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J Thorac Cardiovasc Surg 2003;126:1385-1396
© 2003 The American Association for Thoracic Surgery
Surgery for congenital heart disease |
a Department of Neurology, Children's Hospital, Boston, Mass, USA
b Department of Cardiology, Children's Hospital, Boston, Mass, USA
c Department of Medicine, Children's Hospital, Boston, Mass, USA
d Department of Cardiovascular Surgery, Children's Hospital, Boston, Mass, USA
e Clinical Research Program,e Children's Hospital, Boston, Mass, USA
f Department of Neurology, Harvard Medical School, Boston, Mass, USA
g Department of Pediatrics, Harvard Medical School, Boston, Mass, USA
h Department of Surgery, Harvard Medical School, Boston, Mass, USA
i Department of Biostatistics, Harvard School of Public Health, Boston, Mass, USA
Received for publication June 6, 2002; revisions received August 20, 2002; revisions received March 17, 2003; accepted for publication March 27, 2003.
* Address for reprints: David C. Bellinger, PhD, MSc, Neuroepidemiology Unit, Farley Basement 127, Children's Hospital, 300 Longwood Ave, Boston, MA 02115, USA
david.bellinger{at}tch.harvard.edu
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Abstract |
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METHODS: In a single-center trial, infants with dextrotransposition of the great arteries underwent the arterial switch operation after random assignment to either total circulatory arrest or low-flow cardiopulmonary bypass. Developmental, neurologic, and speech outcomes were assessed at 8 years of age in 155 of 160 eligible children (97%).
RESULTS: Treatment groups did not differ in terms of most outcomes, including neurologic status, Full-Scale or Performance IQ score, academic achievement, memory, problem solving, and visual-motor integration. Children assigned to total circulatory arrest performed worse on tests of motor function including manual dexterity with the nondominant hand (P = .003), apraxia of speech (P = .01), visual-motor tracking (P = .01), and phonologic awareness (P = .003). Assignment to low-flow cardiopulmonary bypass was associated with a more impulsive response style on a continuous performance test of vigilance (P < .01) and worse behavior as rated by teachers (P = .05). Although mean scores on most outcomes were within normal limits, neurodevelopmental status in the cohort as a whole was below expectation in many respects, including academic achievement, fine motor function, visual-spatial skills, working memory, hypothesis generating and testing, sustained attention, and higher-order language skills.
CONCLUSIONS: Use of total circulatory arrest to support vital organs during heart surgery in infancy is generally associated with greater functional deficits than is use of low-flow cardiopulmonary bypass, although both strategies are associated with increased risk of neurodevelopmental vulnerabilities.
Our group has investigated the importance of one aspect of surgical intervention, the method of vital organ support, in the genesis of central nervous system sequelae in children who undergo cardiac surgery in infancy. We undertook a single-center randomized trial (the Boston Circulatory Arrest Trial) of children with dextrotransposition of the great arteries (D-TGA) who underwent the arterial switch operation with deep hypothermia either with predominantly total circulatory arrest (TCA) or with predominantly low-flow cardiopulmonary bypass (LFCPB). Compared with infants in the LFCPB group, infants in the TCA group were at significantly greater risk of seizures and abnormalities on neurologic examination in the perioperative period, neurologic abnormalities and lower motor development scores at 1 year of age, slower expressive language development at 2.5 years of age, and lower fine and gross motor scores as well as speech and language abnormalities and oromotor apraxia at 4 years of age.19-25 Furthermore, throughout the follow-up period, children in both treatment groups have demonstrated higher rates of neurodevelopmental problems than would be expected in a healthy population. At age 4 years, for instance, the mean Full-Scale IQ score was approximately 0.5 SD below the expected population mean, the group had marked difficulties on tests of expressive language, visual-spatial, and visual-motor skills, and 24% met diagnostic criteria for oromotor apraxia.23
Another follow-up evaluation was conducted when children were 8 years old. The more precise and predictive evaluations that can be carried out with 8-year-olds provide a stronger basis for drawing inferences about the nature and severity of treatment group differences than could be achieved at younger ages. Moreover, the children had begun primary school and were being challenged to acquire academic skills such as reading and mathematics, so the practical implications of the deficits noted at earlier evaluations could be determined with greater certainty. In this article we report on the results of the full battery of neurologic, developmental, and speech evaluations conducted at age 8 years and also describe a consistent pattern of strengths and weaknesses, evident in both treatment groups, that may be the result of preoperative abnormalities associated with D-TGA or of operative factors that the treatment groups had in common. In a companion article, we present analyses designed to define, in more quantitative terms, the duration of TCA that is associated with a decline in neurodevelopmental function.
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Methods |
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The arterial switch operation was performed in 171 infants, of whom 165 were alive at the age of 8 years. Five children (3%) living outside the United States were not considered eligible. No children were unavailable for follow-up. Parents of 155 (97%) of the remaining 160 children agreed to participate in the evaluation, which involved assessments by a developmental psychologist, a pediatric neurologist, and a speech pathologist. The psychologist traveled to 6 children whose families were unable to return to Boston. For these children, only developmental examinations were completed.
This study was approved by the Children's Hospital institutional review board and conducted in accordance with institutional guidelines. Parents of all children provided informed consent. All examiners were unaware of a given child's treatment assignment or clinical course or of the results of assessments conducted by the other examiners. The elements of the assessments are detailed in the following sections.
