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Right arrow Congenital - cyanotic

Ann Thorac Surg 2007;83:1425-1430
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Attentional Dysfunction in Children After Corrective Cardiac Surgery in Infancy

Hedwig H. Hövels-Gürich, MDa,*, Kerstin Konrad, PhDb, Daniela Skorzenskia, Beate Herpertz-Dahlmann, MDb, Bruno J. Messmer, MDc, Marie-Christine Seghaye, MDa

a Department of Pediatric Cardiology, Aachen University of Technology, Aachen, Germany
b Department of Child and Adolescent Psychiatry, Aachen University of Technology, Aachen, Germany
c Department of Thoracic and Cardiovascular Surgery, Aachen University of Technology, Aachen, Germany

Accepted for publication October 26, 2006.

* Address correspondence to Dr Hövels-Gürich, Department of Pediatric Cardiology, University Hospital, Aachen University of Technology, Pauwelsstr 30, Aachen D-52057, Germany (Email: hhoevels-guerich{at}ukaachen.de).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: Attentional dysfunction in children after corrective cardiac surgery in infancy has rarely been evaluated and is the topic of the present work.

Methods: Forty unselected children, 20 with tetralogy of Fallot and hypoxemia and 20 with ventricular septal defect and cardiac insufficiency, operated on at a mean age 0.7 (SD 0.3) years with deep hypothermic circulatory arrest and low flow cardiopulmonary bypass, were evaluated at mean age 7.4 (SD 1.6) years by the computerized form of the Attention Network Test providing performance measures of three networks of attention: alerting, orienting, and executive control. Parental ratings of attentional dysfunction were derived from the Child Behavior Checklist. Results were compared with healthy controls, between patient groups, and correlated with perioperative risk factors and current neurodevelopmental status.

Results: Executive control was reduced in the tetralogy of Fallot group, alerting and orienting were found normal and not different between patient groups. Durations of aortic cross clamping inversely correlated with orienting; durations of cardiopulmonary bypass correlated with mean reaction time and inversely correlated with executive control. Motor function and acquired abilities correlated with executive control and orienting. Parent-reported problems on the Child Behavior Checklist inversely correlated with executive control and mean accuracy.

Conclusions: Children with preoperative hypoxemia in infancy due to cyanotic cardiac defects are at increased risk for attentional dysfunction in the field of executive control, compared with normal children and with those who have acyanotic heart defects. Besides unfavorable perioperative influences, preoperative hypoxemia is considered responsible for additional damage to the highly oxygen sensitive regions of the prefrontal cortex and striate body assumed to be associated with the executive control network of attention.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Children after cardiac operations for congenital heart defects with cardiopulmonary bypass (CPB) with or without deep hypothermic cardiac arrest (DHCA) are at known risk of later neurodevelopmental impairment and psychosocial maladjustment [1–14]. Vital organ support due to CPB comprises exposure to cerebral embolic injury, cerebral hypoperfusion and systemic inflammatory response; DHCA leads to prolonged complete cerebral ischemia, including impairment of cerebral metabolism and vascular autoregulation. Besides, cooling and rewarming, aortopulmonary collaterals, pH, hematocrit, glucose level and ultrafiltration can influence neurodevelopmental outcome [15, 16]. We recently reported that children after corrective surgery in infancy for tetralogy of Fallot (TOF) or ventricular septal defect (VSD) with combined DHCA and low flow CPB provide a reduced neurodevelopmental outcome in childhood, compared with healthy children, and that patients with preoperative hypoxemia and cyanosis (TOF) are found to be at higher risk for motor dysfunction than are acyanotic children with cardiac insufficiency (VSD) [17].

The aim of the present study was to evaluate objectively long-term attentional functions by means of the Attention Network Test (ANT), a neuropsychological inventory assessing three anatomically and functionally defined attentional networks [18], at a 10-year follow-up period assessing our uniform cohort of children with TOF or VSD at age 5 to 11 years after corrective surgery in infancy [17] in comparison with healthy controls. Information should be obtained whether the preoperative condition of hypoxemia in infancy is associated with increased attention deficits in childhood, compared with the condition of preoperative cardiac insufficiency. A further purpose was to evaluate the influence of potential risk factors in perioperative management and to what degree neurodevelopmental and parent-reported behavioral outcome is related to long-term attentional functions.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Population
The study was approved by the Ethical Medical Committee of the Aachen University of Technology, and written informed consent of the parents was obtained.

