Characterization of The Supplementary Motor Area Syndrome and Seizure Outcome After Medial Frontal Lobe Resections in Pediatric Epilepsy Surgery

RESEARCHHUMANCLINICAL STUDIES
RESEARCHHUMANCLINICAL STUDIES
TOPIC
Characterization of the Supplementary Motor Area

Syndrome and Seizure Outcome After Medial
Frontal Lobe Resections in Pediatric
Epilepsy Surgery
BACKGROUND: In adults, resection of the medial frontal lobe has been shown to result
in supplementary motor area (SMA) syndrome, a disorder characterized by transient
motor impairment. Studies examining the development of SMA syndrome in children,
however, are wanting.
OBJECTIVE: To characterize the development of SMA syndrome and to analyze seizure
outcomes after surgery in the medial frontal lobe for medically intractable epilepsy.
METHODS: Thirty-nine patients with medically intractable epilepsy who underwent
surgery in the medial frontal lobe were reviewed retrospectively. The progression of
neurological impairment and seizure outcome after surgery was recorded, and the
extent of cortex resected was analyzed.
RESULTS: After resection in the region of the SMA, 23 patients (59%) developed
postoperative neurological impairment; 17 (74%) were identified as SMA syndrome. No
neurological impairment was found after surgery in 16 patients (41%). Six patients (15%)
experienced permanent neurological impairment. The majority of patients (82%) who
developed SMA syndrome had resolution of their symptoms by 1 month postoperatively. Preoperative magnetic resonance imaging finding of lesional cases was associated with a significantly decreased likelihood of developing SMA syndrome (P = .02).
Seizure outcome was favorable after surgery in most patients.
CONCLUSION: Surgery for medically intractable epilepsy in the region of the medial
frontal cortex is effective and associated with reversible neurological impairment in
children. All patients had resolution of their SMA syndrome by 6 months postoperatively.
Aimen S. Kasasbeh, MD*

Chester K. Yarbrough, MD
David D. Limbrick, MD, PhD
Karen Steger-May, MA
James L. Leach, MDk
Francesco T. Mangano, DO
Matthew D. Smyth, MD
*Department of Neuroscience, University
of Arizona, Tucson, Arizona; Department of Neurological Surgery, Saint Louis
Childrens Hospital and; Division of
Biostatistics, Washington University
School of Medicine in St. Louis, St. Louis,
Missouri; kDepartment of Medical Imaging and Department of Neurological
Surgery, Cincinnati Childrens Hospital
Medical Center, Cincinnati, Ohio
Correspondence:
Aimen S. Kasasbeh, MD,
Department of Neuroscience,
University of Arizona,
1548 E Drachman St, PO Box 210476,
Tucson, AZ 85719.
E-mail: aimenk@email.arizona.edu
Received, June 17, 2011.
Accepted, October 15, 2011.
Published Online, November 23, 2011.
Copyright 2011 by the
Congress of Neurological Surgeons
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KEY WORDS: Epilepsy surgery, Pediatric epilepsy, Supplementary motor area

Neurosurgery 70:11521168, 2012
DOI: 10.1227/NEU.0b013e31823f6001
pilepsy is a common neurological disorder

affecting approximately 1% of children,
and nearly 40% of all newly recognized
cases of epilepsy are diagnosed during childhood.1-3 Pediatric epilepsy is associated with
considerable neurocognitive, behavioral, and
developmental impairment4-7; impairment in
quality of life8,9; and increased mortality.10-12
These factors underscore the necessity of proper
treatment of epilepsy in childhood.
Treatment of pediatric epilepsy remains
challenging and demands a multidisciplinary
1152 | VOLUME 70 | NUMBER 5 | MAY 2012
ABBREVIATIONS: SMA, supplementary motor

area; video-EEG, video electroencephalography
www.neurosurgery-online.com
approach. Antiepileptic drugs reduce the recurrence of seizures13-15 but demonstrate considerable, and often restricting, side effects,16 and
their role in affecting long-term remission is
questionable.14,17 Moreover, a significant proportion of patients who are seizure free on
medications relapse after discontinuation of
antiepileptic drug treatment,18-20 and a subset
of patients continue to experience debilitating
seizures despite maximal medical treatment.21-24
For such patients with medically intractable
epilepsy, surgery is often considered for successful multimodal treatment directed at controlling
seizures and averting developmental delay.
Surgical complications of epilepsy surgery have
been declining with increased experience and
Copyright Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited.
POSTOPERATIVE PEDIATRIC SMA SYNDROME
improved diagnostic and surgical techniques.25-27 Surgical resection in the region of the supplementary motor area (SMA),
critical for planning and execution of voluntary motor function,
has been shown in adults to result in a distinctive transient
neurological condition known as SMA syndrome.28-39 First
described after surgical resection by Laplane et al,33 the syndrome
has a strikingly consistent clinical evolution postoperatively,
characterized by transient hemiparesis or motor apraxia with
variable degrees of speech arrest followed by rapid recovery of
neurological impairment.
We examined the development of SMA syndrome in a series of
39 children who underwent surgery for resection of a seizure focus
in the medial frontal cortex. In addition, we analyzed seizure
outcomes after surgery. To the best of our knowledge, this report
represents the largest study of SMA syndrome after surgery in the
medial frontal lobe and is the first to be done in an exclusively
pediatric patient population.
METHODS
Patient Population and Preoperative Evaluation
After Institutional Review Board approval was granted at the St. Louis
Childrens Hospital/Washington University in St. Louis Human
Research Program and Cincinnati Childrens Hospital Medical Center,
medical records of patients who underwent surgical management for
medically intractable epilepsy between 1994 and 2010 were reviewed.
Patients with resections in the medial frontal lobe were included in the
study. Table 1 summarizes the patient and seizure characteristics of
39 patients who met these inclusion criteria. Preoperative evaluation was
tailored for each patient and included magnetic resonance imaging
(MRI), functional MRI, video electroencephalography (video-EEG),

brain positron emission tomography, magnetoencephalography, singlephoton emission computed tomography, subtraction ictal single-photon
emission computed tomography coregistered to MRI, Wada testing,
cerebral angiogram, and neuropsychological evaluation. All but 4
patients underwent invasive monitoring. All evaluation studies were
discussed by a multidisciplinary epilepsy team including pediatric
neurosurgeons, pediatric epileptologists, neuroradiologists, neuropsychologists, EEG technologists, and support personnel.
Study Outcome Measures

Neurological morbidity and seizure control (as determined by the
modified Engel classification40) were assessed in patients who had
a minimum of 6 months of follow-up after undergoing surgery.
Neurological evaluations were performed preoperatively, in the immediate postoperative period, and daily until discharge from hospital.
Additionally, neurological status was recorded at follow-up visits at 1, 6,
12, and 24 months and at extended follow-up (defined as last follow-up
beyond the 24-month visit) postoperatively. Postoperative neurological
morbidity, determined as alteration of neurological function with respect
to preoperative neurological evaluation, was classified as normal (no
change from baseline neurological function), SMA syndrome (contralateral hemiparesis/hemiplegia or apraxia with or without speech
impairment), or permanent neurological deficit (neurological impairment that was sustained after the 6-month evaluation and did not recover
by the last follow-up visit). Surgical complications, including infection
and intracranial hemorrhage, were recorded. For the purpose of analysis,
pathological results were classified as forms of dysplasia, eg, focal cortical
dysplasia, microdysgenesis, heterotopia, and cortical malformation; other
pathology, including gliosis, tumor, and inflammation; normal histopathological specimen.
Operative Approach
TABLE 1. Demographics and Seizure Characteristics in Patients
Who Underwent Surgical Treatment in Medial Frontal Lobe for
Medically Intractable Seizuresa
Total patients, n
Female sex, n (%)
Right handedness, n (%)b
Age at seizure onset, mo
Age at surgery, mo
Time between seizure onset and surgery, moc
Seizure type, n (%)
CPS
CPS-secondary generalized
SPS
SPS-secondary generalized
Multiple seizures/generalized
Seizure types (25th, 75th percentiles), n
Preoperative seizure frequency, n (%)c
Monthly
Weekly
Daily
a
CPS, complex partial seizures; SPS, simple partial seizures.

