354
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Troy E. Dominguez, Gil Wernovsky, J. William Gaynor. (2007) Cause and Prevention of Central Nervous System Injury in Neonates Undergoing Cardiac Surgery. Seminars in Thoracic and Cardiovascular Surgery 19:3, 269-277
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Katja Hülser, Karl‐Otto Dubowy, Herman Knobl, Hans Meyer, Axel Schölmerich. (2007) Developmental outcome and psychosocial adjustment in children after surgery for congenital heart disease during infancy. Journal of Reproductive and Infant Psychology 25:2, 139-151
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J. William Gaynor, Gil Wernovsky, Gail P. Jarvik, Judy Bernbaum, Marsha Gerdes, Elaine Zackai, Alex S. Nord, Robert R. Clancy, Susan C. Nicolson, Thomas L. Spray. (2007) Patient characteristics are important determinants of neurodevelopmental outcome at one year of age after neonatal and infant cardiac surgery. The Journal of Thoracic and Cardiovascular Surgery 133:5, 1344-1353.e3
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Jean A. Ballweg, Gil Wernovsky, J. William Gaynor. (2007) Neurodevelopmental Outcomes Following Congenital Heart Surgery. Pediatric Cardiology 28:2, 126-133
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Gabriel Amir, Chandra Ramamoorthy, R. Kirk Riemer, Corrine R. Davis, Frank L. Hanley, V. Mohan Reddy. (2006) Visual light spectroscopy reflects flow-related changes in brain oxygenation during regional low-flow perfusion and deep hypothermic circulatory arrest. The Journal of Thoracic and Cardiovascular Surgery 132:6, 1307-1312
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Nancy S. Ghanayem, Michael E. Mitchell, James S. Tweddell, George M. Hoffman. (2006) Monitoring the brain before, during, and after cardiac surgery to improve long-term neurodevelopmental outcomes. Cardiology in the Young 16:S3, 103
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Delia M. Talos, Pamela L. Follett, Rebecca D. Folkerth, Rachel E. Fishman, Felicia L. Trachtenberg, Joseph J. Volpe, Frances E. Jensen. (2006) Developmental regulation of α-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. The Journal of Comparative Neurology 497:1, 61-77
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Jo Wray. (2006) Intellectual development of infants, children and adolescents with congenital heart disease. Developmental Science 9:4, 368-378
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George M. Hoffman. (2006) Neurologic Monitoring on Cardiopulmonary Bypass: What Are We Obligated to Do?. The Annals of Thoracic Surgery 81:6, S2373-S2380
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V Y Chock, V M Reddy, D Bernstein, A Madan. (2006) Neurologic events in neonates treated surgically for congenital heart disease. Journal of Perinatology 26:4, 237-242
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Savannah C. Partridge, Daniel B. Vigneron, Natalie N. Charlton, Jeffrey I. Berman, Roland G. Henry, Pratik Mukherjee, Patrick S. McQuillen, Tom R. Karl, A. James Barkovich, Steven P. Miller. (2006) Pyramidal tract maturation after brain injury in newborns with heart disease. Annals of Neurology 59:4, 640-651
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Taeun Chang, Richard A. Jonas. (2006) Neurologic complications of cardiovascular surgery. Current Neurology and Neuroscience Reports 6:2, 121-126
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Joseph D Tobias. (2006) Cerebral oxygenation monitoring: near-infrared spectroscopy. Expert Review of Medical Devices 3:2, 235-243
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Gil Wernovsky. (2006) Current insights regarding neurological and developmental abnormalities in children and young adults with complex congenital cardiac disease. Cardiology in the Young 16:S1, 92
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Catherine L. Dent, James P. Spaeth, Blaise V. Jones, Steven M. Schwartz, Tracy A. Glauser, Barbara Hallinan, Jeffrey M. Pearl, Philip R. Khoury, C. Dean Kurth. (2006) Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion. The Journal of Thoracic and Cardiovascular Surgery 131:1, 190-197
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Catherine L. Dent, James P. Spaeth, Blaise V. Jones, Steven M. Schwartz, Tracy A. Glauser, Barbara Hallinan, Jeffrey M. Pearl, Philip R. Khoury, C. Dean Kurth. (2005) Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion. The Journal of Thoracic and Cardiovascular Surgery 130:6, 1523-1530
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Stephan Schubert, Gisela Stoltenburg-Didinger, Anke Wehsack, Dirk Troitzsch, Wolfgang Boettcher, Michael Huebler, Matthias Redlin, Majid Kanaan, Michael Meissler, Peter E. Lange, Hashim Abdul-Khaliq. (2005) Large-Dose Pretreatment with Methylprednisolone Fails to Attenuate Neuronal Injury After Deep Hypothermic Circulatory Arrest in a Neonatal Piglet Model. Anesthesia & Analgesia 101:5, 1311-1318
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ARJAN B. TE PAS, GERDA WEZEL-MEIJLER, REGINA BÖKENKAMP-GRAMANN, FRANS J. WALTHER. (2005) Preoperative cranial ultrasound findings in infants with major congenital heart disease. Acta Paediatrica 94:11, 1597-1603
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J. William Gaynor, Susan C. Nicolson, Gail P. Jarvik, Gil Wernovsky, Lisa M. Montenegro, Nancy B. Burnham, Diane M. Hartman, Andy Louie, Thomas L. Spray, Robert R. Clancy. (2005) Increasing duration of deep hypothermic circulatory arrest is associated with an increased incidence of postoperative electroencephalographic seizures. The Journal of Thoracic and Cardiovascular Surgery 130:5, 1278-1286
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Gabriel Amir, Chandra Ramamoorthy, R. Kirk Riemer, V. Mohan Reddy, Frank L. Hanley. (2005) Neonatal Brain Protection and Deep Hypothermic Circulatory Arrest: Pathophysiology of Ischemic Neuronal Injury and Protective Strategies. The Annals of Thoracic Surgery 80:5, 1955-1964
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George M. Hoffman, Kathleen A. Mussatto, Cheryl L. Brosig, Nancy S. Ghanayem, Ndidiamaka Musa, Raymond T. Fedderly, Robert D.B. Jaquiss, James S. Tweddell. (2005) Systemic venous oxygen saturation after the Norwood procedure and childhood neurodevelopmental outcome. The Journal of Thoracic and Cardiovascular Surgery 130:4, 1094-1100
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Vesna Jevtovic-Todorovic. (2005) General Anesthetics and the Developing Brain. Journal of Neurosurgical Anesthesiology 17:4, 204-206
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