lower extremity sensory function in children with cerebral palsy

8
Lower extremity sensory function in children with cerebral palsy JOHN F. MCLAUGHLIN 1 , STEVEN D. FELIX 2 , SOGOL NOWBAR 3 , ANNE FERREL 1 , KRISTIE BJORNSON 1 & ROSS M. HAYS 1 1 University of Washington, Washington, USA, 2 Carillon Neurodevelopmental Clinic, Roanoke, VA, USA, 3 Idaho Pulmonary Associates, Boise, ID, USA Abstract Objectives: (1) To determine the feasibility of qualitative sensory testing in the lower extremities (LE) of children with cerebral palsy (CP), especially spastic diplegia. (2) To determine if there is a detectable difference in qualitative LE sensory function in children with CP compared to typical children. (3) To determine if dorsal rhizotomy results in detectable changes in LE sensory function in children with spastic diplegia. Design: Objectives 1 and 2: Prospective observational cohort study. Objective 3: Add-on to prospective interventional studies. Setting: Regional tertiary children’s hospital. Participants: Objectives 1 and 2: 62 children with CP and 65 typical children between 3–18 years of age. Objective 3: 34 children with spastic diplegia. Interventions: Objectives 1 and 2: None. Objective 3: Dorsal rhizotomy. Main outcome measures: Pain, light touch, direction of scratch, vibration, toe position and knee position using standard qualitative techniques. Results: Objective 1: 32 (52%) children with CP and 55 (85%) typical children completed all items ( p ¼ 0.09). Objective 2: Summary scores for separate LE sensory modalities were lower in children with CP for direction of scratch ( p < 0.001), toe position ( p ¼ 0.01) and vibration sense ( p ¼ 0.01). Objective 3: No changes of LE sensory function. Conclusions: LE sensory testing in young children with CP is feasible. There is a qualitative sensory deficit in this sample of children with CP and specifically in children with spastic diplegia that is traditionally associated with dorsal column sensory modalities. A conservative dorsal rhizotomy does not produce a measurable change in LE sensory function in this sample of children with spastic diplegia. Key words: Cerebral palsy, spastic diplegia, rhizotomy, sensation disorders, children. Introduction Cerebral palsy (CP) is a motor disability due to brain injury or maldevelopment occurring in the pre-natal, perinatal or post-natal periods [1]. In spite of advances in perinatal care, the incidence of CP has not decreased. The prevalence of children with impairments secondary to CP remains constant. The traditional emphasis on the motor component may result in neglect of any coexisting sensory impair- ment, especially in the lower extremities. Sensory examinations are often excluded in clinical practice to save time. It is unlikely that brain and concomitant spinal cord injuries, such as are found in some cases of CP [2,3], are solely limited to the motor cortex and/or the motor portion of the spinal cord. Testing with somatosensory evoked potential (SEP) methodology has demonstrated abnormalities in cortical SEP responses to stimulation of the lower extremities of children with spastic diplegia [4]. Damage to central sensory pathways detected with diffusion tensor imaging has recently been reported in two children with spastic diplegia [5]. Normal sensory function is a pre-requisite for unimpeded motor performance. Sensory deficits may contribute to or be responsible for some aspects of motor dysfunction. If sensory function is compromised in children with CP, treatment programmes designed to address such deficits need to be incorporated in the man- agement programme. Researchers in the 1950s and 1960s first documented that up to 70% of Correspondence: John F. McLaughlin, MD, Children’s Hospital and Regional Medical Center, 4800 Sandpoint Way NE, M2-8, PO Box 5371, Seattle, WA 98105-0371, USA. Tel: 206-987-2204. Fax: 206-987-3824. E-mail: [email protected] Received for publication 12 December 2003. Accepted 1 March 2004. Pediatric Rehabilitation, January 2005; 8(1): 45–52 ISSN 1363–8491 print/ISSN 1464–5270 online 45–52 ß 2005 Taylor & Francis Group Ltd DOI: 10.1080/13638490400011181 Dev Neurorehabil Downloaded from informahealthcare.com by University of Alberta on 10/25/14 For personal use only.

