Clinical Nutrition 42 (2023) 848e858

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Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu

Meta-analyses

Global prevalence of malnutrition in patients with chronic obstructive

pulmonary disease: Systemic review and meta-analysis
Mingming Deng a, 1, Ye Lu b, 1, Qin Zhang a, Yiding Bian a, Xiaoming Zhou c, Gang Hou a, *
a
Department of Pulmonary and Critical Care Medicine, Center of Respiratory Medicine, National Center for Respiratory Medicine, National Clinical Research
Center for Respiratory Diseases, China-Japan Friendship Hospital, Beijing, China
b
Department of Respiratory and Critical Care Medicine, Shengjing Hospital of China Medical University, Shenyang 110004, Liaoning Province, China
c
Respiratory Department, Center for Pulmonary Vascular Diseases, Fuwai Hospital, National Center for Cardiovascular Diseases, Chinese Academy of
Medical Sciences and Peking Union Medical College, Beijing, China

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

Article history: Background: Malnutrition is a significant comorbidity among chronic obstructive pulmonary disease
Received 18 December 2022 (COPD), but it has been often ignored. To date, the prevalence of malnutrition and its association with
Accepted 5 April 2023 clinical parameters in the patients with COPD have not been well described. We aimed to investigate the
prevalence of malnutrition and the prevalence of at-risk for malnutrition among COPD and the clinical
Keywords: impact of malnutrition on patients with COPD in a systematic review and meta-analysis.
Chronic obstructive pulmonary disease
Methods: PubMed, Embase, Cochrane Library, and Web of Science were searched for articles describing
Malnutrition
the prevalence of malnutrition and/or at-risk for malnutrition from January 2010 to December 2021.
Risk for malnutrition
Nutrition status
Eligibility screening, data extraction, and quality assessment of the retrieved articles were conducted
Prevalence independently by two reviewers. Meta-analyses were performed to determine the prevalence of
malnutrition and at-risk for malnutrition and the clinical impact of malnutrition on patients with COPD.
Meta-regression and subgroup analyses were performed to explore the sources of heterogeneity. Com-
parisons were made between individuals with and without malnutrition according to pulmonary
function, degree of dyspnea, exercise capacity, and mortality risk.
Results: Out of the 4156 references identified, 101 were read full-text, of which 36 studies were included.
The total number of involved patients included in this meta-analysis was 5289. The prevalence of
malnutrition was 30.0% (95% CI 20.3 to 40.6), compared with an at-risk prevalence of 50.0% (95% CI 40.8
to 59.2). Both prevalences were associated with regions and measurement tools. The prevalence of
malnutrition was associated with COPD phase (acute exacerbations and stable). COPD with malnutrition
showed lower forced expiratory volume 1 s % predicted (mean difference (MD) -7.19, 95% CI -11.86 to
-2.52), higher modified Medical Research Council dyspnea scores (MD 0.38, 95% CI 0.12 to 0.64), poorer
exercise tolerance (standardized mean difference -0.29, 95% CI -0.54 to -0.05), and higher mortality risk
(hazard ratio 2.24, 95% CI 1.23 to 4.06) compared to COPD without malnutrition.
Conclusion: Malnutrition and at-risk for malnutrition are common among COPD. Malnutrition negatively
impacts important clinical outcomes of COPD.
© 2023 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

1. Introduction
Chronic obstructive pulmonary disease (COPD) is a common
worldwide chronic respiratory disease with high morbidity and
* Corresponding author. Department of Pulmonary and Critical Care Medicine,
Center of Respiratory Medicine, China-Japan Friendship Hospital, 2 Yinghuayuan
East Street, Chaoyang District, Beijing 100029, China.
E-mail address: hougangcmu@163.com (G. Hou).
1
These two authors contributed equally to the study.
mortality [1]. The social and economic burden of COPD is increasing
and has become an important public health issue worldwide. The
comorbidities of COPD have received increasing attention from
researchers in relevant fields; however, nutrition-related comor-
bidities of COPD, especially malnutrition, have commonly been
ignored [2,3]. Due to malnutrition's silent epidemic, health experts
are urging countries to pay attention to it and intervene [4]. There is
a linke between malnutrition and decreased quality of life, reduced
lung function, increased exacerbations, and hospitalizations in
patients with COPD [5]. However, the prevalence of malnutrition

