Etiology-specific differences in motor function after hemispherectomy
Introduction
Functional hemispherectomy is a successful treatment for catastrophic childhood epilepsy caused by hemispheric or unilateral multilobar epileptogenic lesions. The spectrum of neurological deficits that occur after surgery shows a great, and thus far largely unexplained, variance among the operated children, making it difficult to predict functional outcome for individual patients. Consistent with conventional ideas about the neuroanatomy of motor pathways (Kandel et al., 2000), the obligatory ipsilateral corticospinal control of motor function after hemispherectomy is characterized by a hemiparesis in which the arm is more affected than the trunk or leg, with a distal-proximal gradient within the extremities (van Empelen et al., 2004). Nevertheless, hand function after hemispherectomy can vary from no functional use, to the preservation of some functions such as grasping or even individual finger movements (Holthausen et al., 1997, Holloway et al., 2000, Staudt, 2002, Devlin et al., 2003, de Bode et al., 2005).
Although strengthening of ipsilateral corticospinal and corticoreticulospinal connections has been assumed to be a major mechanism associated with partial recovery after brain damage (Staudt, 2004a, Benecke, 1991), the heterogeneity of motor outcomes observed after hemispherectomy indicates that the quality of ipsilateral motor control varies. This may be attributed to differences in reorganizational capacity or plasticity, which is more powerful in the immature nervous system than in the adult brain (Kennard, 1936). In addition, hand function in patients with congenital hemiparesis depending on ipsilateral corticospinal pathways was inversely correlated to the timing of brain lesions or malformations acquired at different gestational ages (Staudt, 2004a).
Children who undergo hemispherectomy suffer brain damage during two separate events: during the structural development of the epileptogenic disorder and during the surgery. Given the decrease in reorganizational capacity during maturation, it is likely that the first occurring event has the highest potential of influencing motor outcome. Indeed, a linear and independent correlation between age at surgery and postoperative hand function is lacking and both supportive and contradictive studies have been reported (Muller et al., 1991, Graveline, 1999, Cukiert et al., 2009). Holthausen et al. (1997) was the first to report that the type of the underlying pathology (i.e. the timing of its ontogeny) might be more important than the age at surgery. Results of the relatively few studies that address the age at ontogeny of the epileptogenic disorder in relation to motor outcome after hemispherectomy, are inconsistent (Holthausen et al., 1997, Devlin et al., 2003, de Bode et al., 2005, Lettori, 2008). Our previous study on motor outcome in twelve children after hemispherectomy suggested a specific time course of motor recovery for different body areas. The influence of underlying pathology was not assessed (van Empelen et al., 2004). In this study we aim to assess time course of motor function recovery of specifically the upper extremity (hand) and of gross motor function in relation to the underlying etiology (as an indication for the time during which the first brain damage occurred) in a large cohort of children who underwent functional hemispherectomy.
Section snippets
Methods
This is a retrospective consecutive cohort study of 35 children who underwent functional hemispherectomy for medically intractable hemispheric epilepsy between 1996 and 2007 in the Wilhelmina Children's Hospital, and in whom longitudinal standardized investigations of motor function were performed. The study was approved by the medical ethical and research committee of the University Medical Center Utrecht, and written informed consent was given by all parents.
Muscle strength
Before hemispherectomy patients with developmental etiologies had a significantly better distal arm and leg strength (p = 0.041 and p = 0.036, respectively) compared to the other patients (Fig. 2).