Data from 34 of 39 patients.
c
Data from 38 of 39 patients.
b
NEUROSURGERY
39
19 (49)
24 (71)
62.1 6 50
146 6 57
82.5 6 60
14
4
7
4
10
2
(36)
(10)
(18)
(10)
(26)
(1, 2)
4 (11)
6 (16)
28 (74)
Thirty-five patients (89.7%) had subdural electrocorticographic monitoring with electrode grid and strip arrays, depth electrodes, or
a combination thereof. The operative approach for each patient was
determined after neuroimaging studies, video-EEG, intraoperative and
extraoperative mapping, and evaluation by the St. Louis Childrens
Hospital and Cincinnati Childrens Hospital Medical Center multidisciplinary epilepsy teams. The location and extent of surgical resection
were determined through postoperative MRI and tabulated (Table 2).
This information was available for 34 patients (87.2%). Specimens from
patients were sent for pathological evaluation.
Statistical Methods
Data are presented as mean 6 SD for continuous variables and median
(25th and 75th percentiles) for ordinal variables. For categorical
variables, data are the number of patients (percent of group). Unless
otherwise noted, the Wilcoxon test was used for comparisons of
continuous variables, and the Fisher exact test was used for comparison
of categorical variables. For correlation studies, the Spearman correlation
was used to analyze data. A value of P # .05 was considered statistically
significant. A denominator is included when less than the complete
patient cohort provided data for the categorical variables. The data
analysis was generated with SAS software version 9.2 of the SAS System
for Linux (SAS Institute Inc, Cary, North Carolina).
VOLUME 70 | NUMBER 5 | MAY 2012 | 1153
KASASBEH ET AL
TABLE 2. Extent and Location of Surgical Resection and Association Between Neurological Deficit and Resection Parametersa
Neurological Deficit (25th, 75th Percentiles), cm
Variable
Distance anterior to precentral sulcus, cm
Distance superior to cingulate gyrus, cm
Distance lateral to fissure, cm
Anteroposterior extent of resection, cm
Superior-inferior extent of resection, cm
Transverse extent of resection, cm
0.50
0.60
0.05
3.95
2.90
3.00
Entire
Group
No Impairment
(n = 12)
SMA Syndrome
(n = 16)
(0, 1.62)
(0, 1.00)
(0, 3.29)
(3.07, 5.70)
(2.10, 4.80)
(1.90, 3.70)
2.22
1.00
0.40
3.51
4.12
3.03
0.20
0.52
0.50
4.13
3.15
2.98
(1.00,
(0.30,
(0.00,
(2.25,
(2.30,
(2.15,
3.26)
1.24)
2.52)
4.05)
5.92)
4.35)
(0.00,
(0.00,
(0.00,
(3.34,
(2.04,
(1.80,
1.45)b
0.85)
3.47)
5.73)
4.55)
3.70)
Permanent Impairment
(n = 6)
0.00
0.00
0.05
5.28
2.55
2.90
(0.00,
(0.00,
(0.00,
(3.10,
(2.25,
(1.90,
0.00)b
0.75)b
0.30)
6.75)
3.00)
3.00)
P
.001
.05
.67
.08
.35
.57
a
SMA, supplementary motor area. P value compared groups by analysis of variance with rank-transformed data. When significant, pairwise between-group comparisons were
performed with Tukey-adjusted least-squares means. Significant pairwise comparisons are noted.
b
P , .05 vs no impairment by Tukey-adjusted least-squares means.
RESULTS
Patient and Seizure Characteristics
Thirty-nine patients underwent surgery in the region of the
medial frontal lobe for medically intractable epilepsy at St. Louis
Childrens Hospital and Cincinnati Childrens Hospital Medical
Center from 1994 to 2010 (Table 3). Of the 39 patients included
in the study, 19 (49%) were female and 20 (51%) were male.
Right-handedness was demonstrated in 24 of 34 patients (71%).
The age at onset of seizures was 62.1 6 50 months, and age at the
time of surgery was 146 6 57 months. Surgery was performed
82.5 6 60 months after identification of epilepsy. With regard to
seizure characteristics in the study cohort, 14 (36%) had complex
partial seizures, 4 (10%) had complex partial seizures with
secondary generalized tonic-clonic seizures, 7 (18%) had simple
partial seizures, and 4 (10%) had SPS with secondary generalization. Multiple seizure types were found in 10 patients (26%).
The median number of seizure types in the patient population
was 2. Seizures were experienced daily in 28 patients (74%),
weekly in 6 patients (16%), and monthly in 4 patients (11%). All
patients failed AED therapy with at least 2 drugs at therapeutic
doses. Patient demographics and seizure characteristics are
summarized in Table 1. Table 3 lists individual patient information, including demographics, clinical profile, pathology, and
neurological impairment after surgery.
Neurophysiologic Monitoring and Surgical Resection
Thirty-five patients (90%) underwent invasive subdural monitoring before surgical resection. Lesionectomy was performed in 8
patients (21%). Tailored resections were performed in the
remaining 31 patients (79%), with 5 patients (13%) undergoing
multiple subpial transections in addition to tailored resections. In
all cases, intraoperative cortical stimulation mapping and somatosensory evoked potentials were used to localize the eloquent
primary motor cortex and central sulcus. In cases when intraoperative cortical stimulation mapping and/or somatosensory
evoked potentials were unreliable (particularly in the younger
patients), extraoperative mapping data acquired from subdural

grid electrode placement were used for planning the resections.
Cortical and subcortical stimulation mapping was generally
repeated after the resections to confirm the integrity of the
corticospinal tracts using techniques previously described.41-43
The location and extent of surgical resection are summarized in
Table 2. The median distance of the posterior border of resection
anterior to the precentral sulcus was 0.50 cm. The median
distance of the inferior border of resection superior to the
cingulate gyrus was 0.6 cm. The median distance lateral to the
longitudinal fissure was 0.05 cm. The anteroposterior extent of
resection was 3.95 cm; the superior-inferior extent of resection
was 2.9 cm; and the transverse extent of the resection was 3.0 cm.
Preoperative MRI identified lesional cases in 16 patients (41%)
and nonlesional cases in 23 patients (59%).
Neurological Outcome
After surgical resection in the medial frontal lobe, 17 patients
(44%) developed SMA syndrome. No neurological impairment
was found after surgery in 16 patients (41%). Six patients (15%)
developed neurological impairment that did not resolve at the last
follow-up. The development of postoperative SMA syndrome was
not related to age at seizure onset, age at time of surgery, sex,
handedness, preoperative seizure type, pathology of seizure focus,
use of invasive monitoring, or surgery type. The delay between
onset of seizures and surgery was found to be significantly longer in
patients who developed SMA syndrome (P = .03). Preoperative
MRI did not identify a lesion in 23 patients (59%). The majority
of patients who developed SMA syndrome (82%) had no lesion
identified on preoperative MRI. Three patients (18%) with
postoperative SMA syndrome and 3 patients (50%) with
permanent impairment had lesions identified on preoperative
MRI. In patients with no neurological impairment, a significantly
larger number of patients (10, 62%) were found to have a lesional
diagnosis on preoperative MRI (P = .05).
Of the 17 patients who developed SMA syndrome, 7 had
resolution of symptoms by 1 week postoperatively, another 7 had
NEUROSURGERY
TABLE 3. Demographics, Clinical Profiles, Pathology, and Outcome in Patients Who Underwent Resection of Medial Frontal Lobea
Patient
Age at Surgery,
mo
Sex Handedness
Seizure Type
Side of
Surgery
175
188
106
71
147
68
M
F
M
M
F
F
L
L
L
R
R
R
CPS
CPS
SPS
L
L
R
L
L
R
7
8
137
99
M
M
L
R
L
L
114
N/A
10
11
12
13
200
182
10
196
F
M
F
F
R
R
R
L
14
15
16
109
233
185
F
M
F
R
N/A
R
17
127
18
19
203
195
F
F
L
L
20
148
21
22
23
24
25
26
180
59
169
209
7
183
M
M
F
M
F
F
R
L
R
R
N/A
N/A
27
180
28
97
N/A
Immediate Postoperative
Neurological Impairment
N/A
Nonspecific changes
Cortical dysplasia
Hypoxic-ischemic cell damage
Heterotopia
No significant histopathological
abnormality
AVM and capillary telangiectasia
No significant histopathological
abnormality
Nonspecific changes
No neurological impairment
Contralateral hemiparesis, contralateral facial
weakness
Contralateral hemiparesis (did not resolve by
12-mo follow-up visit)
weakness (hemiplegia did not resolve by
12-mo follow-up visit)
CPS
CPS
R
R
R
L
Nonspecific changes
Nonspecific changes
Subpial and subcortical gliosis
Nonspecific changes
Contralateral hemiplegia
Contralateral hemiparesis
Contralateral hemiparesis, mild contralateral
facial weakness (hemiparesis improved but
did not resolve by 12-mo postoperative visit)
CPS
CPS
R
L
R
Microdysgenesis
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
Contralateral hemiplegia, aphasia
weakness
Contralateral hemiparesis (improved but
did not resolve by 12-mo postoperative
examination)
L
L
Nonspecific changes
Cortical dysplasia
weakness (improved but did not resolve at
12-mo postoperative examination)
Nonspecific changes
L
L
R
R
R
R
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
Meningioangiomatosis
Cortical dysplasia
Cortical dysplasia
Low-grade glial neoplasm with

features of dysembryoplastic
neuroepithelial tumor
Nonspecific changes

weakness, aphasia
Contralateral hemiparesis, aphasia
Contralateral hemiparesis (improved but did
not resolve by 12-mo postoperative exam)
CPS
CPS
CPS
SPS
CPS
SPS
SPS
SPS
SPS
SPS
(Continues)
1
2
3
4
5
6
Pathology
Cortical dysplasia
Cortical dysplasia
Contralateral hemiparesis, facial weakness,
aphasia
resolution of symptoms between 1 week and 1 month postoperatively, and 3 had their SMA syndrome resolve beyond 1
month after surgery. The resolution of SMA syndrome was not
statistically associated with the age at seizure onset, age at time of
surgery, delay between seizure identification and surgery, sex,
handedness, seizure type, use of invasive monitoring, surgery type,
pathologic diagnosis, or preoperative MRI finding of lesion
(Table 4). Of note, a single patient developed SMA syndrome
after surgery for placement of subdural grid and strip electrodes,
not after surgical resection. This patient developed contralateral
hemiplegia and mild expressive aphasia shortly after surgery.
Motor and speech impairment gradually improved with complete
resolution by 1 week postoperatively.
AVM, arteriovenous malformation; CPS, complex partial seizures; SPS, simple partial seizures.
L
L
R
R
132
123
38
39
M
F

Contralateral upper-limb weakness, facial
weakness
Cortical dysplasia
Cortical dysplasia
L
L
CPS
R
L
197
142
36
37
F
M
Contralateral lower limb weakness