Neuropsychologic examination
Children were administered a 5-hour battery of standardized tests designed to evaluate general intelligence, academic achievement, memory, problem solving, visual-spatial skills, fine motor function, attention, and behavior both in the home and at school. General intelligence was assessed with the Wechsler Intelligence Scale for Children—Third Edition (WISC-III).28 Academic achievement was assessed with the Wechsler Individual Achievement Test.29 Each WIAT subscale score was classified according to whether it was significantly lower than expected (P < .05). The presence of such an ability-achievement discrepancy is a commonly used criterion for a learning disability.30 Other sources of data about a child's academic performance were the Adaptive Functioning scales of the Teacher Report Form31 and selected questions from the parent-completed Child Behavior Checklist/4-18.32
Children's neuropsychologic statuses were assessed with the following tests: the Wide Range Assessment of Memory and Learning (screener),33 the Wisconsin Card Sorting Test,34 the Developmental Test of Visual-Motor Integration, 3rd Revision,35 the Trail-Making Test-Intermediate Version,36 the Rey-Osterrieth Complex Figure37 (copy condition), the Grooved Pegboard,36 the Formulated Sentences subtest of the Clinical Evaluation of Language Fundamentals—Third Edition,38 the Controlled Oral Word Association Test,39 the Verbal Fluency subtest of the McCarthy Scales,40 and the Test of Variables of Attention, version 6.0.8 (11.5-minute version, TOVA).41 In addition, a handwriting sample was obtained and scored.42
Data were collected by parent interview on family status, including the marital status of the primary caregiver, maternal and paternal occupations and educational backgrounds, and number of children. Family social class was estimated with the Hollingshead Four Factor Index of Social Status. Parental IQ scores had been determined at a previous assessment.43
Speech production examination
Speech was assessed with the Mayo Test for Apraxia of Speech and Oral Apraxia-Children's Battery (selected items),44 the Oral and Speech Motor Control Test,45 the Goldman-Fristoe Test of Articulation,46 the Auditory Closure subtest of the Illinois Test of Psycholinguistic Ability,47 and the Test of Auditory Analysis.48 The speech pathologist made a clinical judgment regarding the presence or absence of volitional oral movement abnormalities, phonologic awareness abnormalities, and apraxia of speech. If present, an abnormality was classified as mild, moderate, or severe.
Neurologic examination
Findings on the neurologic examination were classified as normal, possibly abnormal, or definitely abnormal. Definite abnormalities were classified as mild (no functional impairment), moderate (functional impairment requiring intervention/therapy), or severe (dependent on assistance). Abnormalities were subclassified as disorders of head shape and growth, neurocognitive abilities, special senses, cranial nerves, motor system, gait, and sensory. Children could be classified as having more than one type of abnormality.
Statistical analysis
The primary outcomes were Full-Scale IQ score from the WISC-III, the Reading and Mathematics Composite scores from the WIAT, and the presence of possible or definite neurologic abnormalities. Treatment group differences were evaluated by means of intent-to-treat analyses. One child with a diagnosis of autism (assigned to the LFCPB group) was included in analyses of neurologic outcomes but not developmental and speech outcomes because the latter assessments could not be completed as a result of the child's lack of social relatedness. All comparisons were adjusted for diagnosis (IVS vs VSD). Comparisons of IQ, language, motor, and continuous speech variables were also adjusted for family social class. For those dependent variables for which a treatment group by diagnosis interaction reached a level considered significant (P < .05), separate P values are reported for the two diagnosis groups.
Continuous outcomes were analyzed with linear regression methods. Paired t tests were used for intraindividual comparisons of scores. Scores on the developmental tests were compared with the expected means from the normative populations. Time-to-completion tasks were analyzed by proportional hazards regression methods. Fisher exact tests were used to analyze binary variables. Exact tests for trend were used to analyze ordered categoric variables and continuous scores that were not normally distributed.
On the basis of an expected follow-up of 148 patients, the study was designed to have 86% power to detect a difference of 0.5 SD in Full-Scale IQ score and 88% power to detect a difference of 25% in the prevalence of possible or definite neurologic abnormalities.
Values are reported as mean ± SD for continuous variables and outcomes. Data are reported as numbers and percentages of children affected for categoric variables and outcomes.
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According to parental reports, between the study evaluations conducted at ages 4 and 8 years 34% of children were evaluated by a speech pathologist, 16% were evaluated by an occupational therapist, 9% were evaluated by a psychiatrist, and 6% were evaluated by a physical therapist. Treatment groups did not differ in the frequencies of these evaluations.
Neuropsychologic outcomes
General intelligence (Table 2)
Treatment groups did not differ significantly in terms of Full-Scale or Performance IQ scores. Among children with a VSD, assignment to TCA was associated with lower Verbal IQ scores (P = .03). Treatment groups differed on one of the four WISC-III index scores and on two of the 13 subtest scores. Among children with a VSD, assignment to TCA was associated with lower scores on the Verbal Comprehension (P = .04), Similarities (P = .03), and Comprehension (P = .02) scales. In general, social class and VSD status explained much more of the variance in Full-Scale IQ scores than did treatment assignment. For instance, social class alone explained 23.7% of the variance and adding VSD status to the model explained an additional 3.2%, whereas adding treatment assignment explained only an additional 0.3%.
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11 points), but this percentage was not different between the TCA (39%) and LFCPB (37%) groups (P = .81), nor was the percentage in either group greater than in the general population (40.5%). For most children with a significant discrepancy (76%), Verbal IQ score exceeded Performance IQ score. The following summary and factor scores were significantly lower than the expected population means: Full-Scale IQ score (P = .02), Performance IQ score (P < .001), Perceptual Organization score (P < .001), and Freedom from Distractibility score (P < .001). Scores on 6 of the 13 subtests, primarily those contributing to the Performance IQ score, were significantly lower than the population mean: Arithmetic score (P = .04), Digit Span score (P < .001), Picture Completion score (P < .001), Picture Arrangement score (P = .007), Object Assembly score (P < .001), and Mazes score (P < .001).
