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Asymmetry of Cerebral Peduncles for Predicting Motor Function Restoration in Young Patients Before Hemispherectomy
Original Article
Asymmetry of Cerebral Peduncles for Predicting Motor Function Restoration in Young Patients Before Hemispherectomy Xiu-Yu Du1, Si-Chang Chen5, Yu-Guang Guan1,3,4, Jing-Jing Gu1, Meng Zhao1, Tian-Fu Li2, Jun-Hong Pan1, Guo-Ming Luan1,3,4
OBJECTIVE: Hemispherectomy has been used successfully for patients with medically intractable epilepsy. However, it is difficult to predict postoperative motor function. The aim of the present study was to analyze whether the preoperative asymmetry of cerebral peduncles could be used to predict motor function restoration before hemispherectomy for young patients with medically intractable epilepsy.
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METHODS: The clinical record and magnetic resonance imaging data of 53 patients were analyzed retrospectively. The correlation between preoperative cerebral peduncle asymmetry ratio (pCPAR) and pre- and postoperative changes in motor function was evaluated, as well as the influencing factors for pCPAR, such as duration and etiology factors. The restoration of motor function was defined as changes in pre- and postoperative hemiparesis.
pediatric patients with medically intractable epilepsy before hemispherectomy. Most patients with nonprogressive pathology and a duration of more than 5 years presented with greater pCPARs, exhibited better restoration of motor function, and had less risk of worsening hemiparesis.
-
RESULTS: The pCPARs of patients with improved and unchanged hemiparesis were significantly greater than that of worsened patients. Patients with a pCPAR of more than 1.5 had an obvious restorative capacity of motor function of the intact hemisphere, and these patients had a lower risk of worsening hemiparesis. The duration in the improved/unchanged and worsened groups was 5.84 3.85 years and 2.67 2.03 years, respectively. Furthermore, there were more patients with no-progressive pathology in the group in whom pCPAR was more than 1.5.
-
CONCLUSIONS: pCPAR is a useful and objective indicator for predicting the restoration of motor function in
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Key words Asymmetry - Cerebral peduncle - Epilepsy - Hemiparesis - Hemispherectomy -
Abbreviations and Acronyms CST: Corticospinal tract MRI: Magnetic resonance imaging pCPAR: Preoperative cerebral peduncle asymmetry ratio RR: Relative risk
INTRODUCTION
H
emispherectomy is a typical procedure for treating refectory epilepsy, which began in 1938 when McKenzie performed the procedure in an adult patient with intractable epilepsy and obtained a satisfactory outcome.1 Subsequently, this technique has been used increasingly by more neurosurgeons. Furthermore, this method has been reported to have excellent seizure control for medically intractable epilepsy, in which 60%e90% of patients have become seizure free or Engle Ia/b after surgery.1-4 However, the procedure increases brain function defects, such as motor function. Hence, patients and their parents have become reluctant to choose this method to treat epilepsy. Following this, some studies have begun to evaluate motor functions. Functional magnetic resonance imaging (MRI),5,6 transcranial magnetic stimulation,6,7 and diffusion tensor imaging8 examinations mostly have been used to evaluate the restoration of cerebral function of the intact hemisphere. However, these methods are difficult to use in young children because young children often are uncooperative. Studies rarely have evaluated the postoperative recovery of motor function,9-11 mainly because of the few number of proper
From the 1Department of Neurosurgery, Epilepsy Center, Sanbo Brain Hospital, Capital Medical University, Beijing; 2Department of Neurology, Sanbo Brain Hospital, Capital Medical University, Beijing; 3Beijing Key Laboratory of Epilepsy, Beijing; 4Beijing Institute for Brain Disorders, Beijing; and 5Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Guo-Ming Luan, Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.05.057 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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patients with hemispherectomy and the heterogeneity of these patients. Wakamoto et al.8 and Mullin et al.12 conducted an MRI volume analysis of the cerebral peduncle to predict postoperative motor function in patients who undergo hemispherectomy. As described by Mullin et al., with a smaller ratio of ipsilateral to contralateral peduncle, patients may acquire better recovery of motor function after hemispherectomy. The present study showed that the reason for the better recovery of preoperative hemiparesis is the greater contralateral and ipsilateral preoperative cerebral peduncle asymmetry ratio (pCPAR). Our findings were in accordance with the results of Mullin et al.; in our study, the pCPAR was the ratio of contralateral to ipsilateral, and the peduncle ratio in study of Mullin referred to ipsilateral to contralateral. In the present study, we aimed to determine whether pCPAR could be used to predict the restoration of motor function in pediatric patients who are scheduled to undergo hemispherectomy. Our focus was on the correlation between pCPAR and the early period recovery of motor function, as well as its affected factors.
