Clinical Nutrition ESPEN 61 (2024) 46e51

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Clinical Nutrition ESPEN

journal homepage: http://www.clinicalnutritionespen.com

Original article

Malnutrition screening tool and nutritional screening tool for

classification of nutritional risk in patients with cancer upon hospital
admission: Comparison of diagnostic performance using Global
Leadership Initiative on malnutrition criteria as reference
Ricardo Alfonso Mercha
n-Chaverra a, b, c, e, *, Daniela Alejandra Acero-Alfonso a, d,
Yeny Marjorie Cuellar-Fernandez a, b, c, Jorge Medina-Parra b, Patricia Savino Lloreda c
a
Grupo de Investigacio
n de Nutricio

n Clínica y Rehabilitacio

n, Fundacio
n Universitaria Sanitas, Clínicas Colsanitas, Grupo Keralty, Bogota
, Colombia
b
Facultad de Medicina, Fundacio
n Universitaria Sanitas, Bogota
, Colombia
c
Centro Latinoamericano de Nutricio
n (CELAN), Chía (Cundinamarca), Colombia
d
Clínica Universitaria Colombia, Clínicas Colsanitas, Grupo Keralty, Bogota
, Colombia
e
Vicepresidencia de innovacio
n y Desarrollo Científico, Clínica Infantil Santa María del Lago, Clínica Reina Sofía Pedia
trica y Mujer, Clínicas Colsanitas,
Grupo Keralty, Bogota
, Colombia

a r t i c l e i n f o s u m m a r y

Article history: Background & aims: Tools for screening of nutrition risk in patients with cancer are usually validated
Received 15 August 2023 against other screening instruments. Here with the performance of Malnutrition Screening Tool (MST)
Accepted 24 February 2024 and Nutritional Screening Tool (NUTRISCORE) to identify the risk of malnutrition was assessed. A full
nutritional evaluation and diagnosis following criteria from the Global Leadership Initiative of Malnu-
Keywords: trition (GLIM) was the reference standard for the classification of malnutrition.
Nutrition assessment
Methods: Diagnostic test prospective analysis of adult patients with a confirmed diagnosis of cancer.
Malnutrition
MST, NUTRISCORE and nutritional evaluation and diagnosis by GLIM criteria were independently per-
Neoplasm
formed within 24 h of admission to a 4th tier hospital in Bogota
, Colombia.
Sensitivity and specificity
ROC Results: From 439 patients the sensitivity and specificity of MST was 75% and 94% and of NUTRISCORE
45% and 97% respectively. The area under receiver operating characteristic (ROC) curves were 0.90 for
MST and 0.85 for NUTRISCORE (p ¼ 0.003).
Conclusion: The MST showed a significantly better diagnostic performance over NUTRISCORE for
detection of malnutrition risk at admission to hospital of patients with cancer.
© 2024 The Author(s). Published by Elsevier Ltd on behalf of European Society for Clinical Nutrition and
Metabolism. This is an open access article under the CC BY license (http://creativecommons.org/licenses/
by/4.0/).

1. Introduction A considerable number of instruments are available for

Malnutrition is present in 20e40% of patients at diagnosis of
cancer [1] and in 70e80% of cases with advanced stages [2]. Loss of
skeletal and cardiac muscle mass and cachexia are common in
patients with cancer, which may bear weight on treatment-related
toxicity, surgical complications, survival and quality of life [2]. Early
detection of malnutrition can therefore have a substantial influence
on clinical outcomes.

, Colombia.
* Corresponding author. Ac. 100 #11b-67, Bogota
E-mail address: ricardomc9275@gmail.com (R.A. Mercha
n-Chaverra).
screening of nutritional risk in different patient populations [3]. The
Nutritional Risk Screening 2002 (NRS-2002) [4] instrument and
MST [5] are commonly used for screening of hospitalized patients,
the Malnutrition Universal Screening Tool (MUST) [6] was created
for screening in all care settings, the Mini Nutritional Assessment
(MNA) is intended for geriatric inpatients, and NUTRISCORE was
recently developed to screen patients with cancer as outpatients
[7]. Nutritional status has been assessed with the Patient Generated
Subjective Global Assessment (PG-SGA) [8] or with GLIM criteria
that focuses on diagnosis of malnutrition in clinical settings [9].
The purpose of this study was to compare the performance of
MST with NUTRISCORE to detect nutritional risk of patients with
cancer upon admission to hospital and use as reference standard a

https://doi.org/10.1016/j.clnesp.2024.02.029
2405-4577/© 2024 The Author(s). Published by Elsevier Ltd on behalf of European Society for Clinical Nutrition and Metabolism. This is an open access article under the CC BY
license (http://creativecommons.org/licenses/by/4.0/).