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Page 1: Lower extremity sensory function in children with cerebral palsy

Lower extremity sensory function in children with cerebral palsy

JOHN F. MCLAUGHLIN1, STEVEN D. FELIX2, SOGOL NOWBAR3, ANNE FERREL1,

KRISTIE BJORNSON1 & ROSS M. HAYS1

1University of Washington, Washington, USA, 2Carillon Neurodevelopmental Clinic, Roanoke, VA, USA,3Idaho Pulmonary Associates, Boise, ID, USA

AbstractObjectives: (1) To determine the feasibility of qualitative sensory testing in the lower extremities (LE) of children withcerebral palsy (CP), especially spastic diplegia. (2) To determine if there is a detectable difference in qualitative LE sensoryfunction in children with CP compared to typical children. (3) To determine if dorsal rhizotomy results in detectable changesin LE sensory function in children with spastic diplegia.Design: Objectives 1 and 2: Prospective observational cohort study. Objective 3: Add-on to prospective interventional studies.Setting: Regional tertiary children’s hospital.Participants: Objectives 1 and 2: 62 children with CP and 65 typical children between 3–18 years of age. Objective 3:34 children with spastic diplegia.Interventions: Objectives 1 and 2: None. Objective 3: Dorsal rhizotomy.Main outcome measures: Pain, light touch, direction of scratch, vibration, toe position and knee position using standardqualitative techniques.Results: Objective 1: 32 (52%) children with CP and 55 (85%) typical children completed all items ( p¼ 0.09). Objective 2:Summary scores for separate LE sensory modalities were lower in children with CP for direction of scratch ( p<0.001), toeposition ( p¼ 0.01) and vibration sense ( p¼ 0.01). Objective 3: No changes of LE sensory function.Conclusions: LE sensory testing in young children with CP is feasible. There is a qualitative sensory deficit in this sample ofchildren with CP and specifically in children with spastic diplegia that is traditionally associated with dorsal column sensorymodalities. A conservative dorsal rhizotomy does not produce a measurable change in LE sensory function in this sample ofchildren with spastic diplegia.

Key words: Cerebral palsy, spastic diplegia, rhizotomy, sensation disorders, children.

Introduction

Cerebral palsy (CP) is a motor disability due to

brain injury or maldevelopment occurring in the

pre-natal, perinatal or post-natal periods [1]. In spite

of advances in perinatal care, the incidence of CP

has not decreased. The prevalence of children with

impairments secondary to CP remains constant. The

traditional emphasis on the motor component may

result in neglect of any coexisting sensory impair-

ment, especially in the lower extremities. Sensory

examinations are often excluded in clinical practice

to save time. It is unlikely that brain and concomitant

spinal cord injuries, such as are found in some

cases of CP [2,3], are solely limited to the motor

cortex and/or the motor portion of the spinal cord.

Testing with somatosensory evoked potential (SEP)

methodology has demonstrated abnormalities in

cortical SEP responses to stimulation of the lower

extremities of children with spastic diplegia [4].

Damage to central sensory pathways detected with

diffusion tensor imaging has recently been reported

in two children with spastic diplegia [5]. Normal

sensory function is a pre-requisite for unimpeded

motor performance. Sensory deficits may contribute

to or be responsible for some aspects of motor

dysfunction.

If sensory function is compromised in children

with CP, treatment programmes designed to address

such deficits need to be incorporated in the man-

agement programme. Researchers in the 1950s

and 1960s first documented that up to 70% of

Correspondence: John F. McLaughlin, MD, Children’s Hospital and Regional Medical Center, 4800 Sandpoint Way NE, M2-8, PO Box 5371,

Seattle, WA 98105-0371, USA. Tel: 206-987-2204. Fax: 206-987-3824. E-mail: [email protected]

Received for publication 12 December 2003. Accepted 1 March 2004.

