2024 - Trujillo - Malnutrition Risk Screening in Adult Oncology Outpatients an ASPEN Systematic

DOI: 10.1002/jpen.
2688
CLINICAL GUIDELINES
Malnutrition risk screening in adult oncology outpatients: An

ASPEN systematic review and clinical recommendations
Elaine B. Trujillo MS, RDN1 | Kunal C. Kadakia MD2 |

Cynthia Thomson PhD, RDN3 | Fang Fang Zhang MD, PhD4 |
Alicia Livinski MA, MPH5 | Kim Pollard RN6 | Todd Mattox PharmD7 |
Anne Tucker PharmD8 | Valaree Williams MS, RDN9 | Declan Walsh MD2 |
10 11
Steven Clinton MD, PhD | Aaron Grossberg MD, PhD |
12
Gordon Jensen MD, PhD | Rhone Levin MEd, RDN13 |
14 15
Jeannine Mills MS, RDN | Anurag Singh MD | Meredith Smith RN16 |
Renee Stubbins PhD, RDN17 | Kathleen Wiley MSN, RN18 |
Kristen Sullivan MPH, MS19 | Mary Platek PhD, RDN15 | Colleen K. Spees PhD, RDN10
1
National Cancer Institute, National Institutes
of Health, Rockville, Maryland, USA Abstract
2
Atrium Health Levine Cancer Institute, Background: Malnutrition screening is not widely practiced in outpatient cancer
Charlotte, North Carolina, USA
centers. This review aims to determine the validity of malnutrition screening tools
3
University of Arizona, Tucson, Arizona, USA
4
and provide recommendations for clinical use.
Tufts University, Boston, Massachusetts, USA
5
Methods: Studies identified by a systematic review assessed the general validity
National Institutes of Health, Bethesda,
Maryland, USA of screening tools in adult oncology outpatients from five databases through
6
City of Hope, Chicago, Illinois, USA 2022. The American Society for Parenteral and Enteral Nutrition (ASPEN) con-
7
Moffitt Cancer Center, Tampa, Florida, USA vened a working group of members from the Academy of Nutrition and Dietetics,
8
MD Anderson Cancer Center, Houston, Academy of Oncology Nurse and Patient Navigators, American Cancer Society,
Texas, USA
9
American Society for Clinical Oncology, American Society for Nutrition, American
Memorial Sloan Kettering Cancer Center,
Middletown, New Jersey, USA Society for Radiation Oncology, Association of Cancer Care Centers, and
10
The Ohio State University, Columbus, Oncology Nursing Society to answer the following questions: (1) should clinicians
Ohio, USA
screen for malnutrition, (2) which malnutrition screening tools are recommended,
11
Oregon Health & Science University,
and (3) what are the clinical applications for malnutrition risk screening in adult
Portland, Oregon, USA
12
University of Vermont, Burlington,
oncology outpatients?
Vermont, USA Results: Twenty of 738 studies met the criteria and were reviewed. Six screening
13
Florida Cancer Specialists & Research tools with specific cut‐points demonstrated validity and are recommended,
Institute, Fort Myers, Florida, USA
14
including the Mini Nutritional Assessment (≤23.5), Malnutrition Screening Tool
Dartmouth‐Hitchcock, Lebanon,
New Hampshire, USA (MST; MST ≥ 2 and patient‐led MST ≥ 2), Malnutrition Universal Screening Tool
15
Roswell Park Comprehensive Cancer (MUST; MUST ≥ 1 and MUST ≥ 2), Nutrition Risk Screening‐2002 (NRS‐2002;
Center, Buffalo, New York, USA
This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2024 The Author(s). Journal of Parenteral and Enteral Nutrition published by Wiley Periodicals LLC on behalf of American Society for Parenteral and Enteral
Nutrition. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
874 | wileyonlinelibrary.com/journal/jpen J Parenter Enteral Nutr. 2024;48:874–894.

19412444, 2024, 8, Downloaded from https://aspenjournals.onlinelibrary.wiley.com/doi/10.1002/jpen.2688 by Readcube (Labtiva Inc.), Wiley Online Library on [02/12/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION | 875
16
Novan Health Cancer Institute,
Winston‐Salem, North Carolina, USA NRS‐2002 ≥ 2 and NRS‐2002 ≥ 3), NUTRISCORE ≥ 5, and Patient‐Generated
17
Houston Methodist Neal Cancer Center, Subjective Global Assessment Short Form (PG‐SGA SF; PG‐SGA SF ≥ 7 and
Houston, Texas, USA
PG‐SGA SF ≥ 8).
18
Oncology Nursing Society, Pittsburgh,
Conclusion: Six screening tools are valid for malnutrition risk identification in
Pennsylvania, USA
19 oncology ambulatory settings and recommended before treatment initiation
American Cancer Society, Atlanta,
Georgia, USA and regularly thereafter, depending on treatment course. Research is needed
to understand to what extent early diagnosis and management of malnutrition
Correspondence
Elaine B. Trujillo, MS, RDN, National Cancer improves the clinical care of oncology patients.
Institute, National Institutes of Health,
Rockville, MD, USA. KEYWORDS
Email: [email protected]
nutrition, nutrition assessment, oncology, research and diseases, weight loss
I NTR O D U C TI O N This paper has been approved by the ASPEN Board of Directors.
Malnutrition is present in 25% to 75% of patients with cancer,1–3

increasing treatment interruptions and toxicities, hospital admissions METHODS
and length of stay, and mortality.4 The Academy of Nutrition and
Dietetics (AND) and the American Society for Parenteral and Enteral A protocol for the systematic review on malnutrition screening tools
Nutrition (ASPEN) recommend the use of a single set of diagnostic used in oncology care was written a priori following the Preferred
criteria, including validated malnutrition screening tools to rapidly Reporting Items for Systematic Reviews and Meta‐Analyses Proto-
identify patients at risk.5 Yet in the United States, where 90% of cols (PRISMA‐P) checklist. The PRISMA checklist was used for re-
patients with cancer are treated in outpatient cancer centers, there is porting this review.9,10
a consistent lack of malnutrition screening. In a 2019 survey,
approximately half (53%) of all cancer centers implemented screen-
ing, with only 35% of those using validated screening tools.6 Con- Eligibility criteria
sequently, the actual incidence and risk prevalence of malnutrition in
outpatient environments remain uncertain. Thus, recommendations Prospective or retrospective quantitative studies, including random-
for malnutrition screening in outpatient cancer centers can better ized studies, cross‐sectional, case‐control, or cohort studies, or sys-
define malnutrition prevalence and impact on patients. tematic reviews or meta‐analyses, were eligible if they calculated the
Although several validated screening tools for the outpatient validity (eg, sensitivity, specificity, accuracy, and/or predictive value) of
oncology setting exist, there is no universally accepted approach or “gold malnutrition screening tools, also known as the index test, against a
standard” tool.7 Diagnosing malnutrition may involve simple assessments reference standard for adult (age ≥16 years) oncology outpatients. The
of appetite and unintentional weight loss, whereas more complex tools index test was defined as a malnutrition screening tool that included
measure anthropometric data and laboratory parameters.5 two or more indicators of malnutrition that generated a malnutrition
Malnutrition screening tools should be standardized, validated, risk score/rating. To be included, the index test had to be compared
and have low interrater variability and high reliability. They should be with at least one of the following four reference standards:
quick and easy to use in clinical practice, allowing for the identifica-
tion of at‐risk individuals and potentially leading to a detailed nutri- • Subjective Global Assessment (SGA).
tion assessment and treatment plan.7,8 • Patient‐Generated SGA (PG‐SGA).
This systematic review purported to assess the literature regarding • Global Leadership Initiative on Malnutrition (GLIM).
malnutrition screening tools to (1) determine the general validity of • The AND/ASPEN Indicators to Diagnose Malnutrition consensus
the tools in adult oncology outpatient settings and (2) evaluate statement recommendations meeting two of the following six
whether the general validity varied based on the characteristics of the characteristics: insufficient energy intake, weight loss, loss of
populations examined (age, cancer type, stage or treatment modality, muscle mass, loss of subcutaneous fat, localized or general fluid
current status, time from diagnosis, and weight status). The clinical accumulation, and diminished functional status as measured by
recommendations aimed to answer specific questions, including: (1) handgrip strength.
should clinicians screen for malnutrition in outpatient cancer centers,
(2) which screening tools are recommended in outpatient cancer Studies not available in English and conducted in nonoutpatient
centers, and (3) what are the clinical applications for malnutrition risk adult settings were excluded. Editorials, commentaries, conference
screening among adult oncology outpatients? abstracts or posters, case reports, case series, systematic reviews, or
876 | TRUJILLO ET AL.
meta‐analyses that included study designs that did not meet the resolved by a different reviewer. If data were missing, the corre-
inclusion criteria were ineligible. sponding author was contacted.
The following data were extracted from each included article:
first author's last name; publication year; study country; partici-
Information sources and search strategy pant's age and sex; sample size; when possible, cancer site and
stage and treatment status and modality; study design; screening
A National Institutes of Health biomedical librarian (A.L.) conducted tool used as the index test; reference standard used; sensitivity and
five citation and abstract database searches using the Cumulative specificity values; positive and negative predictive values; area‐
Index of Nursing and Allied Health Literature (CINAHL Plus; under‐the‐curve values; diagnostic odds ratios; positive and nega-
EBSCOhost), Cochrane Library Database of Systematic Reviews tive likelihood ratios; correlation coefficient; and any other relevant
(Wiley & Sons), Embase (Elsevier), PubMed/MEDLINE (US National statistical results.
Library of Medicine), and the Web of Science: Core Collection The values for sensitivity and specificity were interpreted as
(Clarivate Analytics). The searches were completed in March 2021 follows: a value >80% was good, 60% to 80% was fair, and <60%
and updated in June 2022. was poor.11 The score category for each screening tool used for
Each concept of interest (ie, malnutrition, cancer, and assess- classifying patients at risk was noted.
ment) included a combination of keywords and controlled vocabulary
terms (CINAHL Subject Headings, EMTREE, and/or Medical Subject
Headings). The search terms were developed by the biomedical Study risk‐of‐bias assessment
librarian with feedback and review by the team members. Searches
were limited by publication year (January 2010–June 2022) and Two reviewers assessed the risk of bias for each included article
English language. Search strategies were used to remove specific independently using the Quality Assessment of Diagnostic Accuracy
article types (letters, editorials, commentaries, errata, conference Studies 2 (QUADAS‐2) tool.12 Disagreements between reviewers
abstracts or papers, corrigenda, retractions, and protocols) that were were resolved by discussion between the reviewers and an additional
detailed in our exclusion criteria from the database search results. team member.
See Tables S1–S5 for the final search strategies. The QUADAS‐2 tool assesses four domains of bias: patient
The biomedical librarian used EndNote 20 (Clarivate Analytics) to selection (selection of patients included and whether the chosen
manage database search results and identify duplicate records. study population aligned with the research question), index testing
(centers on the administration and interpretation of the survey), the
index test reference standard (reference standard defined, along with
Selection process appropriate conduct and interpretation of the standard), and the flow
and timing of data collection (timing and interval of reference
A two‐stage screening process was used to select records for inclu- standard and intervention delivery). Each article was scored low,
sion. First, the titles and abstracts of all unique records identified moderate/unclear, or high risk for each domain criterion.
from the database searches were screened using the established
eligibility criteria. Next, for all records included after title and abstract
screening, the full text was obtained and screened using the same Determination of clinical recommendations
eligibility criteria. Two reviewers independently screened each record
at both stages; a different third reviewer resolved any disagreements A core team (E.B.T., K.C.K., C.T., F.F.Z., K.P., T.M., A.T., V.W., D.W.,
between the reviewers. Covidence (Veritas Health Innovations) was M.P., and C.K.S.) compiled and shared the results of the systematic
used for screening. review with the larger working group, comprised of representatives
Before commencing the formal screening process, all participating from nutrition and cancer societies—ASPEN, AND, Academy of
reviewers completed pilot training. The biomedical librarian selected Oncology Nurse and Patient Navigators, American Cancer Society,
and uploaded a random sample of 45 records into Covidence. Two American Society for Clinical Oncology (ASCO), American Society for
pilot sessions of title and abstract screening on 45 records and one Nutrition, American Society for Radiation Oncology, Association of
session of full‐text screening on 10 records were completed. After the Cancer Care Centers (ACCC), and Oncology Nursing Society.
training, the eligibility criteria were further refined and documented in The core team and larger working group, or the leadership
the protocol for implementation. committee, met via a videoconference call and discussed the
results. On the same call, the leadership committee agreed on the
answers to three specific questions, namely: (1) should clinicians
Data extraction process and data items screen for malnutrition in adult outpatient cancer centers, (2) which
criteria are recommended for screening in outpatient cancer
Two reviewers independently extracted data from each included centers, and (3) what are the recommended clinical applications for
article using Microsoft Excel (Redmond, WA). Discrepancies were malnutrition risk screening among adult oncology outpatients?
Those members who were not present on the conference call Study characteristics
received an audio recording of the meeting and were asked for
feedback on the discussion. No members dissented from the All studies were observational (18 cross‐sectional, one longitudinal,
agreed upon clinical recommendations. and one retrospective) and included between 52 and 450 screened
patients. No studies were conducted in the US.
Table 1 describes the general characteristics of the study
RESULTS populations. Of the 18 studies that reported mean age, the
average age of the population was 59.7 years. Males and females
Study selection were represented almost equally (54.7% males). Among the
20 studies, cancer site was represented by a variety of solid and
The database search resulted in 11,551 records, of which 4445 were hematological malignancies, including nine colorectal, eight breast,
duplicates, leaving 7106 unique records. After title and abstract five gastrointestinal, three head and neck, three hematological,
screening, 6368 were excluded, leaving 738 for full‐text screening. three lung, two pancreatic; one central nervous system, one
Of these, 718 did not meet the inclusion criteria and were excluded, gynecological, one esophageal, one prostate, one ovarian, eight
leaving 20 records for inclusion in the review (Figure 1). other cancer types (“other” cancer types were those types that
F I G U R E 1 Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) flow diagram. Database searches retrieved 11,
551 records. After removing 4445 duplicates, 7106 records were screened. Title and abstract screening excluded 6368 records, and 738 records
were fully text screened. Full‐text screening excluded 718 records, leaving 20 records for inclusion.
878
TABLE 1 Baseline population characteristics of included papers.