https://doi.org/10.1016/j.clnu.2023.04.005
0261-5614/© 2023 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
M. Deng, Y. Lu, Q. Zhang et al.
Abbreviations
COPD Chronic Obstructive Pulmonary Disease
AE-COPD Acute Exacerbations of Chronic Obstructive
Pulmonary Disease
CI Confidence Interval
BMI Body Mass Index
FEV1 Forced Expiratory Volume 1 Second
MNA Mini Nutritional Assessment
MNA-SF Short-Form Mini-Nutritional Assessment
SGA Subjective Global Assessment
PG-SGA Scored Patient-Generated Subjective Global
Assessment
ESPEN European Society for Clinical Nutrition and
Metabolism
GLIM Global Leadership Initiative on Malnutrition
NRS-2002 Nutritional Risk Screening 2002
MST Malnutrition Screening Tool
MUST Malnutrition Universal Screening Tool
GNRI Geriatric Nutritional Risk Index
DLCO Diffusion Capacity of Lung for Carbon Monoxide
mMRC modified Medical Research Council
6MWD 6-Minute Walk Distance
GOLD Global Initiative for Chronic Obstructive Lung
Disease
reported in patients with COPD varies widely, ranging from 10 to
60% [6]. This wide variation may be related to choice of nutritional
measurement tools, differences in disease status, and mixing of
patients with malnutrition and those at-risk of malnutrition [7e9].
Underestimating the incidence of malnutrition may further
underrate the importance of nutritional assessment in patients
with COPD in clinical practice. Therefore, there is an urgent need to
aggregate and analyze different studies to come up with a unified
estimate of the prevalence of malnutrition in this population. Based
on current economic and social conditions, the prevalence of
malnutrition and the prevalence of at-risk for malnutrition can be
used as the best evidence-based basis for estimating the prevalence
of nutritional disorder in patients with COPD on a global scale.
Therefore, the aim of our study was to pool the prevalence of
malnutrition and the prevalence of at-risk for malnutrition and the
association between malnutrition and clinical parameters in the
patients with COPD in a systematic review and meta-analysis.
2. Methods
This study was executed in accordance with the Preferred
Reporting Items for Systematic Reviews and Meta-analysis
(PRISMA) guidelines. According to the PRISMA guidelines, in the
current study, the populations were adult patients with COPD, the
exposures were individuals with malnutrition or at-risk for
malnutrition, the comparators were individuals without malnu-
trition or nutritional risk, and the outcomes were the prevalence
and impact of malnutrition on health outcomes in patients with
COPD. This meta-analysis was registered in PROSPERO
(CRD42022301482; www.crd.york.ac.uk/prospero).
2.1. Search strategy
An electronic database search was conducted from January 1,
2010, to December 31, 2021 in four electronic databases (PubMed,
Embase, Cochrane Library, and Web of Science), mainly using the
849
Clinical Nutrition 42 (2023) 848e858
following subject heading and free-text terms: “Pulmonary Dis-
ease, Chronic Obstructive”, “Chronic Obstructive Lung Disease”,
“COAD”, “Chronic Obstructive Pulmonary Diseases”, “Chronic
Obstructive Airway Disease”, “COPD”, “Chronic Obstructive Pul-
monary Disease”, “Airflow Obstruction, Chronic”, “Chronic Airflow
Obstructions”, “Airflow Obstructions, Chronic”, “Chronic Airflow
Obstruction”, “Malnutrition”, “Nutritional Deficiency”, “Nutritional
Deficiencies”, “Undernutrition”, “Malnourishment”, “Malnourish-
ments”, “Nutritional Status”, “Status, Nutritional”, “Nutrition Sta-
tus”, “Status, Nutrition”. An English language restriction was
applied. A hand search of reference lists from the included articles
was also conducted to identify additional potential studies
(Supplemental Material Table S1).
2.2. Selection criteria
Studies included in this review were those reporting the asso-
ciation between nutrition status and COPD as well as those using
valid and objective methods to diagnose COPD rather than self-
reporting. Both observational studies (cross-sectional studies and
cohorts) and clinical trials (randomized and nonrandomized) were
included in our study. The prevalence of malnutrition and the
prevalence of at-risk for malnutrition were reported as a percentage
or calculated from the results. The diagnosis of malnutrition and the
diagnosis of at-risk for malnutrition were based on the following
measurement tools: Subjective Global Assessment (SGA), Scored
Patient-Generated Subjective Global Assessment (PG-SGA), Mini
Nutritional Assessment (MNA), Short-Form Mini-Nutritional
Assessment (MNA-SF), Global Leadership Initiative on Malnutrition
(GLIM) criteria, European Society for Clinical Nutrition and Meta-
bolism (ESPEN) criteria, French criteria 2007, Nutritional Risk
Screening 2002 (NRS-2002), Malnutrition Screening Tool (MST),
Malnutrition Universal Screening Tool (MUST), and Geriatric Nutri-
tional Risk Index (GNRI). The exclusion criteria were as follows: (1)
The study type was a review, case report, conference abstract,
comment, or editorial, (2) The diagnosis of malnutrition was only by
low body mass index (BMI) and/or low fat-free mass index were
excluded as they may jeopardize the malnutrition diagnosis [10],
and (3) The data were obviously incorrect or incomplete.
2.3. Study screening and data extraction
The full texts of relevant studies were reviewed independently
by two authors (M.D. and Y.L.) after the titles and abstracts were
screened. Reference lists of relevant articles were manually
searched. A cross-check of the following data was performed