Table 1. Demographic Characteristics and Clinical Data of Patients
Characteristics Sex, male/female
Improved/Unchanged Group (n [ 32)
Worsened Group (n [ 21)
P Value
22/10
11/10
0.229*
Age at onset, years
2.44 2.83
3.67 3.13
0.146y
Age at surgery, years
8.28 3.65
6.33 3.72
0.065y
Duration, years
5.84 3.85
2.67 2.03
0.001y
18/14
10/11
0.538*
Lateral, left/right Surgical methods
0.319*
Anatomical hemispherectomy
16
8
Functional hemispherectomy
5
7
Hemispherotomy
11
6
Etiology
SUBJECTS AND METHODS
Progressive
A total of 53 clinical records and neuroimaging data of 178 patients who underwent hemispherectomy to treat their intractable epilepsy were analyzed retrospectively. The operation method included anatomical hemispherectomy, functional hemispherectomy, and hemispherotomy. These patients were operated in the Epilepsy Center of Sanbo Brain Hospital, Capital Medical University, between September 2004 and July 2016. The recovery of preoperative hemiparesis after hemispherectomy within 1 month mainly was evaluated. pCPAR was measured according to the method of Warabi et al.13 and Mark et al.14 The 53 patients were divided into 2 groups according to whether the patient had improved hemiparesis. Detailed demographic data are presented in Table 1. Inclusion criteria were 1) patients <13 years old at the time of surgery; 2) patients with preoperative hemiparesis; 3) patients who had no severe complications after the operation, such as intracranial infection, hydrocephalus, intracranial hemorrhage and infarction, and severe brain swelling: 4) patients who had no seizure recurrence for at least 1 month after the operation; 5) patients with retrievable MRI data at 1 month before the operation, and no abnormal signals were found in the contralateral hemisphere; and 6) patients with intact clinical data. Exclusion criteria were 1) patients who underwent another brain surgery after the procedure during the follow-up period and 2) patients who were lost to follow-up. According to the aforementioned criteria, a total of 53 patients were enrolled into the study. We evaluated motor function outcomes using a structural questionnaire designed by Moosa et al.15 According to the questionnaire, we defined an unchanged/improved result as “strength of arm and leg has not changed much after surgery, strength is actually better, walks without any aids and assistance” and a worse result as “strength is worse; walk using aids (ankle device such as AFO, walker, etc.), not able to walk at this time and takes few steps when held or assisted, which had not presented before surgery.”
Nonprogressive
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pCPAR, contralateral/ipsilateral
0.000* 10
19
22
2
1.72 0.55
1.23 0.26
0.000y
pCPAR, preoperative cerebral peduncle asymmetry ratio. *Two-tailed t test. yc2 test.
Calculation Method of pCPAR First, we demarcated the boundaries of bilateral cerebral peduncle. Then, we calculated the area of ipsilateral cerebral peduncle (S1 in Figure 1) and the area of contralateral cerebral peduncle (S2 in Figure 1), with pCPAR defined as the value of S2/S1. The cerebral peduncle area was measured by 2 neuroimaging experts using the method reported by Warabi et al.13 (Figure 1) on an MRI workstation. These experts were blinded to the clinical features of each patient. pCPAR was calculated according to the method reported by V. W. Mark, and the ratio was divided into the contralateral peduncle and ipsilateral peduncle (Figure 1). Statistical Methods Data were presented as mean standard deviation. The c2 test was used for categorical data, and the 2-tailed t test was used to compare the means. Relative risk (RR) was calculated by univariate logistic regression analysis for each of the variables measured: age at onset, duration, age at surgery, etiology, and cerebral peduncle asymmetry ratio. A result was considered statistically significant when the P value was <0.05. RESULTS A total of 53 patients (33 male and 20 female patients, 1e13 years old) were enrolled into the study (Table 1). The clinical records and MRI results of these patients were evaluated. Among these
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Figure 1. S1 is the area of ipsilateral cerebral peduncle, S2 is the contralateral, preoperative cerebral peduncle asymmetry ratio ¼ S2/S1. (AeB) Demarcation of medial boundary of peduncles.
patients, 32 patients (60.4%) had improved or unchanged preoperative hemiparesis, whereas 21 patients had a worse result. Among these 53 patients, 24 patients underwent anatomical hemispherectomy, 12 patients underwent functional hemispherectomy, and 17 patients underwent hemispherotomy. The location of the operation was 18 in left hemisphere and 14 in right hemisphere in the improved/unchanged group and 10 in left hemisphere and 11 in right hemisphere in the worsened group, but there was no significant difference between these 2 groups (P ¼ 0.538). The age at onset was 2.44 2.82 years old in the improved/unchanged group and 3.67 3.13 years old in the worsened group, and there was no significant difference between these 2 groups (P ¼ 0.146). The duration in the improved/unchanged group and worsened group was 5.84 3.85 years and 2.67 2.03 years, respectively (P ¼ 0.001). The value of pCPAR was 1.72 0.55 in the improved/unchanged group and 1.23 0.26 in the worsened group (P ¼ 0.000). Two patients with frequent seizures (>30 times per day) had peduncle asymmetry ratios of 1.0 and 1.1, respectively, and the duration was 1.5 and 0.5 years, respectively. However, both patients had improved preoperative hemiparesis immediately after anatomical hemispherectomy. Etiology factors were divided into 2 groups: progressive pathology (Rasmussen encephalitis, hemimegalencephaly, cortical dysplasia, and SturgeeWeber syndrome, or others), and nonprogressive pathology (traumatic brain injury, cerebral hemorrhage due to lack of vitamin K or birth injury, and so on). In this cohort, 10 patients had progressive pathology and 22 patients had nonprogressive pathology in the improved/unchanged group, whereas 19 patients had progressive pathology and 2 patients had nonprogressive pathology in the worsened group (P < 0.01). The relative risk of worsening hemiparesis was greater in patients with a pCPAR of <1.5 (RR ¼ 3.94, P ¼ 0.029) and a duration of <5 years (RR ¼ 5.46, P ¼ 0.01). In this study, there were 30 patients had a pCPAR of <1.5, whereas 23 patients had a pCPAR of >1.5. There were 31 patients with a duration of <5 years and 22 patients with a duration of >5 years. There were 28 patients with preoperative hemiparesis (pCPAR ¼ 1.77 0.57) and 4 patients without preoperative