Pediatric Rehabilitation, January 2005; 8(1): 45–52

ISSN 1363–8491 print/ISSN 1464–5270 online 45–52 � 2005 Taylor & Francis Group Ltd

DOI: 10.1080/13638490400011181

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Page 2: Lower extremity sensory function in children with cerebral palsy

children with spastic hemiplegia have upper extrem-

ity sensory deficits [6–9]. The most commonly

affected sensory modalities are stereognosis, two-

point discrimination and position sense. Recent

studies of upper extremity sensory function in

children with hemiplegic CP have confirmed the

common presence of deficits in stereognosis and

two-point discrimination [10–13].

Researchers recognize that sensory stimuli influ-

ence motor acts [14]. Umansky [15] hypothesized

that, in the presence of decreased/absent afferent

input to the brain, motor learning and functional

body image formation may not develop completely.

As a result, those with sensory deficits will fail to

incorporate the involved body part into a functional

body image, resulting in limited use of that body

part. This hypothesis is supported by studies in

both animals and humans with congenital or acquired

sensory deficits, in which failure to use the deaf-

ferented limb, in time, results in a learned disuse

phenomenon which brings about a greater deficit of

motor capability in the affected limb [16–18].

Active movement is thought to be required for

creating sensory experiences from which adequate

sensory function and mature motor activities evolve

[19]. Umansky [15] further suggests that motor

development should not be regarded as solely

dependent on sensory function, but should be

considered a function of a combined integrative

pathway between sensory input and motor ability.

Unrecognized sensory deficits may explain much

of the variability in performance among children

with apparently similar motor deficits [13,20]. The

success of constraint-induced therapy may be influ-

enced by sensory function, which adds urgency to

accumulating data on sensory function in children

with CP [18].

A review of the literature reveals a large array of

data on quantitative sensory examinations in adults

[21–23]. These techniques do not appear feasible

for use in testing lower extremity function of young

children. Only modest amounts of data are available

on qualitative sensory examination in healthy young

children [24,25].

No data could be found regarding clinical exam-

ination of the lower extremity sensory function of

children with spastic diplegia in the literature. Some

children with spastic diplegia have abnormal cortical

SEPs that do not change after dorsal rhizotomy (DR)

in the presence of demonstrable electrophysiologic

changes induced at the spinal cord level consistent

with reduction of spasticity [4]. It is not clear how

SEPs relate to the individual modalities such as

vibration, pain, light touch, etc. that seem to have

functional correlation. A further understanding of

sensory function may be particularly important for

evaluating children with spastic diplegia undergoing

DR because of the potential for iatrogenic sensory

impairment [26,27]. In other research on DR

conducted by the team, careful sensory examination

was deemed essential [27].

The first aim of this study was to determine

whether it is feasible to perform qualitative LE

sensory examination in young children with and

without CP. The second aim of this study was to

determine whether there was a detectable difference

in qualitative LE sensory function between samples

of children with and without CP. Qualitative sensory

examination using techniques familiar to clinicians

who examine children was chosen in this study

because it is felt that quantitative or more elaborate

qualitative testing would be difficult for younger

children and impractical in clinical settings. In a

second study reported here, the aim was to use

the same qualitative LE sensory testing battery to

examine children with spastic diplegia before and

after DR to identify sensory changes induced by the

surgical procedure.

Methods

Sensory testing methods

The sensory examination consisted of light touch,

pain sensation, position sense, vibration sense

and direction of scratch. These tests were selected

because they had face validity for use with young

children. Reports supporting the validity and reli-

ability of knee position and direction of scratch

were identified in the literature (see below). The

other tests are familiar to clinicians who frequently

examine young children, cover the primary sensory

modalities and are described in most standard

textbooks, but validity and reliability data were not

found. Before each individual test, a description

of the test along with a practice run was performed.