|
Reference
Age, mean BMI,a mean standard
(SD) or (SD) BMIb malnourished by
First author, median (R), Cancer site Treatment Treatment ormedian category, method % or
year, location Study design N years Male, % andstage, % status, % modality, % (R) % Index test mean (SD)
Abbott Cross‐sectional 300 58.6 (13.4) 51.7 Heme: 31.3 Active: 100 CT ± RT 27.8 (6.8) NA MST (≥2) and PG‐ PG‐SGA BC: 17
2014,13 201614 GI: 21.0 Targeted ± RT SGA, PG‐SGA SF
Australia Breast: 19.7
Stage: NA
Abe Vicente Cross‐sectional Group 1: 75 60.2 (12.2) 48 CRC: 85.3 Pre: 40 CT ± S NA UW: 6.7 NRI, MST, MUST PG‐SGA BC: 66
2013 GI: 14.7 Active: 60 NW: 54.7
Brazil15 III/IV: 82.7 OW/
OB: 38.6
Group 2: 62 61.3 (11.6) 45.2 CRC: 83.9 Post: 100 CT ± S NA UW: 3.2 NRI, MST, MUST PG‐SGA: BC 30.9
GI: 16.1 NW: 46.8
III/IV: 37.1 OW/
OB: 50
Arribas Cross‐sectional 394 61.5 (12.1) 55.1 Variety solid Pre/Active/ CT ± RT: 45.4 26.3 (4.87) NA NUTRISCORE, PG‐SGA BC: 19
2017 tumors: 87.5 Post: 100 RT: 18.8 MST
Spain16 Heme: 12.5 HSCT: 7.1
All stages Other or
included palliative: 28.7
Boleo‐Tome Cross‐sectional 450 62 (13) 60 Breast or Active: 100 RT: curative NA UW: 4 MUST PG‐SGA BC: 30
2012 prostate: 40 (63.3) and NW: 33
Portugal17 Lung: 16.2 palliative (36.7) OW/
CRC: 13.6 OB: 63
III/IV: 60.7
Carrico Cross‐sectional 355 60.6 (13.1) 40.3 Breast: 25.9 Active: 100 CT: 100 25.0 (4.3) UW: 4.5 PG‐SGA SF PG‐SGA BC: 49.8
2021 CRC: 15.8 NW: 48.2
Portugal18 Lung: 14.9 OW/
Panc: 10.1 OB: 47.3
Other: 33.3
Stage: NA
Chen Cross‐sectional 146 60.3 (10.1) 57.5 Lung: 33.6 NA NA 21.7 (3.5) NA NRS‐2002 PG‐SGA:
2022 Panc: 13.0 14.6 (5.5)
China19 Breast: 9.6
Other: 43.8
Stage: NA
De Groot Cross‐sectional 246 61.9 (13.1) 26 Breast: 45 Active: 100 “In‐chair IV NA UW: 14 PG‐SGA SF, GLIM PG‐SGA BC: 29
2020 GYN: 13 treatment”: 100 NW: 47
TRUJILLO
ET AL.
TABLE 1 (Continued)
Reference
20
Australia CRC: 11 OW/
Other: 31 OB: 39
Stage: NA
Demirel Cross‐sectional 124 52 (21–89) 64.5 HN: 59.7 Active: 61.3 CT ± RT: 100 Mean: 26.7 OW or NRS‐2002, MNA SGA BC: 31
2018 CNS: 40.3 Post: 38.7 R: 16–55.7 OB: 62.1
Turkey21 I/II: 13.7
III/IV: 86.3
Di Bella Cross‐sectional 201 60 (48‐69) 57 NA Active: 100 CT or NA NA Patient‐led MST SGA BC: 18
JOURNAL OF PARENTERAL AND ENTERAL NUTRITION
2020 supportive: 100

Australia22
Esfahani Cross‐sectional 71 62.1 (14.4) 79 GI: 100 Pre: 100 CT: 100 21.1 (4.0) NA MS‐score SGA BC: 87
2017 III/IV: 100 PG‐SGA:
Iran23 16.1 (5.0)
Faramarzi Cross‐sectional 52 54.1 (16.8) 76.9 CRC: 100 Pre: 100 RT: 100 23.9 (4.9) NA NRI PG‐SGA BC: 52
2013 II: 38.5
Iran24 III/IV: 61.5
Gabrielson Cross‐sectional 90 54.9 (14.8) 35.6 Breast: 46 Active: 100 CT: 100 25.4 (5.0) NA abPG‐SGA, SGA BC: 36
2013 CRC: 24 PG‐SGA
Canada25 Heme: 13
Other: 17
Stage: NA
Gascon‐Ruiz Cross‐sectional 165 67 (60–74) 64.8 CRC: 49.7 Active: 100 CT: 83 26.2 (4.65) NA MST, MUST, GLIM: 47
2022 Upper GI: 38.8 Other: 17 NUTRISCORE,
Spain26 HN: 11.5 CONUT, MNA‐SF
Metastatic: 69
Hettiarachchi Cross‐sectional 100 58.6 (8.8) 32 Breast: 47 Active: 100 CT: 100 22.2 (3.6) UW; 15 MUST PG‐SGA BC: 45
2018 Ovary: 10 NW: 48 PG‐SGA:
Sri Lanka27 Other: 43 OW/ 14.5 (7.4)
Stage: NA OB: 37
Oh Longitudinal Baseline: 194 60 (10.3) 55.2 CRC: 24.2 Active: 100 CT: 100 24.0 (3.7) NA SNAQ Total N = 152
2019 Completed: 155 Breast: 17 PG‐SGA BC:
Korea28 Other: 58.8 25.0 (visit 1) and
III/IV: 87.1 23.7 (visit 4)
|
(Continues)
879
880
TABLE 1 (Continued)
|
Reference
Orell‐Kotikangas Cross‐sectional 65 61 (33–77) 77 HN: 100 Pre: 100 NA 23.7 OW: 42 NRS‐2002 PG‐SGA BC: 34
2015 III/IV: 81.5 (21–27)
Finland29
Pan Retrospective 102 Median: 48 71.6 HN Pre through ICT and RT: 100 NA NA NRS‐2002 PG‐SGA ≥ 4:
2020 (nasopharynx): Post: 100 6.9–98.0
China30 100
III/IV: 96
Szefel Cross‐sectional 70 ≥50 years 48.6 CRC: 100 NA NA NA OW or NRS‐2002 NA

2020 old only All stages OB: 51
Poland31 included
Zhang Cross‐sectional 312 58.8 (11.8) 47.8 Stomach: 51 Active or CT, RT, S, any 22.2 (4.0) NA NRS‐2002 PG‐SGA BC: 94
2018 Esoph: 29.5 Post: 100 combination:
China32 Other: 19.5 100
Stage: NA
Abbreviations: abPG‐SGA, abridged Patient‐Generated Subjective Global Assessment; BMI, body mass index; CONUT, Controlling Nutritional Status; CNS, central nervous system; CRC, colorectal cancer; CT,
chemotherapy; Esoph, esophageal; GI, gastrointestinal; GLIM, Global Leadership Initiative on Malnutrition; GYN, gynecological; Heme, hematological; HN, head and neck; HSCT, hematopoietic stem cell
transplantation; ICT, induction chemotherapy; IV, intravenous; MNA, Mini Nutritional Assessment; MNA‐SF, Mini Nutritional Assessment Short Form; MS‐score, Malnutrition Screening score; MST,
Malnutrition Screening Tool; MUST, Malnutrition Universal Screening Tool; NA, not available; NRI, Nutrition Risk Index; NRS‐2002, Nutrition Risk Screening‐2002; NW, normal weight; OB, obese; OW,
overweight; Panc, pancreas; PG‐SGA, Patient‐Generated Subjective Global Assessment; PG‐SGA BC, Patient‐Generated Subjective Global Assessment boxes B and C (moderate or severe malnutrition); PG‐
SGA SF, Patient‐Generated Subjective Global Assessment Short Form; Post, after treatment; Pre, before treatment; R, range; RT, radiation therapy; S, surgery; SGA BC, Subjective Global Assessment boxes B
and C (moderate or severe malnutrition); SNAQ, Short Nutritional Assessment Questionnaire; UW, underweight.
a
BMI calculated as weight in kilograms divided by height in meters squared.
b
BMI categories per Centers for Disease Control and Prevention (CDC): UW < 18.5; NW = 18.5 to <25.0; OW = 25.0 to <30.0; OB ≥ 30.0.
TRUJILLO
ET AL.
were present in <10% of the study population), and one cancer used the PG‐SGA as the reference standard, except one that used
type that was not specified. Of the 20 studies, the majority GLIM as the reference standard and had good sensitivity and fair
included patients who were receiving active treatment, including specificity.
chemotherapy, radiation therapy, or chemoradiation, across
the cancer continuum. Specifically, the studies' treatment status
included three pretreatment, one before and during active treat- MUST
ment, nine active treatment, two pre‐/active/posttreatment, two
active/posttreatment, one posttreatment, and two no treatment Four of five studies evaluating the MUST showed fair to good
status reported. Fifty percent of the studies included stage III/IV sensitivity and specificity. Three of the evaluations using the
cancers. MUST had good sensitivity and specificity, one had good sensi-
The average body mass index (BMI) across the studies was tivity and fair specificity, and one had fair sensitivity and poor
24.3 kg/m2 (13 studies), and the BMI category distribution was specificity. Three of five MUST studies used a cut‐point of ≥2; the
7.9% underweight (six studies), 43.2% normal weight (six studies), PG‐SGA was used as the reference standard in three of the five
and 48.5% overweight/obese (eight studies). Malnutrition, according studies. Using GLIM as a reference standard, the MUST had good
to the reference standard, was reported in 19 of the 20 studies and sensitivity and specificity, and the sensitivity and specificity were
ranged from 6.9% to 98%. good in one study using the MUST with a cut‐point of ≥1.
Malnutrition screening tools evaluated for general NRS‐2002

