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Identification of Malnutrition is common in children with cerebral palsy (CP)

(Spender et al. 1988; Stallings et al. 1993a, b; Stevenson et al.


1994; Stallings et al. 1995). While clinicians are most aware
malnutrition in of the nutritional risks in severely affected children, those
with less severe CP frequently experience nutritional defi-
children with ciencies. For many years, small size and low weight were
accepted by clinicians as part of the child’s disability. It is now

cerebral palsy: poor clear that poor nutrition is not a necessary or unalterable
component of CP (Patrick et al. 1986, Sanders et al. 1990,
Amundson et al. 1994, Corwin et al. 1996).
performance of The untoward consequences of malnutrition are numer-
ous and clinically significant (Viteri 1991). Malnourished
weight-for-height patients have decreased muscle strength, including respira-
tory musculature, with resultant impaired cough and pre-

centiles disposition to pneumonia (Laaban 1997, Rigaud et al.


1997). Malnutrition results in increased circulation times
and diminished cardiac work capacity, clinically expressed
as a hypocirculatory state and a predisposition to develop
Lisa J Samson-Fang MD, Assistant Professor of Pediatrics, congestive heart failure when placed under cardiorespirato-
University of Utah; ry stress (Viart 1977, 1978). Malnutrition-related distur-
Richard D Stevenson* MD, Associate Professor of Pediatrics, bances in immune function predispose to infection (Santos
Department of Pediatrics, University of Virginia, 2270 Ivy 1994). Cerebral growth, cognitive development, and motor
Road, Charlottesville VA 22903, USA. progress are impaired (Engsner et al. 1974, Grantham-
McGregor et al. 1991, Husaini et al. 1991, Viteri 1991, Smart
*Correspondence to second author at address above. 1993). Undernourished children show lower levels of
E-mail: rds8z@virginia.edu exploratory activity and attachment behavior which may
affect social–emotional development (Graves 1978).
Irritability and decreased activity have been ascribed clini-
cally to undernourished children (Viteri 1991) and docu-
mented in animal models of malnutrition (Graves 1978).
This study aims to evaluate the use of the United States These characteristics may affect a child’s ability to partici-
National Center for Health Statistics (NCHS) weight-for- pate in play, school, or rehabilitation.
height centiles (WHC) in screening children with cerebral Research documenting the effects of malnutrition specific
palsy (CP) for depleted body fat and to identify an alternate to CP has been limited. Linear growth failure, higher surgical
screening method. Growth data from 276 children aged from morbidity, delay in decubitus ulcer healing, and death have
3 to 12 years with CP were analyzed retrospectively. Height or been reported (Patrick et al. 1986, Shapiro et al. 1986, Jevsevar
a proxy for height, mid-upper arm circumference, weight, and and Karlin 1993, Stallings et al. 1993, Amundson et al. 1994,
skinfold thicknesses were recorded. Mid-upper arm fat area Stevenson et al. 1994, Samson-Fang and Stevenson 1998).
was calculated for each participant. The sensitivities and In view of the high prevalence and negative conse-
specificities of WHC and a number of alternative quences, the identification and correction of malnutrition in
anthropometric screening methods for identifying children with CP is paramount. However, assessing the nutri-
participants with severely depleted fat stores were determined. tional status of a child with CP is not straightforward. In the
WHC <10th centile failed to identify 45% of children with general pediatric setting, clinicians frequently use weight-
severely depleted fat stores. Triceps skinfold thickness <10th for-height centiles (WHC), which are graphically represent-
centile identified 96% of malnourished children. WHC ed on the USA’s National Center for Health Statistics (NCHS)
standards lack adequate sensitivity for identification of growth charts (Hamill et al. 1979). The recent development
severely depleted fat stores in children with CP. Use of triceps of equations to estimate height from segmental measures
skinfold thickness, using cut-off value of <10th centile for may lead to increased use of WHC in populations with dis-
age and sex, is recommended to screen for suboptimal fat abilities (Chumlea et al. 1994, Stevenson 1995).
stores in children with CP. WHC norms, based upon typically developing popula-
tions, may not be a valid nutritional indicator in children with
disabilities. Undernourished children with CP have changes
in body composition and proportion compared with normal-
ly developing peers. Alterations include increased total body
water, severely depleted fat stores, minimally depleted mus-
cle stores, severe short stature, and decreased bone density
(Berg and Isaksson 1970, Stallings et al. 1993, Stallings et al.
1995, Wilmshurst et al. 1996, Henderson et al. 1998). These
changes in body composition and proportion may affect the
extent WHC reflects body fat stores. Luckily there are other
anthropometric methods which can be used to assess the
nutritional status of a child with CP. Stallings et al. studied a