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hemiparesis (pCPAR ¼ 1.39 0.16) in the improved/unchanged group, and the numbers were 13 (pCPAR ¼ 1.24 0.32) and 8 (pCPAR ¼ 1.21 0.16) in worsened group (P ¼ 0.029). There were more patients in the improved/unchanged group with preoperative hemiparesis and with a greater pCPAR, demonstrating that patients with preoperative hemiparesis and with a greater pCPAR were not likely to be much weaker after surgery and patients with normal motor function and smaller pCPAR were more likely to be weaker after surgery. Among patients with a pCPAR of <1.5, 24 individuals had a progressive pathology and 6 individuals had a nonprogressive pathology. Among patients with a pCPAR of >1.5, 5 individuals had a progressive pathology and 18 individuals had a nonprogressive pathology (c2 ¼ 17.84, P < 0.01; Figure 2A). In total, 17 patients with a duration of <5 years and 4 patients with a duration >5 years were in the worsened group and 14 patients with a duration of <5 years and 18 patients with a duration >5 years were in the improved/unchanged group (c2 ¼ 7.23, P ¼ 0.02; Figure 2B). In total, 18 patients with a pCPAR of <1.5 and 3 patients with a pCPAR >1.5 were in the worsened group and 12 patients with a pCPAR of <1.5 and 20 patients with a pCPAR >1.5 were in the improved/unchanged group (c2 ¼ 11.99, P ¼ 0.01; Figure 2C). In total, 31 patients had a duration of <5 years; among them, 24 had progressive pathology and 7 had nonprogressive pathology; 22 patients had a duration of >5 years, and 5 had a progressive pathology and 17 had a nonprogressive pathology (c2 ¼ 15.54, P < 0.01; Figure 2D). DISCUSSION Hemispherectomy has been used successfully for hemispherical intractable epilepsy because of its excellent seizure control.1 However, postoperative neurologic deficits may be observed in many patients after the procedure. 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 Govindan et al.16 predicted motor function by MRI tractography for an 8-year-old girl and obtained excellent motor function reservation. Zsoter et al.7 used transcranial magnetic stimulation and functional MRI to evaluate the sensorimotor system in 4 patients before hemispherectomy and obtained a favorable and correct prediction of hand motor outcome. However, when correlated to infants or younger children, it was harder to achieve an evaluation because of the difficulty in getting infants or younger children to cooperate. In the present study, we reported a simple method to predict postoperative motor function. The foundation of our research is the different motor pathways in children compared with adults. Benecke et al.17 reported that the ipsilateral corticospinal tract (CST) of the intact hemisphere was the anatomical foundation of motor function recovery in patients with early hemispherectomy, and this view was supported by others.19,20 In the present study, most of the cases were younger children. Hence, the motor pathway was mostly in the CST and cerebral
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Figure 2. The relationship between (A) etiology and preoperative cerebral peduncle asymmetry ratio (pCPARP), (B) duration and motor function recovery, (C) motor function recovery and pCPAR, and (D) etiology and duration. (A) There were 24 patients with progressive pathology with pCPAR <1.5 and 6 with nonprogressive pathology. There were 18 with nonprogressive pathology and 5 with progressive pathology in the group with pCPAR >1.5 (c2 ¼ 17.84, P ¼ 0.000). (B) There were 17 patients with duration <5 years in the worsened group and 4 patients with >5 years. There 18 patients with >5 years and 14 patients
peduncle, which include most CST fibers. This was the reason we choose the cerebral peduncle as an indicator to predict motor function for pediatric patients. Another reason was that brain morphologic changes presented functional changes, although we were not able to clarify the mechanism. Some authors21,22 used brain midline shifting to predict the restoration of consciousness. In the present study, we used cerebral peduncle asymmetry to predict the restoration of motor function. Cerebral peduncle asymmetrical change mainly was ascribed to cerebral functional and structural plasticity and reorganization. After hemispherectomy, the fibers from the affected hemisphere in the ipsilateral cerebral peduncle that dominated motor and sensory function decreased, mainly due to Wallerian degeneration.6-8 In the present study, the results show that patients with greater pCPAR and longer durations may have better motor function restoration in their unaffected hemisphere and lower risk of worsening preoperative hemiparesis, especially in patients with nonprogressive pathology. This result is in accordance with the
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with <5 years in the improved/unchanged group (c2 ¼ 7.23, P ¼ 0.02). (C) There were 18 patients in the worsened group with a pCPAR <1.5 and 3 patients with >1.5. In the improved/unchanged group, there were 20 patients with >1.5 and 12 patients with <1.5 (c2 ¼ 11.99, P ¼ 0.01). (D) There were 24 patients with progressive pathology with duration <5 years and 7 with nonprogressive pathology. There were 17 with nonprogressive pathology and 5 with progressive pathology in the group with duration >5 years (c2 ¼ 15.54, P ¼ 0.000).
study reported by Mullin et al.,12 in which postoperative hemiparesis was predicted by cerebellar hemisphere ratio and the volumetric analysis of peduncles in 22 patients who underwent hemispherectomy. Their findings revealed that if the peduncle ratio (ipsilateral/contralateral) was <0.5, none of the patients would have a worsening hemiparesis. The present result indicates that when the pCPAR was >1.5, patients would obtain an improved or unchanged motor function. In addition, the duration and etiology factors were included in the present study. When etiology factors were considered, we found that patients with a nonprogressive pathology (such as hemispherical encephalomalacia, which is ascribed to burn injury, lack of vitamin K, traumatic brain injury, and so on) mostly had greater pCPAR and experienced better recovery of motor function. van der Kolk et al.10 reported that patients with developing or progressive etiologies (such as Rasmussen encephalitis, hemimegalencephaly, cortical dysplasia, or others) more often lost motor function, and they also highlighted the important role of CST in motor function recovery.
