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Motor Development of Infants With Univentricular Heart at the Ages of 16 and 52 Weeks

Rajantie, Irmeli PT, MSc; Laurila, Maarit PT, MSc; Pollari, Kirsi PT, MSc; Lönnqvist, Tuula MD, PhD; Sarajuuri, Anne MD, PhD; Jokinen, Eero MD, PhD; Mälkiä, Esko PT, PhD

doi: 10.1097/PEP.0b013e3182a31704
RESEARCH ARTICLE
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Purpose: To compare the motor development of patients with hypoplastic left heart syndrome (HLHS) and other types of univentricular heart (UVH) with peers who are healthy at the ages of 16 and 52 weeks.

Methods: Motor development was assessed with the Alberta Infant Motor Scale (AIMS).

Results: Both the 23 patients with HLHS and the 13 patients with UVH had lower total AIMS scores in both observations than the controls. At the age of 52 weeks, patients with HLHS had significantly lower scores in all 4 AIMS subscales, whereas patients with UVH had lower scores only in the prone and standing subscales.

Conclusion: Motor development of patients with HLHS or UVH is delayed during the first year of life, especially in the prone and standing subscales.

Motor development of infants with univentricular heart is delayed during the first year of life, especially on the prone and standing subscales of the AIMS. Although the AIMS was found to be a valid and reliable tool for this population, the authors believe more items assessing early standing skills would improve discrimination between typical and delayed motor development.

Children's Hospital (Ms Rajantie and Drs Lönnqvist, Sarajuuri, and Jokinen), University of Helsinki, Helsinki, Finland; Department of Neurology (Ms Laurila), Helsinki University Hospital, Helsinki, Finland; Office of the Ombudsman for Children (Ms Pollari), Jyväskylä, Finland; Faculty of Sport and Health Sciences (Dr Mälkiä), University of Jyväskylä, Jyväskylä, Finland.

Irmeli Rajantie, PT, MSc, Children's Hospital, University of Helsinki, PL 280, 00029 HUS, Helsinki, Finland (irmeli.rajantie@hus.fi).

The authors declare no conflict of interest.

Irmeli Rajantie, Maarit Laurila, and Kirsi Pollari were students in the MSc program at the University of Jyväskylä, Faculty of Sport and Health Sciences, at the time this article was written.

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INTRODUCTION AND PURPOSE

Congenital heart defects have a reported incidence of 4 to 8 per 1000 live births and encompass a broad spectrum of disorders. Two percent of these children have a single functioning ventricle, hypoplastic left heart syndrome (HLHS) or other types of functionally univentricular heart (UVH).1,2 Hypoplastic left heart syndrome refers to a constellation of cardiac anomalies characterized by marked hypoplasia or absence of the left ventricle and severe hypoplasia of the ascending aorta.3 Univentricular heart is a term used to describe a wide variety of structural cardiac abnormalities associated with a single functional ventricular chamber.2 These disorders are among the most serious congenital heart defects and used to be fatal in early infancy.4 The outcome has dramatically changed after Norwood et al5 presented in 1980 a 3-phase operation to reconstruct an univentricular heart by connecting the small aorta to the main pulmonary artery, enlarging the atrial septal defect, and connecting the caval veins directly to the pulmonary circulation. The first operation is performed within the first postnatal week, the second at the age of 3 to 6 months, and the third at the age of 2 to 3 years. With these procedures, 5-year survival rates have been reported to be 50% to 70% for HLHS and up to 90% for other forms of UVH, and the rates seem to be increasing because of improving surgical as well as pre- and postoperative treatment.6,7

Severe congenital heart defects such as HLHS and UVH and their reconstructive surgery may cause widespread neurodevelopmental sequelae characterized by cognitive impairment, speech and language abnormalities, impaired visuospatial and visuomotor skills, motor delays, and learning disabilities.8–10 Patients with HLHS have been found to have higher risk for neurodevelopmental deficits than those with other forms of UVH.9 The mechanisms behind these sequelae are likely multifactorial including abnormal fetal blood flow, chronic cyanosis, cardiopulmonary bypass used during the operations, pre- and postoperative hemodynamic instability, cardiac arrhythmias, and cerebrovascular accidents all having potentially deleterious effects on neurodevelopment.11 According to Watanabe et al,12 the global volume of gray matter was significantly reduced in patients with congenital heart disease compared with normal controls. The study also revealed that preoperative hypoxia is strongly associated with decreased frontal gray matter volume as well as a diagnosis of hypoplastic left heart syndrome. Reduced frontal gray matter volume weakly correlates with psychomotor development.

