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J Thorac Cardiovasc Surg 2002;124:448-458
© 2002 The American Association for Thoracic Surgery
Surgery for Congenital Heart Disease (CHD) |
From the Departments of Pediatric Cardiology,a Neurolinguistics,b Pediatric Neurology,d and Thoracic and Cardiovascular Surgery,e Aachen University of Technology, and the Institute for Medical Research and Information Processing,c Repges & Partner, Aachen, Germany.
Supported by grants of Deutsche Stiftung für Herzforschung, Frankfurt/Main, and Bundesverband Herzkranke Kinder e.V., Aachen, Germany.
Received for publication June 28, 2001. Revisions requested Nov 5, 2001; revisions received Nov 14, 2001. Accepted for publication Dec 14, 2001. Address for reprints: Hedwig H. Hövels-Gürich, MD, Department of Pediatric Cardiology, Aachen University of Technology, Pauwelsstr 30, D-52057 Aachen, Germany (E-mail: hhoevels-guerich{at}ukaachen.de).
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.04 for each). Overall rate of developmental impairment in one or more domains was 55%, compared with 26% at age 5.4 years. Multivariable analysis showed that severe preoperative acidosis and hypoxia predicted reduced motor function (mean deficit 52.7 points, P < .001), whereas longer bypass duration predicted both neurologic (odds ratio per 10 minutes of bypass duration 1.8, P = .04) and speech (odds ratio per 10 minutes of bypass duration 1.9, P = .02) dysfunction, and perioperative and postoperative cardiocirculatory insufficiency predicted neurologic (odds ratio 6.5, P = .04) and motor (mean deficit 6.8 points, P = .03) dysfunction. |
Introduction |
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The arterial switch operation (ASO) to correct transposition of the great arteries (TGA) in neonates has been globally accepted as the method of choice because of low perioperative and postoperative mortality and good midterm results with respect to the cardiologic outcomes and endurance of these children. Concern, however, has been raised by the occurrence of neurologic dysfunction and developmental sequelae that may accompany neonatal cardiac surgery supported by continuous low-flow cardiopulmonary bypass (CPB), either isolated or combined with deep hypothermic cardiocirculatory arrest (DHCA).
Previously, we reported midterm results of cognitive and motor development in preschool- and school-aged children at a mean age of 5.4 years after neonatal ASO performed between 1986 and 1992 with combined DHCA and low-flow CPB.
1 Our patient group had reductions in neurologic and fine and gross motor functions, vocabulary, and acquired abilities, but was within the reference range for formal intelligence testing. In contrast, a second group of children who had undergone ASO between 1994 and 1995 and were assessed in our institution at a mean age of 3.6 years revealed remarkably less developmental impairment than seen in our older children. 2 Midterm results of the Boston Circulatory Arrest Study at the age of 4 years after neonatal ASO 3 demonstrated reduced performance of the full cohort with respect to several domains of testing, including neurologic and motor functions, intelligence, and language. Use of circulatory arrest was associated with worse outcomes in motor and speech functions than seen with the preponderant use of low-flow CPB. Recent results of a developmental evaluation of children aged 3 to 5 years after corrective infant cardiac surgery, including patients after neonatal ASO, add to the evidence of risks concerning neurologic and cognitive function but do not support the assumption of increased risk using cardiac arrest. 4
Limited conclusions can be drawn from these findings with respect to the impact of the different bypass strategies and their concomitant modalities and the impact of preoperative and postoperative risk parameters on final developmental status after neonatal corrective cardiac surgery. The aim of this study was therefore to evaluate for the first time long-term neurologic, motor, cognitive, academic, language, and speech development 10 years after ASO by reassessment of our uniform group of children with TGA. 1 Further information should be obtained as to which factors in preoperative, perioperative, and postoperative management influence long-term outcome and to what degree neonatal surgery performed with DHCA and with CPB by itself may contribute to neurologic and developmental impairment in older school-aged children and adolescents.
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Methods |
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1 In 2000, at a mean (± SD) age of 10.5 ± 1.6 years (range 7.9-14.3 years), 60 of them were reevaluated. The remaining 17 patients were evaluated with a questionnaire. There were no further late deaths. All patients, except those with cerebral palsy, had normal endurance capacity, and none received any cardiac-related medication.