n-Chaverra, D.A. Acero-Alfonso, Y.M. Cuellar-Fernandez et al.
R.A. Mercha
full evaluation of the nutritional status with diagnosis of malnu-
trition following GLIM criteria, thereby providing objective com-
ponents for the classification of malnutrition.
2. Material & methods
Diagnostic test prospective study of adult patients diagnosed
with cancer and admitted to a 4th level hospital in Bogota
,
Colombia. Inclusion criteria were 18 years of age or older, any sex
or gender, admitted for any reason related to the confirmed cancer
diagnosis and with a hospital stay less than 24 h. Patients were
excluded if prescribed pre-surgical immuno-nutrition, showed
difficulty in standing, had neurocognitive impairment, were in
intensive care, or at end of life. Sample size was estimated ac-
cording to Hajian-Tilaki et al. [10] with a sensitivity of 97% based
on Kondrup et al. [4]. Assuming 80% power, 437 patients were
required to detect an expected difference of 2% with 95% confi-
dence. Sampling was consecutive for eligible patients until the
sample size was reached. STARD criteria were followed to report
results [11].
2.1. Test implementation
Tests were conducted independently by 4 nutritionists all with
at least 4 years’ experience and level 1 certification from the
Fig. 1. Recruitment, screening, and nutritional evaluation and diagnosis process.
47
Clinical Nutrition ESPEN 61 (2024) 46e51
International Society for the Advancement of Kynanthropometry
(ISAK). Tests were conducted blind to the results of the other
evaluators and all tests were performed within a maximum of 8 h.
Evaluator one recruited patients. Evaluator 2 applied NUTRISCORE,
evaluator 3 the MST, and evaluator 4 assessed nutritional status and
diagnosed malnutrition following GLIM criteria (Fig. 1).
MST includes 2 components: involuntary loss of weight within
the last six months and loss of appetite in the last week. A score of 2
or more indicates risk of malnutrition [5].
NUTRISCORE includes 4 components: involuntary weight loss
within the last 3 months, loss of appetite in the last week, tumour
location and the relationship with low/medium/high risk of
malnutrition, and type of antineoplastic treatment. A score of 5 or
more indicates nutritional risk [7].
Nutritional status includes 6 components based on the recom-
mendations by the Academy of Nutrition and Dietetics [12]: clinical
history and diagnosis, physical examination, anthropometry,
functionality, food history, and biochemical parameters. GLIM
criteria [9] were used to establish a diagnosis of malnutrition;
aetiologic criteria included reduced alimentary ingestion or
nutrient assimilation issues, and phenotypic criteria included low
BMI, percentage weight loss, and reduced muscle mass, the latter
assessed by calf perimeter NHANES III [13] cut-offs and a physical
exam centered on muscle mass deficit [12]. Nutritional diagnosis by
GLIM requires presence of at least one aetiologic and one