The focus was on the sensory function in the lower

extremities. A forearm site was included for light

touch, pinprick and direction of scratch to facilitate

making a judgement if the child understood these

tasks. All tests were performed bilaterally and

repeated three times at each of the sites tested. The

children were tested in a sitting position and their

vision was obstructed either by having the child

close his/her eyes or by having the parent/guardian

obstruct the child’s view with a blind. All examina-

tions were performed by examiners who were not

blinded to the children’s clinical status.

Light touch was tested by stroking the child with a

cotton ball on the dorsal forearm (C7–8), mid-thigh

(L2–3), mid-shin (L3–4) and mid-dorsum of the foot

(L4–S1). These sites were chosen to represent major

sensory dermatomes with a minimum of difficulty

and time. The child was asked to say ‘yes’ when the

46 J. F. McLaughlin et al.

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Page 3: Lower extremity sensory function in children with cerebral palsy

cotton ball was felt. Pain sensation was tested in

the same sites using the sharp and dull ends of

a safety pin. The child was asked to distinguish

between sharp and dull sensations. For both light

touch and pain sensation, control tests in which the

skin was not touched or pricked were administered

to monitor the child’s attention to the task. Position

sense was examined by moving the great toe in an

upward or downward direction. The children were

asked to identify the position of the toe as ‘up’ or

‘down’.

Vibration sense was tested by applying a 128Hz

fork to the medial malleolus, tibial tuberosity and

first metatarsal head. The child was asked to identify

when he/she could no longer detect a vibration. The

trial was classified as a ‘pass’ if the child reported

cessation of the stimulus at or shortly after the

examiner could no longer feel the stimulus.

Direction of scratch was performed as described

by Hankey and Edis [28] using the wooden end

of a cotton applicator. A 2 cm scratch in a randomly

varied upward or downward direction was applied at

the same locations used to test pain and light touch

(see above). If the child was unable to correctly

identify three out of three tries, a 5 cm stimulus was

performed. If the child again was unable to correctly

identify three out of three stimuli then a 10 cm

scratch was performed.

Position sense of the knee was tested using a

previously described technique [29]. The child was

asked to sit with his/her legs hanging freely over the

edge of the table (at 90� of knee flexion). A cuff with

attached straps was placed around the lower leg that

allowed passive elevation of the leg. The leg was

raised to 15, 30 and 45� and returned to its original

position. The child was asked to reproduce the angle

without visual input.

Feasibility/representative sample study

Study design/sample. The study was performed at

a single tertiary care children’s hospital. It was

designed as a prospective cross-sectional observa-

tional study comparing the LE sensory status of

children with CP to a comparison group without

CP. Children selected were between the ages of

3–18 years and able to comprehend and respond

verbally or non-verbally to the techniques used.

Children with a diagnosis of CP were selected from

specialty clinics. Comparison children attended the

general medical clinic and had no previous history

of sensory deficits or a medical condition known to

be associated with sensory deficits. All comparison

children were developing in a typical manner by

parent report. Informed consent was obtained for

enrollment and testing. The institutional review

board at CHRMC approved the study. All testing

in the feasibility and reliability study was carried out

by one of two trained examiners (SF and SN).

Sensory function before and after dorsal rhizotomy

This study was carried out as part of quality

improvement monitoring of the DR procedure.

The same sensory test battery described above was

used except that knee position was not tested. Lower

extremity test results were analysed. The examina-

tions were carried out by two of the authors ( JM &

RH) at baseline and between 12–24 months later in

34 children participating in a randomized clinical

trial (RCT) with institutional review board approval.

The results of the RCT have been published

previously and are not the subject of this report

[30]. Twenty-nine additional children with spastic

diplegia were tested by the authors prior to DR.

Statistical analysis

Each sensory stimulus was repeated three times

at each site to allow for possible distraction or

inadequate stimuli in one of the trials. The number

of accurate and inaccurate responses for each site

tested for a given sensory modality was recorded.

Two or three accurate responses were considered a

pass for a given site. Credit was given for one missed

trial occurring in any order because young children

are easily distractible and the qualitative method-

ology does not assure exactly equal stimuli at each

trial. The Pearson �2 test was used to analyse the

data site-by-site for each specific sensory modality.

