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Malnutrition risk in hospitalized children: use of 3 screening tools in

a large European population1–3


Michael Chourdakis,4,13 Christina Hecht,4,13 Konstantinos Gerasimidis,5,13 Koen FM Joosten,6
Thomais Karagiozoglou-Lampoudi,7 Harma A Koetse,8 Janusz Ksiazyk,9 Cecilia Lazea,10

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Raanan Shamir,11 Hania Szajewska,12 Berthold Koletzko,4* and Jessie M Hulst6
4
Ludwig-Maximilians-University of Munich, Division of Metabolic and Nutritional Medicine, Dr. von Hauner Children’s Hospital, University of Munich
Medical Centre, Munich, Germany; 5Human Nutrition, School of Medicine, College of Medicine, Veterinary and Life Sciences, Royal Hospital for Sick
Children, University of Glasgow, Glasgow, United Kingdom; 6Erasmus Medical Center, Sophia Children’s Hospital, Department of Pediatrics, Rotterdam,
Netherlands; 7Clinical Nutrition Laboratory, Nutrition/Dietetics Department, Technological Education Institute, Thessaloniki, Greece; 8Beatrix Children’s
Hospital, University Hospital Groningen, Groningen, Netherlands; 9Department of Pediatrics, Nutrition and Metabolic Diseases, The Children’s Memorial
Health Institute, Warsaw, Poland; 10Clinic Pediatrics I, Clinical Emergency Hospital for Children, Cluj-Napoca (Klausenburg), Romania; 11Institute of
Gastroenterology, Nutrition and Liver Diseases, Schneider Children’s Medical Center of Israel, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv,
Israel; and 12Department of Pediatrics, Medical University of Warsaw, Warsaw, Poland

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

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Malnutrition Score (PYMS)14 (16, 17), the Screening Tool for measures and body composition were all performed within the
the Assessment of Malnutrition in Pediatrics (STAMP) (13), and first 24 h after admission. The assessors were a multidisciplinary
the Screening Tool for Risk of Impaired Nutritional Status and team that included research nurses, dietitians, medical students,
Growth (STRONGKIDS) (5)] in a large multicenter study in and nutritionists. A training workshop to harmonize the recruit-
children admitted to hospitals across Europe. In addition, we ment and standardize anthropometric measures and data collection
explored the agreement between the tools (concurrent validity) in the different centers was held in March 2010 in Munich,
and the relation of risk scores to anthropometric measures and Germany.
body-composition measurements as well as clinical variables Demographic and medical data, together with a questionnaire
such as the length of hospital stay (LOS). for nutritional status, were collected during a structured interview
The criteria for the best outcome measure to assess the effect of with patients and (when required) with their caregivers. The
the use of a screening tool are not yet agreed upon, because it is questionnaire integrated the 4 items of the PYMS tool (16, 17),
somewhat controversial as to whether such screening tools should the 3 items of the STAMP tool (13), and the 4 items of the
predict anthropometric measures or clinical outcomes. Therefore, STRONGKIDS screening tool (5) and sorted them by item con-
in this study, we aimed to explore the association of the scores tents. For each patient, the steps of each tool were completed by
provided by the tools with both subnormal BMI and with the LOS. the same investigator in the same order. The total score for each
screening tool was computed during the analysis of the data. The
28 assessors were encouraged not to add the scores for each tool
METHODS during data collection to avoid bias by the knowledge on cate-
gorization in a screening tool. Any decisions on providing nu-
Study design and subjects tritional treatment were made only by attending physicians and
This prospective, European, multicenter cohort study enrolled dieticians, not by assessors. Such decisions were made according
patients from February 2010 to July 2011 in 14 centers in 12 to normal routine procedures and were not influenced by the
countries (Zagreb, Croatia; Copenhagen, Denmark; Lille, France; study data.
Munich, Germany; Thessaloniki, Greece; Petah Tikvah, Israel; Important characteristics of the PYMS (1, 16, 17), STAMP
Milan, Italy; Rotterdam and Groningen, Netherlands; Warsaw, (13, 19), and STRONGKIDS (5, 19) are reported in Supple-
Poland; Cluj-Napoca, Romania; and Oxford and Glasgow, United mental Table 1. The PYMS and STAMP include anthropo-
Kingdom). Patients (1 mo to 18 y old) who were admitted to metric measures (BMI compared with weight and height,
pediatric and pediatric surgery wards with an anticipated length respectively); the STRONGKIDS includes a subjective clinical
of stay .24 h were eligible to participate. Patients were con- assessment of nutritional status. Total scores for each tool were
secutively invited to participate whenever a data collection was computed for those age groups for whom the tools were val-
possible within the first 24 h after admission. Patients who were idated. PYMS was completed for patients aged 1–16 y, STAMP
attending the accident and emergency department of the day was completed for patients aged 2–16 y, and STRONGKIDS was
care unit were excluded. completed for patients aged 1 mo to 18 y. For comparison of the
We excluded children admitted to intensive care because of the 3 tools, only children aged 2–16 y were considered because
limited feasibility to perform detailed anthropometric measures patients within this age range were eligible for screening by all 3
on the day of admission in critically ill children. To identify tools.
children at risk of malnutrition in this group of patients is re- Data on height, weight, midupper arm circumference (MUAC),
dundant because all of these children are, by the nature of their and triceps skinfold thickness (TSFT) were collected. The
critical illnesses (e.g., unconscious and thus unable to eat), at high methods of collection have been described previously by Hecht
risk of malnutrition and therefore should receive the respective et al. (18). Clinical variables, including the LOS as a primary
attention of the medical and dietetic staff. The principle of screening outcome and the frequency of infectious complications (num-
ber of days with a temperature .38.58C and number of days
with antibiotic use) were derived from hospital records after
14 discharge.
Abbreviations used: HFA, height-for-age; LOS, length of hospital stay;
MUAC, midupper arm circumference; PYMS, Pediatric Yorkhill Malnutri- The total score and classification of malnutrition risk (low,
tion Score; SDS, SD-score; STAMP, Screening Tool for the Assessment of medium, or high) was determined for each study participant and
Malnutrition in Pediatrics; STRONGKIDS, Screening Tool for Risk of Im- screening tool. The scores obtained by the 3 screening tools were
paired Nutritional Status and Growth; TSFT, triceps skinfold thickness. then related to anthropometric measures, body compositions, and
RISK OF MALNUTRITION IN HOSPITALIZED CHILDREN 1303
TABLE 1
Scoring of screening tool items for the group of children aged 2–16 y (n = 1724) who completed all tools (n = 1258)1
Scores of children completing ALL tools (n = 1258) Children aged 2–16 y (n = 1724)

