children

Article
Development and Validation of a New Screening Tool with
Non-Invasive Indicators for Assessment of Malnutrition Risk
in Hospitalised Children
Petra Klanjšek 1, *, Majda Pajnkihar 1 , Nataša Marčun Varda 2,3 , Mirjam Močnik 2 , Sonja Golob Jančič 2
and Petra Povalej Bržan 3,4

1 Faculty of Health Sciences, University of Maribor, Žitna ulica 15, 2000 Maribor, Slovenia;
[email protected]
2 Department of Paediatrics, University Medical Centre Maribor, Ljubljanska ulica 5, 2000 Maribor, Slovenia;
[email protected] (N.M.V.); [email protected] (M.M.);
[email protected] (S.G.J.)
3 Faculty of Medicine, University of Maribor, Taborska ulica 8, 2000 Maribor, Slovenia; [email protected]
4 Faculty of Electrical Engineering and Computer Science, University of Maribor, Koroška cesta 46,
2000 Maribor, Slovenia
* Correspondence: [email protected]

Abstract: There is no evidence of the most effective nutritional screening tool for hospitalized
children. The present study aimed to develop a quick, simple, and valid screening tool for identifying
malnutrition risk of hospital admission with non-invasive indicators. A cross-sectional study was
conducted. Children‘s nutritional baseline using a questionnaire, subjective malnutritional risk,
and Subjective Global Nutritional Assessment were assessed on admission. Concurrent validity
Citation: Klanjšek, P.; Pajnkihar, M.;
was assessed using American Society for Parenteral and Enteral Nutrition (ASPEN)and Academy
Marčun Varda, N.; Močnik, M.; Golob
of Nutrition and Dietetics assessment and Subjective Global Nutritional Assessment tool. A new
Jančič, S.; Povalej Bržan, P.
Development and Validation of a
screening tool Simple Pediatric Nutritional risk Screening tool (SPENS) was developed, and sensitivity,
New Screening Tool with specificity and reliability were evaluated. A total of 180 children aged from 1 month to 18 years
Non-Invasive Indicators for were included (142 in the development phase and 38 in the validation phase). SPENS consist of
Assessment of Malnutrition Risk in four variables and shows almost perfect agreement with subjective malnutritional risk assessment
Hospitalised Children. Children 2022, (κ = 0.837) with high sensitivity and specificity (93.3% and 91.3% respectively). Compared with
9, 731. https://doi.org/10.3390/ Subjective Global Nutritional Assessment and ASPEN and Academy of Nutrition and Dietetics
children9050731 assessment, SPENS had sensitivity 92.9% and 86.7%, a specificity of 87.5% and 87.0%, and an overall
Academic Editors: Tzuan A. Chen agreement of 0.78 and 0.728, respectively. Due to the fast, simple, easy, and practical to use, screening
and Jayna Markand Dave the SPENS can be performed by nurses, physicians, and dieticians.

Received: 15 April 2022

Keywords: nutritional risk; pediatrics; undernutrition; validation; computer-based tool
Accepted: 12 May 2022
Published: 17 May 2022

Publisher’s Note: MDPI stays neutral

with regard to jurisdictional claims in 1. Introduction
published maps and institutional affil-
Nutritional status affects all aspects of a child’s health, including growth and de-
iations.
velopment, physical activity, and response to serious illness [1]. In hospitalised children
with different clinical conditions, adequate nutritional status plays a key role in normal
growth processes, responses to concomitant diseases, quality of life, care costs, and sur-
Copyright: © 2022 by the authors.
vival [2,3]. Malnutrition during the period of illness can interrupt treatment, worsen the
Licensee MDPI, Basel, Switzerland. child’s existing health condition, and prolong hospitalisation. In addition to failure to
This article is an open access article thrive [4], malnutrition can have lasting consequences for children, including changes in
distributed under the terms and anthropometric parameters or new emerging diseases [5].
conditions of the Creative Commons Malnutrition is often unrecognised and untreated in hospitalised children [6]. In
Attribution (CC BY) license (https:// previous studies, prevalence rate varies greatly, from 5.1% to 55.6% [7].
creativecommons.org/licenses/by/ The development of malnutrition in hospitalised children is most often influenced
4.0/). by the underlying disease or its worsening [8,9], and further by the presence of chronic

Children 2022, 9, 731. https://doi.org/10.3390/children9050731 https://www.mdpi.com/journal/children

