Role of intraoperative electrophysiological monitoring during ...

Role of intraoperative electrophysiological monitoring during selective
dorsal rhizotomy in children with spastic cerebral palsy regarding
sparing of sphincter innervation
Authors:
Ali S Shalash 1 , Walid Abdel Ghany 2 , Ahmad Elsayed Desoky²
Department of Neurology¹ and Neurosurgery²
Ain Shams University
Cairo
Egypt
Correspondence:
Dr. Walid Abdel Ghany
Department of Neurosurgery
Ain Shams University
Cairo
Egypt
E-mail: wghany@gmail.com
Abstract
Background: Selective dorsal rhizotomy (SDR) is an established strategy for treating spastic
cerebral palsy. The applied techniques and criteria of intraoperative electrophysiological
monitoring (EPM) for selected transected rootlets vary between different centers; therefore,
its validity has been questioned. The aim of this study is to evaluate the applied techniques of
EPM used during SDR for treating spasticity in Egyptian children with cerebral palsy
regarding sparing of sphincters innervation.
Patients and method: Twenty-two children (14 boys and 8 girls) underwent EPM guided
SDR. Percentage of abnormal rootlets (grades 3 + and 4+ Phillips and Park classification),
which are suitable for transection and presence of sphincter related fibers in S1 dorsal root(s)
were estimated. Postoperative outcome assessment for all children was done at one month
and after 6 months was assessed for 8 cases. Assessment protocol includes assessment of
power of quadriceps; range of motion (ROM) of hip abduction; tone grading of adductor
muscles and electromyography of pelvic muscles for evaluation of sphincters.
Results: 52.8% of stimulated rootlets in each stimulated dorsal root were graded as 3+ or 4+
and were transected. In 6 children (27%), either right or left S1 dorsal root anal sphincter
response was recorded and these roots were spared. Postoperative outcome evaluation at the
1 st month postoperative showed statistically insignificant electrographic changes in those
children having sphincter related fibers in S1 dorsal root. Improvement of adductors tone and
ROM, while significant decrease in motor power of quadriceps was found. At 6 months
postoperative, no electrophysiological abnormalities detected in sphincters. Significant
increase of ROM of hip abduction; insignificant decrease of spasticity of adductor muscles;
and insignificant improvement of motor power of quadriceps are detected. No postoperative
complications were detected.
Conclusions: The present study demonstrates that the applied EPM procedures during SDR
provide an objective way for selecting transected rootlets and avoiding postoperative
complications regarding sphincters.
Keywords: electrophysiology; spasticity; dorsal rhizotomy; sphincters, cerebral palsy
1

Introduction:
In the developing world, the prevalence of cerebral palsy (CP) is not well established but
estimates are 1.5-5.6 cases per 1000 live births. 20 Selective dorsal rhizotomy (SDR) is a
widely practiced form of surgical treatment for children with spasticity of cerebral origin,
predominately due to cerebral palsy. 3 In SDR, partial sectioning of the dorsal roots from L2
to S1 or S2 is usually performed. [15, 22, 28] Clinically significant improvements in functional
[4-8, 10, 12, 14, 15, 21, 25, 26, 28]
outcome have been reported by several groups.
Percentage of sectioned rootlets is guided by clinical findings and interoperative
electrophysiological monitoring (EPM). [10, 13, 29] Intraoperative monitoring uses continuous
recording of electromyography (EMG) in lower limb muscles and anal sphincter, and its
response to simulation of selected rootlets. [13, 24, 26] Intraoperative electrophysiological (EP)
stimulation can be valuable in achieving a balance between elimination of spasticity and
[13, 26, 27, 29]
preservation of underlying strength.
EMG monitoring helps also to avoid complications, especially sphincter paralysis and sensory
loss in extremities. 2 There are significant variations among centers in many aspects of the EP
guidance and applied criteria for dorsal rhizotomies. [13, 24, 26, 27] The aim of this study is to
evaluate the applied techniques of EPM used during SDR for treating spasticity in Egyptian
children with cerebral palsy and its rule for preservation of sphincters’ innervation.
2