n-Chaverra, D.A. Acero-Alfonso, Y.M. Cuellar-Fernandez et al.
R.A. Mercha
phenotypic criteria and severity of malnutrition classified by
phenotypic criteria [9].
2.2. Statistical analyses
Analyses were conducted in STATA 15 licensed to the Sanitas
University Foundation. Social and clinical demography were ob-
tained. Quantitative variables were expressed with units of central
tendency and dispersion depending on the normality of distribu-
tion assessed by the ShapiroeWilk test. A p value < 0.05 indicated
statistical significance. Categorical variables were presented as
absolute and relative frequencies. Agreement between the two
index tests (MST and NUTRISCORE) to classify malnutrition risk,
versus no risk, were assessed by Kappa coefficients with no, low,
moderate, substantial, and high levels of agreement indicated by
coefficient values < 0, 0e0.4, 0.41e0.6, 0.61e0.8, >0.81,
respectively.
To assess the operating characteristic of MST and NUTRISCORE
relative to nutritional assessment with diagnosis by GLIM criteria
the sensitivity, specificity, positive and negative likelihood ratios,
and accuracy were estimated for each test score. Sensitivity and
specificity of 80% and above were considered adequate [14] for
identification of nutritional risk (good validity). Sensitivity and
specificity <80% but both >50% indicated acceptable validity and
<50% poor validity. A likelihood ratio (LR) > 1 indicates an associ-
ation with malnutrition, with positive LR > 10 and negative LR < 0.1
signaling a relevant change in pretest probabilities [15,16]. The
areas under the MST and NUTRISCORE curves were compared with
a non-parametric test under the null hypothesis that the curves
were equal.
The study had the approval of the research ethics committee of
the Sanitas University Foundation (CEIFUS 192e19) and all patients
Fig. 2. Flow of participants through the study. The reference standard was an evaluation of nutritional status with final diagnosis of malnutrition by GLIM criteria.
48
Clinical Nutrition ESPEN 61 (2024) 46e51
gave an informed consent. Access to the study protocol is available
upon request.
3. Results
From 498 eligible patients 439 were included and 59 decided
not to participate (Fig. 2). The median (standard deviation, SD) age
at nutritional assessment was 58 [22] years and 52% of patients
were female. The mean body mass index was 24 kg/m2. Seventy-
one percent of the patients came from urban dwellings, 72% had
had high school education, and 64% came from a low-income
background (Table 1).
Most patients (73%) presented with solid tumours and 29% an
advanced stage 4 cancer. The most prevalent neoplasias were
gastrointestinal (20%), lymphoma (19%), and gynaecologic tumours
(11%). Forty-four percent of patients were receiving chemotherapy
alone, 51% were receiving palliative care for symptom management
or receiving treatment other than chemo- or radiotherapy, and 5%
were being treated by radiotherapy with or without chemotherapy
(Table 1).
Nutritional status evaluation and diagnosis by GLIM criteria
showed the prevalence of malnutrition was 52% (30% severe and
22% moderate). The MST and NUTRISCORE tests showed 78%
(moderate) agreement in classifying the risk of malnutrition (Ex-
pected agreement: 54%, Kappa: 0.52, 95%CI: 0.45e0.6, Standard
error: 0.04). There were no adverse events reported from imple-
mentation of reference or index tests.
The prevalence of risk of malnutrition defined by an MST score
of 2 was 42%. Sensitivity and specificity for this score were 75% and
94% (corresponding to an acceptable test validity) respectively with
positive and negative likelihood ratios (LR) of 12.98 and 0.27
respectively (Table 2).

n-Chaverra, D.A. Acero-Alfonso, Y.M. Cuellar-Fernandez et al.
R.A. Mercha Clinical Nutrition ESPEN 61 (2024) 46e51