Children 2022, 9, 731 2 of 16

diseases [10,11]. The latter can be accompanied by the presence of eating disorders [12]
and reduced food intake before or during hospitalisation [13]. The most common gastroin-
testinal factors of malnutrition include nausea and vomiting, constipation, diarrhoea [8,10]
and infections [14]. Surgery, aggressive therapies (e.g., oncology treatment) [15,16] and
neuromotor disabilities [17] are also negatively related to nutritional status. The most
important clinical indicators of children with disease-associated malnutrition ranked on
the basis of the opinions and practices of an international cohort of health professionals are
ongoing weight loss, increased losses, increased requirements, low dietary intake and a
high-risk condition [18].
Early and timely nutritional screening helps to improve nutritional care, accelerate
treatment and recovery, reduce complications, and reduce economic costs in the health sys-
tem [19] as with other diseases where early diagnosis and timely initiation of treatment are
of the utmost importance [20]; therefore, European Society for Paediatric Gastroenterology,
Hepatology and Nutrition (ESPHAGAN) and American Society for Parenteral and Enteral
Nutrition (AESPEN) are recommending nutritional screening for hospitalised children with
paediatric nutritional screening tools (NSTs) which are simple, useful, and cost-effective.
Several NSTs for children admitted to the hospital have been developed and validated [7,21].
In the last decade, most of the studies consider Paediatric Yorkhill Malnutrition Score
(PYMS), Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMP) and
Screening Tool for Risk on Nutritional status and Growth (STRONGkids) [22–24]. Due
to the individual needs of the different study populations, researchers are continuously
developing new NSTs [21]; however, no agreement has been reached on the “gold standard”
for the assessment of malnutrition risk [25]. The last point is also one of the reasons that
the implementation of routine nutritional risk screening upon hospitalisation has not yet
been established in most clinical settings. Among 588 paediatric gastroenterologists and
paediatric dietitians from six countries (Australia, Israel, Spain, Turkey, Netherlands, and
UK) included in a recent study [18] only 23% reported routine use of NSTs at the hospital
(most frequently in Belgium, Netherlands, and UK: 40–50%). The most common approach
was assessment of weight changes (85%), followed by the use of growth charts (77–80%).
Low awareness, lack of guidelines or local policy and lack of resources were recognised
as the most important barriers to the routine evaluation of disease-associated malnutrition
in clinical practice [18].
The development of NSTs modified for each hospital and child diagnosis individually
and with excellent reliability, regardless of the person performing the nutrition screening,
is suggested [26]. Systematic screening with NSTs is not routinely performed in Slovenian
hospitals. A specific NST for identification of the risks of malnutrition in Slovenian children
has not yet been developed.
The proposed study focuses on the development and validation of a reliable NST
Simple Pediatric Nutritional Risk Screening tool (SPENS) for hospitalised children of all
ages (1 month to 18 years), regardless of the child’s disease and the purpose of hospital-
isation. The aim of the study is to develop a useful and time-efficient NST that will be
used for screening in clinical pediatric practise by nurses, physicians, and dieticians. An
implementation of a newly developed SPENS will be the first step towards a systematic
routine for nutritional treatment of children in the Slovenian clinical environment; this
will enable the identification of hospitalised children with risk of malnutrition, which will
further receive appropriate nutritional assessment and timely nutritional interventions.

2. Materials and Methods

2.1. Design
This study employed a cross-sectional design using a questionnaire, full nutritional
assessment, and assessment with Paediatric Subjective Global Nutritional Assessment
(SGNA) [27–29] tool between 25 May and 16 October 2021. A two-phase exploratory
sequential mixed method design was used and made it possible to achieve more compre-
Children 2022, 9, 731 3 of 16

hensive and richer results than either method independently would have achieved [30].
Qualitative data were the basis for conducting a quantitative data analysis.

2.2. Setting and Samples

The setting for this study was one tertiary paediatric clinic in Slovenia. The clinic is the
second-largest clinic in Slovenia. As advised [7,31], consecutive sampling was used in the
quantitative part of the study. The participants were parents with children from 1 month to
18 years old, who have been admitted to the hospital between May and October 2021 with
an expected hospital stay (LOS) of at least 24 hours, regardless of the cause of admission or
the child’s medical condition. For the recruitment of children, we followed the eligibility
criteria (see Supplementary Material S1).
To determine the sample size, we considered the prevalence calculated by the SLOFIT
study, where 4.7% to 9.5% of children in the general Slovenian population were malnour-
ished [32]. Based on a 10% prevalence, a sample size of 138 hospitalised children was
calculated.

2.3. Participants
The sample included 142 parents with children for NST development hospitalised from
25 May 2020 to 21 July 2020 and 38 parents with children hospitalised from 1 September 2020
to 16 October 2020 in the SPENS validation. A total of 180 paediatric and surgery patients
aged 1 month to 18 years choose to participate (32.72%).

2.4. Measures
The final version of the questionnaire was based on a systematic review [7] and an
extensive review of articles related to the causes and consequences of malnutrition in
hospitalised children. The questionnaire contained 94 questions from 15 content sets (see
Supplementary Material S2). Questions used in the form included 277 variables due to
several multiple-choice questions. Measurements of anthropometric parameters were
recorded numerically.
A post-admission subjective malnutritional risk assessment by a physician included:
nutritional history; physical examination (assessment of muscle and subcutaneous fat,
detection of swelling and/or ascites); laboratory blood tests; and anthropometric measure-
ments according to ASPEN and Academy of Nutrition and Dietetics recommendations [33].
Techniques of inspection, palpation, percussion and/or auscultation were used [34]. Each
individual child was then distributed into one of the five categories according to the risk of
malnutrition: high; moderate; low; normal weight; overweight; and obesity.
The SGNA assessment tool was also chosen for identifying malnutrition by a physician.
SGNA assessment combines detailed questionnaire about subjective nutrition-focused
medical history and complete objective physical examination with an overall ranking which
is divided into three categories: well nourished; moderate; and severe malnutrition [29].