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In the present study, we only evaluated the early recovery of motor function, because we consider that motor function in the early period after surgery may be a better substitute for the real restoration of the intact hemisphere compared with the later period. Some studies reported that postsurgical rehabilitative training could improve motor function,23 not only for animals, but also for humans. Furthermore, many other factors may affect motor function, for example, recurrence of seizures, antiepilepsy drugs, personal development, and so on. However, motor function improved immediately after the operation, which was probably due to the disappearance of the seizure. In the present study, 2 patients who had frequent seizure attacks were accompanied by contralateral hemiparesis. At 2 days after surgery, they became seizure free, and the preoperative hemiparesis obviously improved. Pascoal et al.18 reported that a 17-year-old patient had immediate improvement of motor function after the operation, and the reason lies in the removal of interference of the ipsilateral hemisphere. Another factor that may have influenced pCPAR and motor function was duration, which has not been reported. This present result shows that the pCPAR of patients with a duration of <5 years was lower than patients with a duration of >5 years, and a longer duration experienced better motor function recovery. Another study2 conducted by our team on Rasmussen encephalitis reported that early-stage hemispherectomy does not always achieve better outcomes. Limitations In the present study, although we used stricter inclusion and exclusion criteria, there were some limitations. First, because
REFERENCES 1. Fountas KN, Smith JR, Robinson JS, Tamburrini G, Pietrini D, Di RC. Anatomical hemispherectomy. Childs Nerv Syst. 2006;22: 982-991. 2. Guan Y, Chen S, Liu C, Du X, Zhang Y, Chen S, et al. Timing and type of hemispherectomy for Rasmussen’s encephalitis: analysis of 45 patients. Epilepsy Res. 2017;132:109-115. 3. Verdinelli C, Olsson I, Edelvik A, Hallböök T, Rydenhag B, Malmgren K. A long-term patient perspective after hemispherotomy—a populationbased study. Seizure. 2015;30:76-82. 4. WJ1 Peacock, Wehby-Grant MC, Shields WD, Shewmon DA, Chugani HT, Sankar R, et al. Hemispherectomy for intractable seizures in children: a report of 58 cases. Childs Nerv Syst. 1996;12:376-384.
of the heterogeneity of the patients, it was difficult of determine all influential factors. That is, other factors may have affected motor function, such as genes, medicine, and so on. Second, we excluded patients accompanied by the recurrence of seizure, but seizure may not affect the recovery of motor function. Third, as we described previously, preoperative seizures may affect motor function. Hence, preoperative motor function evaluation may be influenced by these seizures. In addition, because of the limited sample size, it was difficult to attain a very persuasive result. In future studies, we plan to collect more data from multicenter or international cooperations.
CONCLUSIONS pCPAR may provide a prediction for the restoration of motor function of the intact hemisphere before hemispherectomy in young patients with hemispherical intractable epilepsy. A diminished restoration of motor function may reveal a worsening hemiparesis after the operation, which mostly happens for lower pCPAR. pCPAR is affected by etiology and duration. Furthermore, patients with nonprogressive pathology and a duration of >5 years mostly presented with a greater pCPAR, showing better restoration of motor function, and had a less risk of worsening in their preoperative hemiparesis. If the pCPAR were to be used to predict motor function recovery, etiology factors and duration also should be taken into account. However, for high-frequency hemispherical medically intractable epilepsy, stopping the seizure is more important than the reservation of motor function?.
7. Zsoter A, Pieper T, Kudernatsch M, Staudt M. Predicting hand function after hemispherotomy: TMS versus fMRI in hemispheric polymicrogyria. Epilepsia. 2012;53:e98-e101. 8. Wakamoto H, Eluvathingal TJ, Makki M, Juhász C, Chugani HT. Diffusion tensor imaging of the corticospinal tract following cerebral hemispherectomy. J Child Neurol. 2006;21:566-571. 9. Ismail FY, Fatemi A, Johnston MV. Cerebral plasticity: windows of opportunity in the developing brain. Eur J Paediatr Neurol. 2017;21:23-48. 10. van der Kolk NM, Boshuisen K, van Empelen R, Koudijs SM, Staudt M, van Rijen PC, et al. Etiology-specific differences in motor function after hemispherectomy. Epilepsy Res. 2013;103:221-230. 11. van Empelen R, Jennekens-Schinkel A, Buskens E, Helders PJ, van Nieuwenhuizen O. Functional consequences of hemispherectomy. Brain. 2004; 127:2071-2079.
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14. Mark VW, Taub E, Perkins C, Gauthier LV, Uswatte G, Ogorek J. Poststroke cerebral peduncular atrophy correlates with a measure of corticospinal tract injury in the cerebral hemisphere. AJNR Am J Neuroradiol. 2008;29:354-358. 15. Moosa AN, Jehi L, Marashly A, Cosmo G, Lachhwani D, Wyllie E, et al. Long-term functional outcomes and their predictors after hemispherectomy in 115 children. Epilepsia. 2013;54: 1771-1779. 16. Govindan RM, Chugani HT, Luat AF, Sood S. Presurgical prediction of motor functional loss using tractography. Pediatr Neurol. 2010;43:70-72. 17. Benecke R, Meyer BU, Freund HJ. Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation. Exp Brain Res. 1991;83:419-426.
5. de Bode S, Mathern GW, Bookheimer S, Dobkin B. Locomotor training remodels fMRI sensorimotor cortical activations in children after cerebral hemispherectomy. Neurorehabil Neural Repair. 2007;21:497-508.
12. Mullin JP, Soni P, Lee S, Jehi L, Naduvil Valappi AM, Bingaman W, et al. Volumetric analysis of cerebral peduncles and cerebellar hemispheres for predicting hemiparesis after hemispherectomy. Neurosurgery. 2016;79:499-507.
18. Pascoal T, Paglioli E, Palmini A, Menezes R, Staudt M. Immediate improvement of motor function after epilepsy surgery in congenital hemiparesis. Epilepsia. 2013;54:e109-e111.
6. Graveline CJ, Mikulis DJ, Crawley AP, Hwang PA. Regionalized sensorimotor plasticity after hemispherectomy fMRI evaluation. Pediatr Neurol. 1998; 19:337-342.
