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Nutrition in Clinical Practice

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Handgrip Strength and Nutrition Status in Hospitalized Pediatric Patients


Catarina Silva, Teresa F. Amaral, Diana Silva, Bruno M. P. M. Oliveira and Antnio Guerra
Nutr Clin Pract 2014 29: 380 originally published online 4 April 2014
DOI: 10.1177/0884533614528985
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research-article2014

NCPXXX10.1177/0884533614528985Nutrition in Clinical PracticeSilva et al

Clinical Research

Handgrip Strength and Nutrition Status in Hospitalized


Pediatric Patients

Nutrition in Clinical Practice


Volume 29 Number 3
June 2014 380385
2014 American Society
for Parenteral and Enteral Nutrition
DOI: 10.1177/0884533614528985
ncp.sagepub.com
hosted at
online.sagepub.com

Catarina Silva, MSc1; Teresa F. Amaral, PhD1,2; Diana Silva, PhD1,3;


Bruno M. P. M. Oliveira, PhD1; and Antnio Guerra, MD, PhD1,3

Abstract
Background: Handgrip strength (HGS) is a useful indicator of nutrition status in adults, but evidence is lacking in pediatric patients.
The aim of this study was to describe the association between undernutrition and HGS in pediatric patients at hospital admission,
quantifying the modifying effect of disease severity, anthropometrics, and other patient characteristics on HGS. Materials and Methods:
Eighty-nine inpatients aged 6 years consecutively admitted were recruited in a longitudinal study. Nutrition status was evaluated
using body mass index (BMI) z scores, and HGS was evaluated at admission and discharge. Results: In the total sample, 30.3% of
patients were undernourished at admission, and 64% lost HGS during the hospital stay. This study showed that HGS at admission
was independently associated with undernutrition defined by BMI z scores ( = 0.256, P = .037). In this multivariate analysis, sex,
age, height, and BMI z scores explained 67.1% of HGS at hospital admission. Conclusion: Lower HGS may be a potential marker of
undernutrition in hospitalized pediatric patients, although HGS data should be interpreted according to sex, age, and height of the patient.
(Nutr Clin Pract. 2014;29:380-385)

Keywords
hand strength; nutritional status; pediatrics; malnutrition

Pediatric malnutrition (undernutrition) is defined as an imbalance between nutrient requirements and intake that results in
cumulative deficits of energy, protein, or micronutrients that
may negatively affect growth, development, and other relevant
outcomes.1 Based on its etiology, undernutrition is illness
related, nonillness related, or both.2
Disease-related undernutrition is associated with worse clinical outcomes in hospitalized pediatric patients, and a timely
and appropriate nutrition intervention is necessary to avoid
clinical complications.3 Scientific societies consistently recommend a routine nutrition assessment for pediatric patients.4,5 In
the United States, nutrition screening at admission is government mandated and a requirement by The Joint Commission,
which accredits hospitals. There remains considerable controversy regarding the most useful anthropometric measurement,
and weight, height, and body mass index (BMI) have limitations in situations of undernutrition, overweight, or obesity.1,6
Impaired muscle strength is a well-known phenomenon
occurring in illness-related undernutrition.7 Handgrip strength
(HGS) is a component of nutrition assessment in adults and a
relevant marker of functional status with low observer and
intraindividual variability.8 HGS is an useful indicator of both
nutrition deficit and nutrition repletion, before changes in body
composition parameters can be measured.8 Strong associations
between HGS and anthropometric parameters in children have
been reported.9,10 HGS has been proposed as a marker of nutrition status,9 but the use of HGS in pediatric populations is

limited, and more research is required in this age range to confirm this association.1
The aim of this study was to describe the association between
HGS and undernutrition in children and adolescents at hospital
admission, quantifying the modifying effect of disease severity,
anthropometrics, and other patient characteristics on HGS.

Methods
Study Sample
Eighty-nine pediatric patients were recruited in a longitudinal
study, between December 2012 and February 2013, from a
pediatric department of a public hospital in Porto, Portugal
(Hospital de So Joo, EPE). Admitted children who met
inclusion criteria were recruited. Inclusion criteria were age 6
From 1Faculty of Nutrition and Food Sciences, University of Porto, Porto,
Portugal; 2UISPA-IDMEC, Faculty of Engineering, University of Porto,
Porto, Portugal; and 3Faculty of Medicine, University of Porto / Pediatric
Service of So Joo Hospital, Porto, Portugal.
Financial disclosure: None declared.
This article originally appeared online on April 4, 2014.
Corresponding Author:
Teresa F. Amaral, Faculty of Nutrition and Food Sciences, University of
Porto, Portugal, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal.
Email: amaral.tf@gmail.com

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381

years, ability to perform HGS, and informed consent from


patients and caregivers. Exclusion criteria were the existence
of upper limb deformities, osteoarticular and neurological diseases, pain, sedation, and comatose status.