Not assessed according to


Item2 0 1 2 3 Total assessed original tool questions

Item 1: current nutritional condition,3 n (%)


PYMS (0, 2) 1152 (92) — 106 (8) — 1538 (89) 186 (11)
STAMP (0, 1, 3) 967 (77) 169 (13) — 122 (10) 1474 (85) 250 (15)
STRONGKIDS (0, 1) 1031 (82) 227 (18) — — 1607 (93) 117 (7)
Item 2: weight loss,4 n (%)
PYMS (0, 1) 1036 (82) 222 (18) — — 1568 (91) 156 (9)

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STAMP (NA) — — — — — —
STRONGKIDS (0, 1) 1027 (82) 231 (18) — — 1633 (95) 91 (5)
Item 3: reduced intake,5 n (%)
PYMS (0, 1, 2) 1004 (80) 228 (18) 26 (2) — 1633 (95) 91 (5)
STAMP (0, 2, 3) 913 (73) — 317 (25) 28 (2) 1633 (95) 91 (5)
STRONGKIDS (0, 1) 861 (68) 397 (32) — — 1633 (95) 91 (5)
Item 4: underlying disease,6 n (%)
PYMS (0, 1, 2) 994 (79) 255 (20) 9 (1) — 1509 (88) 215 (12)
STAMP (0, 2, 3) 670 (53) — 324 (26) 264 (21) 1529 (89) 195 (11)
STRONGKIDS (0, 2) 893 (71) — 365 (29) — 1515 (88) 209 (12)
1
NA, not applicable; 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
Possible scores are shown in parentheses; each tool had different possible scores for each item. The classification of risk level, determined by total
scores, differed between tools. Scores for low risk: PYMS, 0 points; STAMP, 0–1 point; and STRONGKIDS, 0 points. Scores for medium risk: PYMS, 1 point;
STAMP, 2–3 points; and STRONGKIDS, 1–3 points. Scores for high risk: PYMS, 2–7 points; STAMP, 4–9 points; and STRONGKIDS, 4–5 points.
3
PYMS: Is the BMI below the cutoff value shown in the BMI scoring guide? STAMP: Use a growth chart or the percentile quick-reference tables to
determine the child’s weight and height measurements. STRONGKIDS: Is the patient in a poor nutritional status judged by a subjective clinical assessment?
4
PYMS: Has the child lost weight recently? STRONGKIDS: Is there weight loss or poor weight gain (infants ,1 y old) during the last few weeks or
months?
5
PYMS: Has the child had reduced intake (including feeds) for at least the past week? STAMP: What is the child’s nutritional intake? STRONGKIDS: Is
one of the following items present: excessive diarrhea ($5 times/d) or vomiting (.3 times/d), reduced food intake during the last few days, pre-existing
nutritional intervention, or inadequate nutritional intake because of pain?
6
PYMS: Will the child’s nutrition be affected by the recent admission or condition for at least the next week? STAMP: Does the child have a diagnosis
that has any nutritional implication? STRONGKIDS: Is there an underlying illness with risk of malnutrition or expected major surgery?