13. Warabi T, Miyasaka K, Inoue K, Nakamura N. Computed tomographic studies of the basis pedunculi in chronic hemiplegic patients: topographic correlation between cerebral lesion and
19. Nirkko AC, Rösler KM, Ozdoba C, Heid O, Schroth G, Hess CW. Human cortical plasticity: functional recovery with mirror movements. Neurology. 1997;48:1090-1093.
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20. SH1 Jang, Byun WM, Chang Y, Han BS, Ahn SH. Combined functional magnetic resonance imaging and transcranial magnetic stimulation evidence of ipsilateral motor pathway with congenital brain disorder: a case report. Arch Phys Med Rehabil. 2001;82: 1733-1736. 21. Sucu HK, Gelal F, Gökmen M, Ozer FD, Tektas¸ S. Can midline brain shift be used as a prognostic factor to predict postoperative restoration of consciousness in patients with chronic subdural hematoma. Surg Neurol. 2006;66:178-182. 22. Lin CH, Yang JT, Wang TC, Lin MH, Cheng WC, Lee MH. Is preoperative brain midline shift a
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determinant factor for neurological improvement after cranioplasty. J Formos Med Assoc. 2015;114: 577-582. 23. Higo N. Effects of rehabilitative training on recovery of hand motor function: a review of animal studies. Neurosci Res. 2014;78:9-15.
Foundation (2016M601066), the Capital Health Research and Development of Special (2016e1-8012), and Beijing Municipal Science & Technology Commission (Z161100000516230, Z161100002616016). Received 29 January 2018; accepted 9 May 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.05.057 Journal homepage: www.WORLDNEUROSURGERY.org
Conflict of interest statement: This study was supported by the following sources: the Research Fund for the Doctoral Beijing Nova Program (Z141107001814042), Collaboration Between Clinical and Basic Research in Capital Medical University (16JL09), National Natural Science Foundation of China (81671285, 81571275), the China Postdoctoral Science
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.05.057
Asymmetry of Cerebral Peduncles for Predicting Motor Function Restoration in Young Patients Before Hemispherectomy Xiu-Yu Du1, Si-Chang Chen5, Yu-Guang Guan1,3,4, Jing-Jing Gu1, Meng Zhao1, Tian-Fu Li2, Jun-Hong Pan1, Guo-Ming Luan1,3,4
OBJECTIVE: Hemispherectomy has been used successfully for patients with medically intractable epilepsy. However, it is difficult to predict postoperative motor function. The aim of the present study was to analyze whether the preoperative asymmetry of cerebral peduncles could be used to predict motor function restoration before hemispherectomy for young patients with medically intractable epilepsy.
-
METHODS: The clinical record and magnetic resonance imaging data of 53 patients were analyzed retrospectively. The correlation between preoperative cerebral peduncle asymmetry ratio (pCPAR) and pre- and postoperative changes in motor function was evaluated, as well as the influencing factors for pCPAR, such as duration and etiology factors. The restoration of motor function was defined as changes in pre- and postoperative hemiparesis.
pediatric patients with medically intractable epilepsy before hemispherectomy. Most patients with nonprogressive pathology and a duration of more than 5 years presented with greater pCPARs, exhibited better restoration of motor function, and had less risk of worsening hemiparesis.
-
RESULTS: The pCPARs of patients with improved and unchanged hemiparesis were significantly greater than that of worsened patients. Patients with a pCPAR of more than 1.5 had an obvious restorative capacity of motor function of the intact hemisphere, and these patients had a lower risk of worsening hemiparesis. The duration in the improved/unchanged and worsened groups was 5.84 3.85 years and 2.67 2.03 years, respectively. Furthermore, there were more patients with no-progressive pathology in the group in whom pCPAR was more than 1.5.
-
CONCLUSIONS: pCPAR is a useful and objective indicator for predicting the restoration of motor function in
-
Key words Asymmetry - Cerebral peduncle - Epilepsy - Hemiparesis - Hemispherectomy -
Abbreviations and Acronyms CST: Corticospinal tract MRI: Magnetic resonance imaging pCPAR: Preoperative cerebral peduncle asymmetry ratio RR: Relative risk
INTRODUCTION
H
emispherectomy is a typical procedure for treating refectory epilepsy, which began in 1938 when McKenzie performed the procedure in an adult patient with intractable epilepsy and obtained a satisfactory outcome.1 Subsequently, this technique has been used increasingly by more neurosurgeons. Furthermore, this method has been reported to have excellent seizure control for medically intractable epilepsy, in which 60%e90% of patients have become seizure free or Engle Ia/b after surgery.1-4 However, the procedure increases brain function defects, such as motor function. Hence, patients and their parents have become reluctant to choose this method to treat epilepsy. Following this, some studies have begun to evaluate motor functions. Functional magnetic resonance imaging (MRI),5,6 transcranial magnetic stimulation,6,7 and diffusion tensor imaging8 examinations mostly have been used to evaluate the restoration of cerebral function of the intact hemisphere. However, these methods are difficult to use in young children because young children often are uncooperative. Studies rarely have evaluated the postoperative recovery of motor function,9-11 mainly because of the few number of proper
From the 1Department of Neurosurgery, Epilepsy Center, Sanbo Brain Hospital, Capital Medical University, Beijing; 2Department of Neurology, Sanbo Brain Hospital, Capital Medical University, Beijing; 3Beijing Key Laboratory of Epilepsy, Beijing; 4Beijing Institute for Brain Disorders, Beijing; and 5Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China To whom correspondence should be addressed: Guo-Ming Luan, Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.05.057 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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patients with hemispherectomy and the heterogeneity of these patients. Wakamoto et al.8 and Mullin et al.12 conducted an MRI volume analysis of the cerebral peduncle to predict postoperative motor function in patients who undergo hemispherectomy. As described by Mullin et al., with a smaller ratio of ipsilateral to contralateral peduncle, patients may acquire better recovery of motor function after hemispherectomy. The present study showed that the reason for the better recovery of preoperative hemiparesis is the greater contralateral and ipsilateral preoperative cerebral peduncle asymmetry ratio (pCPAR). Our findings were in accordance with the results of Mullin et al.; in our study, the pCPAR was the ratio of contralateral to ipsilateral, and the peduncle ratio in study of Mullin referred to ipsilateral to contralateral. In the present study, we aimed to determine whether pCPAR could be used to predict the restoration of motor function in pediatric patients who are scheduled to undergo hemispherectomy. Our focus was on the correlation between pCPAR and the early period recovery of motor function, as well as its affected factors.
