Early Spontaneous Movements of Infants With Hypoxic-Ischemic Encephalopathy : Pediatric Physical Therapy

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RESEARCH REPORTS

Early Spontaneous Movements of Infants With Hypoxic-Ischemic Encephalopathy

Alkan, Halil PT, PhD; Kahraman, Aysu PT, PhD; Mutlu, Akmer PT, PhD

Author Information
doi: 10.1097/PEP.0000000000000759
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INTRODUCTION

Hypoxic-ischemic encephalopathy (HIE) is a type of brain damage resulting from ischemia and systemic hypoxia due to asphyxia at the placental and pulmonary levels in the fetus and newborn.1 HIE has a prevalence of 3 to 5/1000 live births2 and may lead to cerebral palsy (CP), cognitive delays, epilepsy, and many other permanent neurodevelopmental disorders in children.3

Recovery from damage to a developing brain depends on many factors such as the location and size of the lesion, age, gender, and environment. Owing in part to brain plasticity, early intervention in optimized environmental conditions can enhance recovery.4,5 Therefore, identifying neurological dysfunction as early as possible is important to eliminate or minimize developmental disorders caused by brain damage.6

General movements (GMs) are spontaneous, whole-body motor patterns of varying speeds and amplitudes that appear at about 9 weeks postmenstrual age. At approximately 20 weeks post-term age, they are gradually replaced by voluntary movements. GMs are characterized by a gradual beginning and end, fluency, complexity, elegance, and variability. Based on visual Gestalt perception, GM assessment (GMA) is a noninvasive, fast, inexpensive, and easy neuromotor assessment method that has high reliability and validity and has been used in preterm, term, and post-term aged infants to predict neurological dysfunction.7

GMs are age-specific and classified into 3 main periods, namely preterm, writhing, and fidgety movements (FMs). FMs are reported to be a valid predictor of neurodevelopmental disorders in infants at risk.7–9 Described as small movements of the neck, trunk, and limbs in all directions and of variable acceleration, FMs are present between 9 and 20 weeks post-term age (FM period).10 The absence of FMs in this period is a predictor of CP11,12 or minor neurological dysfunction.12 FMs can also predict various neurodevelopmental disorders such as Rett syndrome and autism and may present as the earliest signs specific to these disorders.11 A detailed evaluation of posture and movements other than FMs can also increase the predictive power in terms of developmental outcomes.12 Therefore, evaluation of FMs as well as concurrent movements and postural patterns in infants with HIE may provide a better understanding of the motor repertoire of these infants and facilitate the development of treatment strategies.

There is no study in the literature evaluating motor repertoire in infants with HIE during the FM period (3-5 months post-term age). Therefore, the aim of the present study was to evaluate the motor repertoire of infants with HIE, to identify concurrent movement and posture characteristics, and to compare them with infants in a group with neurotypical development. We investigated whether changes in motor repertoire were associated with HIE severity. This study sought to answer the following questions:

  1. Do the movements and postures of 3- to 5-month-old infants with HIE differ compared with the group with neurotypical development?
  2. Do the movements and postures of 3- to 5-month-old infants with HIE differ according to the grade of HIE?

METHODS

This retrospective study was carried out in Hacettepe University, Physiotherapy and Rehabilitation Department, Developmental and Early Physiotherapy Unit, between 2016 and 2019. Ethics committee permission was obtained on March 25, 2020, decision number E.4767-4-10.

Participants

Participants were 38 infants (14 females and 24 males) with HIE who were referred to the Developmental and Early Physiotherapy Unit during their FM period. The group with neurotypical development was 38 infants (15 females and 23 males) of the same gestational age who had no serious or risky medical conditions, had undergone GMA at the same age, were followed up until the age of 2 years, and had typical development. Video recordings of infants with HIE and peers in the comparison group were matched on gestational age. Demographic, prenatal, and postnatal data of the infants were collected from the Developmental and Early Physiotherapy Unit database. Preterm infants and those with additional medical problems (such as chromosomal defect, intraventricular hemorrhage, and neuromuscular diseases)12 were excluded from the study. Severity of HIE was recorded from the infants' medical files as grade I, II, or III according to the Sarnat Grading Scale (classifies the degree of encephalopathy based on clinical findings such as level of consciousness, tonus, reflexes, autonomic functions, and seizures).13

General Movements Assessment

From 3 to 5 minutes of video recordings was made of the spontaneous movements of all infants in both the HIE and comparison groups during the FM period. The recordings were made while the infants were awake, active, calm, and lying in the supine position.7,12 The recordings were used for GMA and calculation of the Motor Optimality Score (MOS).12,14

The MOS is the sum of scores in 5 subcategories: FMs, age adequacy of motor repertoire, quality of movement patterns other than FMs, posture, and overall quality of the motor repertoire. The total MOS ranges from a minimum of 5 to a maximum of 28. Scores of 25 or higher indicate optimal motor repertoire, while lower scores indicate less optimal motor repertoire.12,14

Motor repertoire analysis of the infants was performed retrospectively and independently by 2 physical therapists who were certified and experienced in GMA and were blind to the infants' medical histories and neurological conditions. The degree of agreement between the evaluators had an intraclass correlation coefficient (ICC) of 0.983 (95% confidence interval: 0.974-0.989).

