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of Child Neurology

Predictors of Independent Walking in Children With Spastic Diplegia


Ermellina Fedrizzi, Paola Facchin, Michela Marzaroli, Emanuela Pagliano, Gabriella Botteon, Luciana Percivalle and
Elisa Fazzi
J Child Neurol 2000 15: 228
DOI: 10.1177/088307380001500405

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Original Article

Predictors of Independent Walking


in Children With Spastic Diplegia
Ermellina Fedrizzi, MD; Paola Facchin, MD; Michela Marzaroli, MD; Emanuela Pagliano, MD;
Gabriella Botteon, MD; Luciana Percivalle, PhT; Elisa Fazzi, MD

ABSTRACT

A prospective study was carried out to identify predictors of independent walking in 31 children with either spastic diple-
gia or triplegia, observed from the age of 9 to 18 months (mean, 11months) and followed for a mean period of 30 months
(range, 24 to 36 months). Mean age at most recent examination was 41 months (range, 36 to 54 months). We used an 18-item
scheme to chart the acquisition, from the prone position, of prelocomotor, sitting, and locomotor skills. Examinations
were conducted every 6 months and videotaped according to a standardized procedure. At latest assessment 18 (58%) of

the 31 children had achieved walking, 7 (23%) independently and 11 (35%) with assistance; 13 (42%) did not achieve walk-
ing. Ambulatory status was related to developmental quotient and visual acuity: all the children who became independent
walkers had normal visual acuity and in 86% of cases a normal general development quotient. Moreover, we found a sig-
nificant correlation between the number of gross motor skills achieved and the rate of achievement before 2 years of age
and ambulatory status at 3 to 5 years of age. Ability to put weight on the hands while prone and to roll from supine to prone
position by 18 months of age were significantly related to independent walking, while ability to sit without support was
predictive only at around 24 months of age. ( J Child Neurol 2000;15:228-234).

It is important to be able to predict whether children with rarely achieve ambulation,6 children with spastic diplegia
cerebral palsy will walk in order to plan appropriate ther- eventually achieve ambulation in 86% to 91% of cases,~9
apeutic and rehabilitation goals, and to inform the parents. and a similar percentage of spastic triplegia cases (87%)
Spastic diplegia and triplegia, the clinical forms of cere- acquired walking in the series of Campos da Paz.9
bral palsy related to preterm birth, are increasing in fre- Most studies on predictive factors for walking have
quency in relation to the increase in such births and the been retrospective and involved children with all clinical
decrease in perinatal mortality. 1,2 However, the prognosis of forms of cerebral palsy. Furthermore, no studies have
ambulatory outcome in these conditions is more difficult addressed the relationship between ambulatory status, cog-
than in other forms of cerebral palsy because of the variety nitive development, and visuoperceptual disorders in cere-
of factors that can influence ambulatory status during devel- bral palsy. In a review of the literature spanning the past 50
opment. Thus, while children with spastic hemiplegia almost years, Sala and Grant6 reported that primitive reflexes, pos-
always learn to walk3-5 and those with spastic quadriplegia tural reactions, gross motor skills, and the type of cerebral
palsy seemed to be the main factors in predicting the achieve-
ment of ambulation. More specifically, most studies indicate
that age at the achievement of sitting (defined as the abil-
Received March 1, 1999. Received revised April 5, 1999. Accepted for pub- ity to maintain the sitting position without support) is a
lication April 7, 1999.
predictor of ambulatory status. Thus, in Badell-Ribera’s
From the Department of Developmental Neurology, C. Besta Neurological
Institute (Drs Fedrizzi, Marzaroli, Pagliano, Botteon, and Percivalle), Milan,
prospective study7 of 50 children with spastic diplegia, all
the Child Neuropsychiatry Division of the C. Mondino Neurological Insti- of whom became independent walkers, sitting and crawl-
tute (Dr Fazzi), Pavia, and the Department of Child Epidemiology of the ing were achieved at between 18 and 30 months of age, and
University of Padua (Dr Facchin), Padua, Italy. Watt and coworkers5 reported a positive correlation between
Address correspondence to Dr Ermellina Fedrizzi, Department of Devel-
opmental Neurology, C. Besta Neurological Institute, via Celoria, 11, 20133
sitting by the age of 2 years and walking at 8 years. Campos
Milan, Italy. Tel: 39-022-394295; fax: 39-027-0635350; e-mail: da Paz et all investigated the role of age at attainment of
efedrizzi.besta@interbusiness.it. major motor milestones in 272 children with cerebral palsy