162 Developmental Medicine & Child Neurology 2000, 42: 162–168


small group of children with CP and concluded that nutrition- been reported previously (Stevenson et al. 1994). When pos-
al status could be accurately assessed by measuring skinfolds sible, each measure was completed twice and the average
(Stallings et al. 1995). However, in the clinical setting, skin- used for analysis. If scoliosis, joint contractures, or the child’s
folds are rarely measured routinely. If WHC is in the normal level of cooperation precluded accurate measurement, the
range, clinicians often judge the child to be nutritionally measurement was not recorded. Demographic and clinical
sound and do not perform further nutritional assessment. In information was collected by chart review and included type
our tertiary-care setting, it has been noted that many children of CP. Classifications for type of CP were spastic (quadriplegic,
with normal WHC are malnourished when skinfolds are diplegic, and hemiplegic), extrapyramidal, and mixed.
assessed. On several occasions, a primary physician or health For this study, the anthropometric database was retro-
department has discontinued a patient’s nutritional supple- spectively reviewed. Data sets for children with CP aged from
ments because of a normal WHC, despite skinfold thickness 3 to 12 years were included. This age-range restriction was
being in the deficient range. chosen because of the availability of validated equations to
Based upon our clinical experience, we hypothesized that predict height from segmental measures. Data sets with no
NCHS WHC standards perform poorly when used to screen recorded tibia length, mid-upper arm circumference, triceps
for low fat stores in children with CP. The ability of WHC to skinfold, and subscapular skinfold thickness were excluded.
distinguish children with depleted fat stores was evaluated During the 6-year collection period, data sets of 276 children
using an anthropometric database and an anthropometrical- met inclusion criteria. Some children had multiple data sets.
ly derived indicator of body fat stores. Alternative anthropo- In these cases, one set was randomly chosen for analysis. The
metric measures were identified and their ability to identify study population was 48% female, 75% white, 24%
malnutrition in this population was assessed. Recommend- African–American, and 1% Asian–American. Mean age was
ations are made regarding the best method of identifying 6.4 years. The distribution by type of CP was 36% spastic,
malnutrition in children with CP. 29% extrapyramidal, and 35% mixed.

Method INDEPENDENT VARIABLE : BODY FAT ASSESSMENT


An anthropometric database was established at the Kluge Mid-upper arm fat area was decided as our ‘gold standard’
Children’s Rehabilitation Center, Virginia, USA in 1991 for the against which to compare WHC and other anthropometric
purpose of studying growth in children with CP. All children methods for screening for inadequate nutrition.
with CP attending the outpatient clinic or admitted to the in-
patient service at the rehabilitation center were eligible to par- Determination of mid-upper arm fat area
ticipate. At each convenient contact, measurements were Mid-upper arm fat area from triceps skinfold thickness and
recorded including: standing height (Harpenden digital sta- mid-upper arm circumference were calculated using pub-
diometer), recumbent length (digital supine measuring lished equations (Table I). For each participant, mid-upper
table), arm circumference (steel tape measure), tibia length arm fat area was compared with published norms and per-
(Harpenden anthropometer), head circumference (Ross centage of mean for age/sex calculated (Frisancho 1981). For
Inser-TapeTM), knee height (Ross knee height caliper), weight study purposes, low fat area was defined as a mid-upper arm
(digital scale), triceps and subscapular skinfold thickness fat area <5th centile for age and sex.
(Holtain skinfold caliper). Children were weighed in a thin
layer of clothing and dry diaper or underwear. Trained anthro- DEPENDENT VARIABLES
pometrists measured all children using published techniques Weight-for-height centile
(Cameron 1986). All measures were performed on the child’s Using tibia length and published equations (see Table I), height
right side unless the child’s CP was asymmetrical, in which estimates were calculated for each participant (Stevenson
case, measures were taken on the less affected side. Excellent 1995). WHC were calculated using Epi Info (version 6.04b)
intrarater and interrater reliability were established and have software (Dean et al. 1995). Sensitivity and specificity of low