weakness, aphasia
Microdysgenesis
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
Cortical dysplasia
R
L
R
L
L
L
L
CPS
CPS
CPS
R
L
R
R
R
R
R
M
F
F
F
M
F
M
197
158
32
169
171
181
162
29
30
31
32
33
34
35
Age at Surgery,
mo
Sex Handedness
Patient
TABLE 3. Continued
Seizure Type
Side of
Surgery
Pathology
Immediate Postoperative
Neurological Impairment
KASASBEH ET AL
Seizure Outcome
Seizure outcomes as determined by Engel classification40 at
12 months and extended follow-up visits are summarized in
Tables 5 and 6. At 12 month postoperatively, 31 of 37 patients
(84%) had Engel class I or II, and 6 patients (16%) had Engel
class III or IV. Seizure outcome at 12 months postoperatively was
not found to be significantly associated with age at seizure
identification, age at time of surgery, delay between seizure
identification and surgery, sex, handedness, seizure type, use of
invasive monitoring, preoperative MRI identification of lesion,
surgery type, or pathology identified. With regard to surgery type,
lesionectomy had been performed in 8 patients (26%) found to
have Engel class I/II, whereas no patient with Engel class III/IV
had undergone lesionectomy. A Fisher exact test did not
demonstrate a statistically significant relationship between seizure
outcome and type of surgery performed (P = .31).
At extended follow-up, 16 of 22 patients (73%) had Engel class
I/II, whereas 6 patients (27%) had Engel class III/IV. Age at the
time of surgery was 173 6 38 months for patients with Engel class
I/II and 98.9 6 64 months for patients with Engel class III/IV,
significantly longer in patients with favorable seizure outcome
(P = .02). Moreover, the delay between seizure onset and
surgery was significantly longer (P = .05) in patients with Engel
class I/II (108 6 67 months) compared with patients with Engel
class III/IV (45.0 6 25 months). With regard to surgery type,
lesionectomy was performed in 4 patients (25%) found to have
Engel class I/II, whereas 1 patient (17%) with Engel class III/IV
had lesionectomy performed. Seizure outcome at the last followup was not significantly associated with age at seizure identification, sex, handedness, seizure type, use of invasive monitoring,
preoperative MRI identification of lesion, surgery type, or
pathological diagnosis.
Changes in seizure outcome between 1 month and each
subsequent visit were analyzed. The majority of patients maintained the same outcome at 1 month with no decline in Engel class
throughout the follow-up period; 87% at 6 months, 81% at 12
months, 70% at 24 months, and 64% at the last follow-up
maintained the same seizure outcome as at 1-month. The
proportion of patients who had a decline in seizure outcome
.31
.60
.07
.78
.72
.52
.93
.05
.42
.08
89.0 6 48
152 6 44
63.3 6 46
3 (50)
2/4 (50)
1 (17)
5 (83)
3 (50)
2 (33)
3 (50)
27.0 6 39
177 6 27
150 6 64
1 (33)
3 (100)
0
3 (100)
1 (33)
0
0
Engel Class
I
II
III
IV
SMA, supplementary motor area.
76.3 6 46
169 6 17
92.1 6 45
2 (29)
5 (71)
2 (29)
6 (86)
2 (29)
1 (14)
6 (86)
57.6 6 58
126 6 68
62.7 6 60
9 (56)
9/14 (64)
5 (31)
14 (88)
10 (62)
5 (31)
10/15 (67)
Age of seizure onset, mo
Age at surgery, mo
Time between seizure onset and surgery, mo
Female sex, n (%)
Right handedness, n/N (%)
Seizure type, secondary generalized, n (%)
Invasive monitoring, n (%)
Preoperative MRI, lesional, n (%)
Surgery type, lesionectomy, n (%)
Pathology, forms of dysplasia, n/N (%)
NEUROSURGERY
At 12 mo
(n = 37)
25
6
4
2
(68)
(16)
(11)
(5)
At Extended
Follow-up (n = 22)
12
4
5
1
(55)
(18)
(23)
(5)
compared with 1 month was 13% at 6 months, 16% at 12 months,

23% at 24 months, and 32% at the extended follow-up. Analysis
of patient and seizure characteristics and their relation to progression of seizure outcome throughout the follow-up period was
performed. Statistically significant changes were not found
between change in seizure outcome and age at seizure onset, age
at time of surgery, time delay between seizure identification and
surgery, sex, use of invasive monitoring, surgery type, or seizure
type. Interestingly, right-handedness was associated with preservation of Engel class throughout the follow-up period, which
was statistically significant (P = .02 at 12 months, P = .03 at
24 months).
The association between early postoperative seizure recurrence
and seizure outcome at subsequent follow-up visits was studied
(Table 7). Seizure recurrence in the first month postoperatively
was associated with a significantly increased likelihood of seizures
at the 6- and 12-month follow-up visits (P , .001 for both), and
a nonsignificant trend toward seizure recurrence at extended
follow-up visit (P = .12). Furthermore, seizure freedom during
the first month postoperatively was significantly related to
favorable seizure outcome at the 6-month postoperative visit
(P = .009). In contrast to long-term seizure outcome, early
postoperative seizure recurrence was not associated with postoperative neurological outcome.
46.3 6 33
148 6 65
103 6 68
4 (57)
5/6 (83)
0
7 (100)
0
0
6 (86)
Permanent
Impairment (n = 6)
Resolved After
1 mo (n = 3)
Resolved by
1 wk (n = 7)
Resolved Between
1 wk and 1 mo (n = 7)
TABLE 5. Seizure Outcome After Surgery in the Medial Frontal

Lobe
Patients, n (% of Group)
No Impairment
(n = 16)
Variable
Neurological Deficit
SMA Syndrome (n = 17)
TABLE 4. Neurological Impairment After Surgery in the Medial Frontal Lobe and Resolution of Supplementary Motor Area Syndromea
Association of Extent and Location of Resection With

Clinical Characteristics
Analysis of the relation between the extent and location of
resection with patient characteristics and progression of seizure
outcome is shown in Table 8. The dimensions of the surgical
resection and the location of resection did not correlate
significantly with age at seizure identification, age at the time
of surgery, or time delay between seizure identification and time
of surgery (Table 8). Anteroposterior extent of surgical resection
was found to be associated significantly with sex (P = .04), with
male patients undergoing more extensive anteroposterior resections (male patients, 4.40 cm; female patients, 3.14 cm). Other
resection parameters were not associated with sex. Furthermore,
none of the surgical parameters was found to be associated with
handedness. Interestingly, a significantly more extensive resection
lateral to a longitudinal fissure was associated with pathologies
KASASBEH ET AL
TABLE 6. Association Between Engel Class and Patient Characteristicsa

Engel Class at 12 mo
Engel Class at Extended Follow-up
Variable
I/II (n = 31)
III/IV (n = 6)
I/II (n = 16)
III/IV (n = 6)
Age of seizure onset, mo

Age at surgery, mo
Time between seizure onset and surgery, mo
Female sex, n (%)
Right handedness, n (%)
Seizure type, secondary generalized, CPS or SPS, n (%)
Invasive monitoring, n (%)
Preoperative MRI, lesional, n (%)
Surgery type, lesionectomy, n (%)
Pathology, forms of dysplasia, n (%)
61.7 6 52
149 6 60
85.5 6 64
17 (55)
21/27 (78)
6 (19)
27 (87)
14 (45)
8 (26)
22 (71)
48.0 6 36
128 6 43
79.8 6 50
2 (33)
3 (50)
1 (17)
6 (100)
2 (33)
0
3 (50)
.78
.18
.95
.40
.31
1.0
1.0
.68
.31
.37
65.3 6 53
173 6 38
108 6 67
6 (38)
10/13 (77)
2 (12)
14 (88)
7 (44)
4 (25)
10 (62)
53.5 6 63
98.9 6 64
45.0 6 25
4 (67)
4 (67)
0
6 (100)
3 (50)
1 (17)
1 (17)
.44
.02
.05
.35
1.0
1.0
1.0
1.0
1.0
.15
CPS, complex partial seizures; MRI, magnetic resonance imaging; SPS, simple partial seizures.
categorized as dysplasia. Resection parameters were not associated

with seizure outcome at the 12-month and extended follow-up
visits, with the exception of that a significantly smaller transverse
resection was associated with favorable seizure outcome at the
12-month follow-up (P = .05).
Neurological deficit after surgical resection was found to be
strongly associated with the distance of resection margin from the
precentral sulcus (P , .001; Table 2). Postoperative neurological
deficit had a nonsignificant trend association with the anteroposterior extent of surgical resection (P = .08). Moreover,
a significant association was found between distance of the
resection margin superior to the cingulate sulcus and the
development of neurological deficit (P = .05). No significant
association was found between the development of postoperative
neurological deficit and the surgical resection extension lateral to
the longitudinal fissure, the superior-inferior extent of resection,
or the transverse extent of resection.
Permanent Neurological Deficit

Six patients (15%) in this series undergoing medial frontal lobe
resections had permanent deficits that persisted for . 6 months
after surgery (Table 3). They were divided evenly between boys
and girls. Four had left-sided surgery, and 2 had right-sided
surgery. Preoperative MRI identified lesional cases in 3 patients.
Three had cortical dysplasia, 2 had nonspecific changes such as
gliosis, and 1 had no histopathological abnormality. Most of the
deficits (contralateral hemiparesis) had significantly improved but
had not entirely resolved at 6 months and persisted through the
follow-up period. Table 2 summarizes the extent and location of
surgical resection in patients who developed permanent neurological deficit. In no patient was the primary motor cortex
knowingly resected. Distances of resection from precentral sulcus
and cingulate gyrus were significantly shorter in patients who
developed permanent impairment. Furthermore, there was
a trend toward larger anteroposterior dimension of resection in
TABLE 7. Association Between Early Postoperative Seizure Recurrence and Follow-up Engel Class Categories
Early Postoperative Seizure Recurrence (1 Month), n (%)
Follow-up
6 mo
12 mo
Extended follow-up
Seizure Outcome
Early Postoperative Occurrence
Seizure recurrence
Seizure freedom
Engel III/IV
Engel I/II
Seizure recurrence
Seizure freedom
Engel III/IV
Engel I/II
Seizure recurrence
Seizure freedom
Engel III/IV
Engel I/II
9 (100)
0
5 (56)
4 (44)
8 (100)
0
3 (38)
5 (62)
4 (100)
0
1 (25)
3 (75)
Seizure Freedom
6
24
3
27
10
19
3
26
9
9
5
13
(20)
(80)
(10)
(90)
(34)
(66)
(10)
(90)
(50)
(50)
(28)
(72)
P
,.001
.009
.001
.10
.12
1.0
TABLE 8. Association Between Extent and Location of Resection With Patient Characteristics and Seizure Outcomea
Extent and Location of Resection
Variable
Age of seizure onset (n = 34)
r
P
Age at surgery (n = 34)
r
P
Time between seizure onset and
surgery (n = 34)
r
P
Sex
Female (n = 16)
Male (n = 18)
P
Handedness
Left (n = 8)
Right (n = 21)
P
Pathology
Forms of dysplasia (n = 22)
Other (n = 11)
P
Engel class, 12- mo follow-up
I/II (n = 27)
III/IV (n = 5)
P
Engel class, extended follow-up
I/II (n = 13)
III/IV (n = 5)
P
Distance
Anterior to
Precentral
Sulcus, cm
Distance
Superior to
Cingulate
Gyrus
Distance
Lateral to
Fissure
Anteroposterior
Extent of
Resection
Superior-inferior
Extent of
Resection
Transverse
Extent of
Resection
20.23
.19
20.12
.48
20.01
.95
0.09
.62
20.30
.09
20.18
.32
20.12
.50
0.10
.56
.20.03
.88
0.04
.83
20.04
.80
20.24
.17
0.04
.82
0.06
.72
0.12
.50
0.11
.52
0.21
.24
20.10
.56
0.43 (0, 0.95)

