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ABSTRACT INTRODUCTION
Background: Several malnutrition screening tools have been advo- Malnutrition screening has been advocated as part of patients’
cated for use in pediatric inpatients. standard care (1–3). This recommendation is because malnu-
Objective: We evaluated how 3 popular pediatric nutrition screening trition on admission or deterioration of the nutritional status
tools [i.e., the Pediatric Yorkhill Malnutrition Score (PYMS), the during hospitalization has been associated with a prolonged
Screening Tool for the Assessment of Malnutrition in Pediatrics hospital stay and adverse outcomes (e.g., increased rates of
(STAMP), and the Screening Tool for Risk of Impaired Nutritional complications such as infections), although the causality in these
Status and Growth (STRONGKIDS)] compared with and were related
associations remains to be explored (4–7). The early identifi-
to anthropometric measures, body composition, and clinical variables
cation of nutritional risk followed by an appropriate nutritional
in patients who were admitted to tertiary hospitals across Europe.
management were proposed as part of routine clinical practice
Design: The 3 screening tools were applied in 2567 inpatients at 14
(8). The Guidelines for Nutrition Screening by the European
hospitals across 12 European countries. The classification of pa-
Society for Clinical Nutrition and Metabolism provides recom-
tients into different nutritional risk groups was compared between
mendations for adult patients but does not address pediatric
tools and related to anthropometric measures and clinical variables
patients (9). Screening tools for the assessment of malnutrition
[e.g., length of hospital stay (LOS) and infection rates].
Results: A similar rate of completion of the screening tools for each
risk of adults have been available for many years (9–11). Similar
tool was achieved (PYMS: 86%; STAMP: 84%; and STRONGKIDS: pediatric tools have been developed and were only tested in
81%). Risk classification differed markedly by tool, with an overall small cohorts of hospitalized children (5, 7, 12–14). These tools
agreement of 41% between tools. Children categorized as high risk consist of questions related to the patient’s history and mea-
(PYMS: 25%; STAMP: 23%; and STRONGKIDS: 10%) had a longer surements or clinical estimation of body size to assess risk of poor
LOS than that of children at low risk (1.4, 1.4, and 1.8 d longer,
respectively; P , 0.001). In high-risk patients identified with the 1
Parts of the study data were previously presented at the 45th Annual
PYMS, 22% of them had low (,22) body mass index (BMI) SD-
Congress of the European Society for Paediatric Gastroenterology, Hepatology
scores (SDSs), and 8% of them had low height-for-age SDSs. For the
and Nutrition, Stockholm, Sweden, 27–28 April 2012, and at the 34th Annual
STAMP, the percentages were 19% and 14%, respectively, and for the Congress of the European Society for Clinical Nutrition and Metabolism,
STRONGKIDS, the percentages were 23% and 19%, respectively. Barcelona, Spain, 8–11 September 2012.
Conclusions: The identification and classification of malnutrition 2
Supported in part by a European Society for Clinical Nutrition and Me-
risk varied across the pediatric tools used. A considerable portion of tabolism Network Grant (to BK).
3
children with subnormal anthropometric measures were not identified Supplemental Figure 1 and Supplemental Tables 1 and 2 are available
with all of the tools. The data obtained do not allow recommending from the “Online Supporting Material” link in the online posting of the
the use of any of these screening tools for clinical practice. This article and from the same link in the online table of contents at http://ajcn.
study was registered at clinicaltrials.gov as NCT01132742. nutrition.org.
13
These authors shared first authorship.
Am J Clin Nutr 2016;103:1301–10.
*To whom correspondence should be addressed. E-mail: office.koletzko@
med.uni-muenchen.de.
Keywords: hospitalized children, malnutrition, nutritional screen- Received March 10, 2015. Accepted for publication February 22, 2016.
ing, PYMS, STAMP, STRONGKIDS First published online April 20, 2016; doi: 10.3945/ajcn.115.110700.