validity
Several of the nine studies evaluating the NRS‐2002 found good
The following screening tools (index tests) were used in the studies: sensitivity and specificity using cut‐points of either ≥2 or ≥3.
eight used the Malnutrition Screening Tool (MST), four used the Three studies showed good sensitivity and specificity for
Malnutrition Universal Screening Tool (MUST), three used the NRS‐2002 ≥ 2. Although one examination of NRS‐2002 ≥ 3 had
Nutrition Risk Index (NRI), six used the Nutrition Risk Screening‐2002 good sensitivity and specificity, when filtered to studies that used
(NRS‐2002), two used the NUTRISCORE, four used the PG‐SGA the PG‐SGA boxes B and C (BC) or SGA BC reference standard, the
short form (PG‐SGA SF), one used the Controlling Nutritional Status results were either good sensitivity and poor specificity or good
(CONUT), one used the Mini Nutritional Assessment (MNA), one specificity and fair sensitivity. One study using the NRS‐2002 did
used the MNA‐short form, one used the Malnutrition Screening not measure sensitivity and specificity and used a Spearman cor-
score (MS‐score), and one used the Short Nutritional Assessment relation analysis.
Questionnaire (SNAQ).
The reference standard for most of the studies (n = 16) was the
PG‐SGA, followed by the SGA in three studies, and GLIM in one PG‐SGA SF
study. Most studies evaluated the PG‐SGA SF, MST, NRS‐2002, and
MUST. Table 2 describes the index tests. All 16 evaluations using the PG‐SGA SF showed fair to good
performance; the best performance with PG‐SGA SF was at the
cut‐points of ≥7 and ≥8.
General validity of the screeners evaluated
Table 3 contains a summary of the validity scores of the index Others

tests.
NUTRISCORE, evaluated in two studies, performed well when
the reference standard was PG‐SGA BC. Similarly, the MNA
MST performed well in the one study for which it was evaluated. The
NRI, evaluated in three studies, performed poorly, as did CONUT,
Most studies evaluating the MST overall had fair to good sensitivity MS‐score, and SNAQ, in which each were evaluated in only one
and specificity. Although seven of nine studies evaluating the MST study.
used a cut‐point of ≥2, one did not specify the cut‐point, and one Malnutrition screening tools were deemed valid based on at least
used a cut‐point of ≥3. Specifically using MST with the cut‐point of one study reporting good sensitivity and/or specificity (see Table 4).
≥2, six of seven studies, including one that used the patient‐led Valid screening tools and the cut‐points in which they were found
MST, showed fair to good sensitivity and specificity. One study to be valid included MNA ≤ 23.5, MST ≥ 2, patient‐led MST ≥ 2,
using a patient‐led MST with a cut‐point of ≥3 had poor sensitivity MUST, MUST ≥ 1, MUST ≥ 2, NRS‐2002 ≥ 2, NRS‐2002 ≥ 3, NUTRI-
and good specificity. Five of nine studies assessing the MST SCORE ≥ 5, PG‐SGA SF ≥ 7, and PG‐SGA SF ≥ 8.
TABLE 2 Characteristics of malnutrition screening tools.

Screening tool Description
SGA reference standard Nutrition assessment tool based on features of a medical history (weight change, dietary intake change,
gastrointestinal symptoms that have persisted for >2 weeks, changes in functional capacity) and physical examination
(loss of subcutaneous fat, muscle wasting, ankle/sacral edema and ascites).33
PG‐SGA reference Adapted from the SGA and includes additional questions regarding the presence of nutrition symptoms and short‐term
standard weight loss; components of the medical history are completed by patient using checkbox format; physical examination then
performed by health professional; scored PG‐SGA incorporates a numerical score as well as a global rating of well nourished,
moderately or suspected of being malnourished, or severely malnourished; points 0–4 awarded depending on impact of
symptom on nutrition status; total score summed and provides guideline to level of nutrition intervention required; the
higher the score, the greater the risk for malnutrition; a score ≥9 indicates critical need for nutrition intervention.34
GLIM reference standard 3‐step diagnostic structure: screening, diagnosis, and severity grading consisting of 3 phenotypic (weight loss, low BMI, and
reduced muscle mass) and 2 etiologic (reduced food intake/assimilation and disease burden/inflammation) criteria; for
diagnosis of malnutrition, at least 1 criterion from each phenotypic and etiologic component should be present.35
CONUT Screening tool derived from laboratory information including serum albumin level, total cholesterol level, and total
lymphocyte count; depending on the value, each of the laboratory values is scored and undernutrition is categorized
as light (2–4), moderate (5–8), and severe (9–12); a score of 0–1 is normal.36
MS‐score Screener that uses serum albumin, prealbumin, and CA‐125 levels to determine malnutrition risk; patients with serum
albumin level ≤3.5 g/dl, serum prealbumin level <0.20 mg/dl, and serum CA‐125 level >35 U/ml are allocated a score
of 3; patients with 1 or 2 parameter abnormalities are allocated scores of 1 and 2, respectively; and those in whom the
serum albumin level is >3.5 g/dl, serum prealbumin level is >0.20 mg/dl, and serum CA‐125 level is ≤35 U/ml are
allocated a score of 0.23
MST Screening tool that uses a combination of questions, including “Have you lost weight recently without trying?” and
“Have you been eating poorly because of a decreased appetite?” Each answer is scored; a score >2 indicates patient is
at risk for malnutrition and should undergo a more detailed nutrition assessment to identify whether the patient is
malnourished and to determine the most appropriate form of nutrition support.37
MUST Identifies patients who are at risk for malnutrition; scores BMI, unintentional weight loss, and food intake (acute disease‐
related effect inducing a phase of >5 days with no food intake) and separates patients into 3 risk groups (low, medium, and
high); each criterion rated 0–2; all points added up and overall score ≥2 classified as being at nutrition risk.38–40
MNA Assesses nutrition status and includes 18 items in 4 categories (anthropometric, general assessment, nutrition
assessment, and self‐assessment); final tallied score ranges from 0 to 30; scores of 17–23.5 indicate risk for
malnutrition, with <17 indicating malnutrition.38,40,41
MNA‐Short Form A shorter version of MNA with 6 items; final tallied score ranges from 0 to 14; scores of ≤11 signal risk for malnutrition.38,40
NUTRISCORE Screener that includes questions of unintentional weight loss, specific oncologic parameters such as tumor location
and anticancer treatment; sum of all categories range from 0 to 11 points; total score ≥5 indicates at risk.16
NRI Nutrition assessment tool derived from serum albumin concentration and ratio of actual to usual weight; a score of
>100 indicates patient not malnourished, 83.5 to <97.5 indicates moderate malnourishment, and <83.5 indicates
severe malnourishment.42,43
NRS‐2002 Screening tool using severity of disease and nutrition status to predict those who would benefit from nutrition
support; uses 4 questions based on impairment of nutrition status (percentage of weight loss, general condition, BMI,
and recent food intake), disease severity, and age; each category is rated 0 (normal) to 3 (severe), and age ≥70 years
adds 1 point; total scores range from 0 to 7 points; patients with a total score ≥3 classified as “at nutritional risk” could
benefit from nutrition support.38,40,44
Patient‐led MST MST completed by patients attending cancer care ambulatory settings.
PG‐SGA Short Form Also referred to as the abridged PG‐SGA, eliminates the physical examination and disease/condition and metabolic
demand assessment components of the PG‐SGA but retains the medical history component, comprising weight,
history, food intake, nutrition impact symptoms, and activities and function.14
SNAQ Screening tool that asks 3 questions: “Did you lose weight unintentionally?”; “Did you experience decreased appetite
over the last month?”; and “Did you use supplemental drinks or tube feeding over the last month?” Each answer is
scored for maximum score of 5 points; total scores broken down into 3 groups (well nourished, moderately
malnourished, and severely malnourished); each category is associated with a care plan, including supplemental
drinks, snacks, and treatment by an RDN.38,45
Abbreviations: BMI, body mass index; CONUT, Controlling Nutritional Status; GLIM, Global Leadership Initiative on Malnutrition; MNA, Mini Nutritional
Assessment; MS‐score, Malnutrition Screening score; MST, Malnutrition Screening Tool; MUST, Malnutrition Universal Screening Tool; NRI, Nutrition Risk
Index; NRS‐2002, Nutrition Risk Screening‐2002; PG‐SGA, Patient‐Generated Subjective Global Assessment; RDN, registered dietitian nutritionist; SGA,
Subjective Global Assessment; SNAQ, Short Nutritional Assessment Questionnaire.
TABLE 3 Summary of validity scores by malnutrition risk tool (index test).

Reference Sensitivity Specificity
Index test standard (95% CI) (95% CI) Other results (95% CI) First author (year)
MST GLIM 83 72 Accuracy: 76; k = 0.53 Gascon‐Ruiz (2021)26

PPV: 68; NPV: 85
MST (≥2) PG‐SGA BC 70.6 69.7 AUC: 0.77 (0.72–0.82) Abbott (2014)13
MST (≥2) PG‐SGA BC 52 84 NA Abe Vicente (2013)15
MST (≥2) PG‐SGA BC 61.5 91.8 NA Abe Vicente (2013)15
MST (≥2) PG‐SGA BC 84 (74–91) 85.6 (81–89) 0.84 (0.79–0.89) Arribas (2017)16
PPV: 57.7 (48–67);
NPV: 95.7 (93–98)
MST (≥2) PG‐SGA BC 100 90 NA De Groot (2020)20
MST (≥2) SGA BC 81.3 72.4 AUC: 0.823 Gabrielson (2013)25
MST (≥2) patient‐led SGA BC 94 (81–99) 86 (79–91) PPV: 59 (45–71); Di Bella (2020)22
NPV: 99 (95–100)
MST (≥3) patient‐led SGA BC 50 (33–67) 95 (90–98) PPV: 67 (46–84); Di Bella (2020)22
NPV: 90 (84–94)
MUST (≥2) PG‐SGA BC 72 48.9 NA Abe Vicente (2013)15
MUST (≥2) PG‐SGA BC 84 73.4 NA Abe Vicente (2013)15
MUST (≥2) PG‐SGA BC 80 89 PPV: 87; NPV: 100 Boleo‐Tome (2012)17
MUST GLIM 86 81 Accuracy: 83; k = 0.66 Gascon‐Ruiz (2021)26

PPV: 77 NPV: 89
MUST (≥1) PG‐SGA BC 86.70 94.50 AUC: 0.91; k = 0.79 Hettiarachchi (2018)27
PPV: 92.90; NPV: 89.70
NRI (≤97.5 medium/ PG‐SGA BC 68 64 NA Abe Vicente (2013)15

high risk)
NRI (≤97.5 medium/ PG‐SGA BC 55.8 83.6 NA Abe Vicente (2013)15

high risk)
NRI (<83.5–100) PG‐SGA BC 66 60 PLR: 1.65; NLR: 0.56 Faramarzi (2013)24

PPV: 64; NPV: 62
NRS‐2002 (≥2) PG‐SGA ( ≥ 9) 96.8 70 Spearman r = 0.699 Chen (2022)19

k = 0.698
PPV: 95.3; NPV: 77.8
NRS‐2002 (≥2) PG‐SGA ( ≥ 4) 96.9 (84–99) 78.8 (62–89) k = 0.754 Orell‐Kotikangas