Our study was approved by the ethical medical committee of the Aachen University of Technology, Aachen, Germany, and written informed consent was obtained from the patients and their parents. The study comprised a longitudinal comparison with our former evaluation 1 and was designed as a case series with published controls and prognostic factor analyses. The study group consisted of 60 unselected children (77.9% of the survivors), 46 (76.7%) of whom were male and 14 (23.3%) of whom were female. Socioeconomic status of the families 5 was not different from that of a general population (P = 0.11, 
2 test). Seventy-three percent had a simple TGA, 17% in addition had an unimportant ventricular septal defect, 3% had a ventricular septal defect closed during ASO, and 7% had a coarctation of the aorta corrected later. Eighty-five percent of the neonates had undergone atrial balloon septostomy, and all had been treated with prostaglandin E1 before the operation.
Questionnaires for the 17 patients who did not participate in the present follow-up study were completed by the parents and by the treating pediatricians and pediatric cardiologists; participation was determined mainly by the distance of the family's residence from our institution. The children who did not participate in the study were not different from the study patients with respect to socioeconomic background.
Surgical management and perfusion methods
ASO under conditions of DHCA and combined low-flow CPB was performed in our institution by two surgeons (B. J. Messmer, S. H. Daebritz) according to a standardized technique that was based on the Lecompte modification. The CPB circuit included a roller pump, a disposable membrane oxygenator, and an arterial filter. Cooling and rewarming were carried out with a heat exchanger. After induction of general anesthesia, core cooling on CPB was instituted under full-flow conditions (2.7 L/[m2 body surface area · min]) to reach an esophageal temperature of 14°C to 17°C (15.1°C ± 1.0°C). The temperature of the priming fluid was 20°C to 22°C. The priming solution consisted of a pH-balanced crystalloid solution containing 5% glucose and packed red blood cells to achieve a hematocrit value of the circulating volume of 0.25. The duration of core cooling ranged from 7 to 20 minutes (10.8 ± 2.7 minutes). Duration of DHCA ranged from 51 to 67 minutes (60.0 ± 3.1 minutes), and the aortic crossclamping period ranged from 53 to 96 minutes (65.7 ± 8.1 minutes). The surgical procedure was completed under low-flow conditions with a perfusion rate of 0.7 L/(m2 body surface area · min). Rewarming and preparation for weaning from CPB were achieved under full-flow conditions. Total CPB, including core rewarming time, comprised 42 to 98 minutes (63.4 ± 13.7 minutes). During CPB the pH-stat method was used, correcting arterial carbon dioxide tension (Paco2) to the patient's hypothermic temperature to maintain a pH value of 7.40. At the beginning of CPB, phentolamine (0.1 mg/kg) and (since 1990) sodium nitroprusside were added for vasodilatation. Dexamethasone (3 mg/m2 body surface area) was given before sternotomy. The age at repair for the study group ranged from 2 to 39 days (7.1 ± 5.1 days). Two patients were older than 12 days.
Risk factors for neurodevelopmental outcome
The patients' charts were carefully reviewed with respect to perioperative management and preoperative, perioperative, and postoperative complications. For the analysis of the influence of cerebral risk factors on later outcome, a list of 15 definite variables, available in all cases, was considered (Table 1). 6
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7-9 (Table 2). Isolated nonparalytic strabismus was not classified as neurologic disorder and was excluded from further analysis in this setting.
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The Kiphard and Schilling Body Coordination Test 10 was administered to assess standard scores of gross motor function (motor quotient, MQ).
The Kaufman Assessment Battery for Children 11 was performed to evaluate overall standard score of general intelligence (IQ). A second test block of the same battery was undertaken to evaluate acquired abilities (learning, academic knowledge). Three patients (5%) who were older than 12.5 years were assessed according to the norms for children aged 12.0 to 12.5 years.
Language was assessed by evaluating standard scores of expressive (combination of chosen items comprising subtests 4, 12, 14, and 15 of the Kaufman Assessment Battery for Children) and receptive language (combination of chosen items comprising subtests 7, 13, 14, and 16 of the Kaufman Assessment Battery for Children).