Am J Clin Nutr 2016;103:1301–10. Printed in USA. Ó 2016 American Society for Nutrition 1301
1302 CHOURDAKIS ET AL.
nutritional status (15). The tools aim to screen all inpatients and is to identify individuals at risk who might normally be missed so
identify those who were missed during routine admission and that they can receive adequate referral to the clinical nutritional
whose disease outcome would improve or would not deteriorate care team. We also excluded children admitted to day hospital
from a tailored nutritional intervention. However, there has been care because their expected LOSs were ,24 h. Patients with
a lack of sufficient data on the predictive value of such pediatric cerebral palsy or genetic syndromes were not excluded per pro-
screening tools on outcome and objective indexes of malnutri- tocol. Details about the recruitment and protocol have been
tion in large multicenter studies and of a comparative evaluation previously published by Hecht et al. (18).
of the various tools. Addressing these aspects may direct health
professionals on their decision to select the most suitable nu-
tritional screening tool. Methods
We compared the risk scoring of 3 previously proposed Patients were assessed with the use of a set of questions that
pediatric nutrition screening tools, [i.e., the Pediatric Yorkhill considered nutritional risk, and measurements of anthropometric
outcome data. For the cross-tabulation of risk classification Therefore, in all data analyses except for the random-coefficient
between the tools, we decided to group the classification of model, low- and medium-risk patients for each screening tool
malnutrition risk into 2 rather than 3 categories (i.e., high were combined and presented as one group that was compared
compared with medium and low) because children allocated in with high-risk patients.
the high category were the ones that needed to be further referred
for an assessment to the dietetic and clinical team.
The study protocol was accepted by the local research or
medical ethic committees of each participating center. Before
participation, informed written consent was obtained from par-
ents and their caregivers (whenever required).
Statistical analysis
Risk scores were cross-tabulated within the 3 screening tools,
and agreement rates were computed (concurrent validity). Cohen’s
k statistic test was applied to describe the level of agreement
between the 2 tools (20) with the agreement that occurred by
chance taken into account. Baseline characteristics between groups
were compared with the use of Fisher’s exact test or Pearson’s chi-
square test for categorical data. A linear regression analysis was
applied separately for sex to adjust the association of risk of
malnutrition with TSFT and MUAC for age, chronic disease, and FIGURE 1 Malnutrition risk classification on the basis of the 3 screen-
ing tools expressed as percentages of the total number of assessed children
center. Residuals were checked for a normal distribution. In for each tool. PYMS, Pediatric Yorkhill Malnutrition Score; STAMP, Screen-
clinical practice, a substantial intervention (e.g., referral to ing Tool for the Assessment of Malnutrition in Pediatrics; STRONGKIDS,
a dietitian) will only occur in children with a high-risk score. Screening Tool for Risk of Impaired Nutritional Status and Growth.
1304 CHOURDAKIS ET AL.
Age- and sex-specific BMI and weight-for-height SD-scores and further age-adequate WHO reference data were used for
(SDSs) were calculated with the use of WHO reference data; patients aged .5–18 y (http://www.who.int/growthref/en/). MUAC
WHO growth reference study data were used for children aged and TSFT SDSs that were based on WHO reference data were
1 mo to 5 y (http://www.who.int/childgrowth/software/en/) limited to patients aged 3 mo to 5 y.