Data Collection and Variable Definition


Information regarding sex, age, hospital admission and discharge date, and diagnosis on admission was obtained from
the clinical files. Two age groups were defined based on the
median age of the entire sample, the first with children aged
614 years and the second with children aged 1518 years.
Patients were grouped according to the following main diagnosis classes: oncological, 18% (n = 16); surgical, 15.7%
(n=14); orthopedics, 14.6% (n = 13); respiratory, 10.1%
(n=9); gastrointestinal, 8% (n = 7); cardiovascular, 6.7%
(n=6); endocrine, 6.7% (n = 6); infectious, 5.6% (n = 5);
neurological, 5.6% (n = 5); hematological, 4.5% (n = 4); and
nephrological, 4.5% (n = 4).
The severity of disease was defined as follows: mild (score
1)the patient is weak but out of bed regularly; moderate
(score 2)a patient is confined to bed due to illness; and
severe (score 3)the patient is confined to bed due to severe
disease.5 Physical exercise was reported by their parents or
caregivers. Patients were grouped into 4 classes according to
frequency of physical exercise. The first class included patients
who exercised >5 d/wk, the second class exercised 45 d/wk,
the third class exercised 23 d/wk, and the fourth class exercised <2 d/wk.
Anthropometric data were collected by standard procedures
in the first 24 hours of admission.11 Patients were weighed
wearing light clothes using a mechanical scale to the nearest
0.1 kg. Height was measured with a fixed tape to the nearest
0.1 cm. The width and length of the hand were measured using
a digital caliper with 0.1-mm resolution.
Nutrition status was evaluated using BMI z score values.
BMI z scores were obtained by World Health Organization
(WHO) Anthro software (version 3.2.2, January 2011), based
on reference growth curves of the WHO.12 BMI z score
values; BMI z score values < 3 reflected severe undernutrition; 3 to < 2, moderate undernutrition; 2 to < 1, mild
undernutrition; 1 to 1, normal nutrition; >1 to 2, overweight;
and >2, obesity.13 Patients with severe, moderate, or mild
undernutrition were grouped in a single class of undernutrition, and patients who were overweight or obese were
grouped in another single class. Nutrition status was therefore classified according to 3 classes of BMI z scores: undernutrition, normal weight, and overweight/obesity.
HGS was evaluated during admission and discharge,
according to American Society of Hand Therapists procedures, using a calibrated Jamar Hydraulic Hand Dynamometer
(Sammons Preston Rolyan, Bolingbrook, IL, United
States).14,15 Due to its ergonomic features, it was possible to
adjust the dynamometer to the size of the childs hand.

Patients were sitting in a chair or bedridden, with the arm by


the side of the body and the forearm stretched to 90, with
elbows unsupported. The maximal value of 3 consecutive
measurements, in the nondominant arm, was registered in
KgF units. Brief pauses were taken between measurements.
HGS loss percentage during hospitalization was calculated
as follows: % HGS loss = [(HGS at admission HGS at discharge) / HGS at admission] 100. All procedures were performed by the same previously trained nutritionist.
Length of stay (LOS) was calculated as the difference
between the day of admission and the day of hospital discharge. The median of the entire sample distribution was used
to establish the cutoff for LOS. An LOS 6 days was considered a long LOS.

Ethics
The study was designed and conducted in accordance with
the Declaration of Helsinki16 and was approved by the institutional board and ethics committee of the hospital. Patients
and their caregivers were advised about the aims and procedures of the study, as well as their right of refusal. An
informed consent by patients and by their parents or caregivers was obtained. Pediatric patients identified as nutritionally at risk were referred to their doctors and clinical
nutritionists.