Developmental test results in the patients were compared with the published results of an age-matched healthy, German-speaking population, on which the tests or their German adaptations are based. The incidence of abnormal results in a reference population is by definition 16% (14% below the simple SD but above the double SD and 2% below the double SD).
Examination of speech
At the time of assessment, all children had normal hearing, as evaluated by tone threshold audiometry. Speech was assessed with the Oral and Speech Motor Control test 12 and selected items of the children's battery of the Mayo Tests of Speech and Oral Apraxia, 13 both adapted to the German language by our neurolinguists (W.H. and R.S.). In addition, we performed the German version of the Auditory Closure subtest of the Illinois Test of Psycholinguistic Abilities (ITPA), 14 as well as the Test of Auditory Analysis Skills 15 in a German adaptation (W.H. and R.S.), both of which assess auditory comprehension and phonation. Patients were classified as having a normal or an impaired overall speech function according to the total functional score (TFS) 12 comprising 56 items (maximum 112 points) with respect to function of volitional oral movements, articulation, phonation, and coordination of speech. The cutoff point for an impaired speech function was set at a score of less than 110 points, which is equivalent to the median value reported by Robbins and Klee. 12 Reliability of this classification was verified by relating the additional speech assessments to the TFS.
Statistical analysis
Results are expressed as mean ± SD or as numbers with percentages. For comparison of mean values, t tests were applied; for comparison of frequencies, the 2 test was used. For intergroup comparison of clinical variables, the nonparametric Mann-Whitney U test was applied. For comparison of variables at specific times of assessment within a group, the paired nonparametric Wilcoxon test was used. The Spearman rank correlation coefficient was assessed for correlation of independent parameters, and the Fisher exact test was used for the analysis of contingency tables. An 
adjustment for repeated measures was done according to the Bonferroni-Holm method. To study the impact of risk factors on neurodevelopmental outcome parameters, a multivariable analysis was applied with a generalized linear model for continuous outcome parameters and a logistic regression model for binary outcome parameters with 8 independent risk factors, 4 of which were statistically significant in corresponding univariate analysis: severe preoperative hypoxia, durations of DHCA and CPB, perioperative and postoperative cardiocirculatory insufficiency, perioperative and postoperative resuscitation events, perioperative and postoperative clinical seizures, postoperative intraventricular cerebral hemorrhage, and socioeconomic status.
Multivariate discrimination analysis was performed to test the discriminatory power of neurologic and speech functional scores with respect to combined dysfunctions in the domains of motor, cognitive, and academic abilities.
Statistical analysis was performed with the SPSS for Windows software, version 10.0 (SPSS GmbH Software, München, Germany), and with the Statistical Analysis System, version 8.0 (SAS Institute, Inc, Cary, NC). The term significant was used to indicate purely statistical, not clinical, significance.
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Results |
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. Neurologic dysfunction was found to be associated with lower MQ (P < .001) and IQ (P = .001) and with poorer outcomes for acquired abilities (P = .005) and receptive language (P < .001).
Developmental evaluation
Gross motor dysfunction was found in 26.7% of the patients (11.7% below the simple SD and 15% below the double SD for MQ). Reduced formal intelligence was diagnosed in 18.3% (15% below the simple SD and 3.3% below the double SD for IQ), and dysfunction in academic knowledge (acquired abilities) was diagnosed in 23.3% (18.3% below the simple SD and 5.0% below the double SD). Expressive language was found to be reduced in 18.3% (18.3% below the simple SD) and receptive language was found to be reduced in 21.6% (18.3% below the simple SD and 3.3% below the double SD).
Speech evaluation
Dysfunction of speech was found in 24 of the patients (40%). Distribution of TFS is shown in Table 3A. Significant relationship of TFS classification to the results of the nonparametric Mayo Test for Apraxia of Oral Movements, the ITPA Auditory Closure subtest, and the Test of Auditory Analysis Skills confirmed the reliability of this categorization (Table 3B). None of the speech test results were found to be dependent on age at testing (TFS, Spearman correlation coefficient 0.01, P > .2, Mayo, Spearman correlation coefficient 0.05, P > .2, ITPA, Spearman correlation coefficient 0.2, P > .2, Test of Auditory Analysis Skills, Spearman correlation coefficient 0.18, P = .17). Speech dysfunction was also found to be related to lower MQ and IQ and to poorer outcomes for acquired abilities and expressive and receptive language (Table 3B).