0.75 (0, 1.00)
.47
0.05 (0, 3.29)

0.15 (0, 1.80)
1.00
3.14 (2.70, 4.03)

4.40 (3.75, 6.70)
.04
3.00 (2.09, 5.40)

2.90 (2.25, 3.80)
.50
3.27 (2.05, 4.00)

2.73 (1.90, 3.26)
.27
1.00 (0.25, 1.59) 0.36 (0, 0.95)

0.40 (0, 1.83)
0.76 (0, 1.10)
.67
.52
0.68 (0, 2.52)

0.30 (0, 3.41)
.92
4.13 (3.43, 6.40)

3.80 (3.07, 5.60)
.42
2.88 (2.00, 4.30)

3.00 (2.08, 4.80)
.63
3.45 (2.88, 3.95)

3.00 (1.90, 3.80)
.48
0.90 (0, 1.83)

0 (0, 1.00)
.07
0.60 (0, 1.00)

0 (0, 1.00)
.34
1.03 (0, 3.52)

0 (0, 0.80)
.04
3.85 (3.07, 5.70)

4.00 (3.50, 6.75)
.69
3.25 (2.41, 4.80)

2.75 (2.00, 5.10)
.80
3.26 (2.10, 3.80)

2.10 (1.60, 3.00)
.09
0.50 (0, 2.10)

0.50 ()0, 1.00)
.63
0.60 (0, 1.00)

0.00 (0, 3.29)
0.59 (0.45, 0.75) 0.10 (0, 3.52)
.98
.54
4.00 (3.07, 5.60)

3.50 (3.10, 6.75)
.82
3.25 (2.10, 4.80)

2.50 (2.50, 4.80)
.96
2.70 (1.90, 3.29)

3.70 (3.60, 4.43)
.05
0.00 (0, 1.00)

1.00 (0, 2.80)
.43
0.00 (0, 0.80)

0.00 (0, 1.00)
.96
4.00 (3.75, 5.30)

3.50 (2.50, 4.00)
.32
3.50 (2.75, 4.80)

3.25 (2.50, 5.50)
.96
2.10 (1.70, 2.80)

4.50 (2.00, 4.80)
.15
0.94 (0, 2.70)

0.25 (0, 1.00)
.17
0.00 (0, 0)
0.00 (0, 0)
1.0
a
For continuous characteristics, data are Spearman correlation (r) with associated P value. For categorical characteristics, data are median (25th, 75th percentile) for the
distances where P values compare the distances across characteristic subgroups by the Wilcoxon test. Values in parentheses are 25th and 75th percentiles when appropriate.
patients who developed permanent impairment, although this

did not achieve statistical significance (Table 2).
ILLUSTRATIVE CASES
Case 1
Patient 1 is a 4-year-old boy with an unremarkable medical
history who presented to medical attention with seizure activity.
He was evaluated by a neurologist, who treated him with
carbamazepine, levetiracetam, valproate, phenytoin, and zonisamide both alone and in combination. None of these medications
provided adequate seizure control, and the patient continued to
have daily unrelenting seizures despite medical therapy.
His seizures initially involved extension of his right upper
extremity but subsequently evolved into stereotypic movements
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and posturing involving his bilateral upper and lower extremities.

He was evaluated by the multidisciplinary epilepsy team. His
seizure focus was thought to involve the left mesial frontal
lobe. Video-EEG suggested a left-sided seizure focus. A positron
emission tomography scan showed a region of hypometabolism
in the left mesial frontal lobe, and an MRI showed a cortical
abnormality consistent with focal cortical dysplasia in this region.
Invasive monitoring was recommended to the patient and family
to better define the ictal onset and eloquent cortex.
A left-sided frontoparietal craniotomy was performed with
placement of subdural grids and strips overlying the lateral left
frontal, lateral left parietal, mesial left frontal, and mesial left
parietal lobes. Mapping was performed for anatomic localization of
the primary motor cortex. After the initial craniotomy for grids and
strips placement, the patient had seizure activity allowing mapping
KASASBEH ET AL
of his seizure focus to the left SMA. A second craniotomy for

seizure focus resection on postoperative day 2 was performed
(Figure 1). Permanent pathology revealed cortical dysplasia.
After the resection of the seizure focus, the patient had rightsided weakness and was abulic. He received steroids and was
observed in the pediatric intensive care unit. He gradually regained
his ability to ambulate before discharge. At his first outpatient
follow-up, he was noted to be seizure free with complete resolution
of his hemiparesis.
Case 2
Patient 2 is a 12-year-old boy who initially presented to the
epilepsy clinic with seizures beginning at 6 years of age. These
seizures showed stereotypic clonic activity in his left upper and
lower extremities initially but subsequently began involving more
complex movements and posturing. With rare exception, his
seizures occurred at night. He had been on oxcarbazepine,
levetiracetam, topiramate, and valproic acid without adequate
seizure control.
Patient 2 was evaluated with multiple imaging studies, which
included normal MRI and positron emission tomography showing
bilateral temporal hypometabolism. Video-EEG showed evidence
of right frontal seizure focus. After evaluation of all of the

diagnostic studies, invasive monitoring with cortical and
interhemispheric grids and strips was recommended to the patient
and family.
A right-sided frontoparietal craniotomy was performed with
placement of subdural grids and strips overlying the lateral right
frontal and right parietal lobes (Figure 2). A dual-layered array
was placed overlying the mesial right frontal and parietal lobes.
After several days of monitoring, 7 typical seizures were captured,
but the seizure focus was not confidently localized on the
available invasive arrays. Thus, on postoperative day 5, the
patient had additional right parietal and new left frontal subdural
strip electrodes placed to try to exclude a more remote ictal onset.
During these 2 surgeries, the primary motor cortex was mapped
for planning of his resection. After additional monitoring, the
seizure focus was ultimately localized to the right SMA, and
he was taken to the operating room for resection. Permanent
pathology revealed subpial astrocytosis and an increase in neurons
in the white matter of the lesion.
Postoperatively, the patient suffered from a left-sided hemiparesis and facial weakness. His motor function quickly improved,
although he remained with a small amount of left lower-extremity
FIGURE 1. In each intraoperative photo, note that the operative field is oriented as indicated in A. A, intraoperative picture
demonstrating placement of left frontal cortical array. B, intraoperative picture demonstrating motor (M) and sensory (S) cortex.
C, intraoperative image demonstrating resection of the left frontal seizure focus in the supplementary motor cortex. D, plain skull
radiograph demonstrating placement of subdural grids and strips.
FIGURE 2. In each intraoperative photo, note that the operative field is oriented as indicated in A. A, intraoperative picture
demonstrating placement of right frontal and parietal cortical array. B, intraoperative picture demonstrating motor cortex
representing hand control (H). C, intraoperative image demonstrating resection of the right frontal seizure focus in the supplementary motor cortex. D, plain skull radiograph demonstrating placement of subdural grids and strips in the patients index
operation.
weakness 1 month postoperatively. He was last seen in clinic

3.5 years postoperatively without any further seizure activity but
mildly diminished left foot coordination.
DISCUSSION
SMA Anatomy and Function
First described by Penfield and colleagues,44-47 the SMA
comprises a distinct anatomic and functional region of the
cerebral cortex situated largely on the mesial aspect of the superior
frontal gyrus.46 The SMA is limited posteriorly by the precentral
sulcus and inferiorly by the cingulate sulcus and genu of corpus
callosum.46-49 The anterior and lateral borders are less definite.
Early cortical stimulation studies indicated that the SMA extends
up to 5 cm anterior to the precentral sulcus and laterally to the
superior frontal sulcus.49 More recent studies suggest that
the posterior, lateral, and anterior margins may be variable.50
The SMA is considered to be composed of 2 distinct areas:
a caudal SMA proper or F3, which projects directly to primary
motor cortex and to spinal cord, and a rostral pre-SMA or F6,
which receives projections from the prefrontal cortex and
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cingulate motor areas.51 The SMA is principally motor in

function and has reciprocal connections with multiple components of the motor system, including the premotor cortex, primary
motor cortex, cingulate gyri, basal ganglia, and spinal cord (with
direct contributions to the descending corticospinal tracts),
in addition to connections to the contralateral SMA.50,52-57
Although predominantly motor, the SMA also serves a sensory
role46,50 and receives input from sensory cortex and parietal
sensory association areas.53,58 Furthermore, electric stimulation of
the SMA has been demonstrated to result in autonomic responses,
vocalization, inhibition of voluntary activity (most often speech),
assumption of characteristic postures, and changes in sensory
perception.46,59-62 These features may also be evident during
seizures arising from the SMA.59
Stimulation studies have demonstrated a somatotopic organization of the human SMA,50 contrary to its initial description.46
These studies revealed the lower limb, upper limb, and head
representations to extend from the posterior to anterior
margins.50 Sensory representation may be either anterior or
posterior to the motor representation.50 Fontaine et al31 showed
a correlation between immediate postoperative deficits and the
KASASBEH ET AL
anteroposterior extent of SMA resection. Postoperative aphasia

alone developed with resection of the most anterior part of the left
SMA, aphasia with motor impairment in the face and upper limb
with resection extending more posteriorly, and contralateral
hemiparesis and aphasia when the complete left SMA was
resected. Other studies of SMA syndrome after surgical resection
of the medial frontal lobe also indicate increased incidence and
severity of SMA syndrome with increased anteroposterior extent
of resection in the mesial frontal lobe.32,38,39 Such somatotopy is
pertinent because it aids in predicting the extent of postoperative
neurological deficit.
The function of the SMA has been elucidated through various
methods, including cortical stimulation,50,61 electrophysiological
single-cell63,64 and field potential recordings,65 regional cerebral
blood flow measurement,66,67 and functional MRI and positron
emission tomography studies.35,68-71 The SMA is considered
a supramotor region72 with a critical role in multiple aspects of
motor control, including the programming, initiation, and
execution of complex motor sequences.46,49,50,63,72-82 Studies
have demonstrated an increase in regional cerebral blood flow in
the primary motor cortex and SMA during execution of
movement.76,83 Even without execution of movement, an
increase in regional cerebral blood flow was shown in the
SMA while programming a sequence of movements. The SMA
controls proximal extremity muscle movement through direct
connections to the spinal cord. It influences distal extremity
movement indirectly through the primary motor area.84
SMA Syndrome After Surgery
In 1977, Laplane et al33 studied 3 patients who underwent
resection of the medial frontal lobe for intractable epilepsy. After
surgery, a syndrome emerged over 3 stages. First (first and second
weeks), patients developed nearly complete akinesia (more
pronounced contralaterally) associated with variable degrees of
speech arrest. This was followed by a stage of rapid recovery of
motor function of variable duration, although spontaneous
movement remained severely reduced contralaterally, with limited spontaneous speech. Movements in contralateral limbs could
be performed only after repeated spoken commands, and their
strength was almost normal when performed. Third, after gross
recovery of motor function, there was residual motor impairment
in the form of impairment of alternating movements of the
hands. This clinical syndrome was attributed to the resection of
the SMA. The observations of Laplane et al have been confirmed
by other studies of resection of the SMA (Table 9).28-39
In this series, SMA syndrome was characterized primarily by
postoperative contralateral hemiparesis/hemiplegia. Most often,
this was observed hours after surgery and improved gradually over
the next few days, with restoration of motor strength within 1 day
to 1 week of surgery in 41% of cases. The vast majority of cases
(82%) resolved by the first outpatient visit at 1 month. Two
patients (5.1%) experienced impairment in fine motor ability that
was sustained for a period of weeks to months after restoration of
motor strength. Speech impairment was noted in 9 patients