Statistical Analysis

Histogram and probability graphs and Shapiro-Wilk analytical tests were used to examine normal distribution of numerical variables. Descriptive statistics were computed as median and interquartile range (25th-75th percentile values) for nonnormally distributed numerical variables and as number and percentage values for categorical variables. The χ2 test was used to compare 2 categorically independent groups. The Mann-Whitney U test was used to compare 2 nonnormally distributed groups, and the Kruskal-Wallis test was used to compare 3 nonnormally distributed groups. Post hoc analyses of 3 nonnormally distributed groups were performed using the Mann-Whitney U test after Bonferroni correction. ICC was used to measure the strength of interevaluator agreement. A P value less than .05 (P < .05) was considered statistically significant. IBM SPSS Statistics version 24.0 software was used for statistical analyses.

RESULTS

The clinical characteristics of the infants are presented in Table 1. Table 2 has a comparison of MOS and subcategory scores between the groups.

TABLE 1 - Clinical Characteristics of Infants in the HIE and Comparison Groups
HIE (n = 38) Neurotypical (n = 38)
Mean (SD) Mean (SD)
Gestational age, wk 38.68 (1.98) 37.02 (3.34)
Birth weight, g 3103 (535) 2828 (757)
n (%) n (%)
Gender
Female 14 (36.8) 15 (39.5)
Male 24 (63.2) 23 (60.5)
Hypothermia treatment
Yes 35 (92.1) ...
No 3 (7.9) 38 (100)
HIE severity
Grade I 21 (55.3) ...
Grade II 12 (31.6) ...
Grade III 5 (13.2) ...
Abbreviations: HIE, hypoxic-ischemic encephalopathy; SD, standard deviation.

TABLE 2 - Comparison of Motor Optimality Score and Subcategory Scores
HIE (n = 38) Neurotypical (n = 38)
Median (IQR) Median (IQR) P Value
Motor Optimality Score 22 (11.25-24) 25.5 (24-26) .000a
n (%) n (%)
Fidgety movements
Absent 9 (23.7) ... .002a
Abnormal 2 (5.3) ...
Normal 27 (71.1) 38 (100)
Age adequacy of motor repertoire
Not age-adequate 14 (36.8) 1 (2.6) .000a
Reduced 13 (34.2) 1 (2.6)
Age-adequate 11 (28.9) 36 (94.7)
Quality of movement patterns other than fidgety movements
N ˂ A 3 (7.9) ... .006a
N = A 3 (7.9) 13 (34.2)
N ˃ A 32 (84.2) 25 (65.8)
Posture
N ˂ A 15 (39.5) 8 (21.1) .102
N = A 9 (23.7) 7 (18.4)
N ˃ A 14 (36.8) 23 (60.5)
Overall quality of the motor repertoire
CS ... ... .442
Abnormal, not CS 29 (76.3) 26 (68.4)
Smooth and fluent 9 (23.7) 12 (31.6)
Abbreviations: A, abnormal; CS, cramped-synchronized; HIE, hypoxic-ischemic encephalopathy; IQR, interquartile range (25th-75th percentiles); N, normal.
aP < .01.

In the HIE group, 9 (23.7%) infants had no FMs, 2 (5.3%) had abnormal FMs, 15 (39.5%) had more abnormal postural patterns than normal patterns, 14 (36.8%) had age-inadequate movements other than FMs, and in 29 (76.3%) infants, movement patterns lacked the normal smooth and fluent character. There were significant differences between the HIE and comparison groups in total MOS and subcategory scores for FMs, age adequacy of motor repertoire, and quality of movement patterns other than FMs (P < .01) but no differences in the other subcategories (P > .05) (Table 2). The median MOS of the group with neurotypical development indicated optimal motor repertoire, while the infants with HIE had lower total MOS and subcategory scores compared with the comparison group.