Table 1. Demographic Characteristics and Clinical Data of Patients
Characteristics Sex, male/female
Improved/Unchanged Group (n [ 32)
Worsened Group (n [ 21)
P Value
22/10
11/10
0.229*
Age at onset, years
2.44 2.83
3.67 3.13
0.146y
Age at surgery, years
8.28 3.65
6.33 3.72
0.065y
Duration, years
5.84 3.85
2.67 2.03
0.001y
18/14
10/11
0.538*
Lateral, left/right Surgical methods
0.319*
Anatomical hemispherectomy
16
8
Functional hemispherectomy
5
7
Hemispherotomy
11
6
Etiology
SUBJECTS AND METHODS
Progressive
A total of 53 clinical records and neuroimaging data of 178 patients who underwent hemispherectomy to treat their intractable epilepsy were analyzed retrospectively. The operation method included anatomical hemispherectomy, functional hemispherectomy, and hemispherotomy. These patients were operated in the Epilepsy Center of Sanbo Brain Hospital, Capital Medical University, between September 2004 and July 2016. The recovery of preoperative hemiparesis after hemispherectomy within 1 month mainly was evaluated. pCPAR was measured according to the method of Warabi et al.13 and Mark et al.14 The 53 patients were divided into 2 groups according to whether the patient had improved hemiparesis. Detailed demographic data are presented in Table 1. Inclusion criteria were 1) patients <13 years old at the time of surgery; 2) patients with preoperative hemiparesis; 3) patients who had no severe complications after the operation, such as intracranial infection, hydrocephalus, intracranial hemorrhage and infarction, and severe brain swelling: 4) patients who had no seizure recurrence for at least 1 month after the operation; 5) patients with retrievable MRI data at 1 month before the operation, and no abnormal signals were found in the contralateral hemisphere; and 6) patients with intact clinical data. Exclusion criteria were 1) patients who underwent another brain surgery after the procedure during the follow-up period and 2) patients who were lost to follow-up. According to the aforementioned criteria, a total of 53 patients were enrolled into the study. We evaluated motor function outcomes using a structural questionnaire designed by Moosa et al.15 According to the questionnaire, we defined an unchanged/improved result as “strength of arm and leg has not changed much after surgery, strength is actually better, walks without any aids and assistance” and a worse result as “strength is worse; walk using aids (ankle device such as AFO, walker, etc.), not able to walk at this time and takes few steps when held or assisted, which had not presented before surgery.”
Nonprogressive
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pCPAR, contralateral/ipsilateral
0.000* 10
19
22
2
1.72 0.55
1.23 0.26
0.000y
pCPAR, preoperative cerebral peduncle asymmetry ratio. *Two-tailed t test. yc2 test.
Calculation Method of pCPAR First, we demarcated the boundaries of bilateral cerebral peduncle. Then, we calculated the area of ipsilateral cerebral peduncle (S1 in Figure 1) and the area of contralateral cerebral peduncle (S2 in Figure 1), with pCPAR defined as the value of S2/S1. The cerebral peduncle area was measured by 2 neuroimaging experts using the method reported by Warabi et al.13 (Figure 1) on an MRI workstation. These experts were blinded to the clinical features of each patient. pCPAR was calculated according to the method reported by V. W. Mark, and the ratio was divided into the contralateral peduncle and ipsilateral peduncle (Figure 1). Statistical Methods Data were presented as mean standard deviation. The c2 test was used for categorical data, and the 2-tailed t test was used to compare the means. Relative risk (RR) was calculated by univariate logistic regression analysis for each of the variables measured: age at onset, duration, age at surgery, etiology, and cerebral peduncle asymmetry ratio. A result was considered statistically significant when the P value was <0.05. RESULTS A total of 53 patients (33 male and 20 female patients, 1e13 years old) were enrolled into the study (Table 1). The clinical records and MRI results of these patients were evaluated. Among these
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ORIGINAL ARTICLE XIU-YU DU ET AL.
Figure 1. S1 is the area of ipsilateral cerebral peduncle, S2 is the contralateral, preoperative cerebral peduncle asymmetry ratio ¼ S2/S1. (AeB) Demarcation of medial boundary of peduncles.