Statistical Analysis
Frequencies, means, standard deviation (SD), medians, and
interquartile range (IQR) were calculated.
Frequencies were compared using the 2 test. The variables
normal distribution was examined with the KolmogorovSmirnov test. Means and SD values were compared with the
Student t test or 1-way analysis of variance for normally distributed data. Medians and IQR values were compared with the
Mann-Whitney U test for nonnormal distributed data. Analysis
of sample characteristics was stratified by age range and sex.
Analysis of HGS at admission according to other variables was
stratified by age.
The Spearman test was used to evaluate the variables correlations, and this analysis was stratified by age. A multivariate
linear regression was used to identify significant associations
between HGS and other studied variables.
Significant results were considered when P < .05. All analyses were carried out using SPSS version 20.0 (SPSS, Inc, an
IBM Company, Chicago, IL).

Results
Baseline Data
The baseline characteristics of our sample are summarized in
Table 1. The HGS measurement was feasible in all participants,

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Nutrition in Clinical Practice 29(3)

Table 1. Sample Characteristics According to Age Range and Sex.


614 years
Characteristic
Physical activity, No. (%)
>5 d/wk
45 d/wk
23 d/wk
<2 d/wk
Weight, mean (SD), kg
Height, mean (SD), m
BMI z score classes, No. (%)
Undernutrition
Normal weight
Overweight/obesity
Hand length, mean (SD), mm
Hand width, mean (SD), mm
Handgrip strength loss, No. (%)
Severity of disease, No. (%)
Mild
Moderate
Severe
Length of stay, median (IQR), d

1518 years

Female (n = 20) Male (n = 26)


0
7 (35.0)
4 (20.0)
9 (45.0)
31.2 (13.5)
1.34 (0.12)

2 (7.7)
11 (42.3)
8 (30.8)
5 (19.2)
35.4 (15.5)
1.43 (0.15)

9 (45.0)
5 (25.0)
6 (30.0)
110.8 (42.3)
46.2 (14.2)
11 (55.0)

10 (38.5)
12 (46.1)
4 (15.4)
131.9 (40.4)
55.7 (14.7)
14 (53.8)

3 (15.0)
7 (35.0)
10 (50.0)
11.40 (11.9)

10 (38.5)
13 (50.0)
3 (11.5)
7.38 (8.79)

P Value

Female (n = 20)

.198

1 (5.0)
2 (10.0)
9 (45.0)
8 (40.0)
61.3 (15.7)
1.63 (0.07)

6 (26.1)
8 (34.8)
4 (17.4)
5 (21.7)
65.2 (16.6)
1.66 (0.09)

.022

.442
.152

3 (15.0)
8 (40.0)
9 (45.0)
166.2 (6.7)
66.6 (8.6)
13 (65.0)

5 (21.7)
8 (34.8)
10 (43.5)
160.8 (5.9)
69.7 (10.1)
19 (82.6)

.842

.254
.283
.187

10 (50.0)
3 (15.0)
7 (35.0)
8.1 (7.72)

7 (30.4)
11 (47.8)
5 (21.7)
7.17 (3.97)

.072

.633

.346
.036
.273

.094
.033
.938
.013

.079

Male (n = 23) P Value

BMI, body mass index; IQR, interquartile range; SD, standard deviation.

and there were no refusals. The age range of the 89 pediatric


patients was 618 years (mean SD age, 13.0 3.7 years).
At hospital admission, 30.3% of patients from the total
sample were identified as being undernourished. In both age
groups, approximately 40% of female patients reported exercising <2 days per week. Significant differences in physical
activity frequency were observed between female and male
patients in the 15- to 18-year age group (Table 1). In each age
group, significant differences in BMI z score classes according
to sex were not observed (Table 1).
In both age groups, male patients had higher HGS than
did female patients. In the 15- to 18-year age group, HGS
values at admission were higher with increased physical
activity frequency (Table 2). Patients in the 6- to 14-year age
group with severe disease had lower HGS values at admission. Although not reaching statistical significance, undernourished patients in the 6- to 14-year age group had lower
HGS mean values at admission than did obese patients
(Table 2), and HGS was also lower in patients with a long
LOS (Table 2).
HGS was strongly associated with age, weight, height, and
hand length and width (Table 3). Significant variables in bivariate analysis were included in the multivariate linear regression
model. BMI z scores and sex, age, and height explained 67.1%
of HGS at hospital admission (Table 4).
Figure 1 displays the representation of variables significantly associated with HGS in the multivariate regression analysis model.