Two years after hemispherectomy, muscle strength was significantly decreased compared to presurgical values in distal (p = 0.002) and proximal (p = 0.002) arm and distal leg muscles (p = 0.013) in children with developmental etiologies, and in distal arm muscles (p = 0.047) in patients with progressive
Discussion
In our selected etiology cohorts, patients with developmental etiologies had better hand function and distal arm strength prior to surgery than those with other pathologies. After hemispherectomy, however, there was no difference in hand function or arm strength between the groups. Inherently, patients with developmental etiologies more often lost hand function and muscle strength following hemispherectomy. Interestingly, although muscle strength after surgery did not differ between the
Conclusions
Many parents and patients move forward with hemispherectomy knowing that there may be an increase in motor deficits in exchange for the possible benefits of seizure relief. However, to what extent motor function deteriorates is difficult to predict, leaving parents uncertain about their child's future. Our results show that the amount of motor function that is lost differs per etiology group and, more importantly, that certain etiology groups, despite a decrease in hand function and strength,
Acknowledgement
This work was supported by the Epilepsy Fund of the Netherlands [NEF 08-10 to K.B. and K.P.J.B.].
References (35)
- et al.
Outcome after cortico-amygdalo-hippocampectomy in patients with severe bilateral mesial temporal sclerosis submitted to invasive recording
Seizure
(2009) Corticospinal tract development and its plasticity after perinatal injury
Neurosci. Biobehav. Rev.
(2007)Bilateral neuropathologic changes in a child with hemimegalencephaly
Pediatr. Neurol.
(1997)- et al.
Lateralization of motor innervation in children with intractable focal epilepsy—a TMS and fMRI study
Epilepsy Res.
(2010) Early hemispherectomy in catastrophic epilepsy: a neuro-cognitive and epileptic long-term follow-up
Seizure
(2008)- et al.
Residual sensorimotor functions in a patient after right-sided hemispherectomy
Neuropsychologia
(1991) - et al.
Functional recovery in hemiplegic cerebral palsy: ipsilateral electromyographic responses to focal transcranial magnetic stimulation
Brain Dev.
(1999) Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation
Exp. Brain Res.
(1991)- et al.
Cortical reorganization in malformations of cortical development: a magnetoencephalographic study
Neurology
(2004) - et al.
Residual motor control and cortical representations of function following hemispherectomy: effects of etiology
J. Child Neurol.
(2005)
Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence
Brain
Evaluation of gross and fine motor functions in children with hemidecortication: predictors of outcomes and timing of surgery
J. Child Neurol.
The reorganization of sensorimotor function in children after hemispherectomy. A functional MRI and somatosensory evoked potential study
Brain
Prediction of motor functions post hemispherectomy
Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes
Neurology
Principals of Neural Science
Age and other factors in motor recovery for precentral lesions in monkeys
Am. J. Physiol.
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2018, World NeurosurgeryCitation Excerpt :Jonas et al.11 concluded that better preoperative brain development, a shorter seizure history, and better seizure outcomes would consistently lead to better functional outcomes. Van der Kolk et al.15 found that different etiologies might be correlated with differences in functional outcome: patients with developmental (stable and congenital) disease often lose more motor function than patients with acquired disease after hemispherectomy. In the present study, we did not observe a significant difference between etiologic factors and muscle strength; however, we did find that more patients with nonprogressive etiology exhibited improved distal muscle strength in their arms and legs than patients with progressive etiology (7/10 vs. 4/13 and 8/10 vs. 6/13, respectively).
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2018, World NeurosurgeryCitation Excerpt :One of the most obvious complications was hemiparesis, and few studies have focused on evaluating pre- or postoperative motor function,7,12,16,17 which mainly may be due to the limited number of hemispherectomy cases. Most studies on motor function changes after hemispherectomy were case reports and small case series.10,12,18 There are few studies on the prediction of motor function.12
Cerebral plasticity: Windows of opportunity in the developing brain
2017, European Journal of Paediatric NeurologyCitation Excerpt :An intriguing observation here is that there seems to be a distinctive “plasticity capacity” for different brain regions following hemispherectomy. For example, while language and gross motor recovery is more prevalent among subjects, fine motor control and speech recovery is subtle regardless of age at or side of surgery.90,85 Current efforts are being made to evaluate the preoperative use of TMS in guiding epilepsy and tumor resection surgeries.
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2021, Canadian Journal of Neurological Sciences
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