2.5. Procedure
This study was executed in a two-phase mixed-method design, namely an exploratory
sequential design [30]. Research began with the collection and analysis of qualitative data
and the production of a questionnaire, followed by a quantitative phase (development and
validation of the screening tool) where the initial findings were validated and generalised
(Figure 1). The gathering of data and development of a SPENS was conducted from 25 May
to 21 July 2020. The SPENS was developed in August 2020. The validation of the tool was
performed between the 1 September and 16 October 2020.
ldren 2022, 9, x FOR PEER REVIEW 4 of

Children 2022, 9, 731 was conducted from 25 May to 21 July 2020. The SPENS was developed in4 August
of 16 20
The validation of the tool was performed between the 1 September and 16 October 202

Figure 1. Visual
Figure diagram
1. Visual diagramofofan
an exploratory sequential
exploratory sequential design
design with
with the theofcourse
course of the study.
the study.

2.5.1. Collection and Analysis of Qualitative Data and Development of an Instrument

2.5.1.(Questionnaire)
Collection and Analysis of Qualitative Data and Development of an Instrument
(Questionnaire)
The causes and consequences characteristic of malnutrition in hospitalised children
were identified from the literature by an inductive generation of categories [35]. Ques-
The causes and consequences characteristic of malnutrition in hospitalised childr
tions from existing paediatric NSTs were also added [22,24,36–53]. The translation of the
werequestions
identified from
from the literature
English by an
to Slovene and viceinductive generation of categories [35]. Questio
versa was performed.
from existing paediatric was
The questionnaire NSTs were
then also added
reviewed by a team[22,24,36–53].
of assessors (sixThe translation
nurses, of the qu
three physi-
cians). Face validity and the appropriate use of
tions from English to Slovene and vice versa was performed.standardised professional language [54]
was assessed.
The For questions
questionnaire described
was then as partially
reviewed by aunderstandable by the assessors,
team of assessors a better
(six nurses, three phy
formulation of the question was suggested.
cians). Face validity and the appropriate use of standardised professional language [
was assessed. For questions
2.5.2. Gathering described
Data for SPENS as partially understandable by the assessors, a b
Development
ter formulation ofevery
Parents of the question was suggested.
child admitted to the clinic between 25 May 2021 and 21 July 2021
were invited to allow their child to participate in the development study.
Each day of the study period, a list of admissions for the current day was reviewed.
2.5.2. Gathering Data for SPENS Development
After exclusion criteria were applied, a list of children for malnutrition risk assessment
Parents
review wasofprepared
every child admittedtotoone
and distributed the clinic nurse
research between 25 May
who served 2021
as an and 21 July 20
interviewer.
wereAinvited
post-admission
to allow subjective malnutritional
their child risk assessment
to participate and SGNA assessment
in the development study. were
evaluated in each of the first 80 admitted children by two of three
Each day of the study period, a list of admissions for the current physicians andday
in thewas
nextreview
62 admitted children by one physician. Consecutively inter-rater reliability was calculated.
After exclusion criteria were applied, a list of children for malnutrition risk assessm
review was prepared and distributed to one research nurse who served as an interview
A post-admission subjective malnutritional risk assessment and SGNA assessment w
evaluated in each of the first 80 admitted children by two of three physicians and in t
Children 2022, 9, 731 5 of 16

The Kappa value varied between 0.73 (0.39, 1) and 1 (1, 1) which indicated substantial to
almost perfect agreement.
Patient recruitment acted as a secondary examination after admittance. No specialised
interventions were performed, only descriptive data were gathered. A post-admission
interview using a questionnaire and detailed anthropometric measures was carried out
by a research nurse. Parents and/or children answered questions about the factors and
consequences of malnutrition. Children under 4 years of age were expected to answer only
basic questions, all other information was provided by their parents. The results of the
interview were not known to the physicians and the results of nutrition risk and SGNA
assessment were hidden from the research nurse.
Detailed anthropometric measures of weight, height and/or length were taken by a
research nurse using standardised methods described by the World Health Organisation
(WHO) [55]. Body mass index (BMI) by age and sex was calculated using of PediTools [56]
and WHO Anthro [57] software. Mid upper arm circumference (MUAC) was measured
using a regular flexible plastic tape measure at the mid-point between the acromion and
olecranon [41]. Anthropometric data were gathered in Z scores. The WHO Anthro com-
puter program was used to assess the nutritional status of children < 2 years of age [57]. For
children ≥ 2 years of age, Centres for Disease Control and Prevention (CDC) 2000 growth
curves using a computer program included in the PediTools clinical tools for paediatric
practitioners were used [56]. The following indicators of malnutrition were used to deter-
mine malnutrition: weight-for-height/length (WFH/L), BMI, height-for-age (HFA), MUAC
as recommended by ASPEN and Academy of Nutrition and Dietetics (see Supplementary
Material S3) [58]. It is advisable to obtain all indicators when assessing malnutrition in chil-
dren, although only one indicator is needed to diagnose malnutrition [33]. Additionally, for
the purpose of calculating nutritional prevalence, values of BMI which define overweight,
and obesity as recommended, were also used [59].
Results of individual risk malnutrition score given by physician were given in six
risk groups and were consolidated into two risk categories in the development phase of
the SPENS: “not at risk” (normal, overweight, and obese risk category) and “at risk” (low,
moderate, and severe risk category). SGNA categorization was: well nourished; moderate;
and severe malnutrition [29].