Academic achievement (Table 3)
Treatment groups did not differ on any of the WIAT summary scores or subscales. Only for Reading Comprehension score were the frequencies of ability-achievement discrepancies higher for the TCA group than for the LFCPB group (P = .006). According to parental report, 56 (37%) of children were receiving remedial services in school and 15 (10%) had already repeated a grade. Neither outcome was associated with treatment group. Treatment groups did not differ on the following scales of the Teacher Report Form: Academic Performance, Working Hard, Learning, Happy, or Total Adaptive. Children in the TCA group were rated significantly more positively on the Behaving Appropriately scale (P = .05).
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Memory and learning (Table 4)
Treatment groups did not differ in terms of Memory Screening Index score or any subtest. The mean Memory Screening Index score (90.0 ± 15.3) was significantly lower than the expected population mean of 100 (P < .001), as were the mean scores on all subtests but Verbal Memory (Picture Memory score P < .001, Design Memory score P < .001, and Story Memory score P < .001). The children's performance was weakest on the Design Memory subtest, with a mean score approximately 1 SD below the expected score of 10.
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Visual-spatial and visual-motor skills (Table 4)
Treatment group assignment was not significantly associated with score on the Developmental Test of Visual-Motor Integration (P = .57) or with the frequency of scores 1 SD or more below average (42% in TCA group vs 32% in LFCPB group, P = .23). In the cohort as a whole, the mean score was at the 25th percentile.
Treatment groups did not differ in the time needed to complete part A of the Trail-Making Test (P = .66) or the percentage of children whose time was more than 1 SD slower than expected for age (5% in TCA vs 4% in LFCPB, P = .77). Children in the TCA group required more time to complete part B, but only among the subset of children with an IVS (P = .01). In addition, completion times more than 1 SD slower than expected for age were more frequent in the TCA group than in the LFCPB group (24% vs 12%, P = .06). In the cohort as a whole, however, mean times to complete both parts A and B were near the expected means for 8- and 9-year-olds.39
On the Rey-Osterrieth Complex Figure, treatment groups did not differ in the percentages of children whose copies were scored at the lowest level of organization (57% TCA vs 47% LFCPB, P = .25). In the cohort as a whole, the proportion of copies scored at the lowest level (52%) was more than twice the expected frequency of 23%37 (P < .001).
Fine motor function (Table 4)
Children in the VSD subgroup who were assigned to TCA took significantly longer than did the children with VSD assigned to LFCPB to complete the Grooved Pegboard with the nondominant hand (P = .003). The treatment group difference was not significant for the dominant hand (P = .06). A significantly larger percentage of children in the TCA group than in the LFCPB group had a completion time for the nondominant hand that was more than 1 SD slower than expected for age (60% vs 32%; P = .001). Treatment groups did not differ in this respect for the dominant hand (P = .17).
Assignment to the TCA group was associated with significantly poorer alignment and spacing in the handwriting sample (P = .01). The TCA group also scored lower than the LFCPB group on letter size and formation, but these differences did not reach statistical significance.
Attention, vigilance, and reaction time (Table 4)
In the first half of the TOVA, a visual continuous performance test, children assigned to LFCPB had a significantly faster mean response time (P = .01), although they had higher rates of errors of commission (P = .01), anticipatory responses (P = .005), and multiple responses (P = .01). In the second half of the test, the LFCPB group had significantly more anticipatory responses (P = .004) and multiple responses (P = .009). Thus the LFCPB group displayed a significantly more impulsive response style on this test of vigilance than did the TCA group. Because the 11.5-minute version of the TOVA is not normed for 8-year-olds, the children's performance cannot be related to an expected level. However, comparison of the scores to those achieved by 8-year-olds in the norming sample on the 22.5-minute version revealed that in our study group as a whole the rates of errors of omission were nevertheless more than double those of the norming sample in both halves of the task, the rates of errors of commission were more than double in the first half and approximately 50% higher in the second half, and response times were approximately 1 SD slower in both halves. The mean number of multiple responses, described as "rare" in the standardization sample of 8-year-olds,41 exceeded 50 in the second half for our overall cohort.
Language and speech production outcomes (Table 5)
Among children with a VSD, those assigned to TCA received lower scores on the Auditory Closure subtest of the ITPA (P = .007). Children assigned to the TCA group scored lower than children in the LFCPB group on the Test of Auditory Analysis (P = .02). A significantly higher proportion of children assigned to TCA were judged to have abnormal phonologic awareness (59% vs 34%, P = .002). Furthermore, when present, this condition was considered to be more severe (P = .003).
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Among children with a VSD, those in the TCA group achieved a lower score than those in the LFCPB group on the Controlled Oral Word Association Test, a letter fluency task (P = .008). Treatment groups did not differ significantly in terms of mean score on the Verbal Fluency subtest of the McCarthy Scales, a semantic category task (P = .12), although a higher proportion of children in the TCA group achieved a score that was more than 1 SD below the expected mean (33% in TCA group vs 17% in LFCPB group, P = .03). In the cohort as a whole, the mean score on semantic category fluency was close to the expected mean (22.5), whereas the mean score on letter fluency was below the 20th percentile for age.