patients, 32 patients (60.4%) had improved or unchanged preoperative hemiparesis, whereas 21 patients had a worse result. Among these 53 patients, 24 patients underwent anatomical hemispherectomy, 12 patients underwent functional hemispherectomy, and 17 patients underwent hemispherotomy. The location of the operation was 18 in left hemisphere and 14 in right hemisphere in the improved/unchanged group and 10 in left hemisphere and 11 in right hemisphere in the worsened group, but there was no significant difference between these 2 groups (P ¼ 0.538). The age at onset was 2.44 2.82 years old in the improved/unchanged group and 3.67 3.13 years old in the worsened group, and there was no significant difference between these 2 groups (P ¼ 0.146). The duration in the improved/unchanged group and worsened group was 5.84 3.85 years and 2.67 2.03 years, respectively (P ¼ 0.001). The value of pCPAR was 1.72 0.55 in the improved/unchanged group and 1.23 0.26 in the worsened group (P ¼ 0.000). Two patients with frequent seizures (>30 times per day) had peduncle asymmetry ratios of 1.0 and 1.1, respectively, and the duration was 1.5 and 0.5 years, respectively. However, both patients had improved preoperative hemiparesis immediately after anatomical hemispherectomy. Etiology factors were divided into 2 groups: progressive pathology (Rasmussen encephalitis, hemimegalencephaly, cortical dysplasia, and SturgeeWeber syndrome, or others), and nonprogressive pathology (traumatic brain injury, cerebral hemorrhage due to lack of vitamin K or birth injury, and so on). In this cohort, 10 patients had progressive pathology and 22 patients had nonprogressive pathology in the improved/unchanged group, whereas 19 patients had progressive pathology and 2 patients had nonprogressive pathology in the worsened group (P < 0.01). The relative risk of worsening hemiparesis was greater in patients with a pCPAR of <1.5 (RR ¼ 3.94, P ¼ 0.029) and a duration of <5 years (RR ¼ 5.46, P ¼ 0.01). In this study, there were 30 patients had a pCPAR of <1.5, whereas 23 patients had a pCPAR of >1.5. There were 31 patients with a duration of <5 years and 22 patients with a duration of >5 years. There were 28 patients with preoperative hemiparesis (pCPAR ¼ 1.77 0.57) and 4 patients without preoperative
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hemiparesis (pCPAR ¼ 1.39 0.16) in the improved/unchanged group, and the numbers were 13 (pCPAR ¼ 1.24 0.32) and 8 (pCPAR ¼ 1.21 0.16) in worsened group (P ¼ 0.029). There were more patients in the improved/unchanged group with preoperative hemiparesis and with a greater pCPAR, demonstrating that patients with preoperative hemiparesis and with a greater pCPAR were not likely to be much weaker after surgery and patients with normal motor function and smaller pCPAR were more likely to be weaker after surgery. Among patients with a pCPAR of <1.5, 24 individuals had a progressive pathology and 6 individuals had a nonprogressive pathology. Among patients with a pCPAR of >1.5, 5 individuals had a progressive pathology and 18 individuals had a nonprogressive pathology (c2 ¼ 17.84, P < 0.01; Figure 2A). In total, 17 patients with a duration of <5 years and 4 patients with a duration >5 years were in the worsened group and 14 patients with a duration of <5 years and 18 patients with a duration >5 years were in the improved/unchanged group (c2 ¼ 7.23, P ¼ 0.02; Figure 2B). In total, 18 patients with a pCPAR of <1.5 and 3 patients with a pCPAR >1.5 were in the worsened group and 12 patients with a pCPAR of <1.5 and 20 patients with a pCPAR >1.5 were in the improved/unchanged group (c2 ¼ 11.99, P ¼ 0.01; Figure 2C). In total, 31 patients had a duration of <5 years; among them, 24 had progressive pathology and 7 had nonprogressive pathology; 22 patients had a duration of >5 years, and 5 had a progressive pathology and 17 had a nonprogressive pathology (c2 ¼ 15.54, P < 0.01; Figure 2D). DISCUSSION Hemispherectomy has been used successfully for hemispherical intractable epilepsy because of its excellent seizure control.1 However, postoperative neurologic deficits may be observed in many patients after the procedure. 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 Govindan et al.16 predicted motor function by MRI tractography for an 8-year-old girl and obtained excellent motor function reservation. Zsoter et al.7 used transcranial magnetic stimulation and functional MRI to evaluate the sensorimotor system in 4 patients before hemispherectomy and obtained a favorable and correct prediction of hand motor outcome. However, when correlated to infants or younger children, it was harder to achieve an evaluation because of the difficulty in getting infants or younger children to cooperate. In the present study, we reported a simple method to predict postoperative motor function. The foundation of our research is the different motor pathways in children compared with adults. Benecke et al.17 reported that the ipsilateral corticospinal tract (CST) of the intact hemisphere was the anatomical foundation of motor function recovery in patients with early hemispherectomy, and this view was supported by others.19,20 In the present study, most of the cases were younger children. Hence, the motor pathway was mostly in the CST and cerebral
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Figure 2. The relationship between (A) etiology and preoperative cerebral peduncle asymmetry ratio (pCPARP), (B) duration and motor function recovery, (C) motor function recovery and pCPAR, and (D) etiology and duration. (A) There were 24 patients with progressive pathology with pCPAR <1.5 and 6 with nonprogressive pathology. There were 18 with nonprogressive pathology and 5 with progressive pathology in the group with pCPAR >1.5 (c2 ¼ 17.84, P ¼ 0.000). (B) There were 17 patients with duration <5 years in the worsened group and 4 patients with >5 years. There 18 patients with >5 years and 14 patients
peduncle, which include most CST fibers. This was the reason we choose the cerebral peduncle as an indicator to predict motor function for pediatric patients. Another reason was that brain morphologic changes presented functional changes, although we were not able to clarify the mechanism. Some authors21,22 used brain midline shifting to predict the restoration of consciousness. In the present study, we used cerebral peduncle asymmetry to predict the restoration of motor function. Cerebral peduncle asymmetrical change mainly was ascribed to cerebral functional and structural plasticity and reorganization. After hemispherectomy, the fibers from the affected hemisphere in the ipsilateral cerebral peduncle that dominated motor and sensory function decreased, mainly due to Wallerian degeneration.6-8 In the present study, the results show that patients with greater pCPAR and longer durations may have better motor function restoration in their unaffected hemisphere and lower risk of worsening preoperative hemiparesis, especially in patients with nonprogressive pathology. This result is in accordance with the
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with <5 years in the improved/unchanged group (c2 ¼ 7.23, P ¼ 0.02). (C) There were 18 patients in the worsened group with a pCPAR <1.5 and 3 patients with >1.5. In the improved/unchanged group, there were 20 patients with >1.5 and 12 patients with <1.5 (c2 ¼ 11.99, P ¼ 0.01). (D) There were 24 patients with progressive pathology with duration <5 years and 7 with nonprogressive pathology. There were 17 with nonprogressive pathology and 5 with progressive pathology in the group with duration >5 years (c2 ¼ 15.54, P ¼ 0.000).