2.5.3. Development of SPENS

The first phase of the SPENS development included data cleaning and feature selection.
In the second phase, the SPENS was developed using multivariate logistic regression model.

2.5.4. Validation of SPENS

The parents of every child admitted to the clinic between 1 September 2021 and
16 October 2021 were invited to allow their child to participate in the validation study.
In the validation phase, the developed SPENS was used for screening in 38 hospitalised
children. Screening of children was executed as part of routine examinations during
hospitalization by research nurse. A physician also assigned a subjective malnutritional
risk assessment to all children who participated in the screening. The same protocol
as described in the SPENS development phase was used (Figure 1). The results of the
screening were not known to the physician and vice versa. We validated the tool according
to recommendations by Klanjsek et al. [7].
For criterion validity each result in children with risk of malnutrition according to
SPENS was compared with a reference standard subjective malnutritional risk assessment
(n = 38).
For concurrent validity the results obtained by the SPENS were compared with the
SGNA assessment tool using chance-corrected agreement (Kappa-statistics) (n = 38). The
research nurse performed screening assessment with the developed tool, and the physician
performed a nutritional assessment with the SGNA assessment tool and subjective malnu-
tritional risk assessment in the same patients parallel in the same day. Comparison of the
Children 2022, 9, 731 6 of 16

two tools (SPENS and SGNA assessment tool) was made with the subjective malnutritional
risk assessment.

2.6. Data Analysis

Statistical analyses were performed using SPSS software version 28.0 [60] and the
R programming language in the RStudio programming environment [61]. Descriptive
statistics were used for the presentation of demographic data. Numerical variables were
presented with a median (95% CI). Frequencies and percentages were used to describe
categorical variables.
The feature selection process in the development phase included two steps. Relation-
ship between risk factors and subjective malnutritional risk assessment was validated by
Pearson Chi Square test. Furthermore, the importance of the variables was assessed using
the Random Forest (RF) model Importance function, which is based on calculating the
Mean Decrease Accuracy of the model [62]. Variables whose Mean Decrease Accuracy
metric had a value more than 2 were included in the development of the tool. A manual
stepwise multivariate logistic regression (LR) method was used to obtain the model.
The screening tool was validated using the area under the ROC curve (AUC), sensitiv-
ity (Se), specificity (Sp), negative (NPV) and positive (PPV) predictive value.
The agreement between the SPENS and subjective malnutritional risk assessment
was determined by Kappa (κ) value. κ values were rated with the proposed classification
system by Landish and Koch [63]. Se and Sp values were rated as suggested by Bokhorst-de
van der Schueren et al. [64] and Klanjsek et al. [7]. The level of statistical significance was
set at p < 0.05.

2.7. Ethical Considerations

Ethical approval was obtained from the Commission of the Republic of Slovenia for
Medical Ethics (approval number 0120-329/2016-3 KME 40/07/1). Site-specific approval
was obtained for the involved hospital. All participants were recruited after receiving
written information and a verbal explanation of the study and obtaining written consent
from parents.

3. Results
3.1. Characteristic of Children in Development and Validation Phase
Between 25 May to 21 July 2021 and 1 September to 16 October 2021, 550 paediatric
and surgery children were admitted to the hospital; 180 children (32.7%) were successfully
included in the study; 86 (47.8%) were male and 94 (52.2%) females. Median chronological
age of our group (n = 180) was 120.62 (108, 142) months, with minimum 1 month and
maximum 216 months. The median age of children in SPENS development study was
123 (93, 138) months and in SPENS validation study was 143 (113, 169) months. Children
came from a variety of six medical wards. A total of 142 children were included in the devel-
opment phase and 38 in the validation phase. Sample characterization of the development
and validation phase is shown in Supplementary Materials S4.

3.2. Prevalence of Malnutrition of Children in Development and Validation Phase

Prevalence in most of the malnutrition classifications has not varied considerably
between the cohorts of children recruited for the development and validation phase (see
Supplementary Materials S4). Prevalence of malnutrition was 40% in the whole sample
(40.1% in the development and 39.4% in the validation phase) according to the ASPEN and
Academy of Nutrition and Dietetics and 38.4% on the whole sample (38% in development
and 39.5% in evaluation phase) according to the subjective malnutritional risk assessment.

3.3. Development Phase

Structured questionnaire (n = 277 variables) responses were compared with the classifi-
cation of nutritional status by a subjective malnutritional risk assessment using chi-squared
Children 2022, 9, 731 7 of 16

tests (not shown); this analysis identified 144 significant variables related to malnutritional
risk. Additionally, the 144 variables were reduced to 30 most important variables which
had Mean Decrease Accuracy > 2. These variables were then used in multivariate logistic
regression (LR) analysis. The optimal NST, which includes only four variables is presented
in Table 1.