Children in the TCA group had lower scores than children in the LFCPB group on the Mayo Test for Apraxia of Speech and Oral Apraxia (P = .002). There was a tendency for the TCA group to have lower scores than the LFCPB group for the Total Structural Score (P = .09) and the Total Functional Score (P = .08) of the Oral and Speech Motor Control Test, although these differences were small. Treatment group assignment was not associated with the number of errors on the Goldman-Fristoe Test of Articulation (P = .54), with the rate and duration of either monosyllabic or polysyllabic repetitions (P = .52 and P = .62, respectively), or with abnormal performance on the Volitional Oral Movements test (P = .09). When abnormal volitional oral movements were present, however, those noted among children in the TCA group were more severe than those among children in the LFCPB group (P = .03). Significantly more children in the TCA group were judged by the speech pathologist to have apraxia of speech (16% vs 3%, respectively, P = .007), and the apraxia in the TCA group tended to be more severe than the apraxia in the LFCPB group (P = .01).
Neurologic outcomes (Table 6)
Treatment groups did not differ significantly in the proportions of children judged to have a possible or a definite abnormality, although the frequencies of abnormalities in both groups were high (71% vs 64% in the TCA and LFCPB groups, respectively, P = .23). Most findings were judged to be mild, however, and most often involved neurocognitive functions (eg, attention, language), motor function, and gait. Relative to children randomly assigned to LFCPB, those assigned to TCA had more frequent occurrence of cranial nerve and brainstem abnormalities (21% vs 8%, P = .04).
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Discussion |
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Most children performed well within the normal range, with the mean scores of the cohort as a whole on standardized tests of global function (eg, intelligence, academic achievement) only slightly lower than the expected score of 100. Other recent studies have reported that the IQ scores of children with congenital heart disease are not significantly lower than the scores of healthy or sibling control subjects.18,52 It is apparent, however, that children with congenital heart disease who have undergone corrective surgery manifest a variety of neurodevelopmental vulnerabilities of potential long-term importance. Indeed, more than a third of the children in our study cohort had already been identified as requiring remedial academic services. Moreover, their scores on selected domain-specific neuropsychologic tests, as well as clinical observations of their behavior, suggest striking weaknesses relative to the general population in many respects. Because all children with D-TGA require corrective surgery and our primary goal was to compare neurodevelopmental outcomes associated with the two major vital organ support methods, our study design did not include a healthy control group. For many end points, however, the performance in the cohort as a whole was far below what would be expected in the general population (eg, in terms of the number scoring 1 SD or more below the population mean). Therefore we consider it reasonable to draw inferences about the pattern of weaknesses evident in the cohort as a whole and to suggest a behavioral signature for children after surgery to repair D-TGA. This signature is based on grouped data, however, so not all children would be expected to display all features of the pattern.
The most prominent deficits lie in the domains of motor function and visual-spatial skills. Interestingly, visual-spatial processing is the weakest aspect of information processing among children who meet Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition criteria for developmental coordination disorder.53 Other areas of relative weakness include working memory, hypothesis generation and testing, vigilance and sustained attention, and higher-order language skills. This pattern of deficits suggests underlying problems with executive functions, which are called on in organizing and implementing strategies and plans and in modifying them as needed.54 During tasks that required the children to structure, pace, and monitor their behavior, they appeared to get lost in the details. They had difficulty seeing how the pieces fit together to form a coherent, structured whole, whether the task involved the assembly of story elements into a narrative or the placement of specific elements of the Rey-Osterrieth Complex Figure in the proper locations with respect to one another. It appeared that lower-level building block skills were relatively intact, but the children had difficulty integrating or coordinating these skills to accomplish higher-order goals. Whereas most children demonstrated an age-appropriate ability to read individual words in isolation, many scored lower than expected in terms of the ability to read connected discourse for meaning. Similarly, many children who grasped basic mathematic concepts had difficulty applying these concepts to solve specific problems. Like other groups of children with congenital heart disease,55,56 children with D-TGA present many of the neurodevelopmental characteristics of nonverbal learning disabilities.57
The deficits found in the cohort as a whole are similar to the deficits reported in other patients with congenital or acquired heart disease, suggesting that these deficits are not specific to D-TGA. Among adult patients who experience cardiopulmonary arrest or undergo the CABG procedure, visual-motor integration is particularly impaired.58,59 Cerebral anoxia is associated with deficits in visual-spatial function, expressive language, executive functions, and memory.60 Children with heart disease treated with extracorporeal membrane oxygenation demonstrate deficits in visual memory and spatial construction but not in verbal ability or verbal memory.55 Other cohorts of children with D-TGA have been reported to achieve significantly lower scores than their siblings on the Developmental Test of Visual-Motor Integration.52 In another study, children with cyanotic lesions scored lower than control subjects on the copy trial of the Rey-Osterrieth Complex Figure but not on tests of verbal learning or auditory memory.61 Children with cyanotic lesions have higher rates of both gross and fine motor dysfunctions than do control subjects.9,18 Relative to control subjects, children with congenital heart disease also tend to achieve less academic success, as indicated by poorer scores on tests of achievement, higher rates of referral for remedial services, and higher rates of placement in special classes or schools.52,61,62
In our trial, the subgroup of children in the TCA group who also had an associated VSD has consistently displayed the poorest neurodevelopmental outcomes, beginning in the postoperative period.19-23 The factors responsible are not known. The slightly older age of these children at surgery, with the greater risk of chronic hypoxemia and poor cerebral perfusion as a result of hemodynamic instability, might be important, but this seems unlikely given that the children in this group were repaired at a very young age (mean 2 weeks), as well as the fact that children with a VSD are generally less hypoxic than are children with an IVS. This group did not require longer periods of TCA than did the children in the TCA group who did not have a VSD, although they did require a longer period of cardiopulmonary bypass (approximately 30 minutes; Table 1), thus increasing their exposure to ischemia and pump-related sources of brain injury. Group differences in the frequency of preoperative brain injury are another possibility. Previous studies have demonstrated that children with a VSD are more likely than children with other types of congenital heart disease to have preoperative cranial ultrasonographic abnormalities (eg, periventricular and parenchymal echodensities, linear echodensities in the basal ganglia and thalamus),2 and children with acyanotic lesions tend to have more preoperative neurologic and behavioral abnormalities than do children with cyanotic lesions.6 The 22q11 microdeletion, which is associated with considerable neurodevelopmental risk,63 is rare among children with D-TGA with IVS but occurs with greater frequency among children with a VSD.64 Routine genetic testing of children who participate in future trials would be helpful in understanding the factors that predict the neurodevelopmental risks of different patient subgroups.