228

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229

and found that achievement of head balance before All the children underwent physiotherapy according to a neu-
9 months, sitting by 24 months, and crawling by 30 months rodevelopmental approach, from the time of diagnosis and during
were predictors of the achievement of ambulation. follow-up, attending the two centers involved in the research pro-
The purpose of this prospective study was first to iden- ject, with a mean frequency of three sessions per week.
tify predictors of independent walking before 2 years of age
in children with spastic diplegia or triplegia using a functional Assessment of Cognitive Development
motor chart that analyzes the developmental uprighting and Visual Function
sequence from prone position and the prelocomotor skills, At 2 years of age cognitive development was assessed as the gen-

and second, to study the relationship between ambulatory eral quotient of the Griffiths Mental Developmental Scale, exclud-
status and other factors, such as cognitive development ing the locomotor subscale. Each child also underwent an
and visual acuity. ophthalmologic evaluation (fundus oculi, ocular motility, refraction)
and visual acuity assessment (Teller acuity cards; normal value,
more than 10th percentile).
PATIENTS AND METHODS
Statistical Analysis
Patients The nonparametric Kruskal-Wallis analysis of variance (ANOVA)
We enrolled patients with spastic diplegia or triplegia presenting was used to determine whether the distribution of the number of
at the Department of Developmental Neurology, C. Besta Neuro- acquired motor functions differed in relation to ambulatory outcome
logical Institute, Milan, or the Child Neuropsychiatry Division of at the most recent examination. Linear, square, and log-linear
the C. Mondino Neurological Institute, Pavia, from 1993 to 1995. regression analyses were carried out to model the rate of acquisi-
Inclusion criteria were (1) clinical diagnosis of spastic diplegia tion of motor functions in relation to age. The best models were
according to Hagberg and colleaguesl° or spastic triplegia accord- analyzed and compared to each other. It was possible to describe
ing to Michaelis et all (2) enrolment before the age of 2 years, and the typologies of functions related to age. With this aim the 18 func-
(3) likelihood of availability for regular follow-up until at least the tions described in the protocol (Table 1) have been grouped into
age of 8 years. Forty-five patients conforming to the inclusion cri- four performance classes plus an outcome class. Each class includes
teria presented over the study period, but only 31 had a follow-up a series of functions related to ability and motor control in increas-
of at least 24 months by December 1997 (mean, 30 months; range, ing steps (Table 2). For each function class the progressive matu-
24 to 36); these 31 form the population of this study. Fifteen were ration achieved at the different control ages by each subject,
boys and 16 were girls. Mean gestational age was 29 weeks (range, grouped according to the outcome, has been described (Table 3).
24 to 38); mean age at recruitment was 11 months (range, 9 to 18). Finally, two series of stepwise logistic analyses were per-
Mean age at most recent examination was 41 months (range, 36 to 54). formed to determine the predictive values of the variables for two
Ultrasonography revealed early brain damage in 27 patients: outcomes (walking or not walking). In the first analysis the vari-
periventricular leukomalacia in 26 cases and intraperiventricular ables initially included were age, general development quotient, gen-
hemorrhage in one. Nineteen of the children had spastic diplegia eral quotient subscale scores, the achievement of uprighting
and 12 had spastic triplegia. sequences from the prone position, prelocomotor skills, sitting
without support, and the first two items of kneeling. In the second
Achievement of Gross Motor Skills logistic analysis, five motor items only were considered (rolling,
The children were examined every 6 months and the development prone weight on hands, crawling, sitting without support, and
of their motor skills was recorded using an 18-item protocol (Table kneeling upright with support), and these were dichotomized in
1), developed and validated in a previous sturdy. 12 The 18 items were terms of achievement before or after 18 months of age (for sitting,
chosen to reflect the development sequence of acquisition of motor before or after 24 months).
skills in the normal child as described by Touwenl° and Hempel and The aim of the logistic analyses was to obtain models that
Touwen.’4 The number of motor skills attained at each examina- allowed us to attribute an a priori probability of walking for each
tion was noted. For analysis, skills were grouped into four func- patient and for each assessment. By attributing a negative prognosis
tional classes (plus outcome class) as shown in Table 2, each class to each case with an a priori probability lower than 0.5 and a pos-
indicating a progressive stage in the overall acquisition of motor itive prognosis for each case with a probability equal to or greater
ability. Within this grouping, the sitting function was divided into than 0.5, it was possible to formulate an a priori prognostic judg-
three levels: level 1, maintaining the sitting position using both arms; ment about the outcome. Comparison between the prognosis pro-
level 2, maintaining the sitting position with one arm free, and level _
duced from these models and the observed outcome allowed
3, maintaining the sitting position without arm support. evaluation of the two models. These performances were described
Each child was assessed at play in a standardized setting. Activ -
in terms of efficiency,sensibility, and specificity of the models. To
ity was recorded with a hand-held video camera over 30 to 60 mint -