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Overall developmental impairment and longitudinal comparison
Summarizing all examination results, 45% of the study patients were within the test limits with regard to motor, cognitive, academic, language and speech development, as well as neurologic status, whereas 55% showed developmental impairment in one or more domains of evaluation, 13.3% were found to have isolated impairment of speech, and 6.7% revealed dysfunctions in all domains of child development considered in this study.
Compared with our previous results of the same study group examined at a mean age of 5.4 years, 1 acquired abilities were now found to be significantly poorer (P = .02), whereas differences in IQ may have been due to chance (P = .10). The rate of neurologic dysfunction significantly increased, from 9.1% to 26.7% (P = .001), mainly as a result of additional patients showing motor dyspraxia (fine or gross motor coordination disorder). In total, the proportion of patients without any dysfunction decreased from 74% to 45% (Figure 1).
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Influences of preoperative, perioperative, and postoperative risk factors on neurodevelopmental outcomes
Comparison of children with and without impairment revealed that severe preoperative acidosis and hypoxia were related to neurologic and speech dysfunctions (P < .001 and P = .001, respectively, Mann-Whitney U test) and to poorer outcomes with respect to MQ, IQ, acquired abilities, and receptive language (P = .001, P = .004, P = .02, and P = .007, respectively). Duration of CPB was associated with neurologic and speech dysfunctions (P = .001 and P = .003, respectively) and inversely correlated with MQ (Spearman correlation coefficient -0.27, P = .04). Perioperative and postoperative cardiocirculatory insufficiency were related to neurologic dysfunction (P = .02, Mann-Whitney U test). Socioeconomic status was also negatively associated with neurologic and speech functions (P = .02 and P = .009, respectively) and was inversely correlated with standard scores of intelligence and acquired abilities (Spearman correlation coefficient -0.56, P < .001, and Spearman correlation coefficient -0.60, P < .001, respectively), as well as with receptive and expressive language (Spearman correlation coefficient -0.65, P < .001, and Spearman correlation coefficient -0.53, P < .001, respectively). The additional 11 risk factors (Table 1) were not found to be significantly related to any outcome parameters (P > .2 for each).
In the models of multivariable analysis, 7 dependent outcome parameters were considered, each of them related to 8 risk factors as specified previously. Among those, the model was able to confirm 4 variables as independent risk factors with respect to neurodevelopmental outcome. More detailed information is given in Tables 5A and 5B. The presence of severe preoperative acidosis and hypoxia predicted reduced motor function (MQ mean deficit 52.7 points). Duration of CPB was able to predict both neurologic and speech dysfunction (risk elevation 1.8 and 1.9 times, respectively, per 10 minutes of CPB). The presence of perioperative and postoperative cardiocirculatory insufficiency predicted neurologic dysfunction (risk elevation 6.5 times) and motor dysfunction (MQ mean deficit 6.8 points). Socioeconomic status was an independent risk factor for reduced IQ, acquired abilities, and expressive and receptive language.
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Discussion |
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Neurodevelopmental outcomes
Neurologic status
We found marked impairment of clinical neurologic status at age 8 to 14 years after neonatal ASO relative to healthy children and to the results of the same group 5 years ago. 1 The longitudinal increase of neurologic impairment (27%) was due to a higher prevalence of patients with developmental motor coordination disorders, or so-called "soft sign neurology," 8,9,16 rather than to cerebral palsy or organic motor coordination disorders caused by a central or peripheral neurogenic lesion. These soft neurologic signs could not be detected in the previous study because of the earlier developmental stage of the children. Although neurologic dysfunction was mostly mild, clinical relevance of these findings is underlined by significant correlation with motor, cognitive, academic, and psychosocial impairment (Arch Dis Child, in press) in our study group. Our incidence of neurologic impairment was in a range similar to rates reported in other studies for definite neurologic abnormalities among children after neonatal ASO, 3,17 although it was markedly higher than in cohorts operated on later, in 1994 to 1995. 2,4 This may at least in part be due to improved preoperative management, which has been found to exert a significant influence on neurodevelopmental outcome. It must be noted, however, that the children operated later on were younger at examination.