Methods:
Twenty-two children (fourteen boys and eight girls) with a diagnosis of spastic cerebral palsy
underwent selective dorsal rhizotomies (SDR), using intraoperative EMG recording, between
May 2006 and September 2009. All patients were presented to neurology or neurosurgery
outpatient clinic at Ain Shams University Hospitals with intractable spasticity (showing
progressively decreasing or even no response to medical and/or physical therapy).
The patients' ages at surgery ranged from 4 to 15 years, with a median age of 8.3 years.
Twelve of them were diplegic (54%), 8 of the diplegic children (36%) were able to control
bowel at time of surgery. None of the quadriplegic children (46%) was able to control bowel
at time of surgery. Informed consents were taken from patients' parents for surgery and
research. The inclusion criteria were significant lower extremity spasticity which interfered
with passive movement, positioning and care and was intractable to other treatment
modalities. Children with severe fixed contractures at multiple lower limb joints, dyskinesia,
truncal hypotonia and radiological (MRI) abnormality of the basal ganglia were excluded and
they did not undergo the procedure.
Children underwent full preoperative clinical assessment including history taking (especially
perinatal and developmental history and bowel control); general and neurological
examination; and assessment of power of quadriceps (using Medical Research Council Scale
(MRCS) 30 ); range of movement (ROM) of hip abduction (using manual goniometer 11 ); and
tone grading of adductor muscles (using the modified Ashworth scale (MAS) 1 ).
Conventional electromyography for preoperative evaluation of pelvic muscles, anal and
urethral sphincters. Routine laboratory investigations and MRI brain were conducted for all
children.
3

Operative Technique:
Surgery was performed under endotracheal anaesthesia without the use of long-acting muscle
relaxants. Levels of anaesthetic agent were adjusted as needed to obtain good reflex
recording. The patient was positioned prone and the cauda equina was exposed through a L1-
S2 laminotomy/laminectomy, and the sacral roots were identified. The dorsal roots were then
separated from the ventral ones. Rootlets associated with abnormal responses to electrical
stimulation were divided. A very conservative approach to the S2 level was taken. After
identifying the SI and S2 levels and confirming the presence of anal sphincter response,
lumbar roots were mapped. During stimulation, the surgeon held the root or rootlet clear off
the cerebrospinal fluid (CSF). The hooks were separated by 10-20 mm and each root or
rootlet was held without tension.
Intraoperative EMG recording:
EMG recording and stimulation of posterior roots and rootlets were performed, in all children,
using a Myto-II, 4 channel system, EBNeuro, Florence-Italy (2004). Two insulated (Teflon
coated) electrodes were used for the stimulation of rootlets. Pairs of needle electrodes were
placed in 5 muscle groups of each lower extremity: adductor longus, quadriceps (vastus
lateralis), hamstrings, tibialis anterior, and gastrocnemius. Needles were spaced 3-5 cm apart
depending on the size of the patient. Two additional electrodes were placed in the external
anal sphincter. A ground plate was placed on the calf of one limb. As EMG apparatus is a
four-channel system, connected electrodes for different muscles were changed during the
stimulation of different roots.
The interpretation of EMG recording and observation of motor responses were made by the
neurologist. The stimulus intensity varied from 2 to 200 mV, stimulation duration of 1
milisecond, and tetanic stimulation of 50 Hz frequency and pulse duration of one millisecond
was then applied for one second. Different parameters were used in previous studies, and the
parameters used in our study were similar to Newberg et al 16 , Steinbok et al 23 and Staudt et
al. 27 Although we used this range of stimulation strength as Newberg et al 16 , also, response
threshold was low, and rootlet separation was applied by 1–2 cm to avoid stimulation of other
roots. Preservation of sacral roots S2,3,4 is essential is essential for protecting bladder and
sexual functions 16 , so monitoring of S2 and registration of its responses was not done
routinely as the procedure of stimulation was ended by S1 root identification, stimulation and
recording process.
As long as S1 roots were identified both anatomically and with stimulation and nearly 50 %
of rootlets were severed, so we find no need to perform S1 H-reflex intraoperatively to
confirm S1 rhizotomy. Anterior roots required low amplitude single stimulus to produce a
response, compared with dorsal roots. At each root level, the whole posterior root was first
tested with single stimuli then individual rootlets were separated from each other and tested
by turn. Trains of stimuli were applied at gradually increasing voltages, until a motor
response was obtained. Currently, clinical observation and palpation of muscles contraction
during stimulation were performed. Decisions to cut or spare rootlets were made sequentially
as testing proceeded.
The motor response of each root and rootlet was recorded and assigned a grade of 0, 1 +, 2+,
3 +, or 4+ (table 1; figure 1), as employed by previous studies. [3, 13, 18, 28, 32] The principal
criteria for division of rootlets included spread of response (includes response which occurs in
muscle groups not innervated by tested level or/and responses recorded in contralateral side at
the same tested level) or observed/palpated abnormal limb contractions (i.e. grades as 3+ or
4+). Anal sphincter responses were monitored in all patients.
4