Table I: Anthropometric equations used in data analysis

Mid-upper arm fat and muscle areas (mm2)a


From arm circumference (AC in mm) and triceps skinfold thickness (TSF in mm)
Mid-upper arm area (MAA) = π/4 × d2 where d = AC/π
Mid-upper arm muscle area (MAMA) = [AC – πTSF)2]/4π
Mid-upper arm fat area (MAFA) = MAA – MAMA
Estimation of stature (S) from segmental measures (ages 2 to 12 years)b
Tibia length (TL in cm) S = (3.26 × TL) + 30.8 cm Standard error of estimation = 1.4 cm
Knee height (KH in cm) S = (2.69 × KH) + 24.2 cm Standard error of estimation = 1.1 cm
Alternative screening toolsc (Foman et al. 1982, Hammer et al. 1991)
Body mass index (BMI) = Wt/Ht2 where wt = weight (kg) and ht = height (m)
Lean body mass index (LBMI) = Ht2/Wt where wt = weight (kg) and ht = height (m)
Head circumference to arm circumference ratio (HC/AC) = arm circumference (cm)/head circumference (cm)
a Frisancho 1981.
b Stevenson 1995.
c Frisancho 1981, Hammer et al. 1991, Committee on Nutrition American Academy of Pediatrics 1998.

Malnutrition and Cerebral Palsy Lisa J Samson-Fang and Richard D Stevenson 163
WHC to identify children with low arm fat area were deter- published equation (see Table I). For each child, mid-upper
mined. These calculations were performed using WHC cut-off arm muscle was compared with published normative values
values of <5th and 10th centile and χ2 analysis. and calculated percentage of the median for age/sex and
height age/sex.
Alternative screening methods
A number of anthropometric nutritional indicators used to Results
screen for malnutrition in other settings were identified. The children had a high prevalence of depleted fat stores.
These included arm circumference for age, head circumfer- Mid-upper arm fat area was, overall, 77% of expected for
ence to arm circumference ratio, body mass index age/sex, with 38% of participants having arm fat area <5th
(weight/height2), lean body mass index (height2/weight), tri- centile (Table II).
ceps and subscapular skinfold thickness (Frisancho 1981,
1990; Foman et al. 1982; Hammer et al. 1991; Committee on WEIGHT- FOR- HEIGHT CENTILE
Nutrition American Academy of Pediatrics 1998). Their ability The sensitivities and specificities of WHC and other
to identify malnutrition in our study population was calculat- assessed anthropometric screening tools are presented in
ed by using the same methodology described above for WHC. Table III. Low WHC was a highly specific but not a sensitive
Multiple cut-off values for each parameter were examined. indicator of depleted body fat stores. Using WHC <5th
For several, cut-off values relative to height age (e.g. arm cir- centile as a screening tool, the clinician will miss 57% of
cumference for height age) were used because extreme short children with a low arm fat area. Raising the screening cut-
stature was prevalent. off for WHC to <10th centile improved sensitivity minimal-
ly. Assessment of WHC in participants with different types
ADDITIONAL ANALYSIS of CP revealed poor performance in all groups. To account
To assess the impact of altered body proportion and compo- for possible error introduced when calculating height
sition upon WHC, the height z score and mid-upper arm from tibia length, the analysis was repeated using stature
muscle area were calculated for each study participant. and recumbent length in the subset of participants for
Height z scores were calculated using tibia length: height whom these measures were possible. The analysis was also
estimate and Epi Info (version 6.04b) software (Dean et al. repeated using knee-height: height estimates. Sensitivities
1995). Mid-upper arm muscle area was calculated using a remained poor in all analyses.

Table II: Nutritional status of the study population

Mid-upper arm fat area method (MAFA)


n (%) Sex ratio Mean % of median
(F:M) MAFA for age/sex

All participants 276 132:144 77 ± 45


Participants with MAFA >5%a 171 (62) 78:93 98 ± 46
Participants with MAFA <5%b 105 (38) 54:51 43 ± 10
a Mid-upper arm fat area >5th centile for age and sex.
b Mid-upper arm fat area <5th centile for age and sex.