If a child could not co-operate, refused or was

physically unable to complete a particular sensory

task, the response was coded as a null data point.

After performing the site-by-site comparison, the

passes and fails were summed for all anatomic sites

for each modality for each child. Null data points

were excluded. With the exception of toe position,

each child was then assigned a pass for each sensory

modality if no more than one anatomic site was

scored as a fail. For toe position, a pass was assigned

only if both sites were passed. The statistical com-

parison between groups was performed for each

sensory modality using the Pearson �2. Because of

the use of multiple �2 tests, the p-values should be

interpreted conservatively. This study has chosen

to consider p-values less than or equal to 0.01 as

statistically significant.

Post-hoc analyses

Delayed cognition. The impact of delayed cognition

on sensory function was evaluated in two ways using

the data from the feasibility/representative sample

study. The presence of delayed cognition in the

Sensory function in cerebral palsy 47

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Page 4: Lower extremity sensory function in children with cerebral palsy

group of children with cerebral palsy was determined

by parent report supplemented by chart review

and clinical impression independent of the sensory

examination procedure. For the purposes of this

report, ‘delayed cognition’ includes mental retarda-

tion, learning disability and developmental delay.

Typical cognitive development was a selection

criterion for the comparison group and was also

determined by parental report supplemented by

chart review. Within the group of children with CP,

sensory function was compared between children

with and without delayed cognition. LE sensory

function of children with CP and typical cognitive

development was compared to the children with

typical development. The comparison was done for

the sensory modality performance as described in the

statistical analysis section above.

Spastic diplegia. To assemble a larger sample of

children with spastic diplegia, the sensory function

data for all 34 children in the feasibility/representa-

tive sample with the diagnosis of spastic diplegia,

34 children in the DR randomized clinical trial at

baseline and an additional 29 children with spastic

diplegia who were evaluated for DR were pooled and

analysed by sensory modality as described in the

statistical analysis section above. This pooled sample

contains a total of 97 children aged 3–18 years. The

definition of spastic diplegia for all children in this

pooled sample is that of Hagberg et al. [31] and

excludes children with detectable dystonia or ataxia.

Results

Feasibility/representative sample study

Clinical status and demographics. Seventy-five

children with CP and 75 comparison children were

approached for enrollment during scheduled clinic

visits. Thirteen of the children with CP and 10

comparison children declined participation due

to prior commitments or time limitation. Sixty-

two children with CP and 65 comparison children

completed the study. Forty-six children with CP

had typical cognitive development and 16 had some

degree of delayed cognition. The types of CP include

34 children with spastic diplegia, 14 children with

spastic quadriplegia, six with left hemiplegia, four

with right hemiplegia, three with athetoid quadriple-

gia and one with hypotonic CP. Definition of the

type of CP was made by direct examination and used

the taxonomy of Hagberg et al. [31]. The average age

of the children with CP was 9.1 years (SD 4.0), vs

7.8 years (SD 3.85) for the comparison children

( p¼ 0.06). There were 38 boys and 24 girls in the

CP group and 37 boys and 28 girls in the comparison

group.

Feasibility/reliability of lower extremity

sensory examination

. CP Group: Thirty-two (52%) of the children

with CP were able to successfully complete the

LE sensory examination with the youngest child

being 5 years of age. Of the remaining 30 children,

10 were physically unable to perform the knee

position exam secondary to contractures. Comple-

tion of all sensory items in the children with CP

was not achieved in any age group (Table I).

. Comparison Group: The youngest child to suc-

cessfully complete the sensory examination was

4 years 1 month. Fifty-five children (85%) in this

group were able to successfully complete the

sensory examination. The remaining 10 children

either refused a particular test or could not

co-operate with the exam. The most commonly

refused items of the exam included direction of

scratch or pinprick. Lack of co-operation appeared

to be mainly due to distractibility. All children

greater than 5 years of age passed all items on the

sensory examination (Table I). There is a trend

favouring more complete testing in the comparison

group that is not statistically significant ( p¼ 0.09).