evaluate the models’ extendability to new cases, and then to the


utes, include frontal, sagittal anterior, and posterior views, noting~ possibility of using them as a tool of clinical practice, a double val-
the maximum skills attained. Ambulatory status, as determined a1t idation has been carried out. With this aim, 21 new patients, with
the most recent follow-up examination, was classified as follows9 : clinical characteristics (spastic diplegia, recruiting age, and age at
independent ambulation, ambulation only with assistance (sticks ,
the end of follow-up) similar to the patients of the previous study
crutches, or walkers), and ambulation not achieved. were evaluated and a prognosis was assigned based on our mod-

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230

Table 1. Functional Assessment Chart

els by physicians blinded to the instrument we wanted to vali- who achieved autonomous walking had normal visual acu-
date. We therefore calculated the models’ efficiency in the prog- ity, while 46% (6 of 13) of children who did not achieve
nostic classification of new cases. walking had defective visual acuity (Figure 1B).
RESULTS Ambulation in Relation to Achievement
of Early Motor Skills
At latest assessment, 18 (58%) of the 31 children had achieved The relation between acquisition of motor skills and achieve-
walking, 7 (23%) independently and 11 (35%) with assis- ment of walking was analyzed both in terms of the total num-
tance ; the other 13 (42%) did not learn to walk. The age at ber and types of motor skills acquired.
walking was 2 years in 2 cases, 3 years in six cases, 4 years
in seven cases, and 5 years in three cases. Visual function Number of Motor Skills
was severely compromised (less than 10th percentile) in 9 Figure 2 shows the number of motor skills acquired with
children and normal in the remaining 22. Cognitive devel- advancing age for the three outcome groups (independent
opment was assessed (as Griffiths general quotient) in 29 walking, walking with assistance, and no walking). The
of 31 children; in 15 (52%) the general quotient was normal children who did not walk achieved fewer skills than those
(greater than 85), in 6 (21%) it was borderline (71 to 84), and who did. This difference was evident from the earliest
in 8 (28%) it was below normal (less than 70). assessment, and among those who did not walk, the num-
ber of skills learned increased little with the passage of
Ambulation in Relation toCognitive time to reach a plateau of approximately five skills. Among
Development and Visual Impairment the children who achieved walking, those who walked inde-
As shown in Figure lA, most (86%) of the children who pendently achieved more motor skills at a faster rate than
achieved independent walking had normal general quo- those who learned to walk with assistance. However, the dif-
tients on the Griffiths Scale, while in children walking with ference between these two latter groups was rather small
assistance and in those not walking the general quotient was compared to the difference between these groups and the
normal in 55% and in 27% of cases, respectively. All children nonwalkers. Kruskal-Wallis ANOVA showed a significant dif-