(23.1%), typically expressive aphasia and hesitancy of speech. Of
patients with speech impairment, 8 had surgery on the left
hemisphere and 1 had surgery on the right hemisphere. Speech
impairment usually resolved within days of surgery and resolved in
all but 1 patient by the day of discharge. In 1 patient, speech
impairment continued to improve after discharge from the
hospital and was reported to continue to improve at the first
postoperative visit. The degree of speech impairment was often
difficult to assess, however, because of the variability in preoperative speech development in this cohort.
The incidence of SMA syndrome after resections of the SMA in
adults is generally high (50%-100%; Table 9).28-39 A study by
Russell and Kelly37 demonstrated an incidence of SMA syndrome
of only 26% (n = 27) after resection of glial neoplasms involving
the SMA. They attributed the higher incidence in previous series
compared with their own to resection of functional cortex not
infiltrated by tumor. Resection of functional cortex was avoided
in their study by the use of stereotaxis to determine the posterior
margin of the mass. Additionally, Russell and Kelly reported that
no additional cortex was resected for purposes of epilepsy control
in their series. Differences in underlying pathology, surgical
procedure applied, methods of determining the SMA region, and
extent of SMA resection render comparing results of these studies
problematic. In our study, 44% of patients developed SMA
syndrome, comparable to previous reports. Furthermore, 15% of
patients in our study developed permanent neurological deficit
after surgery.
Minimizing the Risk of Permanent Deficit
Cortical resections in eloquent areas such as the SMA region and
rolandic cortex are fraught with risk of permanent neurological
deficits, particularly of contralateral motor function but also
language and cognitive function. However, reluctance to impart
a deficit should not excessively obscure the goal of achieving seizure
freedom in these medically refractory patients. We have not yet
seen a patient rendered seizure free but with postoperative motor
deficit who would trade their freedom from seizures for recovery of
motor function. Nevertheless, every effort is made to localize and
preserve eloquent cortex not involved in the ictal onset.85 During
resections in this region, we find the combination of cortical
stimulation mapping and intraoperative somatosensory evoked
potentials to be nearly universally successful in localizing the
primary motor cortex. Functional MRI and extraoperative
cortical stimulation mapping are also used heavily in grid-based
2-stage resections (35 of our 39 patients). Once the primary
motor cortex and ictal onset/early spread zones are identified,
a tailored resection or lesionectomy is performed. During and
after resection, cortical stimulation mapping is repeated. In most
cases, a good cortical motor response can be elicited after the
resection, with a similar threshold. When this is observed, thus
confirming the integrity of the corticospinal tract, the surgeon
and family can be largely reassured that a postoperative motor
NEUROSURGERY
TABLE 9. Previous Reports of Supplementary Motor Area Syndrome After Surgical Resection of Mesial Frontal Lobea
Study (Year)
Patients
(Pediatric
Patients
and (age), n
Patient
Presentation
Underlying
Pathology (n)
Developed
SMA
Syndrome, %
Developed Other
Neurological
Complications, %
3 (0)
Seizures
N/A (patients underwent

surgery for intractable
epilepsy)
100
N/A
Rostomily
et al36
(1991)
6 (0)
Seizures, hemiparesis,
speech impairment
Low-grade astrocytoma
(4), anaplastic
astrocytoma (1),
metastatic breast
adenocarcinoma (1)
100
N/A
Bleasel et al29
(1996)
10 (2; ages
13, 14)
Seizures
60
N/A
Zentner
et al39
(1996)
28 (0)
89
Bannur and
Rajshekhar28
(2000)
6 (0)
Seizures (in 12 patients,

surgery was indicated
for medically
intractable epilepsy),
hemiparesis, aphasia
Seizures
Cortical dysplasia (2),

subpial gliosis (1),
astrocytoma (2),
ganglioglioma (1),
astroblastoma (1),
abscess (1), no
abnormality (2)
High and low-grade
tumors (19),
nontumorous
lesions (9)
Astrocytoma (grades I
and II)
100
Duffau et al30
(2001)
1 (0)
Seizures
Low-grade glioma
100
Seizure Control
After Epilepsy
Patient 1: significant
impairment up to 15
mo; patient 2: returned
to normal at 1-mo
follow-up; patient 3: was
normal at 8-mo followup
Motor function returned
to near-baseline level 4
to 8 wk postoperatively;
restriction of
spontaneous movement
resolved after several
more weeks; at 6 mo
postoperatively,
patients had returned to
baseline function
Patients returned to
baseline in 2 d-2 mo
N/A
N/A
N/A
3-42 d (Mean, 11 d);

7, Seizure free; 3, $ 2
impairment of fine
seizures a year; 2,
motor function
. 75% reduction
observed for an
in seizure
additional 2 to 6 wk
frequency
N/A
2 Patients returned to
baseline status by 1 wk
postoperatively; longterm follow-up of 5
patients (details of each
patients not available)
showed return to
baseline in 4 patients
(with slowing of rapid
alternating movements)
Patient returned to
Seizure free
baseline after 2 mo
(Continues)
Laplane et al33
(1977)
Duration of Recovery
From SMA Syndrome
Study (Year)
Patients
(Pediatric
Patients
and (age), n
Patient
Presentation
Underlying
Pathology (n)
Developed
SMA
Syndrome, %
Developed Other
Neurological
Complications, %
65
N/A
100
N/A
Krainik et al32
(2001)
23 (0)
Seizures
Fontaine et al31
(2002)
11 (0)
Seizures, headache
Peraud et al34
(2002)
24 (0)
Seizures, speech
disturbances, motor
impairment,
headache, memory
deficits
Astrocytomas (grade II)
83
Russell and
Kelly37 (2003)
27 (0)
Seizures, hemiparesis,
headache
High- and low-grade

tumors
26
Ulu et al38
(2008)
12 (3; ages
10, 11,
and 14 y)
50
N/A
Rosenberg
et al35 (2010)
26 (0)
Seizures (4 patients
Low- and high-grade
underwent surgery for
tumors (9),
medically intractable
nontumorous
epilepsy), hemiparesis
lesions (3)
Seizures, motor and
High- and low-grade
speech impairment
gliomas, metastatic
lesions, cavernoma,
cortical dysplasia,
meningioma
23.1
N/A
Low-grade glioma (17),

anaplastic
astrocytoma (5),
cortical dysplasia (1)
Low-grade astrocytoma
(7), anaplastic
astrocytoma (1),
anaplastic
oligodendroglioma
(2), glioblastoma (1)
Duration of Recovery
From SMA Syndrome
Seizure Control
After Epilepsy
Recovery began after 2

N/A
d-6 wk and was
complete within weeks
to months
N/A
Recovery started
between 3 and 15
d postoperatively;
duration ranged from 3
d-3 mo; impairment in
initiating speech and
movement continued
for prolonged period
despite restoration of
motor strength
20 of 23 Patients
Recovery began in first
remained seizure
postoperative week; at
free in early
12 mo, 32% and 33% of
postoperative
patients who were
period; at 1 y, 3 of
followed up had motor
17 were seizure
deficits and speech
free without AEDs,
impairment,
and 9 were seizure
respectively
free with AEDs; the
remaining 5 had
same or reduced
frequency of
seizures
4% Had SMA syndrome
at the 1-mo
postoperative
examination (down
from 26% on day 1)
1 mo-1 y; Residual fine
motor impairment after
1 year in some patients
N/A
AED, antiepileptic drug; SMA, supplementary motor area.
N/A
N/A
N/A
KASASBEH ET AL
TABLE 9. Continued
deficit is most likely SMA syndrome, and the prognosis for motor
recovery is excellent. Should the cortical stimulation threshold be
significantly increased or responses no longer obtained or if
resection involves the primary motor cortex, a permanent deficit
is more likely the outcome. Nevertheless, substantial improvement is generally the rule (Table 3).
We have observed 2 predominant patterns of recovery in our
patients. Those that ultimately go on to have SMA syndrome
without permanent deficit may have a profound hemiplegia with
neglect in the first hours or days after surgery and recovery of
movement in distal extremities (finger and toe fine movements)
first. Patients with permanent deficits regain proximal movement
first, consistent with pyramidal/corticospinal tract injury. Thus,
a patient with an intact cortical stimulation threshold at the
completion of resection who recovers some finger movement in
the first week most likely has pure SMA syndrome with an
excellent prognosis for recovery. Our 6 patients with residual
permanent deficits demonstrated little improvement before
discharge from the hospital. In those who showed some recovery
before discharge, improvement in proximal movement was
often noted.
Berger et al86 reported that resections within 1 cm of eloquent
cortex have a substantially increased risk of irreversible deficit. We
have found that resections in the SMA region, within 1 cm of the
precentral gyrus, also have the highest rate of postoperative deficit
(Table 2). However, careful preservation of the precentral gyrus
with a subpial aspiration technique back to the precentral sulcus
can result in excellent outcomes with no deficit once the SMA
syndrome resolves. Care should be taken not to undercut the
white matter of the precentral gyrus, and frequent subcortical
mapping during the resection can help ensure the integrity of the
descending tracts of the primary motor areas. For patients who
developed permanent neurological deficit in our series, distances
of resection from precentral sulcus and cingulate gyrus were
significantly shorter compared with those in patients with no
neurological impairment. Moreover, there was a trend toward
larger anteroposterior dimension of resection in patients who
developed permanent impairment. In none of the patients who
developed permanent deficit was the primary motor cortex
knowingly resected. Further studies investigating the development of permanent deficit after resection of the SMA proper vs
pre-SMA are warranted.
Neurological Recovery
The transitory nature of neurological impairment is the
hallmark of SMA syndrome. Of the 17 patients in this study
who developed SMA syndrome, 7 (41%) had resolution of
symptoms by 1 week postoperatively, 7 (41%) had resolution of
symptoms between the 1-week and 1-month follow-up visits, and
3 (18%) had resolution of symptoms after the 1-month follow-up
visit. The rate of resolution of SMA syndrome was not found to
significantly correlate with patient characteristics, seizure characteristics, use of invasive monitoring, or surgery type. Interestingly,
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the delay between seizure identification and surgical resection was