Table 1: Grading of Motor Responses during EPM 18
Grade Motor Response
Grade 0 Unsustained CMAP in any muscle (normal response)
Grade 1+ Sustained CMAP from muscles innervated by the segmental level of the
stimulated dorsal rootlet
Grade 2+ Same as grade 1+ with CMAP in muscles innervated by adjacent segmental
level
Grade 3+ Same as grade 2+ with CMAP in muscles innervated by multiple
ipsilateral segmental levels
Grade 4+ Same as grade 3+ with motor response in the contralateral leg or upper
extremity.
CMAP = compound muscle action potential
The number of rootlets tested and divided at each spinal level was recorded and the average
percentages were calculated by the surgeon based on visual assessment for all patients. The
percentage of S1 roots producing anal sphincter contraction was recorded as well.
Figure 1: EMG record shows continuous response of ipsilateral tibialis anterior, L4 (below); while absence of
contralateral response (above) [grade3+]. Note: The gain (50 uV/division) and sweep speed (10 ms/division) are
the same for all recordings.
5

Statistical analysis:
It is performed by SPSS (Statistical programme of social signs) version 8.0 as follows:
Description of quantitative variables in the form of mean, standard deviation and range;
description of qualitative variables in the form of numbers and percentage; and paired t-test
used to compare change in mean values after six months of the intervention within groups as
regard quantitative variables. Results of comparisons are considered not significant if (p
0.05, significant if (p 0.05), highly significant if (p 0.01) and very highly significant if (p
0.001).
6

Results:
From the twenty-two children, there were 12 patients with diplegia (54%), and 10 patients
with quadriplegia (46 %). In all patients, the underlying etiology was perinatal hypoxia. In
thirteen severely disabled children, the goal of surgery was to facilitate comfort and care, and
in nine children the aim was to improve ambulation.
Mean number of tested rootlets in each level was 5.5 on right side and 6 on left side; mean
number of cut rootlets was 3 on both sides. 52.8% of stimulated rootlets in each stimulated
dorsal root graded as 3+ or 4+ were selected to be sectioned in all children (Fig 2). In 6
children (27%), the S1 dorsal root produced anal sphincter contraction so it was spared. Four
(18%) of those children who had intraoperative anal sphincter response upon stimulation of
either S1 dorsal root were able to control sphincters preoperatively.
In one child, the grade 3+ or 4+ were met in L4 and L5 dorsal roots bilaterally only, while
none of the other stimulated roots had met the criteria. Postoperatively, bowel control is
preserved in all continent 8 children (100%).
Figure 2: Percentage of transected rootlets (grades 3+ and 4+)
Clinical outcome after 6 months of the 8 cases revealed significant increase of ROM of hip
abduction; insignificant decrease of spasticity of adductor muscles; and insignificant
improvement of motor power of quadriceps (Table 2 and Fig. 3). A six-month followup
duration may be short for assessment of motor outcome, but is not for assessment of sphincter
control outcome which is the main point of this work.
Table 2: Mean outcome measurements
Outcome parameter Baseline (preop) 6months
postop
P value Notes
Spasticity of hip adductors 4.13 1.51 0.2 Insignificant
decrease
Range of motion of hip abductor 68.85 95.85 0.03 Significant
muscles (degrees)
increase
Motor power (MRCS) 2.75 3.2 0.32 Insignificant
increase
7