TABLE 2
Cross-tabulation of risk classification between the PYMS, STAMP and STRONGKIDS1
Risk of malnutrition
Low (n = 943) Medium (n = 305) High (n = 416) Low (n = 512) Medium (n = 547) High (n = 315) Low (n = 915) Medium (n = 968) High (n = 206)
2
Age, y 7.4 (3.6–11.3) 5.8 (3.0–11.3) 4.4 (2.0–9.9) 8.3 (4.7–12.0) 7.8 (4.1–12.0) 7.6 (3.8–12.3) 5.1 (1.3–11.2) 4.4 (1.4–10.6) 6.3 (1.9–12.6)
Age group, %
31 d to 0.9 y 0 0 0 0 0 0 21 18 15
1–1.9 y 12 13 24 0 0 0 10 14 10
2–5.9 y 30 37 34 34 39 41 23 26 24
6–12.9 y 40 32 29 49 41 38 29 26 27
13–17.9 y 18 18 13 17 20 21 17 17 24
Female, % 44 50 43 46 45 43 44 45 44
Caucasian, % 92 93 90 94 91 92 92 91 88
Acute admission, % 45 54 65 52 48 53 48 62 58
Chronic disease, % 48 49 48 36 53 75 30 48 89
Surgical, % 20 21 17 16 21 19 25 15 20
BMI SDS 0.52 6 1.233 0.28 6 1.14 20.77 6 1.58 0.46 6 1.17 0.15 6 1.23 20.30 6 1.85 0.42 6 1.25 20.04 6 1.37 21.19 6 1.61
HFA SDS 0.15 6 1.37 0.19 6 1.43 20.19 6 1.54 0.38 6 1.25 0.02 6 1.29 20.34 6 1.62 0.37 6 1.31 0.04 6 1.38 20.86 6 1.97
Nutritional support, %
Before admission 6 11 24 1 9 26 1 11 54
During hospitalization 5 12 25 1 9 27 2 11 56
LOS, d 4 (3–6) 5 (3–8) 5 (3–9) 4 (3–7) 4 (3–7) 5 (3–8) 4 (3–7) 4 (3–7) 6 (3–10)
Secondary outcomes, %
Fever4 10 21 29 10 17 19 13 23 23
Use of antibiotics5 28 44 44 28 33 41 28 43 44
1
RISK OF MALNUTRITION IN HOSPITALIZED CHILDREN
HFA, height-for-age; LOS, length of stay; PYMS, Pediatric Yorkhill Malnutrition Score; SDS, SD-score; STAMP, Screening Tool for the Assessment of Malnutrition in Pediatrics; STRONGKIDS,
Screening Tool for Risk of Impaired Nutritional Status and Growth.
2
Median; IQR in parentheses (all such values).
3
Mean 6 SD (all such values).
4
At least one event day of fever.
5
At least one event day of antibiotic use.
1305
A multilevel mixed-effects Poisson regression was used to Completion of the screening tools
accommodate the general dependence of the LOS on the center of Because each of the 3 screening tools was developed for
the patient and the existing differences in the severity and type of different age ranges, the number of eligible children that these
chronic diseases between centers. Thus, the center was included tools could be applied to varied with the screening tool used.
as a random effect while further allowing varying effects by Approximately 933 patients were either ,2 or .16 y of age and,
chronic disease status. The association of each nutritional risk therefore, the STAMP could not be completed. Similarly, for
classification by the PYMS, STAMP, and STRONGKIDS with the 621 participants aged either ,1 or .16 y, the PYMS could not
LOS was tested with age, sex ,and chronic disease status in- be applied. In total, the PYMS was completed for 1664 subjects
cluded as confounders. An interaction between chronic disease (86% of the children in the targeted group from 1 to 16 y of age),
status and nutritional risk classification was also tested. the STAMP was completed for 1374 study participants (84% of
Furthermore, percentages of children with suboptimal skinfold children in the targeted group from 2 to 16 y of age), and the
thicknesses or MUACs and suboptimal BMI who were correctly
TABLE 4
Relation between the LOS and nutritional risk classification with the use of a random-coefficient model1
PYMS (n = 1669) STAMP (n = 1379) STRONGKIDS (n = 2089)
Risk Coefficient (95% CI) P Coefficient (95% CI) P Coefficient (95% CI) P
Low — — — — — —
Medium 1.112 (1.05, 1.18) ,0.001 1.08 (1.02, 1.14) 0.005 1.19 (1.14, 1.24) ,0.001
High 1.38 (1.32, 1.45) ,0.001 1.37 (1.29, 1.46) ,0.001 1.82 (1.72, 1.93) ,0.001
1
Adjusted for age, sex, and chronic disease status and with the dependence within centers taken into account. LOS,
length of stay; PYMS, Pediatric Yorkhill Malnutrition Score; STAMP, Screening Tool for the Assessment of Malnutrition in
Pediatrics; STRONGKIDS, Screening Tool for Risk of Impaired Nutritional Status and Growth.
2
Comparison with low-risk category (i.e., medium-risk patients stayed 1.11 d longer in the hospital than did low-risk
patients scored with the use of the PYMS).