Outcomes
Fifty-seven children (64%) lost HGS during the hospital stay, 8
(9%) increased, and 24 (27%) maintained the same HGS value
during the hospital stay. Among these patients, the percentage
of HGS loss was 33% in female and 21% in male patients. The
median LOS was 7 days in patients who lost HGS, while it was
4 days in patients who did not lose HGS (P = .006). No significant differences were found in severity of disease scores at
admission and at the end of hospitalization between patients
who lost HGS and those who did not (data not shown).

Discussion
Disease-related undernutrition may be attributed to nutrient loss,
increased energy expenditure, decreased nutrient intake, or
altered nutrient utilization.1 Several studies reported a prevalence of undernutrition between 6% and 51%,17,18 and present
results are in line with previous research, showing around one
third (30.3%) of undernourished patients. In hospitalized children, this is probably an underrecognized condition.1,17,18 Lack
of uniform definitions, heterogeneous nutrition screening practices, and failure to prioritize nutrition as part of patient care are
some of the factors responsible for underrecognition of the prevalence of undernutrition and its impact on clinical outcomes.1
This study importantly showed that HGS at admission was
associated with undernutrition (defined by BMI z scores) independent of sex, age, severity of disease, and anthropometric

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383

Table 2. Handgrip Strength at Admission.


Handgrip Strength, mean (SD), kgF
Characteristic

614 years
1518 years
(n = 46)
P Value
(n = 43) P Value

Sex
Female
6.9 (5.4)
Male
12.2 (7.7)
Physical activity, d/wk
>5
14.0 (8.5)
45
10.0 (6.8)
23
13.0 (7.4)
<2
6.4 (6.1)
BMI z score classes
Undernutrition
8.6 (7.7)
Normal weight
9.2 (6.0)
Overweight/
13.4 (7.2)
obesity
Severity of disease
Mild
11.7 (5.4)
Moderate
11.4 (8.3)
Severe
5.7 (5.0)
Length of stay, d
<6
11.5 (6.3)
6
7.6 (7.7)

.011

18.5 (5.1)
23.6 (9.4)

.038

.092

28.9 (11.1)
22.4 (8.4)
19.5 (5.4)
17.9 (5.7)

.019

.202

22.8 (5.0)
19.6 (8.2)
21.9 (9.0)

.602

.039

21.2 (8.8)
22.6 (8.4)
19.7 (6.8)

.666

.065

20.8 (9.2)
21.8 (6.4)

.679

BMI, body mass index; kgF, kilogram force.

Table 3. Correlation Between Handgrip Strength at Admission


and Other Variables.
Handgrip Strength at Admission
Characteristic

614 Years
(n = 46)

1518 Years
(n = 43)

Total
(N = 89)

Agea
Physical activityb
Weighta
Heighta
BMI z scoresa
Hand lengtha
Hand widtha
Disease severityb
Length of staya

0.724**
0.221*
0.772**
0.689**
0.488**
0.596**
0.409**
0.344*
0.298*

0.325*
0.359*
0.125
0.443**
0.017
0.298
0.438**
0.049
0.029

0.744**
0.221*
0.698**
0.751**
0.384**
0.654**
0.608**
0.191
0.107

BMI, body mass index.


a
Continuous variables.
b
Categorical variables.
*P < .05. **P < .01.

characteristics (weight, height, and hand width and length). To


our knowledge, there are no previous studies to compare these
results.
Undernutrition assessment presupposes accurate measurements of anthropometric variables such as weight and height,
which are plotted on population growth curves against which

Table 4. Linear Model of Multivariate Regression (Dependent


Variable: Handgrip Strength at Admission).
Model
Age
Sex
Disease severity
BMI z score
Weight
Height
Hand length
Hand width

0.512
0.177
0.039
0.256
0.106
0.351
0.193
0.032

P Value

R2

.003
.021
.589
.037
.557
.036
.217
.801

0.671

BMI, body mass index.