independently by two authors (M.D. and Y.L.): first author, publi-
cation year, country, study design, setting, sample size, prevalence
of malnutrition or prevalence of at-risk for malnutrition, age, sex,
predicted forced expiratory volume 1 s (FEV1% predicted), BMI,
measurement tool, nutritional status, COPD phase (acute exacer-
bations of COPD [AE-COPD] and stable COPD), Global Initiative for
Chronic Obstructive Lung Disease (GOLD) stage, sarcopenia status,
and clinical impact of malnutrition: spirometry parameters, dys-
pnea symptoms, exercise capacity, and mortality risk. Any dis-
agreements were discussed by the two authors or resolved with
help from a third author (X.Z.).
2.4. Quality assessment
The Joanna Briggs Institute (JBI) critical appraisal checklist was
used for studies reporting prevalence data [11], while the
NewcastleeOttawa Scale (NOS) was used for caseecontrol and
cohort studies [11]. According to the JBI Critical Appraisal Checklist,
we classified the studies as follows: high quality (7e9 “Yes”
M. Deng, Y. Lu, Q. Zhang et al.
responses); moderate quality (4e6 “Yes” responses); low quality
(1e3 “Yes” responses). An NOS score of 0e3, 4 to 6, or 7 to 9 de-
scribes a study as low quality, moderate quality, or high quality. An
independent quality assessment procedure was conducted by the
two authors (M.D. and Y.L.), and disagreements were resolved by a
third author (X.Z.).
2.5. Statistical analysis
The proportion of patients with COPD who had abnormal
nutritional status in different studies was pooled to estimate the
prevalence of malnutrition and the prevalence of at-risk for
malnutrition in a meta-analysis. To avoid counting twice, estimates
from different studies that used multiple measurement tools to
assess nutritional disorder were combined using their primary
diagnostic criteria. Data analyses were performed by using Stata SE
14.2 (Texas, USA). Freeman-Tukey double arcsine transformation of
prevalence data was applied before pooling and results were back
transformed [12,13]. A random effect was used for all pooled
prevalences and pooled prevalence was reported with 95% confi-
dence intervals (CIs), and heterogeneity based on I2 statistics. P <
0.05 was considered statistically significant. Sensitivity analysis
was carried out to evaluate the impact of each study on the overall
results. Funnel plot and Egger's test were used to evaluate publi-
cation bias. The trim and fill method was used if publication bias
was observed [14].
Meta-regression for continuous variables (sample size, publi-
cation year, mean age, percentage of males, mean FEV1% predicted,
and mean BMI) and subgroup analysis for categorical variables
(geographical region, setting, COPD phase, GOLD stage, sarcopenia
status, and measurement tool) were used to explore the prevalence
variation across studies. Multivariable meta-regressions were also
performed with variables that were significantly associated at the
univariate level. Clinical impact outcomes from studies comparing
patients with COPD who had malnutrition to those who did not
were meta-analyzed using Review Manager 5.4 software. Mean
differences (homogeneous data) or standardized mean differences
(heterogeneous data) and 95% CIs were calculated for continuous
variables. A pooled hazard ratio was calculated based on studies
that provided this information. Random-effects models were used
as the primary method of analysis, and the I2 statistic was used to
describe statistical heterogeneities [15].
3. Results
3.1. Study selection
Figure 1 shows the search and screening flow diagram. The
meta-analysis included 36 publications with 5289 participants.
According to the included studies, the overall quality was “high”
and “moderate” (Supplemental Material Table S2). The prevalence
of malnutrition was reported in 24 studies [2,5,7,8,16e35] and the
prevalence of at-risk for malnutrition was reported in 26 studies
[7,8,16,18,21,24e30,32,35e47].
3.2. Study characteristics
Table 1 gives details on the included studies and their sample
size, which ranged from 29 [7] to 460 [16]. Based on the included
studies, the mean age of participants was 55.6e78.1 years (n ¼ 35).
The male-to-female ratio was 2.23:1 (3654 vs. 1635) in these
studies. Most of the studies were conducted in Asia (16 studies),
followed by Europe (13 studies). A summary of the measurement
tools used to assess the nutritional status in the included studies is
presented (Supplemental Material Table S3).
850
Clinical Nutrition 42 (2023) 848e858
3.3. Prevalence of malnutrition and at-risk for malnutrition
The pooled prevalence of malnutrition in patients with COPD
was 30.0% (95% CI, 20.3 to 40.6) (Fig. 2A). The pooled prevalence of
at-risk for malnutrition in patients with COPD was 50.0% (95% CI,
40.8 to 59.2) (Fig. 2B). The included studies showed significant
heterogeneity (I2 ¼ 97.59% and I2 ¼ 96.77%, respectively; both P <
0.001). The sensitivity analysis, in which the meta-analysis was
serially repeated after exclusion of each study, demonstrated that
no individual study negatively affected the overall prevalence es-
timate obviously (Supplemental Material Figs. S1AeB). Visual ex-
amination of the funnel plot (Supplemental Material Figs. S2AeB)
and Egger's test (Supplemental Material Table S4) (P < 0.001)
revealed publication bias. The results of the trim and fill method
indicated that the results were robust (Supplemental Material
Table S5) (Supplemental Material Figs. S3AeB).
3.4. Meta-regressions and subgroup analyses
In meta-regression analyses, both mean age and mean BMI were