study reported by Mullin et al.,12 in which postoperative hemiparesis was predicted by cerebellar hemisphere ratio and the volumetric analysis of peduncles in 22 patients who underwent hemispherectomy. Their findings revealed that if the peduncle ratio (ipsilateral/contralateral) was <0.5, none of the patients would have a worsening hemiparesis. The present result indicates that when the pCPAR was >1.5, patients would obtain an improved or unchanged motor function. In addition, the duration and etiology factors were included in the present study. When etiology factors were considered, we found that patients with a nonprogressive pathology (such as hemispherical encephalomalacia, which is ascribed to burn injury, lack of vitamin K, traumatic brain injury, and so on) mostly had greater pCPAR and experienced better recovery of motor function. van der Kolk et al.10 reported that patients with developing or progressive etiologies (such as Rasmussen encephalitis, hemimegalencephaly, cortical dysplasia, or others) more often lost motor function, and they also highlighted the important role of CST in motor function recovery.
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PREDICTION MOTOR FUNCTION BEFORE HEMISPHERECTOMY
In the present study, we only evaluated the early recovery of motor function, because we consider that motor function in the early period after surgery may be a better substitute for the real restoration of the intact hemisphere compared with the later period. Some studies reported that postsurgical rehabilitative training could improve motor function,23 not only for animals, but also for humans. Furthermore, many other factors may affect motor function, for example, recurrence of seizures, antiepilepsy drugs, personal development, and so on. However, motor function improved immediately after the operation, which was probably due to the disappearance of the seizure. In the present study, 2 patients who had frequent seizure attacks were accompanied by contralateral hemiparesis. At 2 days after surgery, they became seizure free, and the preoperative hemiparesis obviously improved. Pascoal et al.18 reported that a 17-year-old patient had immediate improvement of motor function after the operation, and the reason lies in the removal of interference of the ipsilateral hemisphere. Another factor that may have influenced pCPAR and motor function was duration, which has not been reported. This present result shows that the pCPAR of patients with a duration of <5 years was lower than patients with a duration of >5 years, and a longer duration experienced better motor function recovery. Another study2 conducted by our team on Rasmussen encephalitis reported that early-stage hemispherectomy does not always achieve better outcomes. Limitations In the present study, although we used stricter inclusion and exclusion criteria, there were some limitations. First, because
REFERENCES 1. Fountas KN, Smith JR, Robinson JS, Tamburrini G, Pietrini D, Di RC. Anatomical hemispherectomy. Childs Nerv Syst. 2006;22: 982-991. 2. Guan Y, Chen S, Liu C, Du X, Zhang Y, Chen S, et al. Timing and type of hemispherectomy for Rasmussen’s encephalitis: analysis of 45 patients. Epilepsy Res. 2017;132:109-115. 3. Verdinelli C, Olsson I, Edelvik A, Hallböök T, Rydenhag B, Malmgren K. A long-term patient perspective after hemispherotomy—a populationbased study. Seizure. 2015;30:76-82. 4. WJ1 Peacock, Wehby-Grant MC, Shields WD, Shewmon DA, Chugani HT, Sankar R, et al. Hemispherectomy for intractable seizures in children: a report of 58 cases. Childs Nerv Syst. 1996;12:376-384.
of the heterogeneity of the patients, it was difficult of determine all influential factors. That is, other factors may have affected motor function, such as genes, medicine, and so on. Second, we excluded patients accompanied by the recurrence of seizure, but seizure may not affect the recovery of motor function. Third, as we described previously, preoperative seizures may affect motor function. Hence, preoperative motor function evaluation may be influenced by these seizures. In addition, because of the limited sample size, it was difficult to attain a very persuasive result. In future studies, we plan to collect more data from multicenter or international cooperations.
CONCLUSIONS pCPAR may provide a prediction for the restoration of motor function of the intact hemisphere before hemispherectomy in young patients with hemispherical intractable epilepsy. A diminished restoration of motor function may reveal a worsening hemiparesis after the operation, which mostly happens for lower pCPAR. pCPAR is affected by etiology and duration. Furthermore, patients with nonprogressive pathology and a duration of >5 years mostly presented with a greater pCPAR, showing better restoration of motor function, and had a less risk of worsening in their preoperative hemiparesis. If the pCPAR were to be used to predict motor function recovery, etiology factors and duration also should be taken into account. However, for high-frequency hemispherical medically intractable epilepsy, stopping the seizure is more important than the reservation of motor function?.
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determinant factor for neurological improvement after cranioplasty. J Formos Med Assoc. 2015;114: 577-582. 23. Higo N. Effects of rehabilitative training on recovery of hand motor function: a review of animal studies. Neurosci Res. 2014;78:9-15.
Foundation (2016M601066), the Capital Health Research and Development of Special (2016e1-8012), and Beijing Municipal Science & Technology Commission (Z161100000516230, Z161100002616016). Received 29 January 2018; accepted 9 May 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.05.057 Journal homepage: www.WORLDNEUROSURGERY.org
Conflict of interest statement: This study was supported by the following sources: the Research Fund for the Doctoral Beijing Nova Program (Z141107001814042), Collaboration Between Clinical and Basic Research in Capital Medical University (16JL09), National Natural Science Foundation of China (81671285, 81571275), the China Postdoctoral Science
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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