Consequently, the neurodevelopment of these children, including the motor performance of survivors, has become a focus of interest. Infants with HLHS or UVH show delayed motor development at the age of 1 year.13–16 According to Sarajuuri et al13 the development of gross motor function of these patients particularly is impaired. The delay in their motor development can be partly due to immobilization resulting from the 1 to 2 operations performed during the first year of life. However, according to several studies, a delay in motor development is common until adolescence in survivors of open heart surgery.7,17–21 Also the aerobic capacity of these children has been reported to be markedly reduced.18,22,23 We did not find any studies describing or analyzing the various components of the delay in motor development. Early recognition and characterization of the developmental delay is necessary to support the motor development of these children.

The aim of this prospective cohort study was to compare motor development of patients with HLHS and UVH with peers who are healthy at the age of 16 and 52 weeks. We also wanted to find out if differences in early motor development between children with HLHS and children with UVH could be found. This study was part of a larger study on the overall neurological development of children with univentricular heart.13

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METHODS

Participants

Fifty-seven patients with HLHS or UVH were admitted to the Children's Hospital, University of Helsinki, between August 2002 and February 2005 and those operated on were offered the possibility to participate in a prospective neurodevelopmental follow-up study.13 In the Finish population of 5.3 million, all pediatric cardiac surgery is performed at this hospital. Two patients with HLHS were not actively treated. One patient was excluded because of an additional thoracoabdominal defect and 2 others because of a chromosomal defect. Nine patients were not included because they failed to provide parental consent. Five patients died before the first observation. One patient was unable to participate in both observations because of inconvenient assessment times and 1 could not participate because of a tracheostomy. The final number of patients with HLHS was 23 and those with UVH equalled 13. Diagnoses of the patients with functionally univentricular heart are listed in Table 1. After a pediatric check-up with normal findings, 47 infants were recruited from low-risk deliveries at the Department of Obstetrics and Gynecology of the Helsinki University Hospital to serve as controls. The age and gender distributions (61% boys among patients and 66% among the controls) as well as 1-minute Apgar scores and gestational age of the patients and controls were similar. All children with HLHS and 5 children with UVH went through the Norwood operation (Table 2).

TABLE 1

TABLE 1

TABLE 2

TABLE 2

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Procedures

Two trained and blinded pediatric physical therapists carried out all assessments, which were recorded on videotape and analyzed according to the Alberta Infant Motor Scale (AIMS) manual. The first physical therapy observation was planned to take place at the age of 4 months. By this age, the patients were supposed to have recovered from the first operation and to be scheduled for a hospital visit for a physical examination and various tests before the second operation. The second observation was planned to take place at 12 months of age. This age is commonly used for evaluation of a child's acquisition of motor skills for the upright position and independent walking.13,15,16,24 Furthermore, at 12 months of age, the patients were supposed to have recovered from the second operation.

Written informed consent from all parents was obtained, and the study was approved by the Ethics committee of the Children's Hospital, University of Helsinki.

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Instruments

The AIMS was used to perform the motor assessment.25 The AIMS is routinely used in clinical settings to identify infants with gross motor delay. Several studies have demonstrated the validity and reliability of the AIMS.21,26–28 The AIMS has shown high concurrent validity (r = 0.97-0.99) with the Bayley Scales of Infant Development and the Peabody Developmental Motor Scales.29,30 Interrater reliability throughout all ages has also been found to be high, ranging from 0.96 to 0.99.27,30,31

The AIMS is a norm-referenced performance-based instrument used in observation and evaluation of the quality of motor development in infants from birth to 18 months of age. The test is most sensitive in the first year of life.31 The AIMS is used in the evaluation of postural control in relation to 4 developmental positions with specific criteria for weight-bearing, postural alignment, and antigravity movements. The test contains 58 items including prone (21 items), supine (9 items), sitting (12 items), and standing (16 items) subscales. A separate score for each of the subscales is obtained. The sum of the 4 subscale scores provides the infant's total AIMS score. The normative data of the AIMS allow the determination of the percentile ranking of an infant's motor development with a peer group matched for age.26,32,33

The AIMS follows the neuromaturational concept and the dynamic systems theory and is used to measure gross motor maturation of infants from birth through the age of independent walking. In the AIMS, the effect of the neurological component on motor development is reflected by a sequence of motor skills, which are used as the basis of assessment. The scale follows the principles of dynamic systems because motor skills are tested by observing infants as they move into and out of 4 positions: prone, supine, sitting, and standing. In theory, this assessment should allow the physical therapist to see the interplay of the child's neuromotor systems within the specific physical context of the motor task.27 The focus of the AIMS is on the assessment of qualitative and functional dimensions of movement rather than on acquisitions of single motor skills.

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Data Analysis

The results are presented as means with standard deviations or as medians with interquartile range. The 95% confidence intervals (CIs) are given for the most important outcomes.