associated with malnutrition prevalence among patients with
COPD (P < 0.05) (Supplemental Material Table S6). No factors were
found to contribute to the heterogeneity in at-risk for malnutrition
prevalence (P > 0.05) (Supplemental Material Table S6).
In subgroup analyses (Table 2), geographic region, setting,
sarcopenia status, COPD phase, and measurement tool were
associated with the prevalence of malnutrition (P < 0.05). The
highest prevalence of malnutrition was 53.5% (95% CI 48.7 to 58.3)
in South America (Brazil). The lowest prevalence of malnutrition
was 16.1% (95% CI 12.4 to 20.1) in Oceania (Australia). The preva-
lence of malnutrition was higher in studies conducted in inpatient
setting (43.0%, 95% CI 26.4 to 60.4) compared with other settings.
The prevalence of malnutrition in the sarcopenia group (65.7%,
95% CI 55.0 to 75.7) was higher than that in the non-sarcopenia
group (15.2%, 95% CI 5.7 to 27.9). The prevalence of malnutrition
in the AE-COPD group (51.8%, 95% CI 31.2 to 72.1) was higher than
that in the stable COPD group (20.7%, 95% CI 11.1 to 32.2)
(P ¼ 0.009). Malnutrition was found to be higher in GOLD stages
IIIeIV group (50.0%, 95% CI 31.7 to 68.4) than those in GOLD stages
IeII group (31.5%, 95% CI 10.9 to 56.7); however, this difference was
not statistically significant (P ¼ 0.244). To provide a range of the
malnutrition prevalence estimates identified by these methodo-
logically diverse studies, estimates were stratified by measure-
ment tool. The malnutrition prevalence estimates ranged from
7.6% for MNA (95% CI 3.5 to 12.9) to 52.5% for SGA (95% CI 33.3 to
71.3) (Table 2).
In subgroup analyses (Table 3) of at-risk for malnutrition prev-
alence, geographic region, setting and measurement tool were
associated with the prevalence (p < 0.05). The highest prevalence
was 76.0% (95% CI 66.4 to 84.0) in Africa (Egypt). The lowest
prevalence was 31.2% (95% CI 24.6 to 38.1) in Oceania (Australia).
The prevalence of at-risk for malnutrition was higher in studies
conducted in inpatient setting (60.3%, 95% CI 47.7 to 72.3) compared
with other settings. The prevalence in the AE-COPD group was
59.0% (95% CI 43.8 to 73.3) and was higher than that in the stable
COPD group, which was 46.2% (95% CI: 37.1 to 55.5); similarly, the
prevalence in GOLD stages IIIeIV group were 60.6% (95% CI 37.8 to
81.2) and was higher than that in the GOLD stages IeII group, which
was 32.9% (95% CI 15.6 to 52.8); However, both differences were not
statistically significant (P > 0.05). To provide a range of the at-risk
for malnutrition prevalence estimates identified by these meth-
odologically diverse studies, estimates were stratified by mea-
surement tools. The at-risk for malnutrition prevalence estimates
ranged from 21.3% for MUST (95% CI 17.7 to 25.2) to 59.9% for NRS-
2002 (95% CI 45.2 to 73.7) (Table 3).
M. Deng, Y. Lu, Q. Zhang et al.
Fig. 1. Flow diagram of the study selection process and numbers of studies identified.
3.5. Clinical impact of malnutrition status on patients with COPD
We investigated whether malnutrition was associated with
FEV1% predicted, modified Medical Research Council (mMRC) score,
and exercise capacity in patients with COPD. For the meta-analysis
of the FEV1% predicted data, 11 studies [2,5,7,8,17,19,23,26,27,32,35]
showed that patients with malnutrition had lower FEV1% predicted
levels with a mean difference of -7.19 (95% CI -11.86 to -2.52;
I2 ¼ 81%, P < 0.05) (Fig. 3A).
The pooled data of six studies [2,8,18,19,27,35] on the mMRC
score showed that patients with malnutrition had a higher mMRC
score than patients without malnutrition (mean difference 0.38;
95% CI 0.12 to 0.64; I2 ¼ 60%, P < 0.05) (Fig. 3B).
Data from five studies were available for meta-analysis of ex-
ercise capacity [2,8,17,26,27]. These were measured via 6-min walk
distance (6MWD) [8,17,26,27] and incremental shuttle walking test
[2]. Patients with malnutrition were associated with poorer exer-
cise capacity than those without malnutrition (SMD -0.29, 95% CI
-0.54 to -0.05; I2 ¼ 48%, P < 0.05) (Fig. 3C).
A total of four studies [8,19,27,31] explored the association
between malnutrition and mortality in patients with COPD, and
found that malnutrition increased mortality risk (hazard ratio
2.24, 95% CI 1.23 to 4.06; I2 ¼ 6%, P < 0.05) (Fig. 3D). There was only
851
Clinical Nutrition 42 (2023) 848e858
one prospective study that explored the correlation between
malnutrition and 1-year acute exacerbations among patients with
stable COPD, and the MNA-SF score was associated with acute
exacerbations (relative risk 0.69, 95% CI 0.48 to 0.99, P ¼ 0.046)
[35].
4. Discussion
In this meta-analysis, 30.0% of patients with COPD were
malnourished, and 50.0% were at-risk for malnutrition. Meta-
regressions indicated that mean age and mean BMI were nega-
tively associated with prevalence of malnutrition. Geographical
region, setting, and measurement tool were associated with het-
erogeneity in malnutrition prevalence and at-risk for malnutrition
prevalence, while sarcopenia status and COPD phase were also
sources of heterogeneity in the prevalence of malnutrition.
Our study found that mean age was negatively associated with
prevalence of malnutrition among patients with COPD. Cosio et al.
[48] found that COPD early in life had a more intense and different
inflammatory response as compared to COPD later in life. Agustí
et al. [49] found that FEV1% predicted ＜80% in early adulthood was
associated with earlier incidence of comorbidities and premature
death as compared to FEV1% predicted ＜80% in later adulthood. A
 Table 1