Table 1. Variables included in the SPENS.

Standard Odds Ratio

. Variables Coefficient Z Score p
Error (95% CI)
(Intercept) −3.6347 0.6128 5.931 <0.001
Loss of subcutaneous fat determined by
physical examination under the 12.795
1 2.5491 0.6598 3.864 <0.001 ***
eyes—(hollowed look, depression and/or (3.695, 50.517)
dark circles) [42].
Loss of subcutaneous fat determined by
physical examination: Ribs, lower back,
11.004
2 sides of trunk—Ribs obvious, but 2.3982 0.6026 3.980 <0.001 ***
(3.522, 38.713)
indentations are not marked. Iliac Crest is
somewhat prominent [42].
Refusal/rejection of food is present 11.761
3 2.4648 0.7031 3.506 <0.001 ***
[65–68]. (3.193, 52.357)
Has a child had poor weight gain over the 3.598
4 1.2805 0.5895 2.172 0.030 *
last few months [38]. (1.135, 11.752)
p: statistical significance; * p < 0.05; *** p < 0.001.

The first two variables include physical examination focused on signs of malnutrition,
the third variable includes the child’s rejection of food, and the last one poor weight
gain. The first two variables were obtained from the Subjective Global Assessment (SGA)
screening tool [42,69]. Variable 3 was identified through an extensive review of the literature
and by the inductive generation of categories. Last variable was obtained from Paediatric
Nutrition Screening Tool (PNST) [38]. The AUC of SPENS is 0.977 (0.922, 1), Se = 93.3% and
Sp = 91.3% with the chosen cut-off value 0.382.

3.4. Validation Phase

3.4.1. Criterion Validity
The SPENS was tested on 38 children. It has shown a very good performance (Table 2).
Among 15 (39.47%) children who were at risk of malnutrition based on the subjective
malnutritional risk assessment, 14 (36.8%) children were classified as at risk of malnutrition
with SPENS. Among 23 (60.53%) children who were not at risk of malnutrition based on
the subjective malnutritional risk assessment, 21 (55.26%) children were classified as not
at risk of malnutrition with SPENS. The AUC on the evaluation set was 0.977 (0.922, 1),
with a sensitivity of 93.3% and a specificity of 91.3%. The developed tool also boasts
high positive and negative predictive value (PPV = 87.5%, NPV = 95.5%); furthermore,
high agreement between the SPENS and predictions with subjective malnutritional risk
assessment (κ = 0.837 (0.659, 1.014)) indicates good reliability.
Children 2022, 9, 731 8 of 16

Table 2. Validation of SPENS with the subjective malnutritional risk assessment.

Subjective Malnutritional SPENS

Risk Assessment Not At-Risk At Risk Total (n)
Not at-risk 21 2 23
At risk 1 14 15
Total (n) 22 16 38
κ value (95% CI) 0.837 (0.659, 1.014)
AUC (95% CI) 0.977 (0.922, 1)
Sensitivity (%) 93.3
Specificity (%) 91.3
PPV (%) 87.5
NPV (%) 95.5
κ: Kappa value, AUC: Area under the ROC curve, NPV: Negative predictive value, PPV: Positive predictive value,
SPENS: Simple PEdiatric Nutritional risk Screening tool, n: number, CI: Confident interval, %: percent.

3.4.2. Concurrent Validity

When comparing the SPENS with SGNA assessment as reference method, SPENS had
a sensitivity of 92.9% and a specificity of 87.5%. The agreement between these two tools
was substantial (κ = 0.78 (0.58, 0.98)). When comparing SPENS with ASPEN as a reference
method, SPENS had a sensitivity of 86.7% and a specificity of 87.0%. The agreement of
these two tools was substantial (κ = 0.728 (0.474, 0.895)) (Table 3).

Table 3. Comparison of the developed screening tool with the other published criteria.

ASPEN and Academy of Nutrition and

Developed SGNA Assessment
Dietetics Assessment
Screening Tool
Not At-Risk At Risk Total (n) Not At-Risk At Risk Total (n)
Not at-risk 21 1 22 20 02 22
At risk 3 13 16 3 13 16
Total (n) 24 14 38 23 15 38
κ value (95% CI) 0.78 (0.58, 0.98) 0.728 (0.474, 0.895)
AUC (95% CI) 0.912 (0.799, 1) 0.868 (0.739, 0.997)
Sensitivity (%) 92.9 86.7
Specificity (%) 87.5 87.0
PPV (%) 81.3 81.3
NPV (%) 95.5 90.9
κ: Kappa value, AUC: Area under the ROC curve, NPV: Negative predictive value, PPV: Positive predictive value,
ASPEN: American Society for Parenteral and Enteral Nutrition, n: number, CI: Confident interval, %: percent.