The study group comprised a total of 40 unselected children, divided into two subgroups. Group A consisted of 20 patients with TOF (age at corrective surgery 0.7 ± 0 .3 years, age at evaluation 7.4 ± 1.4 years). Group B consisted of 20 patients with VSD (age at corrective surgery 0 .7 ± 0.2 years, age at evaluation 7.4 ± 1.9 years). Preoperative and early postoperative clinical data have been described previously [17]. Socioeconomic status was not different from that of a normal population and not different between groups A and B.

The follow-up study had been performed with respect to neurodevelopmental outcome, as reported previously [17], and with special respect to the assessment of attentional functions. Family history concerning attentional problems was uneventful in all patients.

The study was designed as a case series with published controls and prognostic factor analyses.

Control Group
In order to compare the results of the ANT with those of a group of healthy children, 20 children aged 5 to 11 years (8.1 ± 1.7 years) were selected from an ongoing neurodevelopmental study at the Department of Child and Adolescent Psychiatry. All subjects were carefully screened for childhood psychiatric disorders and neurodevelopmental diseases and matched with respect to sex and age to the patient groups. However, intelligence quotient (IQ), as assessed by the Kaufman Battery of Children [19], was significantly higher in the control group (scale of intellectual function 100 ± 9), compared with the patients [17]; therefore, IQ was included in the analysis.

Surgical Management and Perfusion Methods
Corrective surgery was performed in our institution following standardized DHCA and combined low flow CPB. The protocols of bypass modalities and postoperative care have been described previously [17, 20].

Risk Factors for Attentional Functions
Durations of DHCA, aortic cross clamping, and CPB at surgery, current socioeconomic status, the test results of standardized neurodevelopmental follow-up examinations with respect to motor function, intelligence, and acquired abilities, as recently published [17], as well as parental ratings of attentional dysfunction derived from the Child Behavior Checklist (CBCL [Table 1]) [21, 22] were considered as risk factors for attentional functions.


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  		Table 1 Parental Ratings of Attentional Dysfunction
 
Attention Network Test
Background
An influential model of attentional functions has been developed by Posner and Petersen [23]. This model assumes independent neural networks and neuromodulators to subserve different attentional functions, such as alerting, orienting/reorienting, and executive control. Alerting is defined as achieving and maintaining an alert state, orienting and reorienting is required when stimuli occur outside the current focus of attention, and executive control is defined as resolving conflicts between responses. While the alerting system has been associated with right hemisphere frontal and parietal regions modulated by norepinephrine, attention orienting and reorienting is thought to be achieved by a network lateralized to the right temporoparietal cortex and to the right inferior frontal gyrus and to be modulated by the cholinergic system. The executive control network is assumed to include the anterior cingulate and lateral prefrontal cortex and is modulated by dopamine [24].

Experimental paradigm
For the assessment of attentional functions, we used the computerized version of the ANT [18]. The ANT is a combination of a paradigm developed by Posner [25] and a flanker task [26]. It provides performance measures of three networks of attention using the same task: (1) alertness (Alerting), (2) orientation to and selection of stimuli (Orienting), and (3) executive attention functions (Conflict).

The task was presented on the screen of a 14-inch monitor. Four warning cue conditions (no cue, single center cue, single spatial cue, and double cue) were combined with three target conditions (neutral, congruent, incongruent), resulting in 12 experimental conditions. The target was either a single yellow fish (neutral condition) or a fish surrounded by four other fish pointing in the same direction (congruent condition) or to different directions (incongruent condition). The target array was presented at 1.06 degrees of visual angle below or above the fixation cross. Each fish subtended 1.6° of visual angle. Subjects were asked to react to the direction of the target fish in the central position by pressing the corresponding left or right mouse button. The single cue was an asterisk presented at the position of the fixation cross. In the single spatial cue condition, an asterisk appeared at the location of the following target. The double cue involved an asterisk above and one below the position of the target (Fig 1).


Figure 1
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  		Fig 1. Attention Network Test, experimental paradigm. (RT = reaction time.)