M. Deng, Y. Lu, Q. Zhang et al.

Characteristic of participants.

First author (Year)/country Study design Setting No. (%) Sample size Mean ± SD Measurement tool
of nutrition status
Malnutrition At-risk for Male Age, y FEV1% predicted BMI, kg/m2
prevalence malnutrition
prevalence

Battaglia (2011)/Italy [16] Cross-section Outpatient 17 (3.7) 141 (30.7) 376 (81.7) 460 75.0 ± 5.9 54.7 ± 18.3 27.1 ± 5.3 MNAa,b
de Araújo (2021)/Brazil [19] Cohort study Inpatient 120 (50.0) 112 (46.7) 240 68.3 ± 10.2 46 ± 18.2 (n ¼ 241) NA SGAa
Marco (2019)/Spain [27] Prospective cohort Rehabilitation 29 (24.6) 61 (51.7) 95 (80.5) 118 66.6 ± 9.0 37.3 ± 13.4 26.2 ± 6.4 ESPEN criteriaa
MNA-SFb
D

avalos-Yerovi (2021)/Spain [8] Prospective cohort Rehabilitation 75 (44.9) 83 (49.7) 135 (80.8) 167 66.5 ± 9.0 38.36 26.9 ± 6.4 GLIM criteriaa
MNA-SFb
de Blasio (2018)/Italy [20] Cross-section Rehabilitation 52 (19.8) 185 (70.3) 263 69.8 ± 8.0 41.66 26.1 ± 5.7 ESPEN criteriaa
Yoshikawa (2014)/Japan [35] Prospective cohort other 7 (11.7) 29 (48.3) 58 (96.7) 60 72.3 ± 9.2 51.1 ± 19.8 21.0 ± 3.5 MNA-SFa,b
Hsu (2014)/China [24] Cross-section Rehabilitation 4 (4.8) 32 (38.6) 79 (95.2) 83 74.7 ± 7 60.7 ± 20.4 23.7 ± 3.86 MNA-T1a,b
Matkovic (2017)/Croatia [28] Cross-section Outpatient 3 (2.7) 44 (39.6) 76 (68.5) 111 67.7 ± 7.8 48.9 ± 15 27.1 ± 5.8 MNAa,b
Hogan (2017)/Vietnam [7] Cross-section Outpatient 13 (44.8) 6 (20.7) 25 (86.2) 29 69.7 ± 9.6 57 ± 19.7 21.1 ± 3.4 SGAa
MSTb
Nguyen (2019)/Vietnam [5] Cross-section Outpatient 125 (74.4) 151 (89.9) 168 63.9 ± 8.5 49.3 ± 23.1 20 ± 3.2 SGAa
Odencrants (2013)/Sweden [30] Cross-section other 7 (8.6) 41 (50.6) 34 (42.0) 81 65 ± 3.5 NA NA MNAa,b
Dhakal (2015)/Nepal [21] Cross-section Inpatient 55 (55.0) 73 (73.0) 36 (36.0) 100 NA NA NA MNA-SFa,b
Perrot (2020)/France [31] Cross-section Inpatient 28 (51.9) 37 (68.5) 54 68 ± 9 45 ± 16 26.9 ± 7.8 French criteria 2007a
Gupta (2010)/India [22] Cross-section Inpatient 88 (83.0) 92 (86.8) 106 55.58 ± 7.82 55.61 20.58 SGAa
Ingadottir (2018)/Iceland [25] Prospective cohort Inpatient 25 (20.7) 67 (55.4) 52 (43.0) 121 73.7 ± 9 45.7 ± 20.9 22.4 ± 14 ESPEN criteriaa
NRS-2002b
Mete (2018)/Turkey [29] Cross-section Inpatient 18 (17.1) 73 (69.5) 97 (92.4) 105 64.6 ± 10.2 NA NA MNAa,b
Teixeira (2021)/Brazil [33] Prospective cohort Inpatient 102 (58.3) 77 (44.0) 175 68.2 ± 10.4 46.4 ± 19 NA SGAa
Hoong (2017)/Australia [23] Prospective cohort Outpatient 47 (16.4) 194 (67.8) 286 66.6 ± 11 63.81 27.7 SGAa
Kalu

zniak-Szymanowska (2021)/Poland [26] Cross-section Rehabilitation 28 (22.6) 38 (30.6) 74 (59.7) 124 69.4 ± 6.1 50.62 27.99 GLIMa
852

MNA-SFb
Ruby (2021)/Egypt [32] Case-control Outpatient 45 (45.0) 76 (76.0) 100 (100.0) 100 68.12 ± 3.75 48.08 ± 16.81 26.09 ± 5.93 MNA-SFa,b
Ter Beek (2020)/Netherlands [34] Cross-section Rehabilitation 26 (45.6) 28 (49.1) 57 61.2 ± 8.7 36.1 ± 14.7 23.2 ± 4.6 PG-SGAa
Günay (2013)/Turkey [2] Cohort study Outpatient 65 (39.9) 145 (89.0) 163 64.15 ± 8.64 34.46 ± 16.91 23.68 ± 5.97 SGAa
Benedik (2011)/Slovenia [18] Case-control Inpatient 15 (13.9) 93 (86.1) 81 (75.0） 108 71 ± 10 NA 27.0 ± 6.3 MNAa,b
Bauer (2011)/Australia [17] Cohort study Rehabilitation 11 (15.3) 22 (30.6) 72 66.4 ± 8.7 47.8 ± 19.7 26.5 ± 6.5 PG-SGAa
Horadagoda (2017)/Australia [42] Cross-section Inpatient 38 (40.4) 51 (54.3) 94 69.8 ± 8.2 29.1 ± 11.6 25.9 ± 7.7 MSTb
Arslan (2016)/Turkey [36] Prospective cohort Inpatient 50 (55.6) 49 (54.4) 90 68.76 ± 10.85 45.56 NA NRS-2002b
Collins (2018)/UK [39] Prospective cohort Outpatient 93 (21.9) 222 (52.4) 424 72.9 ± 9.982 NA 25.8 ± 6.4 MUSTb
Chen (2018)/China [38] Retrospective cohort Inpatient 239 (54.6) 333 (76.0) 438 70.28 ± 10.16 NA 21.11 ± 3.59 NRS-2002b
Cui (2015)/China [40] Prospective cohort Inpatient 176 (75.5) 163 (70.0) 233 70.29 NA NA NRS-2002b
Huang (2021)/China [43] Retrospective cohort Inpatient 41 (43.2) 80 (84.2) 95 69.94 ± 8.34 38.95 21.15 NRS-2002b
Baldemir (2021)/Turkey [37] Cohort study Inpatient 238 (91.2) 174 (66.67) 261 76.03 ± 7.61 NA 23.94 ± 4.96 NRS-2002b
Fekete (2021)/Hungary [41] Cross-section other 9 (18.0) 19 (38.0) 50 66.30 ± 9.66 45.52 ± 16.18 26.26 ± 6.17 MUSTb
Matsumura (2015)/Japan [45] Cross-section other 33 (52.4) 63 (100.0) 63 78.1 ± 6.6 48 ± 25.54 20.74 ± 3.22 GNRIb
Ogan (2020)/Turkey [46] Prospective cohort Outpatient 20 (48.8) 36 (87.8) 41 71.7 ± 9.2 44.5 ± 14.3 26.1 ± 4.8 NRS-2002b
Shan (2015)/China [47] Prospective cohort Inpatient 25 (43.1) 58 (100.0) 58 62.78 30.93 21.16 NRS-2002b
Law (2016)/Australia [44] Retrospective cohort Inpatient 20 (22.2) 45 (50.0) 90 70.67 40.67 25.89 MSTb