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.

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FIGURE 2 Prevalence of malnutrition risk varied markedly between and within different countries with the use of the different screening tools. 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.

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 and medium High k (95% CI) Agreement, %

PYMS compared with STAMP (n = 1308) 0.47 (0.42, 0.53) 82


Low and medium 897 121
High 118 172
STAMP compared with STRONGKIDS (n = 1318) 0.39 (0.33, 0.45) 83
Low and medium 990 32
High 187 109
STRONGKIDS compared with PYMS (n = 1490) 0.35 (0.28, 0.42) 81
Low and medium 1088 249
High 39 114
1
The horizontal rows labeled “Low and medium” or “High” represent the total n in the first tool of each pair listed; the
vertical columns represent the total n in the second tool of each pair. Intersecting Low and medium/High rows and columns
indicate where both tools agreed. 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.
TABLE 3
Characteristics of children within risk groups of each screening tool1
PYMS (1–16 y old; n = 1664) STAMP (2–16 y old; n = 1374) STRONGKIDS (1 mo to 18 y old; n = 2089)

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

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1306 CHOURDAKIS ET AL.

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

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STRONGKIDS was completed for 2089 subjects (81% of the
identified or misclassified at high risk of malnutrition by each tool children in the targeted group from 1 mo to 18 y of age). For
were calculated and compared with each other. Also, percentages almost one-half of the study group (1258 children; 49%), all 3
of children classified at high risk despite a normal MUAC, TSFT, tools were completed. Completion rates of each individual
or BMI were compared between the 3 tools. To have the same component of the 3 tools are listed in Table 1. Because the
children included for each tool, only children aged 2–5 y were researchers occasionally found it challenging to respond to some
included for the analysis of SDSs for MUAC and TSFT. Data of the steps of the individual tools, a numbers of screens were
management and statistical analyses were carried out with R left incomplete.
2.13.2m software (The R Foundation for Statistical Computing)
and Stata 12.1 software (StataCorp LP).
Malnutrition risk classification
The classification of malnutrition risk of the assessed children
RESULTS by the 3 screening tools showed a substantial variation in the
different tools (Figure 1). In addition, the risk-classification dis-
Patient characteristics tribution varied markedly within and between countries (Figure 2).
A total of 2567 patients (median age: 4.7 y; IQR: 1.4–11.1 y) Overall, the proportion of high-risk patients ranged be-
were enrolled in the study (80% pediatric and 20% pediatric sur- tween 5% and 51% (PYMS: 15–51%; STAMP: 9–51%; and
gery patients). Nearly one-half of the study population were female STRONGKIDS: 5–30%). The greatest difference between the
(44.9%), and 44.8% of subjects had an underlying chronic disease proportions of high-risk patients on the basis of the 3 screening
and were electively admitted (18). Most study participants were of tools within one center was 32% (Greece).
Caucasian origin (91%) and were at home before admission (91%). Among the 1258 patients for whom all 3 tools were completed,
Nutritional support before admission was administered to 11.8% of the distribution of risk classification according to the 3 screening
the study population. During the hospital stay, nutritional support tools is shown in Supplemental Figure 1. In more detail, in this
was given to 12.3% of participants (6.2% of subjects received oral subgroup of 1258 patients, the different tools categorized from
supplements, 6.1% of subjects received tube feeding, and 0.8% 10% (STRONGKIDS) to 22% (STAMP and PYMS) of children in
of subjects received parenteral nutrition with a few overlaps), of the high-risk group. In total, only 87 participants (7% of all
whom 76% of participants were already receiving the support patients with 3 completed tools) were jointly rated as being at
before admission. Approximately 20% of children who received high risk of malnutrition with the use of all 3 tools. Less than
nutritional support before admission were not allocated to a nutri- one-half of the patients (41%) were classified at the same risk
tional support regimen after admission, according to hospital data. level for malnutrition with the use of the 3 different tools. This
The median LOS was 4 d (IQR: 3–7 d). A BMI SDS of less percentage increased to 74% when children with low and me-
than 22 was present in 7.0% of the study population at hospital dium risk were grouped together and compared with the high-risk
admission, whereas 7.9% of the participants had a height-for-age group. The agreement between the tools, with statistical chance
(HFA) SDS of less than 22 at hospital admission. accounted for, was fair to moderate (20).