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231

Table 2. Functional Classes

ference (P =
.004) between the three outcome groups in The regression models that best approximate the empir-
terms of the number of skills attained. ical data are shown in Table 4. The log linear model provided
Regarding the trend of the number of functions achieved the best overall correlation in all three outcome groups, with
by each subject in the three different groups of autonomous Pearson’s r 0.87 in the independent walking group and
=

walking, walking with assistance, and no walking (Figure r = 0.65 in the other two outcome groups.
3) we found an extremely different trend in subjects who
could not walk compared to those who achieved walking Types of Motor Skills Achieved
(with assistance or independently). Subjects who could not The results obtained with motor skills grouped into four
walk seem to have a very uniform trend: they reached or sur- classes are shown in Table 3. It was found that none of the
passed six items in only two cases. Among those who nonwalking children were able to perform all uprighting
achieve walking, the subjects who walk independently have sequences from a prone position before 18 months of age,
rapid growth in the achievement of gross motor skills within while most (71%) of the children who became independent
the first 24 months. The number of functions achieved tends walkers had completed the sequence (Item 6) by 18 months
to stabilize after 36 months. This trend is apparent in all of age and all of them by 24 months. Among the preloco-
cases. Among the subjects who walk with assistance there motor skills, rolling was acquired by all independent walk-
is the highest variability both in the rate of increasing func- ers by 18 months, while the acquisition of creeping occurs
tions or in the age at which this occurs, and in the total num- later, by 24 months. All except one of the children who
ber of functions achieved. achieved independent walking also achieved level 3 sitting

Table 3. Typology of Motor Skills and Ambulatory Status

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232

Figure1. Ambulatory status in relation to (A) cognitive develop-


ment and (B) visual acuity.

(no arm support) by 24 months; the exceptional case


achieved level 3 sitting by 36 months. Only 55% of the chil-
dren who achieved ambulation with assistance achieved level
3 sitting by age 24 months. Only one of the nonwalking
children had achieved level 3 sitting by the latest follow-up

Figure 3. Trend of the number of functions achieved by each sub-


ject belonging to the three different groups of outcome.

examination. Similarly, all the children who walked inde-


pendently were able to sit on their heels by 30 months,
while only one of the nonwalking children was able to do
this by 30 months.
Therefore, for the uprighting and prelocomotor
sequences from the prone position, 18 months seems to be
a good cut-off age to distinguish potential walkers (inde-

pendent or with assistance) from those who will not walk.


As far as the sitting posture and kneeling are concerned, a
better cut-off age seems to be 24 months. Table 5 shows the
two models obtained by logistic regression analysis that best
predicted walking from the independent variables consid-
Figure 2. Ambulatory status in relation to mean number of motor ered before subjects reach 2 years of age. A model with only
skills
acquisitions and age. two variables (putting weight on hands while prone and over-

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233

Table 4. Trend Analysis of Number of vious studies7.9 have reported that the earlier the achieve-
Functions by Age and Outcome*
ment of milestones, the better the prognosis for ambulation,
either independently or with assistance. We found that the
rate of acquisition of gross motor skills in our diplegic and
triplegic children differed significantly by Kruskal-Wallis
ANOVA, in the three outcome groups. Those who became
independent walkers were characterized, as a group, by
rapid and uniform accumulation of early milestones before
30 months of age (Figure 3A), while those who did not
achieve walking were characterized by very slow acquisi-
tion of these skills between the ages of 18 and 30 months
(Figure 3C). This indicates that the period up to 30 months
is critical for determining ambulatory potential in these
*Regression models analysis.
children, and it is therefore important clinically for defin-
ing, within this age, the walking prognosis and consequently
for planning therapeutic goals. By contrast, in children who
all general quotient) correctly predicted walking status in will achieve walking, the prognosis of the future level of
96% of cases with 93% sensitivity and 100% specificity. A sim- ambulation-independent or with assistance-appeared
ilar result was obtained using a model including rolling more uncertain in patients less than 5 years of age.
before 18 months, putting weight on hands when prone, and In fact, the children who walked with assistance
the oculomotor subscale score of the general development (between 3 and 5 years of age) showed variable trends: we
quotient. This model predicted walking status in 94% of the found children who acquired motor milestones at a rate sim-
children with a sensitivity of 96% and a specificity of 91%. ilar to that of the independent walkers, and children who
showed a rate of acquisition similar to that of the nonam-
DISCUSSION bulatory group. We expect that by the time these children
reach 8 years of age they will have provided more infor-
Many professionals in clinical practice develop their own mation to enable prediction, at between 3 and 5 years, of the
ad hoc criteria for predicting ambulatory status in children type of ambulation they achieve.
with cerebral palsy. These criteria might provide reasonable As also reported in previous studies,5,7,9 we found that
prognostic accuracy, but are not necessarily transferable to the acquisition of specific motor skills at an early age was
other contexts, and their a priori errors cannot be assessed. more predictive of future ambulatory status than the total
It is therefore desirable to develop assessment instruments number of functions acquired at a given age. Thus, acqui-
of known validity, transferability, reliability, and limitation, sition of head and chest raising while prone, with the aid of
in order to provide a uniform approach to prognosis and to arm support (Item 6) and rolling from supine to prone posi-