Table III: Sensitivities and specificities of weight-for-height centile and other assessed screening
tools for identification of participants with mid-upper arm fat area <5th centile for age

Mid-upper arm fat area <5% for age/sex


N Sensitivity Specificity X p value

WHC <5% 272 44 91 45 <0.001


WHC <10% 272 54 88 56 <0.001
Arm circumference <10% for age/sex 276 60 88 74 <0.001
Arm circumference <10% for height age/sex 275 34 99 55 <0.001
Body mass index <10% for age/sex 276 65 82 61 <0.001
Body mass index <10% for height age/sex 275 68 80 62 <0.001
Head circumference/arm circumference <0.38 270 94 43 41 <0.001
Lean body mass/index >600 276 93 42 37 <0.001
Triceps skinfold <5% for age/sex 276 78 95 156 <0.001
Triceps skinfold <10% for age/sex 276 96 82 158 <0.001
Subscapular skinfold <5% for age/sex 276 25 98 34 <0.001
Subscapular skinfold <10% for age/sex 276 49 91 54 <0.001

164 Developmental Medicine & Child Neurology 2000, 42: 162–168


Alternative screening tools been used. Stallings et al.’s study of children with diplegia
Arm circumference, body mass index, and subscapular skin- and hemiplegia showed that 29% of participants had a tri-
fold thickness performed poorly as screening tools. Arm cir- ceps skinfold thickness <15th centile (Stallings et al. 1993a).
cumference to head circumference ratio, lean body mass In this study group, 27% of children with diplegia or hemi-
index, and triceps skinfold thickness were more promising plegia had triceps skinfold <10th centile. This suggests
(see Table IV). The positive predictive values of arm circum- excellent agreement in similar tertiary-care populations.
ference to head circumference ratio and lean body mass
index were low. Clinical use would result in extensive over WHC
referral. The positive predictive value for triceps skinfold WHC was not an adequate screen for malnutrition, for sev-
thickness <10th centile was high. Statistical testing using it eral reasons. First, children with CP often experience mal-
in 100 participants with CP showed that the clinician would nutrition of long duration. WHC is a better indicator of
miss two children with low arm fat area and would over refer acute malnutrition than chronic (Waterlow 1973, Waterlow
only 10 with normal arm fat area. et al. 1977, Radheshyam 1987). Second, there was a high
prevalence of extreme short stature. The NCHS derived the
ALTERED BODY PROPORTIONS WHC from cross-sectional measures on children without
To assess the contribution of altered body proportion and disabilities and with normally distributed stature. These
composition to the poor sensitivity of WHC, the participant’s normative values may not be of use in evaluating children
stature and arm muscle area were assessed. The results are with extremely short stature. Waterlow reviewed the litera-
presented in Table V. Short stature was common. The stature ture and concluded that expected weight for height is rela-
of the children with low fat stores was, on average, 2.8 SDs tively independent of age (Waterlow 1973, Waterlow et al.
below that expected for age. Participants maintained muscle 1977). However, his analysis generally focused upon
areas near the average range, despite extremely depleted fat statures within the broad range of normal measurements
stores. While fat-area percentage of the mean changed only for age. Third, WHC may perform poorly as artificially
slightly when adjusted for the population’s height age, mus- added weight may elevate WHC, thus reducing its ability to
cle-area percentage of the mean was higher when adjusted reflect fat stores. Potential added weights in this study
for height age. included clothing and fecal mass, as severe chronic consti-
pation is common in our clinical setting. The use of tibia
Discussion length to estimate height could result in false elevation of
Malnutrition, defined as low mid-upper arm fat area, was WHC if a child has undergrowth of the lower extremities in
common in our population. The high prevalence likely association with motor impairment. A subset of our study
reflects referral bias. It is difficult to compare prevalence with population was able to have a standing height or recum-
that of prior studies as different methods of assessing and bent length measured. For these children, measured and
defining malnutrition in differing diagnostic subgroups have estimated stature were highly correlated, and WHC based

Table IV: Sensitivities, specificities, and predictive values of the more promising alternative
screening methods

Mid-upper arm fat area <5% for age and sex


Sensitivity Specificity PPV NPV

Head circumference/arm circumference <0.38 94 43 50 93


Lean body mass index >600 93 42 49 91
Triceps skinfold <10% for age/sex 96 82 77 97

PPV, positive predictive value; NPV, negative predictive value.