The AIMS scores of the children were determined as a consensus of 2 physical therapists. We also calculated percentages of observed agreement and weighted Kappa statistics for AIMS subscale scores. We adapted a random coefficient model to analyze the differences in the AIMS scores between groups. This method is suitable in situations where repeated measurements are not equally spaced between subjects. Therefore, we could take the age of a child (time of observation) into account and obtain model-based means for the age of 16 and 52 weeks. Generalized linear models for binomial family (log-link) were used to obtain age adjusted risk ratios for the achievement of AIMS subscale scores between patients with HLHS/UVH and controls.

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RESULTS

Participants

Twenty-three patients with HLHS, 13 patients with UVH, and 47 controls participated in the first and second physical therapy observation. The time point of the first physical therapy observation varied greatly because of changes in the timing of the second operation and the preoperative investigation, the general condition of the patients, and as a result of various family-related factors (Figure 1). After the operations, the study examination was not performed until after a recovery period of 1 month.

Fig. 1

Fig. 1

Two patients with HLHS were diagnosed with developmental delay due to global ischemia during the first operation. One patient with HLHS and 1 with UVH were diagnosed with cerebral palsy because of a perioperative cerebral infarct during the second operation. Physical therapy was initiated for these patients. Also, 3 patients with HLHS and 3 patients with UVH patients received physical therapy during the study because of moderately or severely delayed motor development. The physical therapy intervention started between the ages of 3.5 and 12 months. The motor development of 1 control child was found to be mildly delayed at the age of 10 months and physical therapy was initiated at that point.

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Comparison of the Total AIMS Scores Between Patients and Controls

To compare the motor development of patients with that of the control group, the AIMS scores for motor development was recorded. The model-based mean (95% CI) of the total AIMS score in the control group was 13.6 (12.7-14.4) at the age of 16 weeks and 52.3 (49.6-55.0) at the age of 52 weeks (Figure 2). The patients with HLHS or UVH had lower scores, which differed significantly from the controls in both assessments (P < .001 for each patient group). There was no statistically significant difference between the patients with HLHS and UVH (Table 3).

Fig. 2

Fig. 2

TABLE 3

TABLE 3

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Distribution of the AIMS Subscale Scores

At the age of 16 weeks, the scores of both the patients with HLHS or UVH were lower than the controls in the prone (P < .001) and supine (HLHS P < .001, UVH P < .005) subscales. The patients with UVH differed from controls also in the sitting subscale (P < .001). No difference between the subscale scores of the patients with HLHS and UVH were detected (Figure 3, Table 4).

Fig. 3

Fig. 3

TABLE 4

TABLE 4

At the age of 52 weeks, the patients with HLHS had lower scores than the control group in all 4 AIMS subscales (P < .001), whereas the patients with UVH differed from the controls only in the prone and standing subscales (P < .001). There was no statistically significant difference between the patients with HLHS and UVH (Table 4).

The AIMS scores of controls and the patients with HLHS or UVH were proportioned to the standardized 50–percentage percentile ranks of the AIMS test. The values of patients with HLHS/UVH percentile ranks were 15% lower than the corresponding values of control group. The median of the controls (interquartile range) was 1.00 (0.96-1.05) and the median of patients with HLHS or UVH was 0.85 (0.47-0.96).

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Comparison of Achievement of the AIMS Subscale Maximum Scores at the Age of 52 Weeks

In the prone position, 46% of patients and 94% of controls achieved the maximum level of prone subscale scores. Age-adjusted risk ratio was 2.2 (95% CI: 1.5-3.1, P < .001). In the supine position, 71% of patients and 100% of controls achieved the maximum level of supine subscale scores. The age-adjusted risk ratio was 1.5 (95% CI: 1.2-1.8, P < .001).

In the sitting position, 69% of patients and 96% of controls reached the maximum level of sitting subscale scores. The age-adjusted risk ratio was 1.5 (95% CI: 1.2-1.8, P < .001). Nine percent of patients and 26% of controls acquired the highest level of standing subscale scores. The age-adjusted risk ratio was 5.0 (95% CI: 3.2-8.0, P < .001) (Figure 4).

Fig. 4

Fig. 4

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DISCUSSION

In our study, the motor development of patients with HLHS or UVH was found to be delayed during the first year of life as has been demonstrated in other studies.9,17,18,20,21 According to Sarajuuri et al, the motor skills of children with UVH and HLHS were significantly lower than for control subjects at the age of 1 year.13 Also, they found psychomotor development of patients with HLHS and with UVH was significantly inferior to that of control subjects at the age of 30.2 months.34 The total AIMS scores were similarly inferior in patients with HLHS and UVH in our study. Patients were at risk for motor delay because of impaired fetal, pre- and perioperative cerebral blood flow. Also, the immobilization related to several exhausting operations during the first year of life might have influenced the child's motor development. There are also studies indicating that parental overprotection may hinder a child's motor development.35,36