Table 1 GLIM criteria as the standard to identify malnutrition in patients

Summary of patients characteristics. with cancer admitted to hospital. The analyses were prompted by
Social demography the report from Arribas et al. [7] that showed NUTRISCORE was a
Variables n (% o ± DS)
novel, highly accurate and easy to use tool to detect nutritional risk
in patients with cancer in an ambulatory setting. To the best of the
Age (median) 58 ± 22
authors’ knowledge this is the first study to assess NUTRISCORE
Body mass index (kg/m2) 24 ± 4
Sex performance in a hospital setting.
Female 228 (52) Screening tools must have a high sensitivity to correctly classify
Male 211 (48) healthy from non-healthy and reduce the rate of false positives and
Origin
false negatives [14]. The present analysis has shown a better diag-
Rural 129 (29)
Urban 310 (71) nostic performance of MST relative to NUTRISCORE with sensitiv-
Education ities of 75% and 45%, specificities of 94% and 97%, and areas under
None 9 (2) the ROC curve of 0.9 and 0.85 (p ¼ 0.003) respectively. The results
Primary 107 (24) are in contrast with the “NUTRISCORE: A new nutritional screening
High School 122 (28)
tool for oncological outpatients” report by Arribas et al. [7] in which
Technical 70 (16)
University or postgraduate 131 (30) the PG-SGA tool was the gold standard and showed MST and
Income NUTRISCORE sensitivities of 84% and 97%, and specificities of 86%
Low 132 (30) and 96% respectively. These differences in performance between
Mid low 280 (64)
the two studies are likely due to the use of the different gold
Mid high 22 (5)
High 5 (1)
standards and patient population settings.
Clinical The prevalence of the risk of malnutrition was 42% with MST and
Cancer stage 26% with NUTRISCORE. Both tests appraise recent loss of appetite
I 44 (10) and involuntary weight loss, given that reduced appetite and food
II 57 (13)
intake are important determinants of weight reduction [17].
III 93 (21)
IV 125 (29) Involuntary weight loss can be an early sign of cancer and is a
Hematologic 120 (27) marker of disease-related malnutrition that independently predicts
Cancer site survival [9,18].
Head and neck 49 (11)
There are differences between MST and NUTRISCORE that may
Gastrointestinal (stomach, colorectal, 85 (20)
pancreas, and biliary duct)
have relevance with regards to the diagnostic performance. MST
Abdomen and pelvis (kidney, bladder) 27 (6) asks for weight loss in the last 6 months whereas NUTRISCORE in
Gynaecologic 49 (11) the last 3 months. This may enhance the sensitivity of MST for the
Lymphoma 84 (19) diagnosis of nutritional risk. Another difference is the scales. MST
Leukaemia 46 (10)
goes from 0 to 5 with a score of 2 or more indicating nutritional risk
Breast 36 (8)
Prostate 32 (7) [5] whereas NUTRISCORE goes from 0 to 10, to accommodate the
Antineoplastic Treatment additional items on location and type of primary neoplasia and
Chemotherapy 188 (44) treatments received, with a score of 5 or more indicating nutri-
Radiotherapy 9 (2) tional risk [7]. Hence, a patient would be classified as having a
Chemotherapy and radiotherapy 13 (3)
Other, or exclusively symptom management 229 (51)
nutritional risk with MST if the patient is unsure of weight loss in
the last 6 months, but with NUTRISCORE 3 additional points from
the domain pertaining tumour location and treatment would be
needed to reach the cut-off for malnutrition risk. The higher diag-
For a NUTRISCORE of 5, which identifies nutritional risk, the nostic performance of MST may therefore be due to the more
prevalence of malnutrition risk was 26%. Sensitivity and specificity stringent cut-off. Indeed, NUTRISCORE showed a better diagnostic
were 45% and 97% respectively (corresponding to a poor test val- performance with a score cut-off of 3 (79% sensitivity, 76% speci-
idity) and the positive and negative LR were 15.46 and 0.57 ficity) compared with a score cut-off of 5 (45% sensitivity, 97%
respectively (Table 3). specificity). The low sensitivity of NUTRISCORE using a score cut-off
MST showed a significantly larger area under the curve of 0.9 of 5 was also found in a recent report that compared MST and
(95%CI:0.88e0.93) compared to NUTRISCORE with an area of 0.85 NUTRISCORE using the PG-SGA subjective tool as reference [19].
(95%CI:0.82e0.89) (p ¼ 0.003) (Fig. 3). The prevalence obtained with MST is comparable to previous
studies in patients with cancer and with different screening tools.
4. Discussion Fiol-Martínez et al. [20] reported a prevalence of nutritional risk of
41% in 63 cases with hematologic malignancy with MST. Tu et al. [21]
This study assessed the diagnostic performance of MST and found a prevalence of the risk of malnutrition of 36%, 44%, and 53%
NUTRISCORE using a full nutritional evaluation and diagnosis by with the SGA, MUST and Nutritional Risk Index (NRI) respectively in

Table 2
Operating characteristics of MST.

MST operating characteristics

Score n (%) Sensitivity Specificity Accuracy LRþ LR-

0 205 (47) 100 % 0% 53 % 1

1 49 (11) 88 % 86 % 87 % 6.12 0.14
2 71 (16) 75 % 94 % 84 % 12.98 0.27
3 62 (14) 48 % 98 % 72 % 24.77 0.53
4 36 (8) 22 % 100 % 59 % 45.92 0.78
5 16 (4) 6.9 % 100 % 51 % 0.93

49

n-Chaverra, D.A. Acero-Alfonso, Y.M. Cuellar-Fernandez et al.
R.A. Mercha Clinical Nutrition ESPEN 61 (2024) 46e51

Table 3
Operating characteristic of NUTRISCORE.

NUTRISCORE operating characteristic

Score n (%) Sensitivity Specificity Accuracy LRþ LR-

0 61 (14) 100 % 0.0 % 53 % 1

1 78 (18) 98 % 27 % 65 % 1.35 0.06
2 68 (15) 90 % 56 % 74 % 2.04 0.18
3 63 (14) 79 % 76 % 78 % 3.28 0.28
4 60 (13) 64 % 89 % 76 % 6.02 0.41
5 46 (10) 45 % 97 % 70 % 15.46 0.57
6 33 (7) 26 % 99 % 60 % 18.00 0.75
7 15 (4) 13 % 100 % 54 % 0.87
8 11 (4) 6.5 % 100 % 51 % 0.94
9 3 (1) 1.7 % 100 % 48 % 0.98
10 1 (0) 0.4 % 100 % 48 % 0.99