Table V: Mid-upper arm fat and muscle areas mean percents of the median for age and height age for participants with low and
normal fat areas

Category n (%) Height Mid-upper arm fat area Mid-upper arm muscle area
z score Average % Average % of Average % Average % of
of median median for of median median for
for age height age for age height age

All participants 276 –2.0 ± 1.7 77 ± 45 81 ± 41 106 ± 25 120 ± 24


Participants with normal fat storesa 171 (62) –1.6 ± 1.6 98 ± 46 100 ± 40 114 ± 24 125 ± 24
Participants with low fat storesb 105 (38) –2.8 ± 1.6 43 ± 10 47 ±10 93 ± 20 111 ±21
a Children with mid-upper arm fat area >5th centile for age.
b Children with mid-upper arm fat area <5th centile for age.

Malnutrition and Cerebral Palsy Lisa J Samson-Fang and Richard D Stevenson 165
upon standing height or recumbent length continued to needs to be confirmed in a population-based sample of chil-
perform poorly as a screening tool for depleted fat stores. dren with CP.
The use of WHC to screen for malnutrition in other ter-
tiary referral populations has had limited study. It performed STUDY LIMITATIONS
poorly in a group of pediatric oncology patients and its use The performance of WHC and a number of alternative
has been questioned in children with chronic renal disease anthropometric screening tools were assessed in compari-
(Chantler and Holliday 1973, Wilmet et al. 1995). This study son to determination of body fat stores using calculated mid-
contributes to the growing body of evidence that WHC is an upper arm fat area. Many assumptions are made when
inadequate screen for depleted fat stores in populations like- calculating mid-upper arm fat area; bone area is assumed to
ly to experience chronic malnutrition, extreme short stature, be a constant, the arm to be cylindrical in shape, triceps and
or altered body proportions. Such populations might biceps skinfold thicknesses to be equivalent, the skinfold to
include children with malabsorption, complex congenital be twice the average fat rim diameter, the muscle compart-
heart disease, chronic pulmonary or renal disease, and chil- ment to be cylindrical, the cross-sectional areas of the neuro-
dren with chronic infections (e.g. HIV). Clinicians should vascular tissue and the humerus to be relatively small and
consider other methods of assessing nutritional status in ignored, and bone atrophies in proportion to muscle
these populations. wastage during protein–energy malnutrition. These assump-
tions may not hold true in the child with CP (Van Den Berg-
BODY COMPOSITION ANALYSIS Emons et al. 1998). However, at this time, calculation of
This study suggests that alteration in body composition and mid-upper arm fat area represents the best anthropometric
proportion in children with CP may alter the ability of WHC indicator of body fat stores, with published normative values
to reflect fat stores. This might contribute to its poor perfor- available for comparison. Further study, using a more direct
mance as a nutritional indicator. Our study was not designed method of assessing fat stores, would be ideal but would
specifically to assess body composition. The available data require significant funding for a large population.
did allow for assessment of stature and muscle area. On aver- The assumptions, listed above, also apply to calculation of
age, malnourished children were extremely short. Muscle muscle area. Another assumption is that the muscle compart-
area was maintained near expected values for age and sex ment contains only muscle. In animal models of CP, examina-
despite the extreme fat-store depletion. Combining the tion of muscle by light- and electron-microscopy has
maintained muscle area with extreme short stature, muscle revealed normal structure except reduced fiber length
areas for height age were elevated above expected values. (Tardieu et al. 1977). This suggests that our calculations of
This elevation of muscle area for stature may raise WHC. muscle area were not artificially elevated by fibrotic or fatty
Thus the child with severely depleted fat stores may have a tissue within the muscle compartment. It is important not to
WHC within the normal range based upon the excessive con- equate maintenance of muscle area with maintenance of
tribution of muscle tissue to body composition. The preser- muscle mass. Measurement of muscle area in one extremity
vation of the upper-arm muscle area was not an unexpected may not reflect the muscle mass in the rest of the body.
finding (Stallings et al. 1993, 1995). It may reflect the highly Furthermore, despite similar muscle area, the child with
compensated state malnourished children are able to main- extreme short stature will have less muscle mass than a taller
tain (Viteri 1991). An alternative explanation is that abnormal child with equivalent muscle area. Our methodology did not
tone stimulates and maintains muscle bulk (Smith et al. allow for assessment of total-body muscle mass. Berg and
1991). To explore this theory, muscle area of children with Isaksson, using isotope dilution, found low body cellular
quadriplegic CP to that of children with diplegia or hemiple- mass in children with CP (Berg and Isaksson 1970). This sug-
gia was compared in this study. The muscle areas were not gests that muscle mass is diminished. Further studies using
significantly different among these groups. However, chil- more direct methods to assess muscle area and overall mus-
dren with diplegia and hemiplegia may have had training cle mass are needed to confirm these findings.
effects due to use of assistive devices or excessive use of unin- The ability of WHC and other anthropometric tools to
volved extremities which may also stimulate maintenance of identify malnutrition in this population was studied.
muscle bulk. However, the definition of inadequate nutrition in this study
was a cut-off value for mid-upper arm fat area chosen arbi-
ALTERNATE ANTHROPOMETRIC SCREENING TOOLS trarily and referenced against normative data in children
Among the alternate screening devices, only measurements without disability. Ideally, values used to define malnutri-
of triceps skinfold thickness <10th centile performed to tion should be related to clinical outcomes. Research has
standards thought to be clinically acceptable. While several documented numerous negative physiologic consequences
others had adequate sensitivities, their positive predictive of malnutrition but has focused upon populations dissimi-
values resulted in significant overreferral. The higher sensi- lar to ours. The bulk of study has been in developing
tivity of triceps skinfold thickness over subscapular skinfold nations. Extreme poverty, recurrent and chronic infections,
thickness reflects the high centripetal fat ratio previously and micronutrient deficiencies are confounding variables
noted in malnourished populations including children with usually not present in our patients with CP. Other studies
CP (Spender et al. 1988, Stallings et al. 1993). The cut-off have focused on children with cystic fibrosis; the elderly;
point of triceps skinfold thickness <10th centile performed and adults with trauma, burns, or HIV. Data obtained in
well as a screen for depleted fat stores in our tertiary-care these populations may not be relevant. Future research
referral population. In the primary-care setting, where mal- must examine the health consequences of malnutrition in
nutrition may be less prevalent, the positive predictive value this population. For example, would nutritional improve-
may be lower. The usefulness of this screening method ments result in better cognitive and functional outcomes,