RISK OF MALNUTRITION IN HOSPITALIZED CHILDREN 1307
High (n = 128)
The total includes children who completed all tools and had calculated BMI. For 5 children, no BMI could be calculated because the length value was missing. PYMS, Pediatric Yorkhill Malnutrition
A pairwise comparison resulted in a 55% agreement for the
20.88 6 1.50
PYMS with the STAMP (k = 0.31; 95% CI: 0.28, 0.35) and 58%
72
26
30
agreement for the PYMS with the STRONGKIDS (k = 0.33; 95%
CI: 0.29, 0.37). The greatest degree of agreement was shown
between the STAMP and STRONGKIDS (60%; k = 0.37; 95%
CI: 0.33, 0.40). This agreement increased to 74% when a com-
Medium (n = 550)
0.05 6 1.39
Score; SDS, SD-score; STAMP, Screening Tool for the Assessment of Malnutrition in Pediatrics; STRONGKIDS, Screening Tool for Risk of Impaired Nutritional Status and Growth.
the high-risk group. A pairwise comparison between tool pairs
434
88
28
resulted in w80% agreement and is shown in Table 2 (PYMS
compared with STAMP: moderate agreement; PYMS compared
with STRONGKIDS: fair agreement; and STAMP compared with
STRONGKIDS: fair agreement) (21).
0.53 6 1.26
8
518
49
Clinical characteristics of patients in the 3 risk groups for
each tool
Characteristics of children within the risk groups of each
High (n = 274)
screening tool are described in Table 3. The proportion of pa-
20.27 6 1.88
tients with an underlying chronic disease was higher for patients
46
51
177
identified as high risk than for patients identified as medium or
low risk with the use of the STAMP (75% compared with 53%
or 36%, respectively) and the STRONGKIDS (89% compared
with 48% or 30%, respectively). With the use of the PYMS,
Medium (n = 494)
0.14 6 1.23
STAMP
risk categories (48% compared with 49% or 48%, respectively).
75
9
410
The administration of nutritional support, both before admission
or during the hospital stay, was higher for patients identified
with high risk than for patients identified with medium or low
risk with the use of all 3 tools. In addition, high-risk patients
Low (n = 485)
0.45 6 1.18
identified with the use of all 3 tools experienced fever more
BMI SDSs within risk groups of 2–16-y-olds for 3 malnutrition-risk screening tools (n = 1253 of 1258)1
437
42
6
frequently and were prescribed more antibiotics than were
medium-risk-patients and low-risk-patients.
The LOS increased from low- to high-risk patients as identified
with the use of all 3 tools (Table 3). This result was also supported
High (n = 274)
20.78 6 1.55
Mean SDSs for either BMI or HFA differed between the 3 risk
9.1 (6 of 66)
0.23 6 1.16
children with low BMI SDS (,22) were not picked up as being
high risk (and were categorized either in the low- or medium
risk-category) with the use of the 3 tools. Table 5 displays rele-
vant differences in the 3 tools for the group of children (n = 1253)
Low (n = 757)
0.50 6 1.25
adjustment for age, chronic disease, and center. SDSs for the MUAC
,21 to at least 22 SDSs, n
and TSFT for patients 2–5 y of age in relation to the risk groups of
each screening tool are shown in Table 6.
At least 21 SDS, n
,22 SDSs, n
DISCUSSION
The aim of all 3 screening tools is to identify children at risk of
2
TABLE 5
BMI SDS
for application by different users (e.g., pediatricians and nurses) It is arguable what benchmark would be best for assessing the
and in different age groups (5, 13, 17). In addition, the PYMS value of a screening tool. Amaral et al. (3) and Kyle et al. (25)
and STAMP include anthropometric measures, whereas the showed a significant association between the screening score of
STRONGKIDS focuses on identifying children at nutritional risk nutrition risk screening tools and the LOS in adults, but they
on admission by visual inspection of body habitus alone. stated that the LOS is also influenced by many nonnutritional
This study showed marked differences in the number of pa- factors. However, adverse effects of malnutrition and the in-
tients who could be screened with the use of the 3 tools. Also, the fluence of the underlying disease interact and both affect the
scores and classification of malnutrition risk in children varied LOS, which should be considered when assessing associations of
substantially according to the tool used. Few smaller studies that risk scores and secondary outcomes such as fever or the use of
were conducted previously looked into the agreement in nutri- antibiotics.