 
Procedure and data analyses
All subjects were tested individually in the morning hours. The ANT session started with 24 practice trials. Subsequently, three experimental blocks followed, each consisting of 48 trials. Each trial started with the presentation of a fixation cross in the center. After 400 to 1,600 ms, the warning cue appeared for 150 ms in trials involving a cue. After a 450-ms fixation period, either a single fish or five fish were presented. The target display disappeared after response but remained 1,700 ms at maximum. Responses were followed by auditory and visual feedback. Incorrect responses were succeeded by a single low tone. Correct responses were followed by a positive jingle and a short animation of the target fish. Subjects were told that the fish in the middle was hungry and that they should feed the hungry fish by pressing the correct key. The whole procedure lasted approximately 25 minutes.

Dependent variables were reaction times and errors across all experimental conditions. Performance measures of the three networks were calculated by subtracting reaction times of two warning cue/target conditions accordant to the following procedure: efficiency of alertness (Alerting effect) was calculated by subtracting reaction times of runs with double cue from runs without cue. The difference between reaction times of runs with spatial cue and reaction times of runs with center cue yielded the measure for visual-spatial shifting (Orienting effect). Performance measure of the executive attention network (Conflict effect) was determined by subtracting reaction times of congruent runs from reaction times of incongruent runs [27].

In addition, all data were standardized according to the performance of the control group correcting for effects of age and IQ. Children were excluded from the analysis when accuracy was below 60% (2 children in the VSD and 2 children in the TOF group).

Statistical Analysis
Results are expressed as mean (SD), or as percentages. Additionally, results were transformed into standardized residual scores according to the results of our normal control group corrected for the effects of age and IQ. For intergroup comparison of mean values, two independent samples t tests were used. For the comparison of three independent groups, analyses of covariance were calculated, including IQ as covariate. For comparison of frequencies, {chi}2 tests were administered. For intergroup comparison of risk factors, the nonparametric Mann-Whitney U test was used. The Spearman correlation coefficient was assessed for correlation of independent parameters. The Bonferroni-Holm procedure was applied where appropriate. Statistical analysis was performed with the SPSS for Windows software, version 13.0 (SPSS GmbH Software, München, Germany).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Acknowledgments
 References
 
Attentional Functions Compared With Healthy Controls and Between TOF and VSD Patients
Group comparisons among the three groups (TOF, VSD, controls) including IQ as covariate revealed a significant group effect only for the conflict system whereas the two other attentional networks (alerting and orienting) as well as the mean reaction time and mean accuracy did not differ between the groups (Table 2). Pairwise analysis of covariance showed a significantly reduced conflict performance in the TOF group when compared with the control group (p = 0.005) as well as with the VSD group (p = 0.04). That was also confirmed by the group comparison of the two patient groups including age- and IQ-corrected standardized residual scores according to the performance of the control group (t = 2.25, p = 0.03). The VSD group tended to have a reduced conflict performance when compared with the control group (p = 0.08).


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  		Table 2 Attentional Network Test (ANT) After Corrective Surgery in Infancy, Comparison Against Healthy Controls
 
Correlations With Risk Factors
On univariate Spearman correlation analyses, durations of aortic cross clamping and CPB, motor function, acquired abilities, parent-reported externalizing problems, and parent-reported attention problems were found correlated to different standardized ANT scores and to the mean accuracy on a significance level of p less than 0.05 (Table 3).


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  		Table 3 Significant Correlations Between Attentional Functions and Risk Factors
 
Duration of aortic cross clamping was inversely correlated with orienting. Duration of CPB showed an inverse correlation with the conflict performance and a positive correlation with mean reaction time. Motor function was correlated with the conflict performance, and acquired abilities were correlated with orienting. Presence of parent-reported externalizing problems on the CBCL had an inverse correlation with the conflict performance, and presence of attention problems on the CBCL was inversely correlated with mean accuracy.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Acknowledgments
 References
 
Corrective surgical procedures for cardiac defects in infancy should carry the chance for a life that might differ less from that of healthy children compared with patients who undergo surgical intervention at a later age. On the other hand, current understanding of mid- and long-term neurology and development of the operated-on children considers multiple, mostly interrelated preoperative, perioperative, and postoperative risk factors that may adversely affect the central nervous system especially, leading to later deficits of attention, behavior, higher-order executive function, handwriting, and school performance [14]. Therefore, the examination of a uniform group of patients after corrective surgery in infancy with a good general and cardiologic health status and normal endurance capacity at follow-up assessment at school age [17] is particularly appropriate to study their long-term attentional outcome in comparison with healthy children. Moreover, comparison of subgroups with preoperative cyanotic and acyanotic cardiac defects should particularly evaluate the impact of preoperative cyanosis in this setting.