Sensory function by modality. Toe position ( p¼ 0.01),

direction of scratch ( p<0.001) and vibration sense

( p¼ 0.01) were failed by more children with CP

than the comparison children (Table II). Pinprick

Table II. Sensory testing by modality: children with cerebral palsy

and comparison children who correctly identified sensory stimuli.

Modality

Cerebral

palsy* (%)

Comparison*

(%) �2 p

Light touch 39/45 (87) 62/65 (95) 2.7 0.16

Pinprick 36/47 (77) 57/61 (93) 3.9 0.02

Toe position 32/41 (78) 60/63 (95) 7.2 0.01

Vibration sense 31/46 (67) 55/62 (89) 7.4 0.01

Direction of scratch 15/45 (33) 47/63 (75) 18.3 <0.001

Knee position 19/28 (68) 44/56 (79) 1.14 0.3

*Numerator¼number of children who correctly identified thestimuli; Denominator¼number of children who cooperated forthe test procedure (see text). Total n¼62 for the cerebral palsygroup and n¼65 for the comparison group.

Table I. Children with cerebral palsy and comparison children

who could be successfully tested for sensory function by age.

Age (years) Cerebral palsy* (%) Comparison* (%)

3–5 1/12 (8) 10/20 (50)

6–8 9/17 (53) 16/16 (100)

9–11 8/12 (67) 11/11 (100)

12–14 7/10 (70) 13/13 (100)

15–18 7/11 (64) 5/5 (100)

Total 32/62 (52) 55/65 (85)

* Numerator¼number of children who understood andco-operated with the test battery; Denominator¼ total numberof children in age group in the study (see text).

48 J. F. McLaughlin et al.

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Page 5: Lower extremity sensory function in children with cerebral palsy

approached significance ( p¼ 0.02). Light touch

( p¼ 0.16) and knee position ( p¼ 0.3) were not

different. Sensory data for each anatomic site did not

reveal any variation by site and are not presented.

Lower extremity sensory function after

dorsal rhizotomy

The children in the dorsal rhizotomy RCT were

mostly young (DR group: 6.1 (SD 3.0) years, range

2.9–14.3 years; PT Only group 6.8 (SD 4.3) years,

range 3.0–17.3 years). As can be seen by inspection

of Table III, fewer of these children were able to

complete the sensory examination. Toe position

was especially difficult. There was no evidence of

any loss of sensory function after DR in those who

did complete the task. Given the obvious lack of

change, no statistical analysis was performed.

Post-hoc analyses

Delayed cognition. Delayed cognitive function might

influence performance on this sensory test battery.

Within the CP group, children with delayed cogni-

tion appeared to perform slightly less well on some

modalities, but none reached statistical significance.

Children in the CP group with delayed cognition

were then excluded from the between-group analysis.

Significant differences between children with

CP and the comparison group were still present

for direction of scratch ( p<0.001), toe position

sense ( p¼ 0.01) and vibration sense ( p¼ 0.01). No

difference was noted in knee position ( p¼ 0.18),

pinprick ( p¼ 0.02) and light touch ( p¼ 0.13). Data

not shown.

Spastic diplegia/sensory modality. When all sites were

combined for each sensory modality in the pooled

spastic diplegia sample, pinprick ( p¼ 0.001) and

direction of scratch ( p¼ 0.002) were failed by more

children with spastic diplegia than the comparison

children (Table IV). Toe position ( p¼ 0.05)

approached significance. Light touch ( p¼ 1) and

vibration sense ( p¼ 0.46) were not different.

There is a relatively high rate of inability to

complete the sensory test battery compared with

the feasibility/representative sample data associated

with the inclusion of younger children from the

DR sample.