Clinical Nutrition 42 (2023) 848e858

Abbreviations: FEV1, forced Expiratory volume in 1 s; BMI, body mass index; NA, not applicable; MNA, mini nutritional assessment; MNA-SF, short-form mini-nutritional assessment; SGA, subjective global assessment; PG-SGA,
scored patient-generated subjective global assessment; GLIM, global leadership initiative on malnutrition; ESPEN, European society for clinical nutrition and metabolism; NRS-2002, nutritional risk screening 2002; MST,
malnutrition screening tool; MUST, malnutrition universal screening tool; GNRI, geriatric nutritional risk index.
a
For assessment of malnutrition.
b
For assessment of at-risk for malnutrition.
M. Deng, Y. Lu, Q. Zhang et al. Clinical Nutrition 42 (2023) 848e858

Fig. 2. Forest plot showing the prevalence of malnutrition and the prevalence of at-risk for malnutrition among patients with COPD. (A) prevalence of malnutrition among patients
with COPD; (B) prevalence of at-risk for malnutrition among patients with COPD. ES, Effect Size; CI, Confidence Interval; COPD, Chronic Obstructive Pulmonary Disease. Random
effects model used for analysis.

853
M. Deng, Y. Lu, Q. Zhang et al. Clinical Nutrition 42 (2023) 848e858

Table 2
Subgroups analyses of malnutrition.

Sample size N Prevalence, % (95%CI) I2 (%) P

Total (24) 3351 1005 30.0 (20.3e40.6) 97.59 ＜0.001

Region 3351 1005 30.0 (20.3e40.6) 97.59 ＜0.001a
Asia (8) 814 375 39.7 (19.0e62.5) 97.64 ＜0.001
Africa (Egypt) (1) 100 45 45.0 (35.0e55.3) NA NA
South America (Brazil) (2) 415 222 53.5 (48.7e58.3) NA NA
Europe (11) 1664 305 21.0 (11.6e32.2) 96.10 ＜0.001
Oceania (Australia) (2) 358 58 16.1 (12.4e20.1) NA NA
Setting 3351 1005 30.0 (20.3e40.6) 97.59 ＜0.001a
Outpatient (7) 1317 315 28.7 (9.4e53.1) 98.71 ＜0.001
Inpatient (8) 1009 451 43.0 (26.4e60.4) 96.74 ＜0.001
Rehabilitation (7) 884 225 23.9 (14.3e35.1) 92.22 ＜0.001
Other (2) 141 14 9.9 (5.3e15.5) NA NA
Sarcopenia status 441 108 40.3 (16.8e66.4) 96.02 ＜0.001a
Sarcopenia (3) 105 68 65.7 (55.0e75.7) NA NA
Non-sarcopenia (3) 336 40 15.2 (5.7e27.9) NA NA
COPD phase 2513 740 29.1 (17.6e42.2) 97.85 0.009a
Stable COPD (12) 1784 360 20.7 (11.1e32.2) 96.65 ＜0.001
AE-COPD (5) 729 380 51.8 (31.2e72.1) 96.87 ＜0.001
GOLD stage 1007 450 41.5 (27.6e56.2) 95.31 0.244a
I ~ II (7) 370 154 31.5 (10.9e56.7) 95.77 ＜0.001
III ~ IV (8) 637 296 50.0 (31.7e68.4) 95.42 ＜0.001
Measurement tool 3351 1005 30.0 (20.3e40.6) 97.59 ＜0.001a
MNA (6) 948 64 7.6 (3.5e12.9) 83.72 ＜0.001
MNA-SF (3) 260 107 36.1 (13.7e62.1) NA NA
GLIM criteria (2) 291 103 35.0 (29.6e40.6) NA NA
PG-SGA (2) 129 37 27.5 (20.0e35.6) NA NA
SGA (7) 1167 560 52.5 (33.3e71.3) 97.70 ＜0.001
ESPEN criteria (3) 502 106 21.2 (17.6e24.8) NA NA
French criteria 2007 (1) 54 28 51.9 (37.8e65.7) NA NA

Abbreviations: CI, confidence interval; NA, not applicable; COPD, chronic obstructive pulmonary disease; AE-COPD, acute exacerbations of COPD; GOLD, global Initiative for
chronic obstructive lung disease; MNA, mini nutritional assessment; MNA-SF, short-form mini-nutritional assessment; SGA, subjective global assessment; PG-SGA, scored
patient-generated subjective global assessment; GLIM, global leadership initiative on malnutrition; ESPEN, European society for clinical nutrition and metabolism.
a
P value between group.

Table 3
Subgroups analyses of at risk-for malnutrition.