In summary, we found that 8 years after undergoing the arterial switch operation, children who underwent deep hypothermia with predominantly TCA did not differ from children who underwent deep hypothermia with predominantly LFCPB in most of the end points measured. They did, however, continue to manifest greater morbidity in the domain of motor functions, a treatment group difference that has consistently been observed in this trial. In both groups, moreover, performance was below the expected levels in several domains, most notably visual-spatial and visual-motor skills. These findings suggest that although the use of TCA is associated with worse outcomes in certain neurodevelopmental domains, other factors are also important in determining the prognoses of these patients. The relative contributions of genetic polymorphisms and mutations, preoperative health, other operative factors, and postoperative events remain to be determined. Our findings lead us to recommend close developmental surveillance and follow-up of children who have undergone surgery to repair congenital heart disease.
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C. A. Warnes, R. G. Williams, T. M. Bashore, J. S. Child, H. M. Connolly, J. A. Dearani, P. del Nido, J. W. Fasules, T. P. Graham Jr, Z. M. Hijazi, et al. ACC/AHA 2008 Guidelines for the Management of Adults With Congenital Heart Disease: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Develop Guidelines on the Management of Adults With Congenital Heart Disease): Developed in Collaboration With the American Society of Echocardiography, Heart Rhythm Society, International Society for Adult Congenital Heart Disease, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons Circulation, December 2, 2008; 118(23): e714 - e833. [Full Text] [PDF]
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C. A. Warnes, R. G. Williams, T. M. Bashore, J. S. Child, H. M. Connolly, J. A. Dearani, P. del Nido, J. W. Fasules, T. P. Graham Jr, Z. M. Hijazi, et al. ACC/AHA 2008 Guidelines for the Management of Adults With Congenital Heart Disease: Executive Summary: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Adults With Congenital Heart Disease): Developed in Collaboration With the American Society of Echocardiography, Heart Rhythm Society, International Society for Adult Congenital Heart Disease, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons Circulation, December 2, 2008; 118(23): 2395 - 2451. [Full Text] [PDF]
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R. E. Neufeld, B. G. Clark, C. M.T. Robertson, D. M. Moddemann, I. A. Dinu, A. R. Joffe, R. S. Sauve, D. E. Creighton, L. Zwaigenbaum, D. B. Ross, et al. Five-year neurocognitive and health outcomes after the neonatal arterial switch operation J. Thorac. Cardiovasc. Surg., December 1, 2008; 136(6): 1413 - 1421. [Abstract] [Full Text] [PDF]
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 R. van der Rijken, G. Hulstijn-Dirkmaat, F. Kraaimaat, L. Nabuurs-Kohrman, A. Nijveld, B. Maassen, and O. Daniels Open-heart surgery at school age does not affect neurocognitive functioning Eur. Heart J., November 1, 2008; 29(21): 2681 - 2688. [Abstract] [Full Text] [PDF]
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J. Conway, K. K. Wong, C. O'Connell, and A. E. Warren Cardiovascular Risk Screening Before Starting Stimulant Medications and Prescribing Practices of Canadian Physicians: Impact of the Health Canada Advisory Pediatrics, October 1, 2008; 122(4): e828 - e834. [Abstract] [Full Text] [PDF]
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 A. W. Loepke and S. G. Soriano An Assessment of the Effects of General Anesthetics on Developing Brain Structure and Neurocognitive Function Anesth. Analg., June 1, 2008; 106(6): 1681 - 1707. [Abstract] [Full Text] [PDF]
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A. J. Rastan, T. Walther, N. A. Alam, I. Daehnert, M. A. Borger, F. W. Mohr, J. Janousek, and M. Kostelka Moderate versus deep hypothermia for the arterial switch operation -- experience with 100 consecutive patients Eur. J. Cardiothorac. Surg., April 1, 2008; 33(4): 619 - 625. [Abstract] [Full Text] [PDF]
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A. J. Shillingford, M. M. Glanzman, R. F. Ittenbach, R. R. Clancy, J. W. Gaynor, and G. Wernovsky Inattention, Hyperactivity, and School Performance in a Population of School-Age Children With Complex Congenital Heart Disease Pediatrics, April 1, 2008; 121(4): e759 - e767. [Abstract] [Full Text] [PDF]
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G. Wernovsky Improving neurologic and quality-of-life outcomes in children with congenital heart disease: Past, present, and future J. Thorac. Cardiovasc. Surg., February 1, 2008; 135(2): 240 - 242. [Full Text] [PDF]
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 R. Pretre and M. I. Turina Deep Hypothermic Circulatory Arrest Card. Surg. Adult, January 1, 2008; 3(2008): 431 - 442. [Full Text]
