Elsevier

Epilepsy Research

Volume 103, Issues 2–3, February 2013, Pages 221-230
Epilepsy Research

Etiology-specific differences in motor function after hemispherectomy

https://doi.org/10.1016/j.eplepsyres.2012.08.007Get rights and content

Summary

Prediction of functional motor outcome after hemispherectomy is difficult due to the heterogeneity of motor outcomes observed. We hypothesize that this might be related to differences in plasticity during the onset of the underlying epileptogenic disorder or lesion and try to identify predictors of motor outcome after hemispherectomy. Thirty-five children with different etiologies (developmental, stable acquired or progressive) underwent functional hemispherectomy and motor function assessment before hemispherectomy and 24 months after hemispherectomy. Preoperatively, children with developmental etiologies performed better in terms of distal arm strength and hand function, but not on gross motor function tests. Postoperatively, the three etiology groups performed equally poor in muscle strength and hand function, but gross motor function improved in those with acquired and progressive etiologies. Loss of voluntary hand function and distal arm strength after surgery was associated with etiology, intact insular cortex and intact structural integrity of the ipsilesional corticospinal tract on presurgical MRI scans. In conclusion, postoperative motor function can be predicted more precisely based on etiology and on preoperative MRI. Children with developmental etiology more often lose distal arm strength and hand function and show less improvement in gross motor function, compared to those with acquired pathology.

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)

  • A.M. Devlin et al.

    Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence

    Brain

    (2003)
  • C. Graveline

    Evaluation of gross and fine motor functions in children with hemidecortication: predictors of outcomes and timing of surgery

    J. Child Neurol.

    (1999)
  • V. Holloway et al.

    The reorganization of sensorimotor function in children after hemispherectomy. A functional MRI and somatosensory evoked potential study

    Brain

    (2000)
  • H. Holthausen et al.

    Prediction of motor functions post hemispherectomy

  • R. Jonas

    Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes

    Neurology

    (2004)
  • E.R. Kandel et al.

    Principals of Neural Science

    (2000)
  • M. Kennard

    Age and other factors in motor recovery for precentral lesions in monkeys

    Am. J. Physiol.

    (1936)
  • Cited by (24)

    • Presurgical Thalamus and Brainstem Shifts Predict Distal Motor Function Recovery After Anatomic Hemispherectomy

      2018, World Neurosurgery
      Citation 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).

    • Asymmetry of Cerebral Peduncles for Predicting Motor Function Restoration in Young Patients Before Hemispherectomy

      2018, World Neurosurgery
      Citation 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 Neurology
      Citation 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.

    • TMS Mapping of Motor Development After Perinatal Brain Injury

      2016, Pediatric Brain Stimulation: Mapping and Modulating The Developing Brain
    • Hemispherotomy for Epilepsy: The Procedure Evolution and Outcome

      2021, Canadian Journal of Neurological Sciences
    View all citing articles on Scopus
    1

    Tel.: +31 243613396; fax: +31 243541122.

    2

    Tel.: +31 887554003; fax: +31 887555350.

    3

    Tel.: +31 887554030; fax: +31 887555333.

    4

    Tel.: +31 88-7557977; fax: +31 302542100.

    View full text