found to be significantly longer in patients who developed SMA
syndrome. The significance of this finding is uncertain. Patients
with a preoperative MRI lesion were significantly less likely to
suffer neurological impairment after surgical resection. The
majority of patients who developed postoperative SMA syndrome
were not found to have a lesional diagnosis on preoperative MRI.
This may suggest that in nonlesional cases, neuroplastic changes
are more capable of compensating for anatomic resections in the
region of the SMA. Further studies are needed to validate this
hypothesis. Furthermore, male patients were found to have
undergone significantly more extensive anteroposterior resections.
A physiological-anatomical explanation for such a sex difference is
elusive, suggesting that this statistical finding may be attributed to
type II error.
The development of SMA syndrome strongly correlated with
the proximity of surgical resection to precentral sulcus. Moreover,
the anteroposterior extent of surgical resection was also correlated
with the development of SMA syndrome. This is consistent with
previous reports in adults in which patients more frequently
manifested motor impairment with surgical resection extending
further into the caudal SMA.32,34,39 Furthermore, a significant
correlation was found in our series between the development of
the SMA syndrome and the distance of the inferior border of
resection to cingulate sulcus. This finding is consistent with
previous studies in adults.87,88 However, Russell and Kelly37 did
not find a correlation between violation of cingulate gyrus and
increased frequency of SMA in their series. Additionally,
a significantly more extensive resection lateral to longitudinal
fissure was associated with pathologies categorized as dysplasia.
The mechanism of resolution of SMA syndrome is not fully
understood, although recruitment of contralateral SMA and intact
ipsilateral premotor cortex after surgical resection are believed to be
critical in this recovery.35,89-91 Supporting this is the finding that
bilateral surgical resection of the SMA resulted in protracted
motor and speech impairment.92 One proposed hypothesis to
explain restoration of SMA function after surgery in the medial
frontal lobe for tumors is the displacement of functioning SMA
by the tumor.28 Such displacement may partially explain the
transitory nature of SMA syndrome in patients with slowgrowing tumors but does not satisfactorily account for the similar
evolution of SMA syndrome in patients who undergo surgical
resections for other purposes and in whom other underlying
pathology is identified. Several lines of evidence converge on the
occurrence of plastic brain mechanisms reestablishing SMA
function.30,93 Duffau et al30 studied the development of SMA
syndrome after resection of a low-grade glioma invading the
SMA. The patient demonstrated no motor or speech disturbances
at the end of tumor removal. Nearly 30 minutes after the
resection, aphasia and contralateral hemiplegia developed. This
SMA syndrome continued for 10 days and was followed by
gradual improvement, with total recovery observed at 2 months
after the resection. This progression may be explained by shortterm plasticity predicated on unmasking of parallel networks in
KASASBEH ET AL
addition to the residual activity of an oscillatory loop, with longterm recovery attributed to long-term plasticity.30 In the
developing brain, plasticity is undoubtedly an important contributing factor in resolution of SMA syndrome in pediatric
patients.94-96 Future studies elucidating the precise underlying
mechanisms of resolution of SMA syndrome are needed to
validate these hypotheses.
Seizure Outcome
The majority of patients had favorable seizure outcome (Engel
class I or II) at the 12-month and extended follow-up visits (84%
and 73%, respectively). Lesionectomy was performed in 26% of
patients with Engel class I/II at the 12-month postoperative
follow-up, whereas none of the patients who had Engel class III/IV
had lesionectomy. Similarly, at the last follow-up, more patients
with Engel class I/II were found to have undergone lesionectomy.
These findings notwithstanding, our analysis did not demonstrate
a statistically significant relationship between seizure outcome and
type of surgery performed. The absence of statistical significance
compared with patients who underwent other surgical procedures
may be explained by the fact that a large proportion of patients who
did not undergo lesionectomies also had favorable seizure outcome. In addition, the small number of patients who underwent
lesionectomies may have precluded statistical significance. Of
note, age at the time of surgery was significantly higher for patients
with Engel class I/II compared with patients with Engel class
III/IV at the extended follow-up. Furthermore, at the extended
follow-up, the delay between seizure identification and surgery was
significantly longer in patients with Engel class I/II compared with
patients with Engel class III/IV. These findings are not explained
by our data collection but may be related to the underlying cause of
seizure disorder in younger vs older patients undergoing epilepsy
surgery.
Seizure outcome in the early postoperative period remained
largely unchanged throughout the follow-up period. More
extensive anteroposterior extent of surgical resection was found
to be associated with an appreciable, albeit statistically insignificant, decline in Engel class between the 1- and 6-month follow-up
visits. Similarly, a decline was found between the 1-month and
12-month follow-up visits in the proximity of the posterior border
of the surgical resection to precentral sulcus. Additionally, a decline
in Engel class was noted with more extensive superior-inferior
resections. Of note, the number of patients who experienced
deterioration in seizure outcome after the first month postoperatively was small (n = 4-6). This may explain the absence
of statistical significance in our studies. Moreover, the variability
in Engel class changes was not sufficient to allow further statistical
analyses. In addition, early postoperative seizure recurrence was
associated with a significantly increased likelihood of seizures at
the 6-month and 12-month follow-up visits and a nonsignificant
trend toward seizure recurrence at extended follow-up visit.
These findings indicate that early seizure recurrence is a negative
predictor of seizure outcome. Long-term seizure control did
not correlate with dimensions of surgical resection, with the
exception that a significantly smaller transverse resection was