Motor function
Gross motor dysfunction, as judged on the basis of a standardized assessment (MQ), was found to be more prevalent among our patients (27%) than in the general population. This figure is comparable to the frequency of gross motor impairment in our cohort at the age of 5.4 years and to the results in the Boston study at the age of 4 years. 3 The presence of gross motor dysfunction according to MQ showed a high overlap with neurologic abnormalities.
Intelligence
Formal intelligence, as based on IQ assessment, was not reduced relative to healthy children. This finding is consistent with the previous results of our study group 1 and with the results of our recent cohort of younger children, 2 whereas intelligence considerably below population norms after neonatal ASO has been demonstrated in other reports. 3,4,17
Academic achievement
By means of formal testing of acquired abilities, we demonstrated (consistent with another report after neonatal ASO 17) significantly reduced outcomes in age-adapted learning and knowledge relative to the test norms and to the results of the same cohort 5 years ago.
Language and speech
Expressive and receptive language were found to be poorer than population norms among our patients. Speech outcome assessed by the TFS, comprising oral nonspeech functions as well as expressive speech functions (articulation, phonation and coordination), was markedly reduced relative to healthy children. 18 Normal auditory test results demonstrated that this finding could not be attributed to hearing deficits. Rather, general motor dysfunction was present in 40% of the speech-impaired children. In addition, disabilities of central integration appeared to contribute to our high rate of speech dysfunction (40% of the cohort), as suggested by strong correlations of TFS with performance in tests of receptive speech and language. This is underlined by the prevalence of a quite high rate of children with isolated speech impairment (13% of the cohort) without neurologic disorder, in contrast to a minority of children with neurologic disorder who did not have accompanying speech impairment (5% of the cohort). A high prevalence of speech and language dysfunction was also demonstrated in the Boston cohort. 3 In that study as well as in ours, these dysfunctions were strongly associated with motor, cognitive, and academic disabilities, as well as with behavioral and social problems. Therefore speech and language dysfunctions are an important indicator of global developmental impairment. 19-21
Overall impairment
According to the data discussed previously, the increase in detection rate of developmental impairment in one or more domains of assessment (55% vs 26% 5 years ago) is due mainly to the high incidence of neurologic and speech and language disorders, which are more easily detected in older than in younger children.
Risk factors for neurodevelopmental outcomes
The factors influencing neurodevelopmental outcome after neonatal cardiac surgery are complex, involving the interactions of preoperative, perioperative, and postoperative parameters. 22,23 The independent risk factors for neurodevelopmental dysfunction found in this study are discussed here.
Socioeconomic status
In our study group, which represented an even level of socioeconomic status relative to the German population, 5 low socioeconomic status predicted poorer outcome in all cognition-related domains of evaluation as intelligence, academic achievement, and language. This is consistent with similar associations observed in other studies. 3,17 The fact that academic achievement and language in the group as a whole were below expected population norms, however, suggests influences of additional factors.
Preoperative factors
The structural and functional immaturity of the cerebral circulation predisposes the neonate toward acquired cerebrovascular lesions, such as intracranial hemorrhage and hypoxic-ischemic injury. 22 In addition to the well-known general risk of low arterial oxygen saturation in children with cyanotic heart lesions such as TGA, situations of particularly severe preoperative hypoxia, such as were documented in some of our patients before surgery, have a negative impact on later speech and motor functions. Children with TGA represent a group without prevalent risk of genetic abnormality with respect to morbidity of the central nervous system 24 and therefore appear particularly appropriate for investigation of preoperative influences on developmental sequelae after neonatal cardiac surgery. The high incidence of neurobehavioral abnormalities in neonates documented before cardiac surgery and persisting in most after surgery 25 underlines the importance of preoperative brain injury for later developmental outcome. In our study, the outcome of motor development was primarily predicted by severe preoperative acidosis and hypoxia.