4. Discussion
The malnutrition prevalence of hospitalised children in this study was 38.4% which
is still within the reported range 10.4% to 52.7% of malnutrition in previous studies [6,7].
Child malnutrition is common at hospitalization and may worsen during hospitalization or
may be developed a new [6]. Although malnutrition acquired during hospitalization has
been shown to be associated with poorer clinical outcomes, longer hospitalizations, and con-
sequently higher treatment costs, it is still underestimated and often unrecognised [70,71].
The SPENS represents the first paediatric NST developed and validated for hospi-
talised children in Slovenia. The results of this study revealed that the developed tool
is reliable for the early detection of malnutrition risk among hospitalised children aged
1 month to 18 years, regardless of the child’s diagnosis and the purpose of hospitalization.
We found that the physical examination of potential visible signs of loss of subcu-
taneous fat in the face and chest, the child’s refusal/rejection of food, and poor weight
gain in the last few months were the most important nutrition risk factor. These four vari-
ables included in the SPENS were obtained from initially 277 variables included in the
questionnaire through the complex analyzing process in the development phase.
Weight loss in children is shown to be accompanied by a decrease in muscle and
fat mass [39,72]. Only four existing screening [23,42,51,69] and one assessment [29] tool
Children 2022, 9, 731 9 of 16

includes the assessment of muscle/fat loss in children as an indicator of malnutrition.

Physical examination to determine loss of muscle and/or fat mass in children is considered
in the literature to be an “overly subjective” indicator [73]; however, physical contact with
child’s muscles, bones, and fat provides substantial empirical evidence of malnutrition
that is probably more “objective” than asking parents to report exactly what the weight or
height of their child is [74]. In practice, both a comprehensive physical examination and an
inquiry of food intake are invaluable in diagnosing malnutrition in children [58,75].
Children may have poor eating habits that may continue during formal health educa-
tion after the age of 18 years [76]. Poor food intake should be associated with fat and/or
muscle loss, weight loss, poor body growth and other symptoms [33]. Poor food intake
for two to three days can lead to malnutrition in at-risk children, in contrast to well-fed
children without disease or other complex medical conditions [73]. We have found that
existing NSTs often include nutrition-related issues [22–24,36–38,40–43,48,49,52,53,69].
In our developed tool, we ask about poor weight gain over the last few months [38],
similar to other NSTs which ask parents for subjective opinion of weight gain such as poor
or minimal weight gain in child [23,48]. Other published paediatric NSTs often include
anthropometric measurements of body weight [24,37,40,44,45] and height [24,40,44,45] for
later use of reference curves or growth tables [24,37,40]. Anthropometric measurements
have been found to be routinely poorly performed in hospitals at the time of admission [24].
Existing paediatric NSTs also include ideal body weight [44,45], net weight change [47,50],
percentage of weight loss [39,42,49,53,69] and BMI calculation [22,40,47,48,53]. For these
measurements and calculations, screening performers need prior education [22], train-
ing [24], additional equipment [39], and the final assessment of screening is also influenced
by the experience and qualifications of the performer [77]. Due to the above, we have
purposely developed a tool that does not include the necessary additional anthropometric
measurements and calculations.
In the absence of a gold standard for the assessment of the nutritional status in
hospitalised children, subjective malnutritional risk assessment by physician was used
as the criterion for developed NST and for the evaluation of its validity [7,40,43]. It has
been assumed that a subjective malnutritional risk assessment by a physician is most
likely to be accurate, reflecting additional knowledge. The subjective malnutritional risk
assessment has also been used as a reference standard in previous studies [24,78]; however,
the use of other existing screening or assessment nutritional tools as a reference standard
for determining the nutritional status or risk of malnutrition in hospitalised children is not
recommended [7].
Measured properties that are important for the usability of a new screening tool in-
clude at least the results of sensitivity, specificity, positive and negative predictive values,
reliability, and validity [7,54]. For the tool to be truly effective, it should identify those
individuals who are really at risk, so the measured values of sensitivity, specificity, and
predictive values should be high [21,26,54,79–82]. Our study demonstrates a strong validity
of SPENS, with the ROC analysis indicating the validity of the tool to be excellent when
assessed against subjective malnutritional risk assessment. Sensitivity, specificity, positive
and negative predictive value of SPENS were 93.3%, 91.3%, 87.5% and 95.5%, respectively.
Lu et al. [40] explained that NSTs should have a high sensitivity to minimize the number of
false-negative results [82]. Further, sensitivity is more important than specificity, because
a false-positive result will only subject the patient to a detailed nutritional assessment,
whereas a false negative result can result in an undetected condition [78]. A highly sen-
sitive test is clinically important when identifying a serious but treatable condition like
malnutrition, with the main purpose of an NST being to minimize subjects who are at
risk of malnutrition being overlooked and not referred for nutritional assessment and
intervention [43]; therefore, based on the results, the SPENS is a very reliable NST. As
reported in a comprehensive systematic review of 26 validation studies [7], the sensitivity
of the tools ranged from 15% to 100% and the specificity ranged between 0% and 96.54%.
The use of different reference standards could be the reason for differences among the
Children 2022, 9, 731 10 of 16

studies [7,21,26,40,79,81]. Due to the heterogeneity of reference standards, and different