Discussion

Feasibility/representative sample study

The first goal of this study was to establish whether

qualitative sensory testing is feasible in young

children. The results of the study indicate that

sensory testing is feasible in children as young as

5 years in the CP group and 4 years 1 month in the

comparison group. Some children with CP in every

age group demonstrated difficulties in completing

all test items. Children in the comparison group were

uniformly able to complete the exam after 5 years

of age. No children under 4 years of age were

able to successfully complete the examination in

either group. A number of children with CP with

normal test results were noted to be slower in

responding to the stimuli when compared to the

comparison children and to be less sure of their

responses.

Table III. Lower extremity sensory testing by modality in a randomized trial of dorsal rhizotomy: percentage of children in the surgical and

PT only groups at baseline and after 12 months who correctly identified sensory stimuli.

Baseline** Follow-up (>12 months)**

Modality* DRþPT (n¼19) PT only (n¼15) DRþPT (n¼ 17) PT only (n¼10)

Light touch 16/16 (100%) 14/14 (100%) 10/10 (100%) 8/8 (100%)

Pinprick 12/13 (92%) 11/13 (85%) 9/9 (100%) 7/8 (83%)

Vibration sense 9/11 (82%) 13/13 (100%) 7/8 (88%) 7/7 (100%)

Toe position 3/3 (100%) 5/6 (83%) 9/9 (100%) 5/5 (100%)

Direction of scratch 5/5 (100%) 10/10 (100%) 7/8 (88%) 4/4 (100%)

*Knee position not tested.**Numerator¼number of children who correctly identified the stimuli; Denominator¼number of children who co-operated for the testprocedure (see text).

Table IV. Sensory testing by modality: children with spastic

diplegia and comparison sample of children without CP who

correctly identified sensory stimuli.

Modality

Spastic

diplegia* (%)

Comparison*

(%) �2 p

Light touch 77/82 (94) 62/65 (95) 0.16 1

Pinprick 47/67 (70) 57/61(93) 11.4 0.001

Toe position 38/46 (83) 60/63 (95) 4.67 0.05

Vibration sense 58/69 (84) 55/62 (89) 0.59 0.46

Direction of scratch 28/55 (51) 47/63 (75) 9.7 0.002

*Numerator¼number of children who correctly identifiedthe stimuli; Denominator¼number of children who cooperatedfor the test procedure (see text). Total n¼ 97 for pooled spasticdiplegia group. Total n¼ 65 for the comparison group.

Sensory function in cerebral palsy 49

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Page 6: Lower extremity sensory function in children with cerebral palsy

The second goal of this study was to determine

if there are differences in sensory testing in children

with CP. Past studies have shown that such deficits

exist in the upper extremities of children with

hemiplegia. No studies have focused on lower

extremity sensation or have included a comparison

group. The results indicate that, in this sample, there

are differences in lower extremity sensory function

between children with CP and typical children.

Decreased accuracy among children with CP for toe

position and direction of scratch are most prominent

and may have the greatest clinical importance.

Inspection of the data at individual lower extremity

anatomic sites revealed no localization to specific

dermatomes (data not presented). This leads one to

believe that the deficits are central in origin rather

than due to injury to peripheral nerves or discrete

sensory tracts.

Where are the presumed lesions causing the

sensory deficits? Mediation of the most affected

modalities in this sample (vibration, toe position,

direction of scratch) is traditionally assigned to the

dorsal columns. Lesions of the dorsal columns may

not be sufficient to explain the loss of those sensory

modalities traditionally associated with these tracts.

Wall and Noordenbos [32] described three patients

with defined lesions of the spinal cord and concluded

that patients with dorsal column lesions do not

lose one or more of the classic primary modalities

of sensation. Rather, there is a loss of the ability

to carry out tasks where the individual being

tested must simultaneously analyse spatial and

temporal characteristics of the stimulus. Vierck [33]

further demonstrated that monkeys with cut dorsal

columns could differentiate between stationary and

moving stimuli but were severely impaired in their

ability to detect direction of movement. The deficit

noted in the patients may not be localized to the

dorsal columns or their direct projections in the

brain.