Sample size N Prevalence,% (95% CI) I2 (%) P

Total (26) 3704 1839 50.0 (40.8e59.2) 96.77 ＜0.001

Region 3704 1839 50.0 (40.8e59.2) 96.77 ＜0.001a
Asia (13) 1656 1035 55.6 (44.7e66.0) 95.09 ＜0.001
Africa (Egypt) (1) 100 76 76.0 (66.4e84.0) NA NA
Europe (10) 1764 670 43.3 (31.3e55.7) 96.12 ＜0.001
Oceania (Australia) (2) 184 58 31.2 (24.6e38.1) NA NA
Setting 3704 1839 50.0 (40.8e59.2) 96.77 ＜0.001a
Outpatient (6) 1165 380 39.3 (24.8e54.8) 95.64 ＜0.001
Inpatient (12) 1793 1133 60.3 (47.7e72.3) 96.42 ＜0.001
Rehabilitation (4) 492 214 0.42.7 (32.9e52.8) 80.31 0.002
Other (4) 254 112 42.1 (27.0e57.9) 84.53 ＜0.001
COPD phase 2498 1254 51.6 (42.4e60.7) 95.11 0.159a
AE-COPD (7) 1153 719 59.0 (43.8e73.3) 95.94 ＜0.001
Stable COPD (10) 1345 565 46.2 (37.1e55.5) 90.54 ＜0.001
GOLD stage 531 271 48.3 (31.9e64.8) 93.13 0.073a
I ~ II (5) 166 62 32.9 (15.6e52.8) 84.63 ＜0.001
III ~ IV (6) 365 209 60.6 (37.8e81.2) 94.85 ＜0.001
Measurement tool 3704 1839 50.0 (40.8e59.2) 96.77 ＜0.001a
MNA (6) 948 424 53.1 (33.8e71.9) 96.83 ＜0.001
MNA-SF (6) 669 360 55.1 (41.0e68.8) 92.55 ＜0.001
NRS-2002 (8) 1337 856 59.9 (45.2e73.7) 96.27 ＜0.001
MUST (2) 474 102 21.3 (17.7e25.2) NA NA
GNRI (1) 63 33 52.4 (39.4e65.1) NA NA
MST (3) 213 64 28.2 (16.0e42.2) NA NA

Abbreviations: CI, confidence interval; NA, not applicable; COPD, chronic obstructive pulmonary disease; AE-COPD, acute exacerbations of COPD; GOLD, global Initiative for
chronic obstructive lung disease; MNA, mini nutritional assessment; MNA-SF, short-form mini-nutritional assessment; NRS-2002, nutritional risk screening 2002; MST,
malnutrition screening tool; MUST, malnutrition universal screening tool; GNRI, geriatric nutritional risk index.
a
P value between group.

further study of the mechanisms behind COPD comorbidities is BMI was negatively associated with the prevalence of malnu-
required to investigate whether some comorbidities are more trition among COPD in our meta-analysis. BMI is an important
associated with COPD starting earlier in life. component of many malnutrition measurement tools, but using it

854
M. Deng, Y. Lu, Q. Zhang et al. Clinical Nutrition 42 (2023) 848e858

Fig. 3. Clinical impact of malnutrition in patients with COPD. (A) Forest plot for effect of malnutrition on FEV1% predicted; (B) Forest plot for effect of malnutrition on mMRC; (C)
Forest plot for effect of malnutrition on exercise capacity; (D) Forest plot for malnutrition impact on mortality in patients with COPD. CI, Confidence Interval; COPD, Chronic
Obstructive Pulmonary Disease. Random effects model used for analysis.*The hazard ratios from studies adjusted for confounders. **The hazard ratios from study not adjusted for
confounders.

alone may underestimate malnutrition prevalence [19,50,51],
especially among patients with COPD in the following circum-
stances. (1) Patients with severe COPD may exhibit peripheral
edema due to right heart failure or fluid retention caused by chronic
carbon dioxide retention. Elevated BMI cannot effectively reflect
the nutritional status [52]. (2) The vertebral column degeneration
in elderly patients leads to an underestimation of height [53]. (3) It
is difficult to determine the nutritional status by BMI alone of pa-
tients with sarcopenic obesity among COPD, which is characterized
by muscle loss and fat gain [54].
The prevalence of malnutrition is influenced by geographic re-
gions, which can reflect the negative effects of the social and eco-
nomic factors in developing countries [55]. The areas with higher
prevalence are more likely to have nutritional disorders due to a lack
of nutritious foods and differences in dietary habits. Low- and
middle-income countries have low access to lung function testing,
insufficient COPD screening, few effective treatment measures, and a
lack of attention to the public health prevention of COPD [56].
However, the literature included in the current study was mainly
from Asia and Europe. Therefore, the conclusion of regional differ-
ences in the prevalence still needs to be confirmed by further studies.
Our analysis showed that the malnutrition was much more
prevalent in sarcopenia group than in non-sarcopenia group. The
COPD patients with sarcopenic malnutrition might have poorer
survival [31]. The lack of calories and protein required to maintain
muscle mass is thought to cause sarcopenia. And sarcopenia, in
turn, may further aggravate malnutrition by reducing mobility [26].
A causal relationship between sarcopenia and malnutrition could
not be determined in the study due to the small number and the
cross-section design of the studies. More studies are required in the
future, regarding the association between the sarcopenia and
malnutrition in COPD.