Table 3 has a comparison of MOS and subcategory scores of the infants according to HIE grade. There were statistically significant differences among HIE grades in MOS and subcategory scores for FMs, age adequacy of motor repertoire, quality of movement patterns other than FMs, and posture (P < .01), but no significant difference in the subcategory of overall quality of the motor repertoire (P > .05). Pairwise comparisons made after the post hoc test supported that infants with grade III HIE had significantly lower scores than those with grade I and II HIE (Table 3). Higher HIE severity was associated with lower MOS and subcategory scores. The median MOS of infants with grade III HIE was 3 times lower than that of infants with grade I HIE.

TABLE 3 - Comparison of Motor Optimality Score Among Infants With HIE According to Severity
HIE
Grade I (n = 21) Median (IQR) Grade II (n = 12) Median (IQR) Grade III (n = 5) Median (IQR) P Post Hoc
Fidgety score 12 (12-12) 12 (1-12) 1 (1-6) .002a I-III
Age adequacy of motor repertoire 2 (2-4) 1 (1-4) 1 (1-1) .030b I-III
Quality of movement patterns other than fidgety movements 4 (4-4) 4 (4-4) 2 (1.5-4) .013b I-III
Posture 4 (2-4) 1.5 (1-2) 1 (1-1) .001a I-II, I-III
Overall quality of the motor repertoire 2 (2-4) 2 (2-2) 2 (2-2) .068
Motor Optimality Score 24 (22-26) 20 (10-23.7) 8 (6.5-14.5) .000b I-II, I-III
Abbreviations: HIE, hypoxic-ischemic encephalopathy; IQR, interquartile range (25th-75th percentiles).
aP < .01.
bP < .05.

DISCUSSION

This study is the first in the literature to investigate in detail the early spontaneous movements of infants with HIE and compare them with peers who are neurotypical. Infants with HIE had lower MOS and subcategory scores for FMs, age adequacy of motor repertoire, and quality of movement patterns other than FMs.

In a predictive study conducted by Soleimani et al,15 15 infants with HIE were evaluated and 8 (47%) had no FMs. The authors reported that these infants later had abnormal neurological outcomes.15 Another predictive study examining the relationship between brain lesions and quality of GMs reported that 18 (52%) of 34 infants with HIE had no FMs.16 Similarly, in a study conducted on 58 infants with HIE, FMs were absent in 41%.17 In our study, 23.7% of the infants with HIE did not have FMs. The present study is similar to these studies; however, we also evaluated MOS and its subcategories and compared the results with a group with neurotypical development.

There are some studies in the literature evaluating MOS and its subcategories in infants in different risk groups other than HIE and comparing them with peers who are neurotypical. In a study evaluating the motor repertoire of 3- to 5-month-old infants with Down syndrome, Herrero et al18 reported that, compared with infants without neurological deficits, infants with Down syndrome had lower values for total MOS and 3 subcategories. Infants with Down syndrome had higher scores in MOS and its subcategories.18 In their prospective study, Yuge et al14 evaluated motor repertoire in a group of infants determined to be at risk during the FM period. The authors determined that infants with outcomes such as CP, genetic diseases, severe developmental retardation, developmental coordination disorder, pervasive developmental disorders, and attention deficit hyperactivity disorder had lower MOS and subcategory scores compared with the infants with normal neurological outcomes.14 Based on these studies, infants with CP had the poorest motor repertoire results in the FM period compared with infants without neurological deficits. In contrast, in a study investigating the motor repertoire of infants with brachial plexus (BP) lesions, there were no statistical differences between the study group and a comparison group in terms of MOS and its subcategories.19 Although there were clinical differences between infants with BP and healthy infants in terms of motor repertoire, these differences were not reflected in the statistical outcomes. This may be because the central nervous system is not affected in infants with BP lesions, and thus the quality of GMs is not significantly affected.

In our study, infants with HIE and infants without neurological deficits had significant differences in the MOS and 3 of its subcategories (FMs, age adequacy of motor repertoire, and quality of movement patterns other than FMs). This is similar to the results of other studies in the literature. Although there were also clinical differences in the other 2 subcategories of the MOS (posture and overall quality of the motor repertoire), the reason for the lack of statistical difference is not clear. However, it may be attributable to the fact that almost all infants with HIE received hypothermia treatment. This may have led to varying degrees of improvement in their motor repertoire, as hypothermia treatment may improve motor outcomes in infants with HIE.20 Further studies are needed to investigate the relationship between hypothermia treatment and the motor repertoire of infants with HIE in the FM period.