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J. A. Ballweg, G. Wernovsky, R. F. Ittenbach, J. Bernbaum, M. Gerdes, P. R. Gallagher, T. E. Dominguez, E. Zackai, R. R. Clancy, S. C. Nicolson, et al. Hyperglycemia After Infant Cardiac Surgery Does Not Adversely Impact Neurodevelopmental Outcome Ann. Thorac. Surg., December 1, 2007; 84(6): 2052 - 2058. [Abstract] [Full Text] [PDF]
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 S. P. Miller, P. S. McQuillen, S. Hamrick, D. Xu, D. V. Glidden, N. Charlton, T. Karl, A. Azakie, D. M. Ferriero, A. J. Barkovich, et al. Abnormal Brain Development in Newborns with Congenital Heart Disease N. Engl. J. Med., November 8, 2007; 357(19): 1928 - 1938. [Abstract] [Full Text] [PDF]
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M. V. Johnston Congenital Heart Disease and Brain Injury N. Engl. J. Med., November 8, 2007; 357(19): 1971 - 1973. [Full Text] [PDF]
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 S. P Miller and P. S McQuillen Neurology of congenital heart disease: insight from brain imaging Arch. Dis. Child. Fetal Neonatal Ed., November 1, 2007; 92(6): F435 - F437. [Full Text] [PDF]
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D. E. Creighton, C. M.T. Robertson, R. S. Sauve, D. M. Moddemann, G. Y. Alton, A. Nettel-Aguirre, D. B. Ross, I. M. Rebeyka, and and the Western Canadian Complex Pediatric Therapi Neurocognitive, Functional, and Health Outcomes at 5 Years of Age for Children After Complex Cardiac Surgery at 6 Weeks of Age or Younger Pediatrics, September 1, 2007; 120(3): e478 - e486. [Abstract] [Full Text] [PDF]
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K. R. Kanter, W. T. Mahle, B. E. Kogon, and P. M. Kirshbom What is the Optimal Management of Infants With Coarctation and Ventricular Septal Defect? Ann. Thorac. Surg., August 1, 2007; 84(2): 612 - 618. [Abstract] [Full Text] [PDF]
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A. Sarajuuri, E. Jokinen, R. Puosi, M. Eronen, L. Mildh, I. Mattila, L. Valanne, and T. Lonnqvist Neurodevelopmental and neuroradiologic outcomes in patients with univentricular heart aged 5 to 7 years: Related risk factor analysis J. Thorac. Cardiovasc. Surg., June 1, 2007; 133(6): 1524 - 1532. [Abstract] [Full Text] [PDF]
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M. G. McBride, P. M. Kirshbom, J. W. Gaynor, R. F. Ittenbach, G. Wernovsky, R. R. Clancy, T. B. Flynn, D. M. Hartman, T. L. Spray, R. E. Tanel, et al. Late cardiopulmonary and musculoskeletal exercise performance after repair for total anomalous pulmonary venous connection during infancy J. Thorac. Cardiovasc. Surg., June 1, 2007; 133(6): 1533 - 1539. [Abstract] [Full Text] [PDF]
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J. W. Gaynor, G. Wernovsky, G. P. Jarvik, J. Bernbaum, M. Gerdes, E. Zackai, A. S. Nord, R. R. Clancy, S. C. Nicolson, and T. L. Spray Patient characteristics are important determinants of neurodevelopmental outcome at one year of age after neonatal and infant cardiac surgery J. Thorac. Cardiovasc. Surg., May 1, 2007; 133(5): 1344 - 1353. [Abstract] [Full Text] [PDF]
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H. H. Hovels-Gurich, K. Konrad, D. Skorzenski, B. Herpertz-Dahlmann, B. J. Messmer, and M.-C. Seghaye Attentional Dysfunction in Children After Corrective Cardiac Surgery in Infancy Ann. Thorac. Surg., April 1, 2007; 83(4): 1425 - 1430. [Abstract] [Full Text] [PDF]
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 M. Arrica and B. Bissonnette Therapeutic hypothermia. Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2007; 11(1): 6 - 15. [Abstract] [PDF]
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M. L. Schlunt and S. D. Brauer Anesthetic management for the pediatric patient undergoing deep hypothermic circulatory arrest. Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2007; 11(1): 16 - 22. [Abstract] [PDF]
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G. D. Williams and C. Ramamoorthy Brain monitoring and protection during pediatric cardiac surgery. Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 2007; 11(1): 23 - 33. [Abstract] [PDF]
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P. S. McQuillen, A. J. Barkovich, S. E.G. Hamrick, M. Perez, P. Ward, D. V. Glidden, A. Azakie, T. Karl, and S. P. Miller Temporal and Anatomic Risk Profile of Brain Injury With Neonatal Repair of Congenital Heart Defects Stroke, February 1, 2007; 38(2): 736 - 741. [Abstract] [Full Text] [PDF]
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T. Miura, T. Sakamoto, M. Kobayashi, T. Shin'oka, and H. Kurosawa Hemodilutional anemia impairs neurologic outcome after cardiopulmonary bypass in a piglet model J. Thorac. Cardiovasc. Surg., January 1, 2007; 133(1): 29 - 36. [Abstract] [Full Text] [PDF]
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K. J. Visconti, D. Rimmer, K. Gauvreau, P. del Nido, J. E. Mayer Jr, I. Hagino, and F. A. Pigula Regional Low-Flow Perfusion Versus Circulatory Arrest in Neonates: One-Year Neurodevelopmental Outcome Ann. Thorac. Surg., December 1, 2006; 82(6): 2207 - 2213. [Abstract] [Full Text] [PDF]