an individual child is compared.1,19 However, there remains


considerable controversy regarding the most useful measurement and inconsistency in the anthropometric parameters used
to characterize the individual nutrition state.1 First, BMI is not
the best scale for measuring change in nutrition status in children.6 The calculation of weight and height does not distinguish the proportions of muscle tissue, adiposity, bone, and
water in the body. Second, acute illness is often associated with
fluid retention and edema that make weight measurements
unreliable. The accuracy of measurements can also be affected
by dressings, tubes, and other equipment required for care.
Critically ill children are often deemed too ill to be moved for
weight measurements.1 Finally, accurate serial weight and
height measurements are challenging to obtain in hospitalized
children. A large proportion of patients do not have these measurements recorded during their stay in the hospital.20,21 As a
result, alternative nutrition status indicators have been proposed for assessing undernutrition, such as HGS.
In the United States, nutrition screening at admission is a
government mandate and a requirement by The Joint
Commission that accredits hospitals. The Academy of Nutrition
and Dietetics and the American Society for Parenteral and
Enteral Nutrition have recently recommended a standardized
set of 6 characteristics for the diagnosis of undernutrition in
adults, including loss of muscle mass and strength, insufficient
energy intake, weight loss, loss of subcutaneous fat, and localized or generalized fluid accumulation.22 Loss of body protein
in undernutrition has negative implications on muscle strength
and functional status.8 HGS is an important indicator of nutrition status because it responds to nutrition deprivation and
repletion.8 In children, the correlation between hand static force
and fat-free mass or arm muscle area is stronger than with direct
muscle size variables or BMI.10 This supports HGS value as
future nutrition status indicator in children.
HGS has several attributes that reinforce its role as a nutrition status indicator in hospitalized children and adolescents.
The handheld dynamometer has the advantages of being noninvasive, quick and easy to use, and portable, and it does not
require skilled technicians. Patients do not need to be weighed,

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Nutrition in Clinical Practice 29(3)

Figure 1. Visual representation of variables significantly associated with handgrip strength (HGS) in the multivariate regression
analysis model. BMI, body mass index; kgF, kilogram force.

and therefore HGS allows the evaluation of children with fluid


retention. In addition, HGS has proved to have a relatively low
observer and intraindividual variability.23,24 Among this sample, it was very well accepted by all participants and a highly
feasible technique.
Among the 6- to 14-year age group, mean HGS values at
admission were lower than those found in patients with a
long LOS, but without reaching statistical significance. LOS
may reflect the prognosis of the patient and has been frequently used as an outcome. Lower HGS at hospital admission was associated with longer hospital stays in previous
studies conducted among adults.25,26 Previous studies conducted among adults also showed that HGS may be an independent predictor of nutrition status and change in nutrition
status.27 In our bivariate analysis, significant differences
were found between patients who lost HGS and those who
did not during the hospital stay. It will be of major relevance

to evaluate how HGS varies during hospitalization with BMI


z score and nutrition support.
This exploratory study, conducted in a sample of pediatric
patients, first allowed confirmation that these children share
the same characteristics associated with HGS already
described among adults in bivariate analyses. Sex and age are
strongly associated with HGS, as is physical activity.28-30
Height has been more consistently linked to HGS than has
weight,28 although anthropometric changes that occur in children with chronic undernutrition may be followed by
decreased height velocity.1 The size of the hand was also
strongly associated with HGS in children, as previously
reported in adults.30
Children included in this study come from a consecutive
sample recruited in a university hospital pediatric department,
ensuring a wide spectrum of patients and relevant pathologies,
which strengthens the external validity of the study results.

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385

Some limitations should also be discussed. This study has a


small sample size, which does not allow a stratified multivariate analysis according to age groups, but was enough to identify significant associations. Another limitation was the fact
that HGS reference values are not known for children. In this
study, the sample consisted of hospitalized children, and therefore HGS values were considerably lower for both sexes compared with a previous study conducted among healthy
Portuguese children and adolescents9; HGS mean values of the
6- to 14-year age group of the present study vs the 11- to
14-year age group from Carreira et al9 were as follows: female,
6.9 vs 25.3 KgF; male, 12.2 vs 26.9 KgF. HGS cutoffs for children to define undernutrition should be studied in future
research and defined according to age, sex, and height. Finally,
we had information about percentage of HGS loss during the
hospital stay, but we did not collect information about nutrition
support provided, and this will probably be a confounding factor of HGS evolution during the hospital stay. Although a multivariate analysis was conducted, the possibility of not having
fully accounted for potential confounders, such as illness
severity and children cooperation, cannot be ruled out. As childrens collaboration can vary with age, further investigation
conducted with larger samples within more homogeneous children groups would overcome these weaknesses.
In conclusion, HGS at admission was associated with undernutrition defined by BMI z scores in hospitalized children and
adolescents independently of sex, age, disease severity, and
anthropometric characteristics. Lower HGS is a potential
marker of undernutrition in children, although it should be
interpreted according to sex, age, and height of the patient.

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