associated with favorable seizure outcome at the 12-month
follow-up, a finding of unclear significance. A decline in Engel
class over the follow-up period was significantly less probable in
right-handed patients. This may be explained by patients
undergoing more conservative resections when surgery is
performed in the dominant hemisphere. Changes in Engel class
were not correlated with other patient characteristics, seizure
type, or surgery type.
CONCLUSION
Surgery in the region of the medial frontal cortex is associated
with the development of SMA syndrome. In this study of
exclusively pediatric patients, fewer than half of the patients
developed SMA syndrome. The SMA syndrome was characterized
primarily by postoperative contralateral hemiparesis/hemiplegia
that developed within hours of surgery and resolved in the majority
of cases by 1 month postoperatively. Development of postoperative SMA syndrome was related to the anteroposterior extent
of surgical resection and proximity of the resection to the
precentral and cingulate sulci. In addition, surgery in the medial
frontal lobe was associated with favorable seizure outcomes. Our
studies show that resections in the SMA can be performed safely
in children and are associated with reversible neurological
impairment.
Disclosure
The authors have no personal financial or institutional interest in any of the
drugs, materials, or devices described in this article.
REFERENCES
1. Hauser WA, Hesdorffer DC. Epilepsy: Frequency, Causes and Consequences.
New York, NY: Demos; 1990.
2. Berg AT. The epidemiology of seizures and epilepsy in children. In: Shinnar S,
Amir N, Branski D, eds. Childhood Seizures. Basel, Switzerland: Karger; 1995:1-10.
3. Shinnar S, Pellock JM. Update on the epidemiology and prognosis of pediatric
epilepsy. J Child Neurol. 2002;17(suppl 1):S4-S17.
4. Caplan R, Siddarth P, Vona P, et al. Language in pediatric epilepsy. Epilepsia.
2009;50(11):2397-2407.
5. Bailet LL, Turk WR. The impact of childhood epilepsy on neurocognitive and
behavioral performance: a prospective longitudinal study. Epilepsia. 2000;41(4):
426-431.
6. Bjornaes H, Stabell K, Henriksen O, Loyning Y. The effects of refractory epilepsy
on intellectual functioning in children and adults; a longitudinal study. Seizure.
2001;10(4):250-259.
7. Tromp SC, Weber JW, Aldenkamp AP, Arends J, vander Linden I, Diepman L.
Relative influence of epileptic seizures and of epilepsy syndrome on cognitive
function. J Child Neurol. 2003;18(6):407-412.
8. van Empelen R, Jennekens-Schinkel A, van Rijen PC, Helders PJ, van
Nieuwenhuizen O. Health-related quality of life and self-perceived competence
of children assessed before and up to two years after epilepsy surgery. Epilepsia.
2005;46(2):258-271.
9. Hum KM, Smith ML, Lach L, Elliott IM. Self-perceptions of social function 2
years after pediatric epilepsy surgery. Epilepsy Behav. 2010;17(3):354-359.
10. Nashef L, Fish DR, Garner S, Sander JW, Shorvon SD. Sudden death in epilepsy:
a study of incidence in a young cohort with epilepsy and learning difficulty.
Epilepsia. 1995;36(12):1187-1194.
11. Callenbach PM, Westendorp RG, Geerts AT, et al. Mortality risk in children with
epilepsy: the Dutch study of epilepsy in childhood. Pediatrics. 2001;107(6):
1259-1263.
12. Breningstall GN. Mortality in pediatric epilepsy. Pediatr Neurol. 2001;25(1):9-16.
13. Randomized clinical trial on the efficacy of antiepileptic drugs in reducing the risk
of relapse after a first unprovoked tonic-clonic seizure: First Seizure Trial Group
(FIR.S.T. Group). Neurology. 1993;43(3 pt 1):478-483.
14. Musicco M, Beghi E, Solari A, Viani F. Treatment of first tonic-clonic seizure does
not improve the prognosis of epilepsy: First Seizure Trial Group (FIRST Group).
Neurology. 1997;49(4):991-998.
15. Shinnar S, Berg AT, ODell C, Newstein D, Moshe SL, Hauser WA. Predictors of
multiple seizures in a cohort of children prospectively followed from the time of
their first unprovoked seizure. Ann Neurol. 2000;48(2):140-147.
16. Hadjiloizou SM, Bourgeois BF. Antiepileptic drug treatment in children. Expert
Rev Neurother. 2007;7(2):179-193.
17. Shinnar S, Berg AT. Does antiepileptic drug therapy prevent the development of
chronic epilepsy? Epilepsia. 1996;37(8):701-708.
18. Arts WF, Visser LH, Loonen MC, et al. Follow-up of 146 children with epilepsy
after withdrawal of antiepileptic therapy. Epilepsia. 1988;29(3):244-250.
19. Shinnar S, Berg AT, Moshe SL, et al. Discontinuing antiepileptic drugs in children
with epilepsy: a prospective study. Ann Neurol. 1994;35(5):534-545.
20. Tennison M, Greenwood R, Lewis D, Thorn M. Discontinuing antiepileptic
drugs in children with epilepsy: a comparison of a six-week and a nine-month taper
period. N Engl J Med. 1994;330(20):1407-1410.
21. Sillanpaa M, Jalava M, Kaleva O, Shinnar S. Long-term prognosis of seizures with
onset in childhood. N Engl J Med. 1998;338(24):1715-1722.
22. Berg AT, Shinnar S, Levy SR, Testa FM, Smith-Rapaport S, Beckerman B. Early
development of intractable epilepsy in children: a prospective study. Neurology.
2001;56(11):1445-1452.
23. Berg AT, Shinnar S, Levy SR, et al. Defining early seizure outcomes in pediatric
epilepsy: the good, the bad and the in-between. Epilepsy Res. 2001;43(1):75-84.
24. Sillanpaa M, Jalava M, Shinnar S. Epilepsy syndromes in patients with childhoodonset seizures in Finland. Pediatr Neurol. 1999;21(2):533-537.
25. Behrens E, Schramm J, Zentner J, Konig R. Surgical and neurological complications
in a series of 708 epilepsy surgery procedures. Neurosurgery. 1997;41(1):1-9.
26. Dorward IG, Titus JB, Limbrick DD, Johnston JM, Bertrand ME, Smyth MD.
Extratemporal, nonlesional epilepsy in children: postsurgical clinical and neurocognitive outcomes. J Neurosurg Pediatr. 2011;7(2):179-188.
27. Hemb M, Velasco TR, Parnes MS, et al. Improved outcomes in pediatric epilepsy
surgery: the UCLA experience, 1986-2008. Neurology. 2010;74(22):1768-1775.
28. Bannur U, Rajshekhar V. Post operative supplementary motor area syndrome:
clinical features and outcome. Br J Neurosurg. 2000;14(3):204-210.
29. Bleasel A, Comair Y, Luders H. Surgical ablations of the mesial frontal lobe in
humans. Adv Neurol. 1996;70:217-235.
30. Duffau H, Lopes M, Denvil D, Capelle L. Delayed onset of the supplementary
motor area syndrome after surgical resection of the mesial frontal lobe: a time
course study using intraoperative mapping in an awake patient. Stereotact Funct
Neurosurg. 2001;76(2):74-82.
31. Fontaine D, Capelle L, Duffau H. Somatotopy of the supplementary motor area:
evidence from correlation of the extent of surgical resection with the clinical
patterns of deficit. Neurosurgery. 2002;50(2):297-303.
32. Krainik A, Lehericy S, Duffau H, et al. Role of the supplementary motor area in
motor deficit following medial frontal lobe surgery. Neurology. 2001;57(5):871-878.
33. Laplane D, Talairach J, Meininger V, Bancaud J, Orgogozo JM. Clinical
consequences of corticectomies involving the supplementary motor area in man.
J Neurol Sci. 1977;34(3):301-314.
34. Peraud A, Meschede M, Eisner W, Ilmberger J, Reulen HJ. Surgical resection of
grade II astrocytomas in the superior frontal gyrus. Neurosurgery. 2002;50(5):
966-975.
35. Rosenberg K, Nossek E, Liebling R, et al. Prediction of neurological deficits and
recovery after surgery in the supplementary motor area: a prospective study in 26
patients. J Neurosurg. 2010;113(6):1152-1163.
36. Rostomily RC, Berger MS, Ojemann GA, Lettich E. Postoperative deficits and
functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. J Neurosurg. 1991;75(1):62-68.
37. Russell SM, Kelly PJ. Incidence and clinical evolution of postoperative deficits after
volumetric stereotactic resection of glial neoplasms involving the supplementary
motor area. Neurosurgery. 2003;52(3):506-516.
NEUROSURGERY
38. Ulu MO, Tanriover N, Ozlen F, et al. Surgical treatment of lesions involving the
supplementary motor area: clinical results of 12 patients. Turk Neurosurg. 2008;18
(3):286-293.
39. Zentner J, Hufnagel A, Pechstein U, Wolf HK, Schramm J. Functional results
after resective procedures involving the supplementary motor area. J Neurosurg.
1996;85(4):542-549.
40. Engel JJ, Van Ness PC, Rasmussen TB, Ojemann LM. Surgical treatment of the
epilepsies. In: Engel JJ, ed. Outcome With Respect to Epileptic Seizures. New York,
NY: Raven Press; 1993:609-621.
41. Sanai N, Berger MS. Intraoperative stimulation techniques for functional pathway
preservation and glioma resection. Neurosurg Focus. 2010;28(2):E1.
42. Keles GE, Lundin DA, Lamborn KR, Chang EF, Ojemann G, Berger MS.
Intraoperative subcortical stimulation mapping for hemispherical perirolandic
gliomas located within or adjacent to the descending motor pathways: evaluation
of morbidity and assessment of functional outcome in 294 patients. J Neurosurg.
2004;100(3):369-375.
43. Ojemann SG, Berger MS, Lettich E, Ojemann GA. Localization of language
function in children: results of electrical stimulation mapping. J Neurosurg. 2003;
98(3):465-470.
44. Penfield W, Roberts L. Speech and Brain Mechanisms. Princeton, NJ: Princeton
University Press; 1959.
45. Penfield W. The supplementary motor area in the cerebral cortex of man. Arch
Psychiatr Nervenkr Z Gesamte Neurol Psychiatr. 1950;185(6-7):670-674.
46. Penfield W, Welch K. The supplementary motor area of the cerebral cortex;
a clinical and experimental study. AMA Arch Neurol Psychiatry. 1951;66(3):289-317.
47. Penfield W, Rasmussen T. The Cerebral Cortex of Man: a Clinical Study of
Localization of Function. New York, NY: Macmillan; 1950.
48. Picard N, Strick PL. Motor areas of the medial wall: a review of their location and
functional activation. Cereb Cortex. 1996;6(3):342-353.
49. Talairach J, Bancaud J. The supplementary motor area in man (anatomofunctional
findings by stereo-electroencephalography in epilepsy). Int J Neurol. 1966;5:
330-347.
50. Lim SH, Dinner DS, Pillay PK, et al. Functional anatomy of the human
supplementary sensorimotor area: results of extraoperative electrical stimulation.
Electroencephalogr Clin Neurophysiol. 1994;91(3):179-193.
51. Tanji J. The supplementary motor area in the cerebral cortex. Neurosci Res. 1994;
19(3):251-268.
52. Hutchins KD, Martino AM, Strick PL. Corticospinal projections from the medial
wall of the hemisphere. Exp Brain Res. 1988;71(3):667-672.
53. Jurgens U. The efferent and afferent connections of the supplementary motor area.
Brain Res. 1984;300(1):63-81.
54. Macpherson J, Wiesendanger M, Marangoz C, Miles TS. Corticospinal neurones
of the supplementary motor area of monkeys: a single unit study. Exp Brain Res.
1982;48(1):81-88.
55. Schell GR, Strick PL. The origin of thalamic inputs to the arcuate premotor and
supplementary motor areas. J Neurosci. 1984;4(2):539-560.
56. Wiesendanger M, Wiesendanger R. The supplementary motor area in the light of
recent investigations. Exp Brain Res Suppl. 1984;9:382-392.
57. Wiesendanger M. Recent developments in studies of the supplementary motor
area of primates. Rev Physiol Biochem Pharmacol. 1986;103:1-59.
58. Eccles JC. The initiation of voluntary movements by the supplementary motor
area. Arch Psychiatr Nervenkr. 1982;231(5):423-441.
59. Green JR, Angevine JB, White JC Jr, Edes AD, Smith RD. Significance of the
supplementary motor area in partial seizures and in cerebral localization.
Neurosurgery. 1980;6(1):66-75.
60. Morris HH III, Dinner DS, Luders H, Wyllie E, Kramer R. Supplementary motor
seizures: clinical and electroencephalographic findings. Neurology. 1988;38(7):
1075-1082.
61. Penfield W, Jasper H. Epilepsy and the Functional Anatomy of the Human Brain.
Boston, MA: Little, Brown and Co; 1954.
62. Woolsey CN, Erickson TC, Gilson WE. Localization in somatic sensory and
motor areas of human cerebral cortex as determined by direct recording of evoked
potentials and electrical stimulation. J Neurosurg. 1979;51(4):476-506.
63. Mushiake H, Inase M, Tanji J. Neuronal activity in the primate premotor,
supplementary, and precentral motor cortex during visually guided and internally
determined sequential movements. J Neurophysiol. 1991;66(3):705-718.
64. Tanji J, Shima K. Role for supplementary motor area cells in planning several
movements ahead. Nature. 1994;371(6496):413-416.
KASASBEH ET AL
65. Lang W, Obrig H, Lindinger G, Cheyne D, Deecke L. Supplementary motor area