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G. Oppido, C. P. Napoleone, S. Turci, B. Davies, G. Frascaroli, S. Martin-Suarez, A. Giardini, and G. Gargiulo Moderately Hypothermic Cardiopulmonary Bypass and Low-Flow Antegrade Selective Cerebral Perfusion for Neonatal Aortic Arch Surgery Ann. Thorac. Surg., December 1, 2006; 82(6): 2233 - 2239. [Abstract] [Full Text] [PDF]
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G. Amir, C. Ramamoorthy, R. K. Riemer, C. R. Davis, F. L. Hanley, and V. M. Reddy Visual light spectroscopy reflects flow-related changes in brain oxygenation during regional low-flow perfusion and deep hypothermic circulatory arrest J. Thorac. Cardiovasc. Surg., December 1, 2006; 132(6): 1307 - 1312. [Abstract] [Full Text] [PDF]
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D. H. Freed, C. M.T. Robertson, R. S. Sauve, A. R. Joffe, I. M. Rebeyka, D. B. Ross, J. D. Dyck, and the Western Canadian Complex Pediatric Therapies P Intermediate-term outcomes of the arterial switch operation for transposition of great arteries in neonates: Alive but well? J. Thorac. Cardiovasc. Surg., October 1, 2006; 132(4): 845 - 852. [Abstract] [Full Text] [PDF]
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 T. Jones and M. Elliott Paediatric CPB: Bypass in a High Risk Group Perfusion, July 1, 2006; 21(4): 229 - 233. [Abstract] [PDF]
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 M. A. Padula and A. M. Ades Neurodevelopmental Implications of Congenital Heart Disease NeoReviews, July 1, 2006; 7(7): e363 - e369. [Full Text] [PDF]
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G. M. Hoffman Neurologic Monitoring on Cardiopulmonary Bypass: What Are We Obligated to Do? Ann. Thorac. Surg., June 1, 2006; 81(6): S2373 - S2380. [Abstract] [Full Text] [PDF]
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T.-Y. Hsia and P. J. Gruber Factors Influencing Neurologic Outcome After Neonatal Cardiopulmonary Bypass: What We Can and Cannot Control Ann. Thorac. Surg., June 1, 2006; 81(6): S2381 - S2388. [Abstract] [Full Text] [PDF]
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J. R. Kaltman, G. P. Jarvik, J. Bernbaum, G. Wernovsky, M. Gerdes, E. Zackai, R. R. Clancy, S. C. Nicolson, T. L. Spray, and J. W. Gaynor Neurodevelopmental outcome after early repair of a ventricular septal defect with or without aortic arch obstruction J. Thorac. Cardiovasc. Surg., April 1, 2006; 131(4): 792 - 798. [Abstract] [Full Text] [PDF]
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L. R. Blackmon, A. R. Stark, and and the Committee on Fetus and Newborn, American A Hypothermia: A Neuroprotective Therapy for Neonatal Hypoxic-Ischemic Encephalopathy Pediatrics, March 1, 2006; 117(3): 942 - 948. [Full Text] [PDF]
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A D Edwards and D V Azzopardi Therapeutic hypothermia following perinatal asphyxia. Arch. Dis. Child. Fetal Neonatal Ed., March 1, 2006; 91(2): F127 - F131. [Abstract] [Full Text] [PDF]
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B. W. McCrindle, R. V. Williams, P. D. Mitchell, D. T. Hsu, S. M. Paridon, A. M. Atz, J. S. Li, J. W. Newburger, and for the Pediatric Heart Network Investigators Relationship of Patient and Medical Characteristics to Health Status in Children and Adolescents After the Fontan Procedure Circulation, February 28, 2006; 113(8): 1123 - 1129. [Abstract] [Full Text] [PDF]
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J. M. Schultz, T. Karamlou, I. Shen, and R. M. Ungerleider Cardiac Output Augmentation During Hypoxemia Improves Cerebral Metabolism After Hypothermic Cardiopulmonary Bypass Ann. Thorac. Surg., February 1, 2006; 81(2): 625 - 633. [Abstract] [Full Text] [PDF]
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J. W. Newburger and D. C. Bellinger Brain Injury in Congenital Heart Disease Circulation, January 17, 2006; 113(2): 183 - 185. [Full Text] [PDF]
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P. S. McQuillen, S. E.G. Hamrick, M. J. Perez, A. J. Barkovich, D. V. Glidden, T. R. Karl, D. Teitel, and S. P. Miller Balloon Atrial Septostomy Is Associated With Preoperative Stroke in Neonates With Transposition of the Great Arteries Circulation, January 17, 2006; 113(2): 280 - 285. [Abstract] [Full Text] [PDF]
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C. L. Dent, J. P. Spaeth, B. V. Jones, S. M. Schwartz, T. A. Glauser, B. Hallinan, J. M. Pearl, P. R. Khoury, and C. D. Kurth Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion J. Thorac. Cardiovasc. Surg., January 1, 2006; 131(1): 190 - 197. [Abstract] [Full Text] [PDF]
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W. T. Mahle, K. J. Visconti, M. C. Freier, S. M. Kanne, W. G. Hamilton, A. M. Sharkey, R. E. Chinnock, K. J. Jenkins, P. K. Isquith, T. G. Burns, et al. Relationship of Surgical Approach to Neurodevelopmental Outcomes in Hypoplastic Left Heart Syndrome Pediatrics, January 1, 2006; 117(1): e90 - e97. [Abstract] [Full Text] [PDF]