limit values, it is almost impossible to compare different NSTs with each other and conclude
which is the best [7]; moreover, comparing the relative advantages of different NSTs is
misleading, as different tools have been designed for different diagnostic and/or prognostic
purposes [83].
Completion of SGNA is lengthy and time-consuming. SGNA is classified as a nutri-
tional assessment aid form and not as an NST, it detects children with already developed
malnutrition more than children at risk of malnutrition [81]; nevertheless, many NSTs have
been validated with SGNA. In the study of White et al. [38] the sensitivity and specificity
for the PNST compared with the paediatric SGNA were fair [7], scoring 77.8% and 82.1%, re-
spectively. The sensitivity and specificity for the SGNA compared with the WHO and CDC
2000 criteria were fair (BMI: Se = 96.5%, Sp = 72.5%; WFA: Se = 85.7%, Sp = 69.7%) or poor
(HFA: Se = 46.2%, Sp = 66.5%) [7,38]. SGNA were relatively poor at detecting patients who
were stunted or overweight, with a sensitivity and specificity < 67%. Gerasimidis et al. [84]
compared STAMP, PYMS, and SGNA to a full dietetic assessment. They found that SGNA
poorly identified malnourished children (Se = 15%, Sp = 100%). The agreement between the
SGNA and the PYMS were slight (κ = 0.12; 95% CI −0.11, −0.34) and agreement between
the SGNA and dietetic assessment were fair (κ = 0.24; 95% CI 0.10, 0.50) [84]. In other
studies, SGNA has also been used as a reference standard for the nutritional status of
hospitalised children [38,43], which is not recommended [7]. The sensitivity and specificity
of the SPENS when compared to SGNA was good (Se = 92.9%, Sp = 87.5%).
Sequential sampling should be used to avoid bias and to make the screening tool
suitable for all clinical features and age groups of children [7]. Therefore, we also used
sequential sampling in this study. The number of children involved in research for the
development and/or validating of NSTs is like other studies [24,41,43,48,49,53].
In some cases, screening performers report that NSTs are time-consuming [40,85], im-
practical for use in all hospitalised children, and would increase daily workload [86]. More
often, it is reported that NSTs are fast [24,37,38,43,50,53] and simple [24,38,43,48,50,52,53].
The results of the screening with developed SPENS are obtained by a quick physical ex-
amination of the child and two simple questions that each parent and/or the child knows
how to answer; it does not include anthropometric measurements, the use of tables, other
necessary calculations, and invasive interventions like the PNST [38] and Nutrition screen-
ing tool for childhood cancer (SCAN) [43]. Due to the above, the implementation of our
tool should not represent time complications even in the continuous work of health care
providers. Compared with Pediatric Nutritional Screening Score (PNSS), STAMP, St An-
drews Healthcare Nutrition Screening Instrument (SANSI), Patient-Generated Subjective
Global Assessment of nutritional status (PG-SGA), Clinical Assessment of Nutritional Sta-
tus and the Score (CANSCORE) and SGNA, which are time-consuming [40,81,85], SPENS
was efficient, fast (approx. 1–2 min), simple, easy, and practical to use. Screening with
PNSS, SANSI and PG-SGA tools took 10 min to complete [40,46,53], while STAMP was
completed in 10 to 15 min [79]. PNSS and STAMP require the interpretation of growth
charts, SANSI and PG-SGA require prior weight knowledge and BMI and/or weight
loss/change calculations and CANSCORE is a scoring system based on nine ‘superficial’
readily detectable signs of malnutrition [51].
An important part of the limitations in the development of tools is the level of reading
comprehension, ambiguity, jargon, positive and negative text, and words that each per-
former can interpret in their own way [54]. In the SPENS, the first two questions contain a
concrete descriptive explanation of what child’s body part should look like for the screening
performer to confirm the answer as positive.
Similarly to the Pediatric Digital Scaled MAlnutrition Risk screening Tool (PeDiS-
MART) [37], SPENS can be integrated into an existing computer program at the clinic,
which employees already used to manage the treatment and care interventions of hospi-
talised children; this would allow for a quick calculation, ease of use and time savings for
the final screening result.
Children 2022, 9, 731 11 of 16