Today, GMA is widely used to predict neurodevelopmental disorders as well as to identify disorder-specific movement patterns, mainly in CP.7–9 This is done by means of detailed evaluation to identify absent or abnormal FMs, poor or abnormal movements other than FMs, age-inadequate movements other than FMs, postural abnormalities, and lack of smoothness and fluency in the movements. Future clinical types and functional levels of CP can be predicted by specific abnormal movement patterns that occur during the FM period.8 In our study, 9 (23.7%) infants in the HIE group had no FMs, 2 (5.3%) had abnormal FMs, 15 (39.5%) had more abnormal posture patterns than normal patterns, 14 (36.8%) had age-inadequate movements other than FMs, and the movement patterns of 29 infants (76.3%) lacked the normal smooth and fluent character. Considering that HIE can lead to CP, cognitive delays, epilepsy, and other permanent neurodevelopmental disorders in children,3 future long-term studies are recommended to examine whether the motor repertoire features of infants with HIE in the FM period can be used to reliably predict disease outcomes. Using GMA, Soloveichick et al21 detected abnormal movement patterns in 4 preterm infants with grade III intraventricular hemorrhage. As a result of early rehabilitation interventions for the identified abnormal movement patterns, these infants not only had normal FMs, but they also showed normal neurological development at preschool age.21 The present study also highlights that detecting abnormal movement patterns and posture in infants with HIE is important for early intervention and rehabilitation.

Early identification of infants with motor dysfunction creates an opportunity for necessary interventions.22 In the literature, most of the studies on infants with HIE are follow-up studies investigating long-term neurodevelopmental3,23,24 and motor performance outcomes of HIE.23–26 In a study by Shukla et al,25 the Peabody Developmental Motor Scale-2 was used to evaluate motor performances of 12- to 14-month-old infants with grade II or III HIE. The authors reported that infants with grade III HIE had greater developmental delay in all subcategories (locomotion, stationary, object manipulation, grasping, and visual motor integration).25 In a follow-up study conducted by van Schie et al,23 the motor performance of young children with grade I or II HIE was evaluated using Bayley-2 when the children were 2 years old and the Movement Assessment Battery at age 7. The authors reported that, in both age groups, children with grade I HIE had better motor performance than children with grade II HIE.23 In a similar study, Ellis et al24 reported that 1-year-old infants with grade I HIE had better motor outcomes than those with grade II. Similarly, in our study, infants with grade III HIE had lower MOS total and subcategory scores for FMs, age adequacy of motor repertoire, quality of movement patterns other than FMs, and posture compared with infants with grade I HIE. It was also observed that the infants' MOS total and subcategory scores decreased as HIE grade increased, with the median MOS of infants with grade III HIE being 3 times lower than that of infants with grade I HIE. HIE grade should be taken into consideration when planning and implementing early intervention and rehabilitation for infants with HIE. MOS and posture subcategory scores were also significantly different between grades I and II, with higher scores in grade I. The lack of a significant difference in the overall quality of the motor repertoire subcategory based on HIE grade may be related to the disproportional number of infants in each grade, particularly the very small number in the grade III group. The present study describes the motor repertoire of infants with HIE in the FM period and also documents the association between motor repertoire during the FM period and HIE severity.

Limitations

Our study has some limitations, the first of which is the low number of infants with grade III HIE. Second, since the study data were collected retrospectively from the unit database, the medical data recorded concerning infants in this database are limited by the knowledge level of the registrants.

CONCLUSIONS

Compared with the group with typical neurological development, 3- to 5-month-old infants with HIE had lower MOS and subcategory scores for FM, age adequacy of motor repertoire, and quality of movement patterns other than FMs. In addition, more severe HIE was associated with poorer motor repertoire in these infants. These results suggest that detailed GMA of 3- to 5-month-old infants with HIE can be used for early prediction of possible developmental delays in the future, which will enable early intervention and rehabilitation in this population.