PPV: 81.6; NPV: 96.3 (2015)29
NRS‐2002 (≥2) PG‐SGA ( ≥ 4) 76.3 90.9 MYI: Pan (2020)30

0.672
NRS‐2002 (≥3) PG‐SGA ( ≥ 9) 74.6 90 Spearman r = 0.468 Chen (2022)19

k = 0.396
PPV: 97.9; NPV: 36
NRS‐2002 (≥3) PG‐SGA ( ≥ 9) 86.7 (62–96) 90 (79–96) k = 0.717 Orell‐Kotikangas

PPV: 72.2; NPV: 95.7 (2015)29
NRS‐2002 (≥3) PG‐SGA BC 77.3 (57–90) 97.7 (88–100) k = 0.784 Orell‐Kotikangas

PPV: 94.4; NPV: 89.4 (2015)29
NRS‐2002 (≥3) SGA BC 96.0 58.0 PPV: 63; NPV: 96 Szefel (2020)31
NRS‐2002 PG‐SGA NA NA Spearman r: Zhang (2018)32

−0.24 (men) and
−0.41 (women)
NRS‐2002 (≥3) SGA BC 67.5 92.9 PLR: 12.2; NLR: 0.13 Demirel (2018)21
k = 0.713
PPV: 97.7; NPV: 68.4
(Continues)
TABLE 3 (Continued)
Reference Sensitivity Specificity

Index test standard (95% CI) (95% CI) Other results (95% CI) First author (year)
NUTRISCORE (≥5) PG‐SGA BC 97.3 (91–100) 95.9 (93–98) AUC: 0.95 (0.92–0.98) Arribas (2017)16
PPV: 84.8 (76–92); NPV:
99 (98–100)
NUTRISCORE GLIM 64 88 Accuracy: 78; k = 0.54 Gascon‐Ruiz (2021)26

PPV: 80; NPV: 77
abPG‐SGA (≥6) SGA BC 93.8 77.6 AUC: 0.956 Gabrielson (2013)25
abPG‐SGA (≥7) SGA BC 84.4 89.7 AUC: 0.956 Gabrielson (2013)25
PG‐SGA SF (≥8) SGA BC 96.9 86.2 AUC: 0.967 Gabrielson (2013)25
PG‐SGA SF (≥3) PG‐SGA BC 80.4 72.3 NA Abbott (2016)14
PG‐SGA SF boxes 1–3 (≥2) PG‐SGA BC 90.2 67.5 NA Abbott (2016)14
PG‐SGA SF box 3 (≥1) PG‐SGA BC 82.4 69.9 NA Abbott (2016)14
PG‐SGA SF boxes 1 and PG‐SGA BC 86.3 71.1 NA Abbott (2016)14

3 (≥2)
PG‐SGA SF boxes 2 and PG‐SGA BC 82.4 63.1 NA Abbott (2016)14

3 (≥1)
PG‐SGA SF (≥2) PG‐SGA BC 92 76 AUC: 0.82 (0.77–0.86) Carrico (2021)18
PG‐SGA SF boxes 1–3 (≥2) PG‐SGA BC 77 76 AUC: 0.78 (0.77–0.82) Carrico (2021)18
PG‐SGA SF boxes 1 and PG‐SGA BC 75 80 AUC: 0.78 (0.73–0.83) Carrico (2021)18

3 (≥2)
PG‐SGA SF box 3 (≥2) PG‐SGA BC 71 82 AUC: 0.77 (0.73–0.82) Carrico (2021)18
PG‐SGA SF boxes 2 and PG‐SGA BC 79 75 AUC: 0.78 (0.73–0.83) Carrico (2021)18

3 (≥2)
PG‐SGA SF (≥5) PG‐SGA BC 89 80 PPV: 45; NPV: 98 De Groot (2020)20
CONUT GLIM 21 89 Accuracy: 61; k = 0.40 Gascon‐Ruiz (2021)26

PPV: 60; NPV: 61
MNA (≤23.5) SGA BC 96.5 92.1 PLR: 12.2; NLR: 0.04 Demirel (2018)21
k = 0.886
PPV: 96.5; NPV: 92.1
MNA‐SF GLIM 99 45 Accuracy: 68 k = 0.12 Gascon‐Ruiz (2021)26

PPV: 57 NPV: 98
MS‐score (≥1) PG‐SGA BC 96.8 (83.8–99.4) 50.0 (15.0–85.0) AUC: 0.914 Esfahani (2017)23
PPV: 93.8 (79.9–98.3)
NPV: 66.7 (20.8–93.9)
SNAQ PG‐SGA BC NA NA Visit 1 (n = 152) Oh (2019)28

Pearson r = −0.53
Visit 4 (n = 123)
Pearson r = −0.59
Note: PPV and NPV at 95% CI. abPG‐SGA is equivalent to PG‐SGA SF.
Abbreviations: abPG‐SGA, abridged Patient‐Generated Subjective Global Assessment; AUC, area under curve; CI, confidence interval; CONUT,
Controlling Nutritional Status; GLIM, Global Leadership Initiative on Malnutrition; k, Cohen's kappa; MNA, Mini Nutrition Assessment; MNA‐SF, Mini
Nutrition Assessment Short Form; MS‐score, Malnutrition Screening score; MST, Malnutrition Screening Tool; MUST, Malnutrition Universal Screening
Tool; MYI, maximum Youden index; NA, not available; NLR, negative likelihood ratio; NPV, negative predictive value; NRI, Nutritional Risk Index; NRS‐
2002, Nutrition Risk Screening‐2002; PG‐SGA BC SF, Patient‐Generated Subjective Global Assessment boxes B and C (moderate or severe malnutrition)
Short Form; PLR, positive likelihood ratio; PPV, positive predictive value; r, correlation coefficient; SGA BC, Subjective Global Assessment boxes B and C
(moderate or severe malnutrition); SNAQ, Simplified Nutritional Appetite Questionnaire.
General validity based on population characteristics DeGroot et al. reported outcomes for patients receiving intra-
including age, cancer type, cancer stage or cancer venous chemotherapy. A PG‐SGA SF score of ≥5 and a “severe
treatment modality, health status, time interval from malnutrition” score by GLIM were independently associated with
diagnosis, and/or weight status 1‐year mortality risk.20
Few studies examined the validity of screening tools in relation to

specific population characteristics. Hence, it is challenging to draw Risk of bias in studies
conclusions on the validity of these screening tools based on age,
the timing relative to diagnosis, weight status, type of cancer, cancer Figure 2 details the risk‐of‐bias evaluation for each study. Twelve
stage, and treatment protocol. Only four studies investigated the studies clearly outlined the criteria for eligible participants and
validity of the screening tools assessing factors such as sex, age, received low (n = 11) or moderate/unclear risk (n = 1) designations
cancer site, and treatment. Only one study conducted malnutrition for the patient selection criteria. The remaining eight studies were
screenings at three different time intervals. categorized as high risk because of the insufficient description of the
The study of Demirel and Atasoy focused on distinguishing selected participants. Within the “index test” domain, 11 studies had
sensitivity and specificity according to age, treatment status, and a low risk of index bias and the remainder had moderate (n = 5) or
cancer site.21 They conducted a comparison of three different high risk of bias (n = 5). The high risk of bias was due to the lack of
screening tools. The population consisted of individuals with head clarity as to whether the index test results were interpreted without
and neck cancers or central nervous system tumors undergoing knowledge of the reference test outcomes and an absence of pre-
chemoradiation. Screening tools demonstrated substantial or mod- specified thresholds for the index test. The third domain examined
erate agreement irrespective of the patient's age or treatment status. the risk of bias attributable to the reference standard used, wherein
The prevalence of malnutrition in patients with head and neck cancer most (n = 14) studies were deemed at low risk of bias. Two studies
was between 32% and 46%, whereas it remained <10% among were high risk and four were moderate risk, primarily owing to the
patients with brain tumors. Nutrition risk was higher in treatment absence of clarity about whether the reference standard results were
than in follow‐up groups with a range of 32% to 39% compared with interpreted without prior knowledge of index test results. Lastly, the
8% to 17%, respectively. There was substantial agreement between fourth domain focused on the flow and timing of the tests conducted
the SGA and MNA across both groups.21 throughout the study period. Thirteen studies were deemed low risk
Gascon‐Ruiz et al. separated screening scores by cancer site, because of the clear description of the time interval between the
evaluating outpatients with tumors in the upper gastrointestinal index and reference tests and the inclusion of all patients evaluated.
tract, head/neck, and colorectal locations.26 Based on the GLIM Three studies were high risk and four were moderate risk, primarily
criteria, malnutrition and tumor location was correlated. Specifically, owing to the lack of inclusion of all patients who completed the index
malnutrition was more prevalent in patients with cancer of the test in the final analysis and the lack of clarity regarding the interval
head/neck or upper gastrointestinal tract compared with colorectal between the index and reference tests.
locations. Malnutrition was also associated with tumor progression
but not the type of treatment.
Orell‐Kotikangas et al. calculated Spearman correlation coeffi- CLINICAL RECOMMENDATIONS
cients separately for males and females with cancer of the head/
neck.29 The PG‐SGA revealed malnutrition in 30% of males and 47% This is the first systematic review to examine malnutrition screening
of females. On the NRS‐2002, a notable positive correlation occurred tools specifically designed and validated for use in ambulatory set-
between the PG‐SGA and the scored PG‐SGA. The latter is employed tings for adults and for those with cancer.
to triage patients for nutrition intervention, with scores ≥4 indicating
necessity for nutrition intervention and ≥9 indicating critical Question 1. Should clinicians screen for malnutrition in
necessity.29 outpatient cancer centers?
Arribas et al. observed outpatients with solid or hematologic
malignancies. Patients underwent either oncology‐related palliative or Recommendation: Yes, all patients should undergo malnutrition
symptomatic treatment. Significant variations influenced by the location screening using a validated tool with a nutrition‐specific follow‐up plan
and the type of treatment in nutrition status were observed.16 for those at risk.
Pan et al. assessed nutrition risk in patients with nasopharyngeal Recommendation Rationale: The recommendation that all
cancer at various stages. Nutrition risk and moderate or severe patients undergo screening is based on our expert opinion. Although
malnutrition (by PG‐SGA ≥ 4) rose significantly as treatment pro- not every patient with cancer is malnourished, every patient with
gressed. Seven of 100 patients were at nutrition risk before cancer is at risk for malnutrition. Our data demonstrate the validity of
chemotherapy and this increased to 24 after chemotherapy. By the multiple screening tools in detecting malnutrition risk in adult
end of radiotherapy, all participants were at nutrition risk. As treat- oncology outpatients receiving treatment. Using reference standards,
ment advanced, nutrition risk worsened.30 such as the SGA, PG‐SGA and GLIM, malnutrition rates varied
TABLE 4 Index tests with good sensitivity and specificitya. between 7% and 94%, which is consistent with the previously re-
Index tests with Index tests with Index texts with ported prevalence of 40% to 80%.46 Approximately 15% to 50% of all
good sensitivity good specificity good sensitivity and patients with cancer present with nutrition deficiencies at the time of
(# of studies) (# of studies) specificity diagnosis before the initiation of active cancer treatment.3,46
— CONUT (1) — The consequences of untreated malnutrition are serious.
Severely malnourished patients have a twofold to fivefold higher
MNA ≤ 23.5 (1) MNA ≤ 23.5 (1) MNA ≤ 23.5
mortality compared with patients with little or no evidence of
MNA‐SF (1) — —
malnutrition.47,48 Malnutrition is associated with a lower tolerance
MS‐score ≥1 (1) — — to anticancer treatments because of increased toxicity, lower com-
MST (1) — — pliance, and reduced response to treatments49 and increased com-
plication rates, poor postoperative outcomes, longer hospitalization,
MST ≥ 2 (3) MST ≥ 2 (4) MST ≥ 2
and a poor quality of life.1,50,51 Patients with cancer also face
MST ≥ 2 MST ≥ 2 MST ≥ 2 patient‐led a deterioration in their health‐related quality of life in terms of psy-
patient‐led (1) patient‐led (1)
chological, cognitive, social, and emotional functions.1,52,53
— MST ≥ 3 — To potentially reverse malnutrition, stop unintentional weight
patient‐led (1)
loss or gain, improve quality of life, reduce treatment toxicity, support
MUST (1) MUST (1) MUST the management of treatment‐associated symptoms, and lower the
MUST ≥ 1 (1) MUST ≥ 1 (1) MUST ≥ 1 risk of mortality, diagnosing malnutrition should be made as early as
possible.54
MUST ≥ 2 (1) MUST ≥ 2 (1) MUST ≥ 2
Several systematic reviews and international panels recommend
— NRI ≤ 97.5 med/high — that all patients with cancer be screened for risk of malnutrition
risk (1)
regularly with a valid malnutrition screening tool.55,56 Our updated
NRS‐2002 ≥ 2 (2) NRS‐2002 ≥ 2 (1) NRS‐2002 ≥ 2 evaluation of the literature supports these prior reports.
NRS‐2002 ≥ 3 (2) NRS‐2002 ≥ 3 (4) NRS‐2002 ≥ 3
Question 2. Which malnutrition screening tools are
— NUTRISCORE (1) —
recommended in outpatient cancer centers?
NUTRISCORE ≥ 5 (1) NUTRISCORE ≥ 5 (1) NUTRISCORE ≥ 5
PG‐SGA SF ≥ 2 (1) Recommendation: Six tools—MNA, MST, MUST, NRS‐2002, NU-