100
90
80
70
60
50
40
30
20
10
0
baseline(preop) 6 mths post op.
Tone of hip adductors
Passive ROM of hip
adductors
Motor power of
quadriceps(MRCS)
Figure 3: Comparison of outcome parameters between preoperative and postoperative assessment at 6 months.
8

Discussion:
The concept of SDR is improving spasticity and range of movement, with preservation of
muscle strength, by identifying components of dorsal roots involved in spasticity on the basis
of intraoperative electrophysiological stimulation. [3, 13, 26 31] Comparable to other studies, a
decrease of spasticity, and increase of ROM, with preservation of power were detected. The
impact of EPM on clinical outcome, a matter of debate, could not be addressed and needs
further comparable research (EP guided SDR versus non EP guided SDR).
Controversy regarding the utility of EP recording has centered around the lack of technical
standardisation [19, 24] ; absence of normal controls 19 ; the inconsistency of motor responses 26 ;
the effect of anaesthetic drugs on spinal reflexes 2 ; time consumption by the procedure [19, 26] ;
and the variability of segmental innervations of lower-extremity muscles [18, 26] . Variation in
EPM techniques during SDR is established in different centers and the need for EPM has
been questioned. [13, 24, 32] To overcome different obstacles facing EMG recording; muscle
relaxants are not used; depth of anaesthesia were minimal during recording; and time
consumption is decreased by time.
The intraoperative EMG monitoring during SDR provides valuable information and help to
neurosurgeons. First, it differentiates ventral roots, which need low amplitude to be
[15, 19, 26]
stimulated, from dorsal roots, hence decreasing its related motor complications.
Second, EP monitoring, beside intraoperative clinical assessment, provide objective way to
determine the percentage of selected rootlets. The alternative way is the random transection
of dorsal roots from L2-S1 according to clinical severity. [ 13, 23, 24, 26] The average percentage
of different groups ranges from 18%-68%, with most centers cutting more than 40%.
[ 15, 16, 24,
28]
A high percentage (64%) is associated with using other criteria for selecting transected
rootlets as tonic contraction of related muscle during stimulation and occurrence of after
discharge. 29 Percentage of transected rootlets in this study (52.8%) is within the reported
[3, 13, 16, 23, 26, 28, 31]
range of the previous studies.
Third, EMG mapping of anal sphincter fibers running in S1 roots enables safe transaction of
S1 rootlets producing optimum functional outcome, without sphincteric dysfunction. Deletis
et al 2 recorded sphincteric EMG response from stimulation of S1 in 8 out of 31 patients (25%)
underwent SDR. Moreover, Ojemann et al 17 detected EMG responses on stimulation of
dorsal roots of L4 and caudally. Similarly, we spared 27% of S1 roots that produced anal
sphincter EMG response on stimulation. This explans the preserved sphincteric control in all
patients in whom either S1 roots contain sphincter related fibers and, in the other hand, no
sphincteric disturbance occur in those in whom S1 stimulated rootles showed no sphincteric
responses and were transected, and these findings are going with Deletis et al 21 and Ojemann
et al 17 findings. The preservation of other sacral roots (S2-4) is essential for protecting
bladder and sexual functions. 16 Lastly, EPM, in SDR and other cauda equina and sacral
surgery, identifies and distinguishes roots from fibrous tissue or filum terminal. 9
9

Conclusion:
The applied EPM procedures during SDR provide an objective way for selecting transected
rootlets and avoiding postoperative complications especially those of sphincteric dysfunction.
We recommend routine use of EPM during SDR especially for those children with
preoperative sphincteric control. Further research on larger numbers of cases and for longer
followup periods is required to determine its impact on clinical outcome.
11

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