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A. H. Schultz, G. P. Jarvik, G. Wernovsky, J. Bernbaum, R. R. Clancy, J. A. D'Agostino, M. Gerdes, D. McDonald-McGinn, S. C. Nicolson, T. L. Spray, et al. Effect of congenital heart disease on neurodevelopmental outcomes within multiple-gestation births J. Thorac. Cardiovasc. Surg., December 1, 2005; 130(6): 1511 - 1516. [Abstract] [Full Text] [PDF]
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C. L. Dent, J. P. Spaeth, B. V. Jones, S. M. Schwartz, T. A. Glauser, B. Hallinan, J. M. Pearl, P. R. Khoury, and C. D. Kurth Brain magnetic resonance imaging abnormalities after the Norwood procedure using regional cerebral perfusion J. Thorac. Cardiovasc. Surg., December 1, 2005; 130(6): 1523 - 1530. [Abstract] [Full Text] [PDF]
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G. Amir, C. Ramamoorthy, R. K. Riemer, V. M. Reddy, and F. L. Hanley Neonatal Brain Protection and Deep Hypothermic Circulatory Arrest: Pathophysiology of Ischemic Neuronal Injury and Protective Strategies Ann. Thorac. Surg., November 1, 2005; 80(5): 1955 - 1964. [Abstract] [Full Text] [PDF]
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F. L. Hanley Religion, politics...deep hypothermic circulatory arrest J. Thorac. Cardiovasc. Surg., November 1, 2005; 130(5): 1236 - 1236. [Full Text] [PDF]
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J. W. Gaynor, S. C. Nicolson, G. P. Jarvik, G. Wernovsky, L. M. Montenegro, N. B. Burnham, D. M. Hartman, A. Louie, T. L. Spray, and R. R. Clancy Increasing duration of deep hypothermic circulatory arrest is associated with an increased incidence of postoperative electroencephalographic seizures J. Thorac. Cardiovasc. Surg., November 1, 2005; 130(5): 1278 - 1286. [Abstract] [Full Text] [PDF]
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L. Wise-Faberowski, H. Zhang, R. Ing, R. D. Pearlstein, and D. S. Warner Isoflurane-Induced Neuronal Degeneration: An Evaluation in Organotypic Hippocampal Slice Cultures Anesth. Analg., September 1, 2005; 101(3): 651 - 657. [Abstract] [Full Text] [PDF]
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I. Hagino, V. Anttila, D. Zurakowski, L. F. Duebener, H. G.W. Lidov, and R. A. Jonas Tissue oxygenation index is a useful monitor of histologic and neurologic outcome after cardiopulmonary bypass in piglets J. Thorac. Cardiovasc. Surg., August 1, 2005; 130(2): 384 - 392. [Abstract] [Full Text] [PDF]
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 S. G Raja, A. Shauq, and M. Kaarne Outcomes after Arterial Switch Operation for Simple Transposition Asian Cardiovasc Thorac Ann, June 1, 2005; 13(2): 190 - 198. [Abstract] [Full Text] [PDF]
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A. Undar, W R. Owens, M. C. McGarry, D. L Surprise, V. D Kilpack, M. W Mueller, E D. McKenzie, and C. D Fraser Jr Comparison of hollow-fiber membrane oxygenators in terms of pressure drop of the membranes during normothermic and hypothermic cardiopulmonary bypass in neonates Perfusion, May 1, 2005; 20(3): 135 - 138. [Abstract] [PDF]
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P. M. Kirshbom, T. B. Flynn, R. R. Clancy, R. F. Ittenbach, D. M. Hartman, S. M. Paridon, G. Wernovsky, T. L. Spray, and J. W. Gaynor Late neurodevelopmental outcome after repair of total anomalous pulmonary venous connection J. Thorac. Cardiovasc. Surg., May 1, 2005; 129(5): 1091 - 1097. [Abstract] [Full Text] [PDF]
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A. Dodge-Khatami, A. Kadner, F. Berger, H. Dave, M. I. Turina, and R. Pretre In the Footsteps of Senning: Lessons Learned From Atrial Repair of Transposition of the Great Arteries Ann. Thorac. Surg., April 1, 2005; 79(4): 1433 - 1444. [Abstract] [Full Text] [PDF]
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E. McGrath, D. Wypij, L. A. Rappaport, J. W. Newburger, and D. C. Bellinger Prediction of IQ and Achievement at Age 8 Years From Neurodevelopmental Status at Age 1 Year in Children With D-Transposition of the Great Arteries Pediatrics, November 1, 2004; 114(5): e572 - e576. [Abstract] [Full Text] [PDF]
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T. P. Graham Jr The year in congenital heart disease J. Am. Coll. Cardiol., June 2, 2004; 43(11): 2132 - 2141. [Full Text] [PDF]
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A. F. Corno A lost opportunity. J. Thorac. Cardiovasc. Surg., June 1, 2004; 127(6): 1857 - 1858. [Full Text] [PDF]
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R. H. Jones The year in cardiovascular surgery J. Am. Coll. Cardiol., May 5, 2004; 43(9): 1706 - 1714. [Full Text] [PDF]
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R. M. Ungerleider and J. W. Gaynor The Boston Circulatory Arrest Study: An analysis J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1256 - 1261. [Full Text] [PDF]
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