PG‐SGA SF ≥ 3 (2) TRISCORE, and PG‐SGA SF—with various cut‐points demonstrated
validity and are recommended in ambulatory settings.
PG‐SGA SF ≥ 4 (1)
Rationale for recommendation: The following tools, which have
PG‐SGA SF ≥ 5 (1) been shown to be sensitive and specific, are recommended for
PG‐SGA SF ≥ 6 (1) use with the following cut‐points. Further details can be found in
PG‐SGA SF ≥ 7 (1) PG‐SGA SF ≥ 7 (1) PG‐SGA SF ≥ 7 Table 5.
PG‐SGA SF ≥ 8 (1) PG‐SGA SF ≥ 8 (1) PG‐SGA SF≥ 8

• MNA ≤ 23.5
PG‐SGA SF Box 3 • MST ≥ 2
≥ 1 (1)
• Patient‐led MST ≥ 2
PG‐SGA SF • MUST (cut‐point not specified)
Box 3 ≥ 2 (1)
• MUST ≥ 1
PG‐SGA SF boxes 1 • MUST ≥ 2
and 3 ≥ 2 (1) • NRS‐2002 ≥ 2
PG‐SGA SF boxes • NRS‐2002 ≥ 3
1–3 ≥ 2 (1) • NUTRISCORE ≥ 5
PG‐SGA SF boxes 2 • PG‐SGA SF ≥ 7
and 3 ≥ 1 (1) • PG‐SGA SF ≥ 8
Abbreviations: CONUT, Controlling Nutritional Status; MNA, Mini
Nutrition Assessment; MS‐score, Malnutrition Screening score; MST, Successful implementation of screening tools requires they be
Malnutrition Screening Tool; MUST, Malnutrition Universal Screening brief, economically viable, and highly sensitive and have good spec-
Tool; NRI, Nutritional Risk Index; NRS‐2002, Nutrition Risk Screening‐
ificity.55 The clinical utility of a screening tool guides routine clinical
2002; PG‐SGA SF, Patient‐Generated Subjective Global Assessment
Short Form. practice. Table 6 organizes screening tools based on “ease of use.”
a
The values for sensitivity and specificity were interpreted as follows: a Level 1's are the simplest and quickest, whereas Level 4's are the
value >80% was considered good, 60%–80% fair, and <60% poor. most intricate and time‐consuming. The MST and patient‐led MST,
F I G U R E 2 Detailed risk‐of‐bias evaluation. Colored dots designated risk level: green, low risk; yellow, medium/unclear risk; and red, high
risk. Risk of bias was assessed for participant selection, index test, reference standard, and flow and timing. Applicability was evaluated for
participant selection, index test, and reference standard.
TABLE 5 Recommended screening tools for ambulatory cancer patients and their respective patient population.
Screening tool Study N Cancer site, % Cancer stage, % Treatment status Treatment modality
21
MNA (≤23.5) Demirel 124 HN: 59.7 I/II: 13.7 III/ Active: 61.3 CT ± RT: 100
CNS: 40.3 IV: 86.3 Post: 38.7
MST (≥2) Abe Vicente15 75 CRC: 85.3 III/IV: 82.7 Pre: 40 CT ± S

Group 1 GI: 14.7 Active: 60
Abe Vicente15 62 CRC: 83.9 III/IV: 37.1 Post: 100 CT ± S

Group 2 GI: 16.1
Arribas16 394 Variety solid All stages included Pre/Active/ CT ± RT: 45.4
tumors: 87.5 Post: 100 RT: 18.8
Heme: 12.5 HSCT: 7.1
Other/palliative: 28.7
DeGroot20 246 Breast: 45 NA Active: 100 “In‐chair IV

GYN: 13 treatment”: 100
CRC: 11
Other: 31
Gabrielson25 90 Breast: 46 NA Active: 100 CT: 100

CRC: 24
Heme: 13
Other: 17
MST (≥2) patient‐led Di Bella22 201 NA NA Active: 100 CT or supportive: 100

26
MUST Gascon‐Ruiz 165 CRC: 49.7 Metastatic: 69 Active: 100 CT: 83 Other: 17
Upper GI: 38.8
HN: 11.5
MUST (≥1) Hettiarachchi27 100 Breast: 47 NA Active: 100 CT: 100

Ovary: 10
Other: 43
MUST (≥2) Abe Vicente15 62 CRC: 83.9 III/IV: 37.1 Post: 100 CT ± S
Group 2 GI: 16.1
Boleo‐Tome17 450 Breast or prostate: 40 III/IV: 60.7 III/IV: 60.7 RT: curative—63.3,
Lung: 16.2 palliative—36.7
CRC: 13.6
NRS‐2002 (≥2) Chen19 146 Lung: 33.6 NA NA NA

Panc: 13.0
Breast: 9.6
Other: 43.8
Orell‐Kotikangas29 65 HN: 100 III/IV: 81.5 Pre: 100 NA
Pan30 102 HN (nasopharynx): 100 III/IV: 96 Pre through ICT and RT: 100
Post: 100
NRS‐2002 (≥3) Chen19 146 Lung: 33.6 NA NA NA

Panc: 13.0
Breast: 9.6
Other: 43.8
Orell‐Kotikangas29 65 HN: 100 III/IV: 81.5 Pre: 100 NA

31
Szefel 70 CRC: 100 All stages included NA NA
16
NUTRISCORE (≥5) Arribas 394 Variety solid All stages included Pre/Active/ CT ± RT: 45.4
tumors: 87.5 Post: 100 RT: 18.8
Heme: 12.5 HSCT: 7.1
Other/palliative: 28.7
TABLE 5 (Continued)
Screening tool Study N Cancer site, % Cancer stage, % Treatment status Treatment modality
25
PG‐SGA SF (≥7) Gabrielson 90 Breast: 46 NA Active: 100 CT: 100
CRC: 24
Heme: 13
Other: 17
PG‐SGA SF (≥8) Gabrielson25 90 Breast: 46 NA Active: 100 CT: 100

CRC: 24
Heme: 13
Other: 17
Abbreviations: CNS, central nervous system; CRC, colorectal cancer; CT, chemotherapy; GI, gastrointestinal; GYN, gynecological; heme, hematological;
HN, head and neck; HSCT, hematopoietic stem cell transplantation; ICT, induction chemotherapy; IV, intravenous; MNA, Mini Nutritional Assessment;
MST, Malnutrition Screening Tool; MUST, Malnutrition Universal Screening Tool; N, number of patients; NA, not available; NRS‐2002, Nutrition Risk
Screening‐2002; Panc, pancreas; PG‐SGA SF, Patient‐Generated Subjective Global Assessment Short Form; Post, after treatment; Pre, before treatment;
R, range; RT, radiation therapy; S, surgery.
TABLE 6 Recommended screening tools and levels of “ease Question 3. What are the recommended clinical
of use”. applications for malnutrition risk screening among adult
Ease of use Screening tool oncology outpatients?
Level 1 MST
Recommendation: All patients with cancer should undergo routine
Patient‐led MST
malnutrition risk screenings using a valid tool after diagnosis and
Level 2 NUTRISCORE throughout treatment. Risk identification calls for a comprehensive
PG‐SGA SF nutrition assessment by a trained nutrition professional, such as a re-
Level 3 MUST gistered dietitian nutritionist (RDN).