Perioperative and postoperative factors
Although acute manifestations of neurologic injury in the early postoperative period are often transient, they may be predictive of increased long-term neurodevelopmental dysfunction. 26 The risk for brain injury comprises disturbances in post-CPB cerebral perfusion, intrinsic vasoregulation, and cardiocirculatory function. 23 In our study, cardiocirculatory insufficiency, defined as low cardiac output situations resistant to intensive care treatment in the early postoperative period, was found to be an independent risk factor for later neurologic and motor disorders. Postoperative clinical seizures, evident in as many as 15% of neonates after cardiac surgery, 27,28 have been found to be associated with reduced developmental impairment after ASO. 3,29 In our study group, however, no correlation could be detected between the occurrence of clinically detected seizures and later development. This is consistent with our previous results on the same study group at age 5.4 years 1 as well as on our younger cohort 2 and may be due at least in part to the low incidence of clinical postpump seizures in our patients, among whom postoperative electroencephalography was not routinely performed.
Low-flow cardiopulmonary bypass
The technique of vital organ support during cardiac surgery in our institution includes a combination of low-flow CPB and DHCA. The risks of low-flow CPB comprise the exposure to cerebral embolic injury, cerebral hypoperfusion, and global inflammatory response continuing into the postoperative period. 30-32 In this study, longer duration of CPB was detected as an independent risk factor for poorer outcomes in neurologic and speech functions at age 10.5 years after ASO, whereas it had marginally increased the risk of intellectual impairment at the age of 5.4 years. 1 A recent report on the possibly deleterious effects of CPB on intelligence of patients after surgical closure of atrial septal defect versus those after interventional closure (device implantation) underlines the necessity of a critical attitude with respect to current CPB strategies. 33
Children who needed additional patch closure of a ventricular septal defect, usually associated with longer support times, have been found to be at increased risk for poorer developmental outcomes. 3,34 We could not confirm this observation, probably because of the small number of patients with that constellation.
Deep hypothermic cardiocirculatory arrest
DHCA leads to prolonged complete cerebral ischemia, including impairment of cerebral metabolism and vascular autoregulation. 22,35 Predominant exposure to DHCA, as opposed to predominant use of low-flow CPB, was associated with worse outcomes in motor and speech development at the age of 4 years after neonatal ASO, 3 whereas the institution of cardiac arrest and its duration did not affect neurologic and cognitive outcomes in a group of preschool-aged children after infant heart surgery. 4 In this study, multivariable analysis did not point to DHCA duration, although longer than usual, as an independent risk factor for adverse neurodevelopmental outcome, consistent with our previous findings. 1,2 This underlines results from animal studies, in which neurologic impairment did not occur until circulatory arrest times exceeded 60 minutes. 36
Other aspects of intraoperative management
Adequate degree and duration of the cooling period are important to reach the profoundly hypothermic brain temperatures that lead to sufficient reduction of cerebral metabolism. 37 Too-rapid cooling may exert adverse effects on cognitive functions. 38 Although duration of cooling on CPB in our patients was shorter than recommended, this factor did not have a negative impact on developmental outcome.
There is evidence that cerebral hyperthermia of 2°C or 3°C above core temperatures in children after CPB, as measured by jugular venous bulb temperature, typically occurs in the perioperative period after termination of CPB, inducing the risk of neurologic sequelae caused by hypoxic-ischemic lesions. 36,39,40 Conflicting evidence exists concerning the pH management during CPB. Whereas the pH-stat strategy was found preferable in the postoperative period, 22,41,42 use of the alpha-stat versus the pH-stat acid-base strategy during reparative infant cardiac surgery was not related to either improved or impaired neurodevelopmental outcomes 1 year after surgery. 43 Experimental data recently proved pH-stat CPB management in combination with DHCA to be superior to alpha-stat CPB with respect to neurologic outcome. 44 In our institution, the pH-stat method was always used.
Limitations
In this study the number of patients for multivariable analysis was somewhat limited. Therefore statistical power to identify predictors of developmental delay was limited to those with high associations.
Conclusions
Our study points out that developmental impairment 10 years after neonatal ASO with combined DHCA and low-flow CPB, as performed in our institution, was more prevalent than in both the general population and the same study group at the age of 5 years. Reduced cognitive function according to formal intelligence testing, however, was not observed.
In our experience, the risk of long-term neurodevelopmental impairment after neonatal corrective cardiac surgery is related to the deleterious effects of the global perioperative management and to special adverse effects of prolonged CPB duration. Severe preoperative acidosis and hypoxia and postoperative hemodynamic instability must be considered as important additional risk factors.
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