tional risk classification with the use of the PYMS, STAMP, and We think that it is important for the tools to agree in the
STRONGKIDS and also showed this agreement to be modest detection of high-risk patients, including those with subnormal
(19, 22–24). A lack of agreement may be explained by the fact BMI, HFA, and skinfold-thickness measurements, which was not
that the tools are different although they contain similar steps. the case in the current study. We considered high-risk patients to
Although several components within the tools are similar, there be those who needed to be referred for a more detailed as-
are discrepancies in the scoring, duration of recall history, and sessment and were more likely to need a nutritional intervention.
approaches used to assess body size. Moreover, screening tools are also aiming to identify children
By definition (item 1), the PYMS was expected to categorize at risk of deterioration of malnutrition risk because of an acute
all children with BMI SDSs ,22 into the high-risk category. medical insult despite normal anthropometric measures at hos-
However, this was not the case for a low number of children pital admission. This identification encompasses a large pro-
(7of 96 children) with subnormal BMI that were not identified portion of children who are admitted in acute settings in
correctly with the use of the PYMS. developed countries, and the intervention and prevention of
In this study, we assessed the discriminant validity of the weight loss are probably as important as the correction of
screening outcomes of each tool against body composition and weight loss and growth catch-up in children who are already
explored their ability to predict adverse clinical outcomes. For malnourished (26).
each tool, we showed a reverse association between malnutrition Some strengths of our study are its multicenter setting and
risk with body composition and a positive association with the the large number of participants from different countries. To our
LOS. In particular, for each tool, children who scored a high risk best knowledge, this is the first study that compares 3 different
of malnutrition stayed longer in the hospital and had lower mean screening tools in a large pediatric population. We used one
MUAC and TSFT values than did patients with low or medium growth reference (the WHO growth standard) for all children and
risk. It should be emphasized that sensitivity and cutoffs of the thereby excluded the variation between different country-specific
MUAC are still debatable, and the MUAC might be a more valuable growth charts. However, we did not use disease-specific growth
tool in the assessment of markedly malnourished children. How- charts that were available (e.g., for cerebral palsy patients) be-
ever, the MUAC is often considered useful in the clinical assess- cause these charts are available for only a few selected diagnoses
ment and follow-up of patients. and have generally not been based on pan-European patient
The association between the risk-score classification and LOS populations. We also acknowledge that our study may have
was strongest with the STRONGKIDS. However, it was unclear suffered from a sample-selection bias, because some children who
how much of this association was explained by disease severity were severely sick may not have joined the study. In addition,
and how much was attributed to the effect of malnutrition. a substantial number of children were receiving nutritional
RISK OF MALNUTRITION IN HOSPITALIZED CHILDREN 1309
support at study entry, which most likely reflected the profile of members of the European Society for Clinical Nutrition and Metabolism
patients who regularly attended the highly specialized hospitals Network project as listed in Hecht et al (18) for their help on site.
that participated in this study. An additional potential limitation The authors’ responsibilities were as follows—MC: coordinated intra-
group reviews and communication, helped with the statistical analyses, and
of this study is the fact that we did not perform a full nutritional
drafted the manuscript; MC, CH, KG, KFMJ, BK, and JMH: commented on
assessment as a reference for the comparison of screening scores the first and subsequent drafts of the manuscript; CH: contributed to the
(1, 17). Moreover, with our data, we could not account for the writing of the study protocol and the first draft of the manuscript, coordi-
effects of disease groups or severity on the association between nated the study, participated in conducting the study, and performed the data
malnutrition risk and clinical outcomes. The power to detect entry, management, and analyses; KG: participated in the initial part of the
nutrition-associated infections was limited by the generally short study design, contributed to the sample collection, and coordinated intra-
LOS of the patients included in the study, which reflects current group reviews and communication; KFMJ, TK-L, HAK, JK, CL, RS, HS,
clinical practice. Large differences were shown between coun- and JMH: participated in the initial part of the study design, contributed to
the sample collection, and were responsible for the data acquisition, data
tries, which may have reflected differences in population char-