Rationale for recommendation: This recommendation is based on
NRS‐2002
our expert opinion and supported by multiple national and interna-
Level 4 MNA tional organizations who recommend regular malnutrition risk
Abbreviations: MNA, Mini Nutritional Assessment; MST, Malnutrition screening among adult oncology patients, including ASPEN, AND, the
Screening Tool; MUST, Malnutrition Universal Screening Tool; NRS‐2002, Commission on Cancer, and the ACCC.57–60 ASCO guidelines for
Nutrition Risk Screening‐2002; PG‐SGA SF, Patient‐Generated Subjective
geriatric oncology recommend evaluation of nutrition status in older
Global Assessment Short Form.
patients with cancer.61 The European Society for Clinical Nutrition
and Metabolism advises regular screening for malnutrition risk or
presence in all patients with cancer.55,62 An independent panel,
both encompassing two questions about weight and appetite, are convened during a National Institutes of Health workshop, also
designated as Level 1. NUTRISCORE incorporates two questions supports the recommendation of malnutrition screening at the time
from the MST and considers tumor site and treatment status, quali- of cancer diagnosis and at regular intervals throughout the course of
fying it as a Level 2. The PG‐SGA SF is a patient‐led tool derived from treatment and survivorship.63
the PG‐SGA designed to be straightforward for patients to complete What constitutes “routine” screening may depend on the type of
and is categorized as Level 2. The MUST and NRS‐2002 necessitate cancer, treatment course, and stability of the clinical situation. Screening
both BMI calculation and an indication of disease severity. These are is recommended every 4 to 8 weeks during treatment and may require
classified as Level 3. The MNA requires a clinical assessment and additional screening depending on the stage of treatment (eg, surgery or
anthropometrics, making it more time‐consuming and categorizing it radiotherapy/chemotherapy). Clinical judgment should guide the
as a Level 4. necessity of malnutrition screening during survivorship.
Ideally, screening tools should be “quick and easy” to use, with Timely identification of malnutrition is crucial in providing
minimal to no calculations, biological samples, complex measure- appropriate nutrition care. Those identified as at risk need a nutrition
ments, or clinical examinations. These criteria benefit facilities in assessment completed by an appropriately trained healthcare pro-
which staffing is limited. Although several screening tools are fessional, such as an RDN. Nutrition assessment should be conducted
straightforward and take into consideration additional factors such as regularly, particularly when clinical conditions change and should be
tumor site and treatment status, others demand detailed assess- part of regular clinical consultations.64
ments, disease severity indicators, and/or anthropometrics requiring To organize and perform screening for nutrition risk, assessment
more time and effort. Yet these advanced screening tools could of nutrition and metabolic parameters, medical nutrition therapy, and
provide a more comprehensive profile of a patient's nutrition status. monitoring of outcomes, each institution involved in treating patients
with cancer needs to define standard operating procedures, not collaboratively.67 A coordinated approach with defined respon-
responsibilities, and a quality control process.55 sibilities within the team is needed for malnutrition screening.
The success of the screening tool largely depends on the users. The lack of staffing and resources may limit the implementation
Nurses or ancillary staff are usually involved in the initial nutrition of screening measures. Unlike the inpatient setting, RDN staffing in
screening during new patient registration. Inputs from nutrition and ambulatory cancer settings is lacking.68 In the US, there is an average
nursing leadership are vital for choosing and implementing a of 1.7 full‐time equivalent RDNs employed in outpatient oncology
screening tool that is relevant for the target population and user‐ centers and one RDN for every 2308 patients.6 Reimbursement for
friendly. Establishing a multidisciplinary team for the selection and nutrition services is an obstacle to increasing RDN staffing. Many
implementation of the screening tool provides a deeper under- centers do not bill for nutrition services. Although medical insurance
standing of the work constraints and capabilities of the nurses and providers are increasingly covering nutrition counseling by RDN
other staff. This enables optimal use of their skills to gather the practitioners, the Centers for Medicare and Medicaid Services do not
necessary information.38 reimburse nutrition services for oncology patients.6
Staff need training and education before implementing a selected RDNs should be sufficiently staffed on cancer teams with high
screening tool. Communication should start early to ensure proper malnutrition rates, such as head/neck, or lung cancers and treatment
preparation. Refer to Table S6 for a staff checklist sample, useful for teams for chemotherapy and radiation therapy. The RDN presence in
implementing malnutrition screening. Continuous training may en- outpatient oncology care should match the prevalent need to manage
hance compliance and completion rates. The nutrition and nursing malnutrition effectively. The lack of sufficient RDNs in outpatient
teams need to establish a system to monitor and audit the consist- oncology teams can lead to gaps in patient care.
ency, accuracy, and appropriateness of screening procedures, and In the US, an estimated 1.9 million individuals were diagnosed
this may be established by selecting malnutrition as an ongoing with cancer in 2023.69 Considering that malnutrition affects 25% to
quality measure. Well‐defined roles for each healthcare professional 75% of patients with cancer,1–3 between 475,000 and 1.425 million
involved in nutrition screening is crurcial.38 The RDN should be an individuals may be at risk for malnutrition. Although achieving 100%
integral part of the care team. A policy needs to be in place defining screening might be challenging, screening rates of close to 75% are
the responsibilities of staff in the nutrition care process. feasible. Prior research confirms the integration of a large percentage
The electronic health record (EHR) enables streamlined screening of malnutrition screening into the EHR in ambulatory cancer cen-
and automated RDN referrals and consultations. Implementing ters.65 Seventy‐four percent of nearly 70,000 patients with cancer
nutrition screenings in the EHR is feasible and can offer consistent were screened for malnutrition using the MST in the EHR at two
long‐term results.65 Depending on the screening tool, the EHR pro- large institutions. Roughly 5% of patients with cancer undergoing
gramming may be straightforward, with the ability to automatically medical treatment were at risk, whereas approximately 12% of pa-
38
compute scores based on the responses to screening questions. tients undergoing radiation treatment were at risk.65
Programming screening tools that require more details may be Based on previous findings that oncology RDNs evaluate or
challenging to automate. Yet, even complex tools like the PG‐SGA counsel an average of 7.4 patients in an 8‐h workday,6 1.2 RDN full‐
have been successfully integrated with the Epic EHR system.66 time equivalents would be required to provide proactive nutrition
Storing data in the EHR grants easy access to previous screening counseling to patients identified at risk for malnutrition.65 Given that
information, offering valuable insights into nutrition changes in pa- the annual salary for practicing RDNs in the US in all positions is
tients over time and insights into facility management of patients at $70,000 per year,70 the 1.2 RDN full‐time equivalents would equate
nutrition risk. to $84,000 per year. Poor nutrition status is associated with higher
hospital costs. These high costs are primarily due to increased rates
of hospital admissions, readmissions, more frequent consultations
Other considerations with primary care providers, and increased use of medications.71–73
Consequently, the financial burden of failing to address malnutrition
Barriers in implementing malnutrition screening in is substantial.
outpatient cancer centers This review has several limitations. The studies were conducted
outside the US, limiting their applicability in the US healthcare sys-
Implementing malnutrition screening can be challenging, with barriers tem. Most research was focused on common solid tumors. Further-
including nonstandardized patient referral protocols, limited admin- more, the impact of malnutrition screening on clinical outcomes was
istrative support, competing staff time constraints, limited RDN ser- not reported by these studies and therefore cannot inform these
vices, lack of screening tools and implementation consensus, and recommendations. More work is required for hematologic malig-
limited frontline or nursing support.6 nancies. As GLIM is a relatively recent screening and assessment tool,
Varying responsibility for the identification of malnutrition is its use as a reference standard was less frequent. Finally, a more
another barrier.64 Even though healthcare professionals recognize structured methodology, like the Delphi method, could have provided
the role of nutrition in patient recovery, nutrition care often happens a clearer and more reliable framework for gathering expert opinions
in an isolated manner with team members working concurrently but and reaching clinical recommendations.
TABLE 7 Future research directions.