The ANT produces reliable single-subject estimates of uncorrelated networks related to three anatomically and functionally defined components of attention: altering, orienting, and executive function [18, 29]. This inventory has been standardized for healthy children [28] and is considered convenient and useful in evaluating attentional abnormalities asscociated with cases of brain injury, stroke, schizophrenia, and attention-deficit disorder. As a computerized measure, it is capable to detect even minor functional differences (in the range of msec), compared with paper-and-pencil inventories. An elevated sensitivity has also been described by Visconti and colleagues [30], who found an increased rate of errors of commission on the computerized Connors Continuous Performance Test of Sustained Attention, compared with the paper-based Trail Making Test. In the present study, we therefore used for the first time the ANT for children after cardiac surgery to examine impacts of hypoxemia and CPB modalities on different regions of the brain and to evaluate potential associations with the results of conventional neurodevelopmental inventories.

An important result of our study was a significant negative influence of preoperative hypoxemia in children with TOF on the executive control system of attention (conflict), compared with healthy controls and with children who have ventricular septal defect and cardiac insufficiency. However, one must consider that this difference might have only been detected because of the high sensitivity of the inventory. Tasks involving conflict have been shown to activate dorsal anterior cingulate (conflict monitoring) and prefrontal brain areas (conflict resolving) [31], which are known to be especially sensitive to reduced oxygen supply, which has also been demonstrated histologically in several experimental animal settings of cardiopulmonary bypass [32–34]. That reduced executive attentional functions were correlated with problems in executive motor functions (gross motor function and coordination) in our study also points to the special involvement of these oxygen-sensitive brain regions. For school-age children after neonatal arterial switch operation for transposition of the great arteries, Bellinger and associates [35] report a more impulsive response style on the test of variables of attention that corresponds to deficits in the performance of the executive control system of attention in our study. This observation, and the additional fact that expressive (executive) rather than receptive functions of speech and language have been found reduced in children after cardiac surgery [2, 4, 35], may point to comparable patterns of brain damage with respect to different higher-order executive motor functions [14].

Parent-reported problems on the CBCL were found to be correlated with reduced attentional functions on the ANT, pointing to a valid association between objective and subjective measures of attention.

Although prolonged durations of CPB and aortic cross clamping were found to be related to reduced orientation to and selection of stimuli (orienting), to a reduced conflict performance, and to a reduced processing efficiency within the networks, quantified by longer reaction times in our study as after neonatal arterial switch operation [18, 35], we could show that our perioperative management of CPB modalities was not associated with generally reduced attention network functions, as demonstrated in our children with VSD and cardiac insufficiency. In our study, however, it was not possible to differentiate, as in the Boston Circulatory Arrest Study [7], the impact of DHCA duration and further perioperative variables on attentional functions because of the uniform bypass modalities and the reduced number of patients. Our results underline the assumption that preoperative hypoxemia in infancy mainly contributes to the risk of reduced attentional functions in later childhood. As our sample size was rather small, however, replication including larger samples is required.

In conclusion, children with preoperative hypoxemia in infancy due to cyanotic cardiac defects are at increased risk for attentional dysfunction with special respect to the network of executive control, representing monitoring and resolving of conflict, compared with healthy children and with children who have acyanotic heart defects and cardiac insufficiency. The Attention Network Test is a useful instrument to detect attentional dysfunctions reflecting distinct oxygen-sensitive brain areas, related to clinically relevant neurodevelopmental disorders in the domains of motor function, academic performance, and parent-reported behavior in school-age children after cardiac surgery for congenital heart disease.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
References
 
The study was supported by grants of "Bundesverband Herzkranke Kinder e.V.," Aachen, Germany.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

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