In this study, we present a detailed analysis of motor development of patients with HLHS/UVH during the first year of life by comparing the motor development of these children with controls who were healthy using the 4 AIMS subscales (prone, supine, sitting, and standing). At the age of 16 weeks, the difference between patients with HLHS and the controls was smaller than that between patients with UVH and the controls. At the age of 52 weeks, patients with HLHS differed in all AIMS subscale scores from controls whereas patients with UVH differed only in the prone and standing subscale scores. All patients with HLHS and 5 patients with UVH went through 2 phases of the Norwood operations during this assessment period. This fact was associated with the components of delay in the early motor development of patients. The prone subscale was the most demanding for both HLHS and UVH groups in both observations. Only half of the patients reached the maximum scores in the prone subscale at the age of 52 weeks. By this age, children are supposed to attain the skills in the prone subscale. Also, the standing subscale appeared to be more demanding for patients at the age of 52 weeks compared with healthy controls. Almost all the controls reached the maximum scores in all AIMS subscales except in the standing subscale at the age of 52 weeks.

Because of several exhausting operations and the recommendation not to lie in the prone position during the first month postoperatively, patients with HLHS/UVH were not able to practice age-related motor skills such as upper extremity weight-bearing, weight shift, rotations, and head and trunk control against gravity. Normally, these particular skills appear during the first months of life. The prone position is a crucial element for the development of antigravity movements and upright trunk control.32 According to Dudek-Shriber et al,32 4-month-old infants, who spent less than 30 minutes per day in prone, were intolerant of the prone position. Prone positioning appears to be associated with infant's acquisition of motor milestones and the quality of motor development. Prone positioning provides a basis for the development of more advanced skills.37 Even sleeping position has an effect on the early motor development of the infant. Prone sleepers attain several motor milestones earlier than supine sleepers.38–40

In the supine and sitting subscales, the difference between patients and controls was not as remarkable as that observed in the prone and standing subscales. One third of the patients did not attain the maximum scores in the supine and sitting subscales at the age of 52 weeks. To reach the maximum scores in the supine and sitting subscales, children should be able to roll from supine to prone with rotation, have trunk control for independent sitting, and should easily be able to move in and out of the sitting position. Sitting skills require trunk extension and upper extremity weight-bearing, which is hypothesized to be facilitated in the prone position. Infants, who are provided with the opportunity to be in the prone position, appear to be able to develop movement skills and weight-bearing patterns against gravity which support the attainment of prone milestones and also milestones in the sitting and standing positions.38–40

In this study, only 9% of patients and 26% of infants in the control group reached the maximum AIMS score in the standing subscale at the age of 52 weeks. The reason why only 26% of controls reached the maximum scores in the standing subscale might be influenced by the fact that the assessment was carried out at the time when the infants were in the process of developing standing and independent walking skills. Among children that are typically developing, there is also large variation in milestone acquisition. Some children are not able to stand alone until an average age of 16.9 months and walk alone until an average age of 17.6 months.24 During the process of learning to stand independently, infants must learn to balance within significantly reduced stability limits compared with those used, for example, during sitting, and to control many additional degrees of freedom as they add coordination of the leg and thigh segments to those of the trunk and head.41 Patients with HLHS or UVH had obviously fewer opportunities to practice their motor skills in different positions with the effect most conspicuous in the standing subscale.

The results of this study indicate that the AIMS is a reliable and valid method that can be used for the evaluation and discrimination of the motor development of typically developing children and children with severe heart defects. However, according to our study, there is no statistically significant difference between the early standing skills of patients and controls at the age of 16 weeks in contrast to the standing skills of the groups at the age of 52 weeks. In the AIMS, there are 16 different items to assess standing skills. Most of these items are focused on the infant's ability to reach the standing position and the ability to walk with and without support, whereas there are only 2 to 3 items focused on early standing skills. We argue that including more items assessing early standing skills would improve discrimination between typical and delayed motor development. The AIMS, however, is an appropriate assessment tool that can help to detect the need for physical therapy and determine its timing.

A limitation of this study was that blinding was unsuccessful especially in the first observation because of symptoms and obvious visible signs in the appearance of the patients.

The results of this study provide clinically important information for physical therapists who are expected to evaluate young children and accurately determine whether an infant is eligible for early intervention.

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CONCLUSION

The results of this study indicate that the motor development of children with HLHS or UVH is delayed. Motor development is most delayed in the prone and standing positions. Our results indicate that the AIMS provides a reliable measurement that can be used for the evaluation of motor performance of patients with HLHS or UVH.

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ACKNOWLEDGMENTS

The authors thank Ritva Haajanen, PT, for her valuable work in the motor assessment of these children. They also thank Hannu Kautiainen, BA, and Salme Järvenpää, MSc, for statistical advice and reviewing the statistical analysis of this study.

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Keywords:

hypoplastic left heart syndrome; infant; infant development; motor skills

© 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association.