Other authors have found that cerebral lesions

may produce sensory impairments similar to those

described here. Fox and Klemperer [34] described

seven patients with known cerebral lesions that

produced impaired position and vibration sense.

They further described various dysesthesias of

vibration sense in patients with these cerebral lesions.

One of the older patients with mild spastic

diplegia volunteered that vibration sense in the

lower extremities was qualitatively different and less

clear compared to the upper extremities. This may

indicate a sensory lesion that is cerebral in origin.

Knee position was not different between groups.

This may be due to the difficulty both groups had in

understanding and performing the task. In addition,

it was cumbersome to perform and did not seem as

useful as other tests.

Sensory function after dorsal rhizotomy

No loss of lower extremity sensory function was

detected following DR. The improvement noted

(Table III) is most likely attributable to maturation,

since most of the younger children were at least

5 years old at the time of follow-up. The absence of

sensory loss is consistent with the adverse events

questionnaire data reported in the original study

which revealed only transient post-operative changes

that would not be detected by this test battery [30].

The dorsal root tissue transection percentage was

a conservative 34% (range 20–56%) in the RCT. It

was not anticipated that the electrophysiologic

testing procedure to select rootlets for sectioning

would result in a lower percentage of root tissue

sectioning than in other similar studies. A more

aggressive transection rate might lead to detectable

sensory changes. Given the independent evidence

from the adverse event monitoring that there were

no clinically detectable sensory losses associated with

DR, the pre- and post-testing presented here provide

some support for the reliability of the sensory test

battery that was used. On the other hand, one cannot

exclude the possibility that a more sensitive measure

such as SEP testing might have detected differences.

Post-hoc analyses

In this study, delayed cognition did not make a

difference in the ability of children with CP to

correctly identify sensory stimuli. It is important to

keep in mind the fact that children with cognitive

function below that of a typically developing 3 year

old were excluded a priori from the study because

they were unable to comprehend the sensory testing

protocol. Cognitive testing was not performed in this

study, but depended on parental report and existing

data. Parental report is known to be sufficiently

reliable to allow the type of categorical classification

used in this study [35]. These factors preclude

any conclusions regarding the possible association of

increased sensory dysfunction in children with more

severe intellectual impairment.

If the pooled sample of children with spastic

diplegia is representative of the larger population,

the presence of deficits in accurate perception of

pinprick and direction of scratch is common. When

compared to the total sample of children with CP,

the children with spastic diplegia have fewer deficits.

In particular, disturbance of vibration sense does

not appear to be associated with spastic diplegia.

The sample of children with CP other than spastic

diplegia is too small to allow any reliable conclusions

about the possibility of distinct patterns of sensory

deficits by type of spastic CP (e.g. quadriplegia,

hemiplegia).

50 J. F. McLaughlin et al.

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Page 7: Lower extremity sensory function in children with cerebral palsy

Conclusion

Qualitative lower extremity sensory testing is feasible

in typical children at 4 years of age and in some

children with CP as young as 5 years of age. Children

with CP may have qualitative differences in sensory

testing most notably in functions traditionally related

to the dorsal columns. These differences in sensation

appear to be central in origin, consistent with

anatomic localization of the motor impairments in

CP. The data provide no evidence that a conservative

DR procedure is likely to produce a measurable

sensory deficit in children with spastic diplegia.

The data do not reveal any evidence that adaptive

cognitive ability less than age level but above that of a

3-year-old impairs ability to respond to qualitative

sensory testing as described here.

Acknowledgements

Susan Astley PhD provided consultation regarding

statistical questions. The authors thank the children

and families for their participation. The research was

supported in part by a grant from the National

Institute of Neurological Disease and Stroke #RO1-

NS27867 and from the United Cerebral Palsy

Research and Educational Foundation. These data

were presented in part at the Annual Meeting,

American Academy for Cerebral Palsy and

Developmental Medicine, San Antonio, TX, 1998,

USA.

No commercial party having a direct financial

interest in the results of the research supporting this

article has or will confer a benefit on the authors

or on any organization with which the authors are

associated.

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