855
M. Deng, Y. Lu, Q. Zhang et al.
Based on our subgroup analysis, patients with AE-COPD had
higher prevalence of malnutrition than patients with stable COPD.
This may be related to the increase in resting energy consumption,
further decrease in food intake and physical activity, and further
increase in inflammatory factors [44]. Nutritional interventions for
AE-COPD can improve their prognosis and reduce the length of
hospital stay, and the risk of 30-day re-hospitalization [57]. This
suggests that attention should be paid to the screening and
assessment of malnutrition among AE-COPD. Additionally, we
sought to summarize whether malnutrition increases the risk of
acute exacerbation of COPD, but only one prospective study found
this result [35]. In the future, it will be worthwhile to explore how
malnutrition and acute exacerbations of COPD relate, especially if
they influence each other to promote the deterioration.
The GOLD stage was not the source of heterogeneity in the
prevalence of malnutrition in our meta-analysis. GOLD stage is
based on FEV1% predicted to assess the severity of airflow limita-
tion. As a heterogeneous disease, COPD exhibits a wide range of
clinical symptoms. Therefore, a single pulmonary function index
cannot comprehensively assess the severity and prognosis of COPD
[58,59]. There is still a lack of research on whether the prevalence of
malnutrition varies according to the levels of multidimensional
indicators. It is now widely recognized that COPD is a systemic
disease. Therefore, as one of the comorbidities of COPD, malnutri-
tion may be influenced by several factors, such as systemic
inflammation and exercise tolerance etc., which may explain the
lack of its association with GOLD stage.
The measurement tool influenced the malnutrition prevalence
and the at-risk for malnutrition prevalence among patients with
COPD. To interpreting the results of this meta-analysis, it is impor-
tant to note that the prevalence estimates were generated by
different measurement tools due to the lack of gold-standard di-
agnostics for malnutrition. Currently, most nutrition measurement
tools are without capable for adequate validity, especially when they
are used alone [60]. The MNA in particular has been poorly validated
against some kind of other nutrition measurement tools [9,61,62].
Additionally, the “risk of malnutrition” forwarded by MNA-SF has
only been referenced to the full version of the MNA questionnaire,
which has yet to be fully validated in an appropriated way. There-
fore, to reflect the heterogeneity of the measures included in this
meta-analysis, a range of prevalence estimates (7.6%e52.5% for
malnutrition prevalence vs. 21.3%e59.9% for at-risk for malnutrition
prevalence) were reported in addition to a single measure (30.0% vs.
50.0%). At present, the malnutrition assessment tools used in COPD
are mostly developed from other special populations. In addition,
there are no specific sreening tools for at-risk for malnutrition in
COPD. NRS-2002 might perform well in predicting outcome [60].
Considering the benefit of prevention for malnutrition, high levels of
validity, agreement, and reliability tools for screening of at-risk for
malnutrition are important [63]. It is possible to improve nutritional
status through a variety of interventions with effective-based evi-
dence. Oral nutritional supplementation, for example, may prevent
further weight loss and increase FFMI in the patient with COPD; In
some cases, smaller volumes/calories maybe more appropriate;
Additionally, education and advice about nutrition may have short-
term effects on intake [64,65]. Since malnutrition is a complex
subject, there is not yet a world-wide gold standard for malnutri-
tion. A variety of malnutrition screening and assessment tools have
been developed with the original intent and focus of calling on
clinicians to identify malnutrition and focus on the impact of
malnutrition on patients' prognosis and clinical symptoms. Overall,
the most urgent thing is to use these proven tools to increase the
identification for malnutrition.
Our results further suggest that malnutrition had a consistently
negative impact on clinical outcomes of COPD, affecting FEV1%
856
Clinical Nutrition 42 (2023) 848e858
predicted, mMRC, and exercise capacity. We also found that
malnutrition increased the risk of death in patients with COPD.
Further studies need to be conducted to confirm the association
between malnutrition and mortality in patients with COPD due to
the small number of included studies. Considering these negative
effects, it is necessary to be vigilant about the occurrence of
malnutrition in COPD. In the future clinical practice, physicians
should pay more attention to nutritional screening of COPD.
The study had several limitations. First, heterogeneity between
the different measures in evaluation of the prevalence estimates is
obviously. Heterogeneity in epidemiological meta-analyses
exploring the prevalence of conditions could vary consistently
across studies and is nowadays largely accepted, when proper
study of heterogeneity is performed [66e71]. Second, about 44%
(16/36) of the studies were conducted in inpatient setting. The
prevalence estimates might be overestimate. It is necessary to
conduct more epidemiological studies on malnutrition in patients
with COPD to investigate the accurate prevalence. Third, unpub-
lished and non-English studies were excluded. Finally, The results
of this study reflect the lack of consensus and difficulty in diag-
nosing malnutrition in patients with COPD. There is a need for a
consensus to establish the criteria for diagnosing malnutrition in
COPD to ensure accurate diagnosis and lower the misclassification
rates. Given these limitations, the results should be interpreted
with caution. Larger multi-center studies evaluating malnutrition
prevalence in patients with COPD and using standardized criteria
for defining malnutrition in COPD are urgently needed.
5. Conclusion
The prevalence of malnutrition and the prevalence of at-risk for
malnutrition among COPD were 30.0% and 50.0%, respectively.
Malnutrition has a negative impact on important clinical outcomes
of patients with COPD. Given malnutrition's negative impact on
health outcomes, it may be worthwhile to focus future strategies on
early detection of malnutrition during clinical assessments of pa-
tients with COPD to mitigate its impact on individuals' lives.
Author contributions
Mingming Deng and Ye Lu contributed equally to this article. GH
conceived this manuscript and was responsible for conceptualiza-
tion and study design. MD, YL, and XZ conducted the database
search, study evaluation, and data extraction. MD and YL conducted
the statistical analysis. MD, YL, XZ, QZ, and YB participated in the
manuscript writing and revising. All authors interpreted the data
analyses. All authors have read and approved the final manuscript.
Funding statement
This research was supported by National High Level Hospital
Clinical Research Funding (2022-NHLHCRF-LX-01), the Elite Medi-
cal Professionals project of China-Japan Friendship Hospital (No.
ZRJY2021-BJ08), the Non-profit Central Research Institute Fund of
Chinese Academy of Medical Sciences (No. 2020-PT320-001).
Funding information for this article has been deposited with the
Crossref Funder Registry.
Availability of data and material
Upon request to the corresponding author.
Conflicts of interest
All the authors report no conflicts of interest in this work.
M. Deng, Y. Lu, Q. Zhang et al.
Acknowledgements
None.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.clnu.2023.04.005.
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