Motor outcome after perinatal stroke and early prediction of unilateral spastic cerebral palsy
Introduction
Perinatal stroke is defined as a group of heterogeneous conditions in which a (multi)focal disruption of blood flow secondary to arterial (perinatal arterial ischaemic stroke [PAIS]) or venous (cerebral sinovenous thrombosis [CSVT]) thrombosis or embolization occurred between 20 weeks postmenstrual age and the 28th postnatal day [1]. Haemorrhagic stroke (HS) is also included under the umbrella of perinatal stroke [2]. Primary HS tends to affect near-term and term infants, whereas periventricular haemorrhagic infarction (PVHI) is a lesion that primarily affects preterm infants and is a serious complication of germinal matrix-intraventricular haemorrhage [3,4]. The overall incidence of perinatal stroke is approximately 1:1600–1:2300 live births [5].
After perinatal stroke, 30–68% of the infants develop cerebral palsy (CP), of which unilateral spastic CP (USCP) is the most common form due to the focal nature of the brain injury [[6], [7], [8], [9]]. However, large variations exist between studies and there remains some uncertainty about the outcome according to the type of brain lesion.
CP is typically diagnosed between the ages of 12 and 24 months [10]. However, due to significant activity-dependent cortical plasticity predominantly occurring early in life, it is important to diagnose CP as early as possible to benefit from intervention during this limited time-window [11]. Recently, it has been recommended to combine neonatal magnetic resonance imaging (MRI), a standardized neurological examination with the Prechtl General Movements Assessment (GMA) to predict CP before five months corrected age [11]. Regarding the GMA, in particular, the absence of fidgety movements (FMs) predicts CP with a sensitivity of 98% and a specificity of 94% in high-risk infants [12]. Moreover, other motor signs predictive for USCP may occur at an early age. For example, asymmetric hand function has been identified as one of the earliest clinical signs of USCP [13]. Recently, a new assessment tool was developed for detecting upper limb asymmetry in infants at risk of developing USCP. The Hand Assessment for Infants (HAI) quantifies hand function, both bimanually and for each hand separately, in infants between 3 and 12 months post-term age (PTA) [14]. It has been demonstrated that a unilateral HAI score of the affected hand, in combination with gestational age and gender, predicts USCP before 5 months of age with an accuracy of 93% (95% CI 0.86–100) [15].
Numerous studies have reported outcomes after perinatal stroke or unilateral brain lesions, however, studies on early detection of USCP based on the GMA and HAI are few [[15], [16], [17], [18]]. To our knowledge, no studies have yet compared both tests for early prediction of USCP.
The aims of this study were (1) to report on motor outcomes after perinatal stroke, taking into consideration brain lesion type and timing of injury; (2) to investigate whether there is a difference in early spontaneous movements and motor patterns (as determined using GMA and HAI) between infants who later developed USCP and those who did not; and (3) to determine the predictive value of the GMA and HAI for detection of USCP.
Section snippets
Patients
This was a prospective observational study involving infants with perinatal stroke. The study comprised newborns who were admitted to the neonatal intensive care unit (NICU) of hospitals in Flanders, Belgium (UZ Gent, AZ Sint-Jan Brugge, UZ Leuven, UZ Brussel, UZ Antwerpen and ZNA Middelheim), between October 2015 and October 2018. Inclusion criteria were a diagnosis of perinatal stroke confirmed by neonatal brain imaging and having a video recording for the GMA during the fidgety movements
Patients and stroke characteristics
In total, 46 infants were enrolled in the study. Motor outcome was available for 45 infants, resulting in a sample of 45 infants. All infants had one video recording available for GMA and in 35 children, a HAI evaluation was also performed. However, one infant's HAI evaluation was performed at 27 weeks PTA (outside the time frame); thus, these results were not included. The flowchart is depicted in Fig. 1 and the characteristics of the infants are shown in Table 1. Gestational age ranged from
General findings
The present study explored the outcome of perinatal stroke and the possibly early diagnosis of USCP in high-risk infants. To our knowledge, this is the first study to evaluate the predictive value of the GMA and HAI in a sample of patients at high risk of USCP. Our results showed that GMA (absent/sporadic FMs) and the HAI had a good predictive value (≥85% sensitivity) for detecting USCP.
The first aim of this article was to the report motor outcomes after perinatal stroke. Overall, 33% of the
Conclusion
Early diagnosis of CP is important and can lead to early intervention. This study emphasizes that early detection of USCP is possible before the age of 5 months PTA. GMA is feasible in a population with perinatal stroke for early prediction of USCP. However, it is important to note that normal GMA must be interpreted with caution in this particular population, considering the high rates of false positive cases. Furthermore, asymmetrical FMs might be observed, which could be an indicator for
Funding source
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The authors wish to thank all of the infants and families who participated in this study and the physicians who helped recruit the infants. We also wish to thank Randi Tynes Vågen for her input as the third tie-breaking observer for the GMA classification.