The strengths of the study are the large pre-specified sample

size, the choice of reference standard, and the blind comparison of
two index tests, both implemented within an 8-h window, which
add robustness to the ROC estimates. The various types and stages of
cancer diagnoses also provide a wide spectrum of the natural history
of the disease. However, this in turn limits the generalisability of the
results when screening for malnutrition in patients with specific
cancer types. Another limitation was that calf perimeters were not
adjusted by the body mass index which may have led to under-
diagnosis of malnutrition in patients with excess weight.
The implication for clinical practice is that the use of increas-
ingly more accurate tools to screen for nutritional risk enables
health care professionals to detect malnutrition early and rapidly.
Well-nourished patients are more likely to tolerate treatment or
heal faster which may have a considerable impact on cost-
effectiveness, and primordially, on quality of life and survival.

Fig. 3. Receiver operating characteristic (ROC) curves for MST and NUTRISCORE.
45 patients with colorectal cancer. In a larger study Zheng Feng et al.
showed in 875 hospitalized patients with gynaecological cancer a
prevalence of 55% using the Prognostic Nutritional Index (PNI) [22].
The use of subjective tools as the reference standard is a main
limitation of nutritional screening tool studies [7,19,21,23e26]. The
use of a full nutritional assessment and diagnosis following the
GLIM criteria as the gold standard affords objective components to
the classification of malnutrition. Notably Henriksen et al., in 2022
[8] used GLIM criteria to diagnose malnutrition in 426 patients after
surgery for colorectal cancer and reported MST sensitivity of 56%,
specificity of 89%, and prevalence of moderate and severe malnu-
trition of 36%. The current study followed a similar approach but
obtained sensitivity of 75%, specificity of 94%, and prevalence of
moderate and severe malnutrition of 53%. These differences are
likely due to the population characteristics of the studies. The
present analysis included various cancer types in hospitalized pa-
tients whereas Henriksen et al. only assessed patients with colo-
rectal cancer several months (mean of 5.5 months) after hospital
discharge, i.e. in an ambulatory setting.
Malnutrition is highly prevalent in patients with cancer ranging
from 20% to 70% and reaching 80% in advanced stages or in those
admitted to hospital, and 10%e20% of deaths are related to
malnutrition [27e30]. The Latin American Study of Malnutrition in
the Oncology Practice (LASOMO) showed a prevalence of moderate
and severe malnutrition of 59.1% using the SGA tool in 1842 pa-
tients from 52 hospitals in 10 countries [31]. In the present study
the prevalence of moderate and severe malnutrition in 439
patients with cancer from a single institution using the GLIM
criteria was 52%.
50
5. Conclusion
The study has shown a prevalence of malnutrition of 52% in
patients with cancer admitted to a 4th tier hospital in Bogota
Colombia. The MST showed better diagnostic performance than
NUTRISCORE to detect nutritional risk in a hospital setting using a
full nutritional evaluation with diagnosis by GLIM criteria as the
reference standard. Further research is needed with a larger sample
set to assess the performance of the screening tools in patients with
specific tumour types and stages and to adjust for comorbidities.
Funding
Colsanitas Clinics, Sanitas University Foundation, and Latin
American Center for Nutrition.
Author contribution
Mercha
n-Chaverra R.: conceptualization, methodology, investi-
gation, writing e review and editing, funding acquisition. Acero-
Alfonso D.: investigation, writing e original draft, visualization.
Cuellar-Ferna
ndez Y.: conceptualization, investigation, data cura-
tion, writing e review and editing, project administration, funding
acquisition. Medina-Parra J.: methodology, validation, formal
analysis, data curation, writing e review & editing. Savino Lloreda
P.: writing e review & editing, supervision, funding acquisition.
Declaration of competing interest
Mercha
n-Chaverra R, consultant and speaker for Boydorr
nutrition. Cuellar-Fern

andez Y, consultant and speaker for Boydorr
nutrition and Alpina. Savino Lloreda P, scientific advisor for Boydorr

n-Chaverra, D.A. Acero-Alfonso, Y.M. Cuellar-Fernandez et al.
R.A. Mercha
nutrition. Acero-Alfonso D and Medina-Parra J declare the have no
conflict of interest.
Acknowledgements
The authors wish to thank members of the department of
clinical nutrition of the Clínica Universitaria Colombia for help in
development of the project and active participation in patient
recruitment, and to Santiago Uribe Lewis and Jennifer Lewis Uribe
for editorial assistance.
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