REFERENCES

1. Volpe J. Hypoxic-ischemic encephalopathy. In: Neurology of the Newborn. 5th ed. Philadelphia, PA: WB Saunders Company; 2008:245–400.
2. Lee AC, Kozuki N, Blencowe H, et al. Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990. Pediatr Res. 2013;74(S1):50–72.
3. Shah P, Riphagen S, Beyene J, Perlman M. Multiorgan dysfunction in infants with post-asphyxial hypoxic-ischaemic encephalopathy. Arch Dis Child Fetal Neonatal Ed. 2004;89(2):F152–F155.
4. Kolb B, Mychasiuk R, Williams P, Gibb R. Brain plasticity and recovery from early cortical injury. Dev Med Child Neurol. 2011;53:4–8.
5. Kolb B, Mychasiuk R, Muhammad A, Gibb R. Brain plasticity in the developing brain. Prog Brain Res. 2013;207:35–64.
6. Novak I, Morgan C, Adde L, et al. Early, accurate diagnosis and early intervention in cerebral palsy: advances in diagnosis and treatment. JAMA Pediatr. 2017;171(9):897–907.
7. Einspieler C, Prechtl HF. Prechtl's assessment of general movements: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11(1):61–67.
8. Yang H, Einspieler C, Shi W, et al. Cerebral palsy in children: movements and postures during early infancy, dependent on preterm vs. full term birth. Early Hum Dev. 2012;88(10):837–843.
9. Bruggink JL, Cioni G, Einspieler C, Maathuis CG, Pascale R, Bos AF. Early motor repertoire is related to level of self-mobility in children with cerebral palsy at school age. Dev Med Child Neurol. 2009;51(11):878–885.
10. Einspieler C, Prechtl HF, Ferrari F, Cioni G, Bos AF. The qualitative assessment of general movements in preterm, term and young infants—review of the methodology. Early Hum Dev. 1997;50(1):47–60.
11. Burger M, Louw QA. The predictive validity of general movements—a systematic review. Eur J Paediatr Neurol. 2009;13(5):408–420.
12. Ferrari F, Einspieler C, Prechtl HF, BOS A, Cioni G. Prechtl's Method on the Qualitative Assessment of General Movements in Preterm, Term and Young Infants. London, England: Mac Keith Press; 2004.
13. Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress: a clinical and electroencephalographic study. Arch Neurol. 1976;33(10):696–705.
14. Yuge M, Marschik PB, Nakajima Y, et al. Movements and postures of infants aged 3 to 5 months: to what extent is their optimality related to perinatal events and to the neurological outcome? Early Hum Dev. 2011;87(3):231–237.
15. Soleimani F, Badv RS, Momayezi A, Biglarian A, Marzban A. General movements as a predictive tool of the neurological outcome in term born infants with hypoxic ischemic encephalopathy. Early Hum Dev. 2015;91(8):479–482.
16. Ferrari F, Todeschini A, Guidotti I, et al. General movements in full-term infants with perinatal asphyxia are related to basal ganglia and thalamic lesions. J Pediatr. 2011;158(6):904–911.
17. Cioni G, Prechtl HF, Ferrari F, Paolicelli PB, Einspieler C, Roversi MF. Which better predicts later outcome in fullterm infants: quality of general movements or neurological examination? Early Hum Dev. 1997;50(1):71–85.
18. Herrero D, Einspieler C, Aizawa CYP, et al. The motor repertoire in 3-to 5-month old infants with Down syndrome. Res Dev Disabil. 2017;67:1–8.
19. Kahraman A, Mutlu A, Livanelioglu A. Assessment of motor repertoire in 3-to 5-month-old infants with obstetric brachial plexus lesion. Pediatr Phys Ther. 2020;32(2):114–119.
20. Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev. 2013;2013(1):CD003311.
21. Soloveichick M, Marschik PB, Gover A, Molad M, Kessel I, Einspieler C. Movement Imitation Therapy for Preterm Babies (MIT-PB): a novel approach to improve the neurodevelopmental outcome of infants at high-risk for cerebral palsy. J Dev Phys Disabil. 2020;32(4):587–598.
22. Spittle AJ, Doyle LW, Boyd RN. A systematic review of the clinimetric properties of neuromotor assessments for preterm infants during the first year of life. Dev Med Child Neurol. 2008;50(4):254–266.
23. van Schie PE, Schijns J, Becher JG, Barkhof F, van Weissenbruch MM, Vermeulen RJ. Long-term motor and behavioral outcome after perinatal hypoxic-ischemic encephalopathy. Eur J Paediatr Neurol. 2015;19(3):354–359.
24. Ellis M, Shrestha L, Shrestha P, Manandhar D, Bolam A, De L Costello A. Clinical predictors of outcome following mild and moderate neonatal encephalopathy in term newborns in Kathmandu, Nepal. Acta Paediatr. 2001;90(3):316–322.
25. Shukla T, Shrikhande D, Shrikhande S. The developmental motor outcomes of infants with hypoxic ischaemic encephalopathy II and III between the ages of 12-14 months at Rural Medical College, Loni, Maharashtra. J Adv Med Dental Sci Res. 2018;6(6):109–113.
26. Adhikari S, Rao KS. Neurodevelopmental outcome of term infants with perinatal asphyxia with hypoxic ischemic encephalopathy stage II. Brain Dev. 2017;39(2):107–111.
Keywords:

fidgety movements; general movements; hypoxic-ischemic encephalopathy; infant; Motor Optimality Score

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