Topic area Study direction
Amplified research scope Study malnutrition and nutrition interventions across various cancer types, stages, and treatments, including in
outpatient settings.
Body composition measurement Develop better screening methods to capture body composition and identify loss of muscle volume or function
and develop more rigorous analysis of body composition's relationship with various cancer treatment outcomes.
Clinical outcomes Analyze the connection of screening to assessment, interventions, and clinical outcomes.
Cost‐effectiveness Evaluate the economic impact of preventing and treating malnutrition in cancer patients.
Diversity inclusion Study those with different body composition before and during treatment to understand the relationship
between physiologic muscle wasting and cancer treatment.
Early intervention Identify and intervene early in at‐risk and malnourished individuals.
Implementation Practice dissemination and implementation science to ensure malnutrition screening and follow‐on medical
nutrition therapy are routinely provided to all oncology patients.
Integrated approach Incorporate RDNs and their expertise into the healthcare team.
Intervention efficacy Develop more effective interventions.
Patient‐centered outcomes Investigate patient‐reported outcomes and the impact of malnutrition screening programs and multidisciplinary
interventions on quality of life, physical function, and symptom burden in advanced disease.
Standardization Determine the most effective and practical application of screening for various cancer patient populations and in
a variety of oncology settings.
Timing Study optimal timing for nutrition screening and intervention and frequency of screening.
Trajectory Research the longitudinal disease trajectory and changes in body composition/nutrition status.
Technological advances Assess the feasibility and effectiveness of remote screening, digital data capture, and telehealth referrals for at‐
risk patients.
Abbreviation: RDN, registered dietitian nutritionist.
Future research directions recommendations. This report provides a framework for healthcare
professionals. It clarifies who should be screened, the appropriate
There are existing knowledge gaps regarding nutrition risk screening, screening tools to be used, and the proper implementation.
its implementation, potential cost savings, and most importantly Indeed, barriers to implementing screening exist, but so do viable
potential improved health outcomes. Research is crucial to close solutions. Widespread standardization and implementation of
existing gaps and push the field forward. The end goal is to provide malnutrition screening would serve to reduce the massive under-
the necessary evidence and practice guidelines that can enhance diagnosis of this common and debilitating issue. Furthermore,
health outcomes through nutrition screening and interventions for appropriate screening would justify the additional funding and
patients with cancer. Table 7 outlines priority research topics and resources needed to optimally test how the timely management of
recommendations. malnutrition might improve the clinical care of oncology patients.
A UT H O R C O N T R I B U TI O NS
CONCL US I ONS Elaine B. Trujillo contributed to the conceptualization, data curation,
formal analysis, investigation, methodology, project administration,
Many patients in adult oncology ambulatory care are malnourished supervision, validation, visualization, original draft, and review and
and require timely medical nutrition therapy. Malnutrition screening editing. Kunal C. Kadakia contributed to the methodology, validation,
is crucial for the early identification of patients requiring nutrition review and editing, data curation, formal analysis, investigation, and
intervention and across various cancer types, stages, and treatments. project administration. Cynthia Thomson contributed to the review
There exist several validated and reliable screening tools for and editing, methodology, validation, conceptualization, data cura-
malnutrition risk identification in the ambulatory oncology population, formal analysis, investigation, project administration, software,
tion. Implementation is inexpensive, requires minimal time, and can and visualization. Fang Fang Zhang contributed to the methodology,
be efficient. validation, writing—review and editing, data curation, formal analysis,
We identified several validated screening tools that should be investigation, visualization. Alicia Livinski contributed to the meth-
integrated into cancer care and are the basis of our clinical odology, validation, conceptualization, data curation, formal analysis,
investigation, project administration, resources, software, and review Walsh is an American Society for Clinical Oncology representative.
and editing. Kim Pollard contributed to the methodology and review Kathleen Wiley is an Oncology Nursing Society representative.
and editing. Todd Mattox contributed to the conceptualization, data The working group was endorsed by the Academy of Oncology
curation, formal analysis, investigation, methodology, resources, Nurse and Patient Navigators, American Cancer Society, American
software, validation, and review and editing. Anne Tucker contributed Society for Nutrition, American Society for Radiation Oncology,
to the conceptualization, data curation, formal analysis, investigation, Association of Cancer Care Centers, and Oncology Nursing Society.
methodology, validation, and review and editing. Valaree Williams The working group was supported by the Academy of Nutrition and
contributed to the methodology and review and editing. Declan Dietetics.
Walsh contributed to the methodology and review and editing. Ste- Disclaimer: Any recommendations in this paper do not constitute
ven Clinton contributed to the review and editing. Aaron Grossberg medical or other professional advice and should not be taken as such.
contributed to the methodology, review and editing, and project To the extent that the information published herein may be used to
administration. Gordon Jensen contributed to the conceptualization, assist in the care of patients, this is the result of the sole professional
methodology, and review and editing. Rhone Levin contributed to the judgment of the attending healthcare professional whose judgment is
review and editing. Jeannine Mills contributed to the methodology the primary component of quality medical care. The information
and review and editing. Anurag Singh contributed to the methodol- presented here is not a substitute for the exercise of such judgment
ogy, review and editing, and project administration. Meredith Smith by the healthcare professional. Circumstances in clinical settings
contributed to the methodology and review and editing. Renee and patient indications may require actions different from those
Stubbins contributed to the review and editing. Kathleen Wiley recommended in this document and in those cases, the judgment of
contributed to the methodology and review and editing. Kristen the treating professional should prevail. This paper was approved by
Sullivan contributed to the methodology and review and editing. the ASPEN Board of Directors.
Mary Platek contributed to the conceptualization, data curation,
formal analysis, investigation, methodology, project administration, ORC I D
software, validation, visualization, original draft, and review and Elaine B. Trujillo http://orcid.org/0000-0002-8480-2427
editing. Colleen K. Spees contributed to the conceptualization, data Anne Tucker http://orcid.org/0000-0003-3431-0106
curation, formal analysis, investigation, project administration, Aaron Grossberg http://orcid.org/0000-0003-4690-4948
supervision, validation, methodology, original draft, and review and Gordon Jensen http://orcid.org/0000-0001-5223-7622
editing.
RE F ER EN CES
A C KN O W L E D G M E N T S 1. Bossi P, De Luca R, Ciani O, D'Angelo E, Caccialanza R. Malnutrition
We thank Samantha Werts‐Pelter for her support of our quality management in oncology: an expert view on controversial issues and
future perspectives. Front Oncol. 2022;12:910770.
evaluation.
2. Kadakia KC, Symanowski JT, Aktas A, et al. Malnutrition risk at solid
tumor diagnosis: the malnutrition screening tool in a large US cancer
CO NFL I CT OF INTERES T S T ATEME NT institute. Supp Care Cancer. 2022;30(3):2237‐2244.
The authors declare no conflict of interest. 3. Muscaritoli M, Lucia S, Farcomeni A, et al. Prevalence of malnutrition
in patients at first medical oncology visit: the PreMiO study.
Oncotarget. 2017;8(45):79884‐79896.
DIS CL OSURES 4. Nutrition in Cancer Care (PDQ)‐Health Professional Version. National
Aaron Grossberg received funding from the National Cancer Insti- Cancer Institute. Updated May 16, 2024. Accessed November 13,
tute, Brenden Colson Center for Pancreatic Care at Oregon Health & 2023. https://www.cancer.gov/about-cancer/treatment/side-effects/
appetite-loss/nutrition-hp-pdq
Science University, and Knight Cancer Institute. Anurag Singh
5. White JV, Guenter P, Jensen G, Malone A, Schofield M; Academy
received funding from the National Cancer Institute, Department of of Nutrition and Dietetics Malnutrition Work Group; A.S.P.E.N.
Defense, and National Comprehensive Cancer Network/Astra‐ Malnutrition Task Force; A.S.P.E.N. Board of Directors. Consensus
Zeneca. Anne Tucker received funding from Up to Date, Inc. Valaree statement of the Academy of Nutrition and Dietetics/American
Society for Parenteral and Enteral Nutrition: characteristics recom-
Williams received funding from AbbVie, Nestlé, Catalyst‐The Training
mended for the identification and documentation of adult mal-
Lab, and Great Valley Publishing. nutrition (undernutrition). J Acad Nutr Diet. 2012;112(5):730‐738.
Steve Clinton is an American Society for Clinical Oncology rep- 6. Trujillo EB, Claghorn K, Dixon SW, et al. Inadequate nutrition
resentative. Aaron Grossberg is an American Society for Radiation coverage in outpatient cancer centers: results of a national survey.
J Oncol. 2019;2019:7462940.
Oncology representative. Gordon Jensen is an American Society for
7. Reber E, Schönenberger KA, Vasiloglou MF, Stanga Z. Nutritional
Nutrition representative. Rhone Levin is an Association of Cancer risk screening in cancer patients: the first step toward better clinical
Care Centers representative. Jeannine Mills is an Academy of outcome. Front Nutr. 2021;8:603936.
Nutrition and Dietetics representative. Anurag Singh is an American 8. Serón‐Arbeloa C, Labarta‐Monzón L, Puzo‐Foncillas J, et al. Mal-
nutrition screening and assessment. Nutrients. 2022;14(12):2392.
Society for Radiation Oncology representative. Meredith Smith is an
9. Moher D, Shamseer L, Clarke M, et al.; PRISMA‐P Group. Preferred
Academy of Oncology Nurse and Patient Navigators representative. reporting items for systematic review and meta‐analysis protocols
Kristen Sullivan is an American Cancer Society representative. Declan (PRISMA‐P) 2015 statement. Syst Rev. 2015;4(1):1.
10. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 28. Oh SY, Koh SJ, Baek JY, et al. Validity and reliability of Korean
statement: an updated guideline for reporting systematic reviews. version of simplified nutritional appetite questionnaire in patients
BMJ. 2021;372:n71. with advanced cancer:a multicenter, longitudinal study. Cancer Res
11. Miller J, Wells L, Nwulu U, Currow D, Johnson MJ, Skipworth RJE. Treat. 2019;51(4):1612‐1619.
Validated screening tools for the assessment of cachexia, sarcope- 29. Orell‐Kotikangas H, Österlund P, Saarilahti K, Ravasco P, Schwab U,
nia, and malnutrition: a systematic review. Am J Clin Nutr. 2018; Mäkitie AA. NRS‐2002 for pre‐treatment nutritional risk screening
108(6):1196‐1208. and nutritional status assessment in head and neck cancer patients.
12. Whiting PF, Rutjes AWS, Westwood ME, et al.; QUADAS‐2 Group. Supp Care Cancer. 2015;23(6):1495‐1502.
QUADAS‐2: a revised tool for the quality assessment of diagnostic 30. Pan X, Wang C, Li R, et al Applicability of the nutrition risk screening
accuracy studies. Ann Intern Med. 2011;155(8):529‐536. 2002 combined with a Patient‐Generated Subjective Global
13. Abbott J, Teleni L, McKavanagh D, Watson J, McCarthy A, Assessment in patients with Nasopharyngeal carcinoma. Cancer
Isenring E. A novel, automated nutrition screening system as a Manag Res. 2020;12:8221‐8227.
predictor of nutritional risk in an oncology day treatment unit 31. Szefel J, Kruszewski WJ, Szajewski M, Ciesielski M, Danielak A.
(ODTU). Supp Care Cancer. 2014;22(8):2107‐2112. Bioelectrical impedance analysis to increase the sensitivity of
14. Abbott J, Teleni L, McKavanagh D, Watson J, McCarthy AL, screening methods for diagnosing cancer cachexia in patients with
Isenring E. Patient‐Generated Subjective Global Assessment Short colorectal cancer. J Nutr Metab. 2020;2020:3874956.
Form (PG‐SGA SF) is a valid screening tool in chemotherapy out- 32. Zhang YH, Xie FY, Chen YW, et al. Evaluating the nutritional status
patients. Supp Care Cancer. 2016;24(9):3883‐3887. of oncology patients and its association with quality of life. Biomed
15. Abe Vicente M, Barão K, Silva TD, Forones NM. What are the most Environ Sci. 2018;31(9):637‐644.
effective methods for assessment of nutritional status in outpatients 33. Detsky A, McLaughlin JR, Baker J, et al. What is subjective global
with gastric and colorectal cancer? Nutr Hosp. 2013;28(3):585‐591. assessment of nutritional status? JPEN J Parenter Enteral Nutr.
16. Arribas L, Hurtós L, Sendrós MJ, et al. NUTRISCORE: a new nutri- 1987;11(1):8‐13.
tional screening tool for oncological outpatients. Nutrition. 2017;33: 34. Ottery FD. Rethinking nutritional support of the cancer patient:
297‐303. the new field of nutritional oncology. Semin Oncol. 1994;21(6):
17. Boléo‐Tomé C, Monteiro‐Grillo I, Camilo M, Ravasco P. Validation of 770‐778.
the malnutrition universal screening tool (MUST) in cancer. Br J Nutr. 35. Cederholm T, Jensen GL, Correia MITD, et al. GLIM criteria for the
2012;108(2):343‐348. diagnosis of malnutrition—a consensus report from the global clinical
18. Carriço M, Guerreiro CS, Parreira A. The validity of the Patient‐ nutrition community. Clin Nutr. 2019;38(1):1‐9.
Generated Subjective Global Assessment Short‐form© in cancer 36. Ignacio de Ulíbarri J, González‐Madroño A, de Villar NG, et al.
patients undergoing chemotherapy. Clin Nutr ESPEN. 2021;43: CONUT: a tool for controlling nutritional status. First validation in a
296‐301. hospital population. Nutr Hosp. 2005;20(1):38‐45.
19. Chen Y, Xiang Q, Li C, et al. Nutritional risk and assessment for 37. Ferguson M, Capra S, Bauer J, Banks M. Development of a valid and
patients with cancer pain. Nutr Cancer. 2022;74(1):168‐174. reliable malnutrition screening tool for adult acute hospital patients.
20. De Groot LM, Lee G, Ackerie A, van der Meij BS. Malnutrition Nutrition. 1999;15(6):458‐464.
screening and assessment in the cancer care ambulatory setting: 38. House M, Gwaltney C. Malnutrition screening and diagnosis tools:
mortality predictability and validity of the Patient‐Generated Sub- implications for practice. Nutr Clin Pract. 2022;37(1):12‐22.
jective Global Assessment Short form (PG‐SGA SF) and the GLIM 39. Elia M The ‘MUST’ Report: Nutritional Screening of Adults: A Multi-
criteria. Nutrients. 2020;12(8):2287. disciplinary Responsibility. British Association for Parenteral and
21. Demirel B, Atasoy BM. Comparison of three nutritional screening Enteral Nutrition; 2003.
tools to predict malnutrition risk and detect distinctions between 40. Platek ME, Hertroijs DFL, Nicholson JM, Parekh N. Sensitivity and
tools in cancer patients receiving radiochemotherapy. Nutr Cancer. specificity of malnutrition screening tools used in the adult hos-
2018;70(6):867‐873. pitalized patient setting: a systematic review. Top Clin Nutr. 2015;
22. Di Bella A, Croisier E, Blake C, Pelecanos A, Bauer J, Brown T. Assessing 30(4):289‐301.
the concurrent validity and interrater reliability of patient‐led screening 41. Vellas B, Guigoz Y, Garry PJ, et al. The mini nutritional assessment
using the malnutrition screening tool in the ambulatory cancer care (MNA) and its use in grading the nutritional state of elderly patients.
outpatient setting. J Acad Nutr Diet. 2020;120(7):1210‐1215. Nutrition. 1999;15(2):116‐122.
23. Esfahani A, Somi MH, Asghari Jafarabadi M, et al. A new score for 42. Naber T, Schermer T, de Bree A, et al. Prevalence of malnutrition in
screening of malnutrition in patients with inoperable gastric ade- nonsurgical hospitalized patients and its association with disease
nocarcinoma. Jpn J Clin Oncol. 2017;47(6):475‐479. complications. Am J Clin Nutr. 1997;66(5):1232‐1239.
24. Faramarzi E, Mahdavi R, Mohammad‐Zadeh M, Nasirimotlagh B. 43. Buzby G, Williford W, Peterson O, et al. A randomized clinical trial of
Validation of nutritional risk index method against Patient‐ total parenteral nutrition in malnourished surgical patients: the
Generated Subjective Global Assessment in screening malnutrition rationale and impact of previous clinical trials and pilot study on
in colorectal cancer patients. Chin J Cancer Res. 2013;25(5):544‐548. protocol design. Am J Clin Nutr. 1988;47(2 suppl):357‐365.
25. Gabrielson DK, Scaffidi D, Leung E, et al. Use of an abridged scored 44. Kondrup J. Nutritional risk screening (NRS 2002): a new method
Patient‐Generated Subjective Global Assessment (abPG‐SGA) as a based on an analysis of controlled clinical trials. Clin Nutr. 2003;
nutritional screening tool for cancer patients in an outpatient set- 22(3):321‐336.
ting. Nutr Cancer. 2013;65(2):234‐239. 45. Kruizenga HM, Seidell JC, de Vet HCW, Wierdsma NJ, van Bokhorst–de
26. Gascón‐Ruiz M, Casas‐Deza D, Torres‐Ramón I, et al. Comparation van der Schueren MAE. Development and validation of a hospital
of different malnutrition screening tools according to GLIM criteria screening tool for malnutrition: the short nutritional assessment
in cancer outpatients. Eur J Clin Nutr. 2022;76(5):698‐702. questionnaire (SNAQ). Clin Nutr. 2005;24(1):75‐82.
27. Hettiarachchi J, Madubhashini P, Miller M. Agreement between the 46. Ravasco P. Nutrition in cancer patients. J Clin Med. 2019;8(8):1211.
malnutrition universal screening tool and the Patient‐Generated 47. Aaldriks AA, van der Geest LGM, Giltay EJ, et al. Frailty and mal-
Subjective Global Assessment for cancer outpatients receiving nutrition predictive of mortality risk in older patients with advanced
chemotherapy: a cross‐sectional study. Nutr Cancer. 2018;70(8): colorectal cancer receiving chemotherapy. J Geriatr Oncol. 2013;
1275‐1282. 4(3):218‐226.
48. Pressoir M, Desné S, Berchery D, et al. Prevalence, risk factors and 64. Kiss N, Loeliger J, Findlay M, et al. Clinical oncology society of
clinical implications of malnutrition in French comprehensive cancer Australia: position statement on cancer‐related malnutrition and
centres. Br J Cancer. 2010;102(6):966‐971. sarcopenia. Nutr Diet. 2020;77(4):416‐425.
49. Bozzetti F. Forcing the vicious circle: sarcopenia increases toxicity, 65. Trujillo EB, Shapiro AC, Stephens N, et al. Monitoring rates of mal-
decreases response to chemotherapy and worsens with chemo- nutrition risk in outpatient cancer centers utilizing the malnutrition
therapy. Ann Oncol. 2017;28(9):2107‐2118. screening tool embedded into the electronic health record. J Acad
50. Shen Y, Hao Q, Zhou J, Dong B. The impact of frailty and sarcopenia Nutr Diet. 2021;121(5):925‐930.
on postoperative outcomes in older patients undergoing gastrec- 66. Christie W. Malnutrition in cancer patients. Today's Dietitian. 2022;
tomy surgery: a systematic review and meta‐analysis. BMC Geriatr. 24(5):32.
2017;17(1):188. 67. Marshall AP, Takefala T, Williams LT, Spencer A, Grealish L, Roberts S.
51. Saitoh‐Maeda Y, Kawahara T, Miyoshi Y, et al. A low psoas muscle Health practitioner practices and their influence on nutritional intake of
volume correlates with a longer hospitalization after radical hospitalised patients. Int J Nurs Sci. 2019;6(2):162‐168.
cystectomy. BMC Urol. 2017;17(1):87. 68. Trujillo EB, Dixon SW, Claghorn K, Levin RM, Mills JB, Spees CK.
52. Löser A, Avanesov M, Thieme A, et al. Nutritional status impacts Closing the gap in nutrition care at outpatient cancer centers:
quality of life in head and neck cancer patients undergoing (chemo) ongoing initiatives of the oncology nutrition dietetic practice group.
radiotherapy: results from the prospective HEADNUT Trial. Nutr J Acad Nutr Diet. 2018;118(4):749‐760.
Cancer. 2022;74(8):2887‐2895. 69. American Cancer Society. Cancer Facts & Figures 2023. American
53. Ehrsson YT, Fransson P, Einarsson S. Mapping health‐related quality Cancer Society; 2023.
of life, anxiety, and depression in patients with head and neck cancer 70. Academy of Nutrition and Dietetics. Compensation & Benefits Sur-
diagnosed with malnutrition defined by GLIM. Nutrients. 2021;13(4): vey of the Dietetics Profession. Academy of Nutrition and Dietet-
1167. ics; 2021.
54. Beirer A. Malnutrition and cancer, diagnosis and treatment. Memo. 71. Kruizenga H, van Keeken S, Weijs P, et al. Undernutrition screening
2021;14:168‐173. survey in 564,063 patients: patients with a positive undernutrition
55. Arends J, Bachmann P, Baracos V, et al. ESPEN guidelines on screening score stay in hospital 1.4 d longer. Am J Clin Nutr. 2016;
nutrition in cancer patients. Clin Nutr. 2017;36(1):11‐48. 103(4):1026‐1032.
56. Arends J. Malnutrition in cancer patients: causes, consequences and 72. Leandro‐Merhi VA, Aquino JLB. Relationship between nutritional status
treatment options. Eur J Surg Oncol. 2024;50(5):107074. and the clinical outcomes of patients with and without neoplasms
57. American College of Surgeons, Commission on Cancer. Optimal according to multiple correspondence analysis. Arq Gastroenterol. 2017;
Resources for Cancer Care 2020 Standards. American College of 54(2):148‐155.
Surgeons; 2019. 73. Leandro‐Merhi VA, Braga de Aquino JL Comparison of nutritional
58. Cancer Nutrition Services. A Practical Guide for Cancer Programs. The diagnosis methods and prediction of clinical outcomes in patients
Association of Community Cancer Centers; 2012. with neoplasms and digestive tract diseases. Clin Nutr 2015;34(4):
59. Mueller C, Compher C, Ellen DM; American Society for Parenteral 647‐651.
and Enteral Nutrition (A.S.P.E.N.) Board of Directors. A.S.P.E.N.
Clinical Guidelines: Nutrition Screening, Assessment, and Interven-
tion in Adults. JPEN J Parenter Enteral Nutr. 2011;35(1):16‐24. SUPP ORTING INFO RM ATION
60. Thompson KL, Elliott L, Fuchs‐Tarlovsky V, Levin RM, Voss AC, Additional supporting information can be found online in the Sup-
Piemonte T. Oncology evidence‐based nutrition practice guideline porting Information section at the end of this article.
for adults. J Acad Nutr Diet. 2017;117(2):297‐310.e47.
61. Mohile SG, Dale W, Somerfield MR, et al. Practical assessment and
management of vulnerabilities in older patients receiving chemo-
therapy: ASCO guideline for geriatric oncology. J Clin Oncol. 2018; How to cite this article: Trujillo EB, Kadakia KC, Thomson C,
36(22):2326‐2347. et al. Malnutrition risk screening in adult oncology
62. Muscaritoli M, Arends J, Bachmann P, et al. ESPEN practical guideline: outpatients: an ASPEN systematic review and clinical
clinical nutrition in cancer. Clin Nutr. 2021;40(5):2898‐2913.
recommendations. J Parenter Enteral Nutr. 2024;48:874‐894.
63. Hiatt RA, Clayton MF, Collins KK, et al. The pathways to prevention
program: nutrition as prevention for improved cancer outcomes. doi:10.1002/jpen.2688
J Natl Cancer Inst. 2023;115(8):886‐895.