References (37)
- et al.
Perinatal stroke
Semin. Pediatr. Neurol.
(2019) - et al.
New insights (and new interrogations) in perinatal arterial ischemic stroke
Thromb. Res.
(2011) - et al.
Early prediction of unilateral cerebral palsy in infants with asymmetric perinatal brain injury - model development and internal validation
Eur. J. Paediatr. Neurol.
(2019) - et al.
Fidgety movements - tiny in appearance, but huge in impact
J. Pediatr.
(2016) - et al.
Are sporadic fidgety movements as clinically relevant as is their absence?
Early Hum. Dev.
(2015) - et al.
Perinatal stroke causes abnormal trajectory and laterality in reaching during early infancy
Res. Dev. Disabil.
(2015) Brain plasticity following early life brain injury: insights from neuroimaging
Semin. Perinatol.
(2010)- et al.
The effectiveness of Baby-CIMT in infants younger than 12 months with clinical signs of unilateral-cerebral palsy; an explorative study with randomized design
Res. Dev. Disabil.
(2018) - et al.
Occurrence of and temporal trends in fidgety general movements in infants born extremely preterm/extremely low birthweight and term-born controls
Early Hum. Dev.
(2019) - et al.
Ischemic perinatal stroke: summary of a workshop sponsored by the national institute of child health and human development and the national institute of neurological disorders and stroke
Pediatrics
(2007)
Diagnosis of perinatal stroke I: definitions, differential diagnosis and registration
Acta Paediatr.
Ultrasonographic features and severity scoring of periventricular hemorrhagic infarction in relation to risk factors and outcome
Pediatrics
Prevalence and predictors of perinatal hemorrhagic stroke: results from the kaiser pediatric stroke study
Pediatrics
Cerebral palsy after perinatal arterial ischemic stroke
J. Child Neurol.
Incidence and outcomes of symptomatic neonatal arterial ischemic stroke
Pediatrics
Neonatal cerebral infarction and neuromotor outcome at school age
Pediatrics
Cerebral palsy--don't delay
Dev. Disabil. Res. Rev.
Early, accurate diagnosis and early intervention in cerebral palsy: advances in diagnosis and treatment
JAMA Pediatr.
Cited by (9)
Neonatal Arterial Ischemic Stroke Secondary to Carotid Artery Dissection: A Case Report and Systematic Literature Review
2023, Pediatric NeurologyCitation Excerpt :All the patients of our series developed important neurological deficits such as unilateral cerebral palsy associated with a severe intellectual disability. When considering NAIS due to other (more frequent) etiologies, disabilities in motor, learning, behavior, language, and mental health are otherwise reported in different grades of severity, in relation with the infarction dimensions.2,4,26,29 As regards epilepsy, it was reported at follow-up in nearly half of patients in our literature cohort, similarly to what was reported for other types of arterial ischemic stroke, which is considered the most frequent stroke category associated with structural epilepsy development (50% of presumed perinatal AIS and 71% of NAIS), probably because of the involvement of the cerebral cortex.
Neurological and Functional Outcomes after Pediatric Stroke
2022, Seminars in Pediatric NeurologyCitation Excerpt :More sensitive measures of UE asymmetry and more detailed long term outcome measures are required to understand the impact of perinatal stroke on participation. Pascal et al. found that even infants with perinatal stroke who did not develop unilateral cerebral palsy had significant asymmetries in hand use,43 suggesting that patients might still have motor disability even without a diagnosis of CP. Important determinants of outcome include size, location, and age of infarct onset.
Early interventions in infants with unilateral cerebral palsy: A systematic review and narrative synthesis
2021, Research in Developmental DisabilitiesCitation Excerpt :Consequently, over the past years, efforts have been made to reduce the average age at CP diagnosis to below the age of twelve months (Maitre, Burton et al., 2020; Maitre, Jeanvoine et al., 2020). Specifically for infants at risk for uCP, the Hand Assessment for Infants was recently developed and seems very promising in diagnosing infants with uCP even before six months of age (Pascal et al., 2020; Ryll et al., 2019; Wagenaar et al., 2020). Such an early diagnosis enables prompt referral to diagnostic-specific centres which allows tailored parental counselling as well as the implementation of early intervention within the clinical care program of these infants, coinciding with improved parental satisfaction and family mental health (Baird et al., 2000; McIntyre et al., 2011; Novak et al., 2017).
Detecting Asymmetry of Upper Limb Activity with Accelerometry in Infants at Risk for Unilateral Spastic Cerebral Palsy
2024, Physical and Occupational Therapy in PediatricsUpper extremity asymmetry due to nerve injuries or central neurologic conditions: a scoping review
2023, Journal of NeuroEngineering and Rehabilitation