give the families of these children a more reliable prediction tion (Item 4) before 18 months of age predicted independent
of future development. This was the purpose of the present walking in a high percentage (71% and 100%, respectively)
study. We used a simple 18-item instrument, developed at of our children at between 3 and 5 years of age. Achievement
our center, 12 for the regular assessment of achieved gross of Item 6 before 18 months was therefore an earlier indicator
motor skills in relation to age. More complex instruments, of independent walking than achievement of the sitting
such as the Gross Motor Functional Measure or Gross Motor position, which was acquired by 24 months only in the inde-
Performances Measure 15 give too much information and pendent walkers, and is in accordance with the findings of
are used more as tools for evaluation than for prediction. Campos da Paz and coworkers,9 who reported achieve-
We found a significant correlation between the rate of ment of head balance by 9 months of age as the first mile-
attainment of motor milestones and ambulatory status. Pre- stone prognostic for autonomous walking. This finding is
important for prognosis as well as treatment. Early ability
to hold the head and chest upright against gravity, to put
Table 5. Logistic Models to Predict Walking
weight on the hands with elbows extended, and to rotate the
body from supine to prone are indicative, in diplegic and
triplegic patients, of a variety of motor behavior involving
the trunk and shoulders, which are less compromised than
the pelvis and legs, and provide balance and stability when
shifting weight from one side to the other. These compe-
tencies in uprighting sequences from the prone position
and in rolling are prerequisites for independent sitting and
independent walking: if they are acquired before 18 months
they can be defined as earlier predictors of ambulation than
sitting by 2 years of age. We also found a relationship

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234

between ambulatory status at age 3 to 5 years, general information or as few predictors as possible), the stepwise
development quotient, and visual acuity, in agreement with method has been used. It consists of analyzing one explana-
the findings of Watt et all in their prospective study. The asso- tory variable at a time, selected because it explains most of
ciation between severity of motor involvement, delay in the variability compared to the previous step (or to the use
cognitive development, and visuoperceptual disorders could of the intercept alone if it is the first variable taken into con-
be related to periventricular leukomalacia, the typical lesion sideration). At every new step of the analysis the estimates
of spastic diplegia. Furthermore, the development of motor, of the previous parameters are reassessed and their signif-
cognitive, and visual skills is very closely linked at an early icance is redefined. There can be strengthening, or divi-
age, and the development of behavior reflects the com- sion, of the predicting power among different parameters.
plexity of all these interacting factors. The analyst can define, through a series of evaluations, a cut-
These considerations could explain the results obtained off of significance that allows the inclusion or exclusion of
from our logistic regression analysis, which indicated that the predictors. The analysis will end when none of the new
ability to achieve walking can be predicted before the age variables reaches the cut-off.
of 2 years from two variables only: ability to lift the head and
chest against gravity, using the hands as support, and the ocu- Acknowledgment
lomotor subscale score of the Griffiths Developmental This work was supported by grants from the Fondazione Pierfranco e Luisa Mar-

Scale. Evidently the acquisition of these skills is a very iani, Milan, Italy.

early indicator of the eventual acquisition of other skills,


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