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)

54.6 (36 of 66)


STRONGKIDS
bined classification of low and medium risk was compared with

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).

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Low (n = 575)

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)

22.7 (15 of 66)


patients with a chronic disease were equally classified into the 3

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

by the effect estimates of the multivariate regression analysis with


age, sex, chronic disease, and center taken into account (Table 4).
147
67
60

Risk categorization and anthropometric measures


Medium (n = 222)

Mean SDSs for either BMI or HFA differed between the 3 risk
9.1 (6 of 66)
0.23 6 1.16

groups within each tool (Table 3; for additional details, see


PYMS

Supplemental Table 2). In addition, a considerable number of


190
30
2

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

who completed all 3 tools and had BMI data available.


687
66
4

The MUAC and TSFTwere measured in 2263 study participants


(88%) and 2094 study participants (82%), respectively. Linear
regression results for all 3 screening tools showed a significant
relation between malnutrition risk and MUAC for both sexes after
All values are means 6 SDs.
,22 SDSs and not categorized
in the high-risk group, % (n)

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

malnutrition on admission to select patients for additional eval-


1

uation and a potential intervention. However, there are differences


concerning the use of these tools because they were designed
1308 CHOURDAKIS ET AL.
TABLE 6
MUAC and TSFT SDSs for children 2–5 y old within the risk groups for 3 malnutrition risk screening tools1
PYMS (n = 407) STAMP (n = 389) STRONGKIDS (n = 401)

Low Medium High Low Medium High Low Medium High

MUAC SDSs 0.52 6 1.17 2


0.24 6 1.18 20.27 6 1.13 0.44 6 1.15 0.31 6 1.11 20.21 6 1.33 0.67 6 1.13 0.17 6 1.29 20.81 6 1.16
At least 21 SDS, n 197 75 82 119 149 69 156 173 19
,21 to at least 22 13 12 16 10 18 13 5 27 9
SDSs, n
,22 SDSs, n 4 0 8 1 1 9 0 7 5
TSFT SDSs 1.13 6 1.22 0.85 6 1.12 0.42 6 1.33 0.96 6 1.23 0.88 6 1.15 0.75 6 1.50 1.09 6 1.23 0.87 6 1.30 0.34 6 1.32
At least 21 SDS, n 192 81 84 117 150 70 140 178 23

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,21 to at least 8 2 10 7 4 8 7 9 3
22 SDSs, n
,22 SDSs, n 0 1 4 1 2 2 0 4 1
1
For MUAC SDSs, calculations included all children (PYMS: n = 407; STAMP: n = 389; STRONGKIDS: n = 401) who completed the tool and had an MUAC
measurement. For TSFT SDSs, calculations included all children (PYMS: n = 382; STAMP: n = 361; STRONGKIDS: n = 365) who completed the tool and had
a TSFT measurement. MUAC, midupper arm circumference; 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; TSFT, triceps skinfold thickness.
2
Mean 6 SD (all such values).

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-

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interpretation, and analysis; BK: conceived the study, participated in its de-
acteristics or clinical practice. Furthermore, our study evaluated sign, contributed to the writing of the study protocol, and helped to draft the
the screening tools in the specific study population enrolled, and manuscript; and all authors: read and approved the final manuscript. The
the extrapolation of results to other populations must be done presented data were part of a PhD thesis accomplished by CH at the Medical
cautiously. Faculty of the Ludwig-Maximilians-University of Munich. KG, KFMJ, and
Although significant associations were observed for all 3 JMH have been involved in the development of the STRONGKIDS and
tools between high risk of malnutrition with an increased LOS PYMS, respectively. None of the authors reported a conflict of interest
and suboptimal anthropometric measures, the agreement between related to the study.
tools in the classification of the same patients at same risk of
malnutrition was modest. Although screening tools have the
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