166 Developmental Medicine & Child Neurology 2000, 42: 162–168


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Acknowledgements
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The authors wish to thank L Virgil Cater, Collen Amra, Judy
children and adolescents. American Journal of Disease of
Jacobson, Carla Wheaton, Carmen Booker, and Vivienne Spauls who
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were anthropometrists during the study period. We are grateful to
Henderson RC, Lin PP, Green WB. (1998) Bone-mineral density in
the children and families who consented to measurement. We are
children and adolescents who have spastic cerebral palsy.
also grateful to James A Blackman MD MPH, Professor of Pediatrics at
Journal of Bone and Joint Surgery 77A: 1671–81.
the University of Virginia and Director of Research at the Kluge
Husaini M, Karyadi L, Husaini Y, Karyadi S, Pollitt E. (1991)
Children’s Rehabilitation Center for his guidance. This study was
Developmental effects of short-term supplementary feeding in
supported by Genentech Foundation for Growth and Development,
nutritionally-at-risk Indonesian infants. American Journal of
United Cerebral Palsy Research and Educational Foundation, The
Clinical Nutrition 54: 799–804.
Kluge Research Fund of the University of Virginia, and The Research
Jevsevar DS, Karlin LI. (1993) The relationship between
Development Fund of the University of Virginia.
preoperative nutritional status and complications after operation
for scoliosis in patients who have cerebral palsy. Journal of Bone
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