activation while tapping bimanually different rhythms in musicians. Exp Brain Res.
1990;79(3):504-514.
66. Gelmers HJ. Cortical organization of voluntary motor activity as revealed by
measurement of regional cerebral blood flow. J Neurol Sci. 1981;52(2-3):149-161.
67. Roland PE, Meyer E, Shibasaki T, Yamamoto YL, Thompson CJ. Regional
cerebral blood flow changes in cortex and basal ganglia during voluntary
movements in normal human volunteers. J Neurophysiol. 1982;48(2):467-480.
68. Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RS, Passingham RE. Motor
sequence learning: a study with positron emission tomography. J Neurosci. 1994;
14(6):3775-3790.
69. Santosh CG, Rimmington JE, Best JJ. Functional magnetic resonance imaging at 1
T: motor cortex, supplementary motor area and visual cortex activation. Br J
Radiol. 1995;68(808):369-374.
70. Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD,
Frackowiak RS. Cortical areas and the selection of movement: a study with
positron emission tomography. Exp Brain Res. 1991;84(2):393-402.
71. Rao SM, Binder JR, Bandettini PA, et al. Functional magnetic resonance imaging
of complex human movements. Neurology. 1993;43(11):2311-2318.
72. Orgogozo JM, Larsen B. Activation of the supplementary motor area during
voluntary movement in man suggests it works as a supramotor area. Science. 1979;
206(4420):847-850.
73. Cadoret G, Smith AM. Comparison of the neuronal activity in the SMA and the
ventral cingulate cortex during prehension in the monkey. J Neurophysiol. 1997;77
(1):153-166.
74. Chauvel PY, Rey M, Buser P, Bancaud J. What stimulation of the supplementary
motor area in humans tells about its functional organization. Adv Neurol. 1996;70:
199-209.
75. Danks RA, Aglio LS, Gugino LD, Black PM. Craniotomy under local anesthesia
and monitored conscious sedation for the resection of tumors involving eloquent
cortex. J Neurooncol. 2000;49(2):131-139.
76. Fox PT, Fox JM, Raichle ME, Burde RM. The role of cerebral cortex in the
generation of voluntary saccades: a positron emission tomographic study.
J Neurophysiol. 1985;54(2):348-369.
77. Fried I, Katz A, McCarthy G, et al. Functional organization of human
supplementary motor cortex studied by electrical stimulation. J Neurosci. 1991;
11(11):3656-3666.
78. Goldberg G. Supplementary motor area structure and function: review and
hypothesis. Behav Brain Sci. 1985;8(4):567-616.
79. Hikosaka O, Sakai K, Miyauchi S, Takino R, Sasaki Y, Putz B. Activation of
human presupplementary motor area in learning of sequential procedures:
a functional MRI study. J Neurophysiol. 1996;76(1):617-621.
80. Humberstone M, Sawle GV, Clare S, et al. Functional magnetic resonance
imaging of single motor events reveals human presupplementary motor area. Ann
Neurol. 1997;42(2):632-637.
81. Kansaku K, Kitazawa S, Kawano K. Sequential hemodynamic activation of motor
areas and the draining veins during finger movements revealed by cross-correlation
between signals from fMRI. Neuroreport. 1998;9(9):1969-1974.
82. Weilke F, Spiegel S, Boecker H, et al. Time-resolved fMRI of activation patterns in
M1 and SMA during complex voluntary movement. J Neurophysiol. 2001;85(5):
1858-1863.
83. Roland PE, Larsen B, Lassen NA, Skinhoj E. Supplementary motor area and other
cortical areas in organization of voluntary movements in man. J Neurophysiol.
1980;43(1):118-136.
84. Schneider R, Gautier JC. Leg weakness due to stroke: site of lesions, weakness
patterns and causes. Brain. 1994;117(pt 2):347-354.
85. Behdad A, Limbrick DD Jr, Bertrand ME, Smyth MD. Epilepsy surgery in
children with seizures arising from the rolandic cortex. Epilepsia. 2009;50(6):
1450-1461.
86. Berger MS, Kincaid J, Ojemann GA, Lettich E. Brain mapping techniques to
maximize resection, safety, and seizure control in children with brain tumors.
Neurosurgery. 1989;25(5):786-792.
87. Nemeth G, Hegedus K, Molnar L. Akinetic mutism associated with bicingular
lesions: clinicopathological and functional anatomical correlates. Eur Arch
Psychiatry Neurol Sci. 1988;237(4):218-222.
88. von Lehe M, Schramm J. Gliomas of the cingulate gyrus: surgical management and
functional outcome. Neurosurg Focus. 2009;27(2):E9.
89. Freund HJ. Premotor areas in man. Trends Neurosci. 1984;7(12):481-483.
90. Krainik A, Lehericy S, Duffau H, et al. Postoperative speech disorder after medial
frontal surgery: role of the supplementary motor area. Neurology. 2003;60(4):
587-594.
91. Krainik A, Duffau H, Capelle L, et al. Role of the healthy hemisphere in recovery
after resection of the supplementary motor area. Neurology. 2004;62(8):1323-1332.
92. Freund HJ. Premotor area and preparation of movement. Rev Neurol (Paris). 1990;
146(10):543-547.
93. Aizawa H, Inase M, Mushiake H, Shima K, Tanji J. Reorganization of activity in
the supplementary motor area associated with motor learning and functional
recovery. Exp Brain Res. 1991;84(3):668-671.
94. Johnston MV, Ishida A, Ishida WN, Matsushita HB, Nishimura A, Tsuji M.
Plasticity and injury in the developing brain. Brain Dev. 2009;31(1):1-10.
95. Johnston MV, Nishimura A, Harum K, Pekar J, Blue ME. Sculpting the
developing brain. Adv Pediatr. 2001;48:1-38.
96. Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human
cerebral cortex. J Comp Neurol. 1997;387(2):167-178.
COMMENT
he authors present an elaborate study on the occurrence and outcome

of supplementary motor area (SMA) syndrome and epilepsy outcome
among children with refractory epilepsy undergoing invasive monitoring
and resections. This series is the largest to date describing the rate and
outcome of SMA syndrome in general and in children in particular.
Thirty-nine children with refractory epilepsy underwent resections of
lesions (or nonlesional epileptic foci) located completely or partially in the
SMA region. Twenty-three (60%) had postoperative neurological
impairment; 75% was transient and attributed to SMA syndrome. The
authors found a significant correlation between the distance from the
posterior resection margin and the precentral sulcus and the occurrence of
neurological impairment.
Seventeen of 23 children (74%) with no lesion had a new neurological
impairment as opposed to 6 of 10 children (37%) with lesions. Of the
nonlesional cases, 14 (82%) were SMA syndrome compared with 3 (50%)
of the lesional cases. This may be explained by the concept that resection of
nonlesional foci may be more extensive and thus cause more morbidity
compared with a lesionectomy (or even a lesionectomy plus when
additional resection is tailored). However, in nonlesional cases, brain
plasticity secondary to chronic seizures (often resulting from an anatomically ill-defined pathology such as cortical dysplasia or gliosis)
compensates for the anatomic resection of the SMA compared with
lesional cases in which brain plasticity has less occurred.
An additional point worth noting is the correlation between early
postoperative seizure recurrence and long-term epilepsy outcome. Early
seizure recurrence was associated with long-term seizures, and seizure
freedom during the first postoperative month was associated with longterm seizure freedom.
The authors are to be complimented on this interesting and important
study.
Jonathan Roth
Zvi Ram
Tel-Aviv, Israel

Characterization of The Supplementary Motor Area Syndrome and Seizure Outcome After Medial Frontal Lobe Resections in Pediatric Epilepsy Surgery

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Characterization of The Supplementary Motor Area Syndrome and Seizure Outcome After Medial Frontal Lobe Resections in Pediatric Epilepsy Surgery

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RESEARCHHUMANCLINICAL STUDIES

Characterization of the Supplementary Motor Area

Aimen S. Kasasbeh, MD*

SANS LifeLong Learning and

KEY WORDS: Epilepsy surgery, Pediatric epilepsy, Supplementary motor area

pilepsy is a common neurological disorder

1152 | VOLUME 70 | NUMBER 5 | MAY 2012

ABBREVIATIONS: SMA, supplementary motor

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POSTOPERATIVE PEDIATRIC SMA SYNDROME

(MRI), functional MRI, video electroencephalography (video-EEG),

Study Outcome Measures

CPS, complex partial seizures; SPS, simple partial seizures.

VOLUME 70 | NUMBER 5 | MAY 2012 | 1153

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1154 | VOLUME 70 | NUMBER 5 | MAY 2012

patients), extraoperative mapping data acquired from subdural

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Low-grade glial neoplasm with

Contralateral hemiparesis, contralateral facial

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POSTOPERATIVE PEDIATRIC SMA SYNDROME

VOLUME 70 | NUMBER 5 | MAY 2012 | 1155

Contralateral hemiparesis, aphasia

Contralateral lower limb weakness

1156 | VOLUME 70 | NUMBER 5 | MAY 2012

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SMA, supplementary motor area.

compared with 1 month was 13% at 6 months, 16% at 12 months,

TABLE 5. Seizure Outcome After Surgery in the Medial Frontal

SMA Syndrome (n = 17)

POSTOPERATIVE PEDIATRIC SMA SYNDROME

Association of Extent and Location of Resection With

VOLUME 70 | NUMBER 5 | MAY 2012 | 1157

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TABLE 6. Association Between Engel Class and Patient Characteristicsa

Engel Class at Extended Follow-up

Age of seizure onset, mo

categorized as dysplasia. Resection parameters were not associated

Permanent Neurological Deficit

Early Postoperative Occurrence

1158 | VOLUME 70 | NUMBER 5 | MAY 2012

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POSTOPERATIVE PEDIATRIC SMA SYNDROME

0.43 (0, 0.95)

0.05 (0, 3.29)

3.14 (2.70, 4.03)

3.00 (2.09, 5.40)

3.27 (2.05, 4.00)

1.00 (0.25, 1.59) 0.36 (0, 0.95)

0.68 (0, 2.52)

4.13 (3.43, 6.40)

2.88 (2.00, 4.30)

3.45 (2.88, 3.95)

0.90 (0, 1.83)

0.60 (0, 1.00)

1.03 (0, 3.52)

3.85 (3.07, 5.70)

3.25 (2.41, 4.80)

3.26 (2.10, 3.80)

0.50 (0, 2.10)

0.60 (0, 1.00)

4.00 (3.07, 5.60)