2024 - Trujillo - Malnutrition Risk Screening in Adult Oncology Outpatients an ASPEN Systematic

Uploaded by

Copyright:

Available Formats

2024 - Trujillo - Malnutrition Risk Screening in Adult Oncology Outpatients an ASPEN Systematic

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

2024 - Trujillo - Malnutrition Risk Screening in Adult Oncology Outpatients an ASPEN Systematic

Uploaded by

Copyright:

Available Formats

DOI: 10.1002/jpen.

Malnutrition risk screening in adult oncology outpatients: An

Elaine B. Trujillo MS, RDN1 | Kunal C. Kadakia MD2 |

874 | wileyonlinelibrary.com/journal/jpen J Parenter Enteral Nutr. 2024;48:874–894.

Malnutrition is present in 25% to 75% of patients with cancer,1–3

TABLE 1 Baseline population characteristics of included papers.

2020 supportive: 100

Szefel Cross‐sectional 70 ≥50 years 48.6 CRC: 100 NA NA NA OW or NRS‐2002 NA

Malnutrition screening tools evaluated for general NRS‐2002

Table 3 contains a summary of the validity scores of the index Others

TABLE 2 Characteristics of malnutrition screening tools.

TABLE 3 Summary of validity scores by malnutrition risk tool (index test).

MST GLIM 83 72 Accuracy: 76; k = 0.53 Gascon‐Ruiz (2021)26

MST (≥2) PG‐SGA BC 52 84 NA Abe Vicente (2013)15

MST (≥2) PG‐SGA BC 61.5 91.8 NA Abe Vicente (2013)15

MST (≥2) PG‐SGA BC 100 90 NA De Groot (2020)20

MST (≥2) SGA BC 81.3 72.4 AUC: 0.823 Gabrielson (2013)25

MUST (≥2) PG‐SGA BC 72 48.9 NA Abe Vicente (2013)15

MUST (≥2) PG‐SGA BC 84 73.4 NA Abe Vicente (2013)15

MUST (≥2) PG‐SGA BC 80 89 PPV: 87; NPV: 100 Boleo‐Tome (2012)17

MUST GLIM 86 81 Accuracy: 83; k = 0.66 Gascon‐Ruiz (2021)26

NRI (≤97.5 medium/ PG‐SGA BC 68 64 NA Abe Vicente (2013)15

NRI (≤97.5 medium/ PG‐SGA BC 55.8 83.6 NA Abe Vicente (2013)15

NRI (<83.5–100) PG‐SGA BC 66 60 PLR: 1.65; NLR: 0.56 Faramarzi (2013)24

NRS‐2002 (≥2) PG‐SGA ( ≥ 9) 96.8 70 Spearman r = 0.699 Chen (2022)19

NRS‐2002 (≥2) PG‐SGA ( ≥ 4) 96.9 (84–99) 78.8 (62–89) k = 0.754 Orell‐Kotikangas

NRS‐2002 (≥2) PG‐SGA ( ≥ 4) 76.3 90.9 MYI: Pan (2020)30

NRS‐2002 (≥3) PG‐SGA ( ≥ 9) 74.6 90 Spearman r = 0.468 Chen (2022)19

NRS‐2002 (≥3) PG‐SGA ( ≥ 9) 86.7 (62–96) 90 (79–96) k = 0.717 Orell‐Kotikangas

NRS‐2002 (≥3) PG‐SGA BC 77.3 (57–90) 97.7 (88–100) k = 0.784 Orell‐Kotikangas

NRS‐2002 PG‐SGA NA NA Spearman r: Zhang (2018)32

Reference Sensitivity Specificity

NUTRISCORE GLIM 64 88 Accuracy: 78; k = 0.54 Gascon‐Ruiz (2021)26

abPG‐SGA (≥6) SGA BC 93.8 77.6 AUC: 0.956 Gabrielson (2013)25

abPG‐SGA (≥7) SGA BC 84.4 89.7 AUC: 0.956 Gabrielson (2013)25

PG‐SGA SF (≥8) SGA BC 96.9 86.2 AUC: 0.967 Gabrielson (2013)25

PG‐SGA SF (≥3) PG‐SGA BC 80.4 72.3 NA Abbott (2016)14

PG‐SGA SF boxes 1–3 (≥2) PG‐SGA BC 90.2 67.5 NA Abbott (2016)14

PG‐SGA SF box 3 (≥1) PG‐SGA BC 82.4 69.9 NA Abbott (2016)14

PG‐SGA SF boxes 1 and PG‐SGA BC 86.3 71.1 NA Abbott (2016)14

PG‐SGA SF boxes 2 and PG‐SGA BC 82.4 63.1 NA Abbott (2016)14

PG‐SGA SF (≥2) PG‐SGA BC 92 76 AUC: 0.82 (0.77–0.86) Carrico (2021)18

PG‐SGA SF boxes 1 and PG‐SGA BC 75 80 AUC: 0.78 (0.73–0.83) Carrico (2021)18

PG‐SGA SF box 3 (≥2) PG‐SGA BC 71 82 AUC: 0.77 (0.73–0.82) Carrico (2021)18

PG‐SGA SF boxes 2 and PG‐SGA BC 79 75 AUC: 0.78 (0.73–0.83) Carrico (2021)18

PG‐SGA SF (≥5) PG‐SGA BC 89 80 PPV: 45; NPV: 98 De Groot (2020)20

PG‐SGA SF (≥4) PG‐SGA BC 92 71 PPV: 37; NPV: 98 De Groot (2020)20

PG‐SGA SF (≥3) PG‐SGA BC 94 62 PPV: 31; NPV: 98 De Groot (2020)20

CONUT GLIM 21 89 Accuracy: 61; k = 0.40 Gascon‐Ruiz (2021)26

MNA‐SF GLIM 99 45 Accuracy: 68 k = 0.12 Gascon‐Ruiz (2021)26

SNAQ PG‐SGA BC NA NA Visit 1 (n = 152) Oh (2019)28

Few studies examined the validity of screening tools in relation to

PG‐SGA SF ≥ 2 (1) Recommendation: Six tools—MNA, MST, MUST, NRS‐2002, NU-

PG‐SGA SF ≥ 7 (1) PG‐SGA SF ≥ 7 (1) PG‐SGA SF ≥ 7 Table 5.

PG‐SGA SF ≥ 8 (1) PG‐SGA SF ≥ 8 (1) PG‐SGA SF≥ 8

MST (≥2) Abe Vicente15 75 CRC: 85.3 III/IV: 82.7 Pre: 40 CT ± S

Abe Vicente15 62 CRC: 83.9 III/IV: 37.1 Post: 100 CT ± S

DeGroot20 246 Breast: 45 NA Active: 100 “In‐chair IV

Gabrielson25 90 Breast: 46 NA Active: 100 CT: 100

MST (≥2) patient‐led Di Bella22 201 NA NA Active: 100 CT or supportive: 100