Due to the simplicity of the SPENS, we believe that the screening performer does not
need prior education or training like in the case of the NST PYMS [22,84], STAMP [24],
PeDiSMART [37] or SANSI [53]. To overcome the usual barrier to performing screening in
a clinical setting, it is important that the introduction of NSTs into the clinical setting does
not require special training on its use and interpretation, and that its completion does not
take much time [43].
According to ASPEN’s four principles, NSTs should include at least the first three [87].
The SPENS does include the first three principles, but not the fourth principle related
to “Disease severity”. The latter is also not included in CANSCORE [51], SANSI [53],
PNST [38], Paediatric Nutrition Rescreening Tool (PNRT) [41], Infant Early Nutrition
Warning Score (iNEWS) [52] and two NSTs designed for children with cystic fibrosis [47,48].
We suggest that the nutritional screening with the SPENS is performed directly at
admission or in the first 24 hours after the child is admitted and is repeated weekly
during the child’s hospitalization. Other authors of NSTs similarly define the time of
screening [22,23,37,38,40,43,49,50,53]. Continuous nutritional screening of the child during
hospitalization helps to identify those whose nutritional status is deteriorating [33].
First, the main limitation of this exploratory study is the relatively small sample.
During the SARS-CoV-2 pandemic, the number of hospitalizations was lower, researchers’
access to the clinic was reduced due to measures, and some parents refused to participate
due to fear of COVID-19 infection.
Second, the inter-rater reliability of the tool in yielding the same patients by different
assessors was not assessed. And the intra-rater reliability of the tool in the same patients
by the same assessor on two occasions (within 24 h period) also was not assessed. Due
to SARS-CoV-2 pandemic, restricted measures at the clinic and staffs work overload also
produced some limitations. Further studies will focus on the inter and intra-rater reliability,
validity, and effectiveness of SPENS in larger number of hospitalised children.
Last, our study was a single-centre case study. A multicentre prospective cohort study
would allow the cross-validation of the developed tool in a more diverse demographic.
According to the recommendations [7], the published NSTs are not completely valid,
reliable, useful, and acceptable for patients and screening providers. Further research is
needed to confirm the applicability of each existing screening tool in the clinical setting [7,81]
while further research, refinement and development of the tools are needed.

5. Conclusions
The results of our study justify the introduction of screening to determine the risk of
malnutrition in hospitalised children in regular clinical practice. The SPENSs validation
results are very high, which means that only a few more steps of modification (integration
into the clinic’s computer program) would be needed to get the tool ready for routine use
in the clinical setting. SPENS is simple, fast, easy, and practical to use; it can be performed
by nurses, physicians, and dieticians without special training, and does not require any
anthropometric measurements and is not specific for any disease and age of a child. SPENS
also includes the first three ASPEN’s principles.
Children 2022, 9, 731 12 of 16

Supplementary Materials: The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/children9050731/s1, Supplementary Material S1: Inclusion and
exclusion criteria; Supplementary Material S2: Questionnaire’s content sets; Supplementary Material
S3: Indicators of malnutritional status using anthropometric measures; Supplementary Material S4:
Characterization of the study sample.
Author Contributions: Conceptualization, P.K., M.P., N.M.V. and P.P.B.; methodology, P.K., M.P.,
N.M.V. and P.P.B.; software, P.K. and P.P.B.; validation, P.K. and P.P.B.; formal analysis, P.K and P.P.B.;
investigation, P.K., N.M.V., M.M. and S.G.J.; resources, P.K., N.M.V., M.M. and S.G.J.; data curation,
P.K. and P.P.B.; writing—original draft preparation P.K. and P.P.B.; writing—review and editing, P.K.,
M.P., N.M.V., M.M., S.G.J. and P.P.B.; visualization, P.K. and P.P.B.; supervision, M.P., N.M.V. and
P.P.B.; project administration, P.K., M.P., N.M.V. and P.P.B. All authors have read and agreed to the
published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: The study was carried out in a qualified institution and was
conducted in accordance with the provisions of the Declaration of Helsinki, the Oviedo Convention,
and the principles of the Slovenian Code of Medical Deontology. Ethical approval was obtained from
the Commission of the republic of Slovenia for Medical ethics (approval number 0120-329/2016-3
KME 40/07/1, date of approval 7 September 2016). Site-specific approval was obtained for the
involved hospital.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the
study. Written informed consent has been obtained from the patient(s) to publish this paper.
Data Availability Statement: The data supporting this study’s findings are available from the
corresponding author upon reasonable request.
Acknowledgments: The authors would like to thank all the participant children and their parents,
and the health staff and to the management of the paediatric clinic for their cooperation in this study.
Conflicts of Interest: The authors declare no conflict of interest.

Abbreviations

ASPEN American Society for Parenteral and Enteral Nutrition

ESPHAGAN European Society for Paediatric Gastroenterology, Hepatology and Nutrition
WHO World Health Organization
CDC Centres for Disease Control and Prevention
BMI Body Mass Index
MUAC Mid Upper Arm Circumference
WFH/L Weight-for-height/length
HFA Height-for-age
AUC Area under the ROC curve
Se Sensitivity
Sp Specificity
NPV Negative predictive value
PPV Positive predictive value
SGNA Subjective Global Nutritional Assessment
SGA Subjective Global Assessment
PNST Paediatric Nutrition Screening Tool
STAMP Screening Tool for the Assessment of Malnutrition in Paediatrics
PYMS Paediatric Yorkhill Malnutrition Score
SCAN Nutrition Screening tool for childhood Cancer
PNSS Pediatric Nutritional Screening Score
SANSI St Andrews Healthcare Nutrition Screening Instrument
PG-SGA Patient-Generated Subjective Global Assessment of nutritional status
CANSCORE Clinical Assessment of Nutritional Status and the Score
PeDiSMART Pediatric Digital Scaled MAlnutrition Risk screening Tool
PNRT Paediatric Nutrition Rescreening Tool
Children 2022, 9, 731 13 of 16

iNEWS Infant Early Nutrition Warning Score

SPENS Simple PEdiatric Nutritional risk Screening tool

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