Clinical Nutrition ESPEN 49 (2022) 246e251

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Clinical Nutrition ESPEN

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

Original article

Chronic obstructive pulmonary disease outpatients bear risks of both

unplanned weight loss and obesity
Tobias Christensen b, Sabina Mikkelsen b, Lea Geisler b, Mette Holst a, b, *
a
Department of Clinical Medicine, Aalborg University, Denmark
b
Centre for Nutrition and Intestinal Failure, Aalborg University Hospital, Denmark

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

Article history: Background & aims: Malnutrition is commonly seen in chronic obstructive pulmonary disease (COPD)
Received 4 December 2021 and has been associated with negative outcomes. The objective of this study was to examine unintended
Accepted 11 April 2022 weight loss (UWL) within three months, as a primary indicator for disease related malnutrition among
COPD outpatients, to evaluate the prevalence of UWL, and to identify possible characteristics for UWL.
Keywords: Methods: A cross-sectional study including a patient questionnaire and medical record data extraction
Malnutrition
was made with all patients visiting a Danish COPD outpatient clinic.
Chronic obstructive pulmonary disease
Results: Among the 200 included patients (68.7 ± 11.2 years of age), UWL was seen in 21.5%, with a
Outpatients
Initial screening
median weight loss of 3.5 (2e16) kg. Underweight (BMI<18.5 kg/m2) was recognized in 13.5%, while
Unintended weight loss 34.5% were obese (BMI>30 kg/m2). Reduced food intake (RFI) within the past week was experienced
Nutrition impact symptoms among 22.0% of the patients. The most common nutrition impact symptoms (NIS) were shortness of
breath, reduced appetite and nausea. NIS, RFI and BMI<18.5 kg/m2 were associated to UWL, while co-
morbidities, hospitalization within three months and resent exacerbations showed no association to
UWL.
Conclusions: A high prevalence of UWL was found in COPD outpatients, and NIS and RFI as characteristics
associated with UWL. Shortness of breath, reduced appetite and nausea were the most common NIS. This
study found 13.5% of patients underweight, 23.5 overweight and 34.5% obese. Underweight as well as
obesity may have negative consequences for the patient and the community.
© 2022 The Author(s). Published by Elsevier Ltd on behalf of European Society for Clinical Nutrition and
Metabolism. This is an open access article under the CC BY license (http://creativecommons.org/licenses/
by/4.0/).

1. Introduction have been shown to be malnourished and it has been frequently

shown and unintended weight loss (UWL) in the previous 3e12
Malnutrition is a commonly seen problem and is often caused by months, depending on setting is often reported [9,11,12,15]. UWL is
an underlying disease [1]. Malnutrition challenges the individual as included as an element in all malnutrition risk screening tools used
well as the community, as it is associated with depression, reduced in COPD patients [16e18]. Malnourished COPD patients have been
physical ability, longer hospitalizations and rehabilitation, reduced shown to be at greater risk of further exacerbations, and the risk of
quality of life, poorer response to treatment and increased mor- negative outcomes accelerates with stage of COPD from mild/
tality [1e8]. Malnutrition and low body mass index (BMI) among moderate to severe [9,15,19].
patients diagnosed with chronic obstructive pulmonary disease Reduced food intake (RFI) among COPD patients affects the
(COPD) is widely known [9e11]. Several studies found that COPD patients muscle strength, which may potentially lead to worsened
patients with low BMI experience decreased lung function and respiratory muscle function [19]. RFI among COPD patients is also
spirometry values [12e15]. Among patients with COPD, 10e45% associated with low physical activity, which reduces skeletal
muscle mass and bone tissue [9,18]. It is difficult to determine
whether malnutrition is caused by worsening of COPD but based
* Corresponding author. Department of Clinical Medicine, Aalborg University and on previous studies an association between malnutrition and the
Centre for Nutrition and Intestinal Failure, Department of Gastroenterology, Aalborg stage of COPD is known. Based on existing evidence, there is a
University Hospital, Sdr. Skovvej 5, 1. 9000, Denmark.
E-mail addresses: tobiasc311@gmail.com (T. Christensen), sabina.l.mikkelsen@
need for a greater attention to strengthening nutritional status
live.dk (S. Mikkelsen), l.geisler@rn.dk (L. Geisler), mette.holst@rn.dk (M. Holst). among COPD patients. Therefore, The Danish Health Authority

https://doi.org/10.1016/j.clnesp.2022.04.010
2405-4577/© 2022 The Author(s). Published by Elsevier Ltd on behalf of European Society for Clinical Nutrition and Metabolism. This is an open access article under the CC BY
license (http://creativecommons.org/licenses/by/4.0/).
T. Christensen, S. Mikkelsen, L. Geisler et al. Clinical Nutrition ESPEN 49 (2022) 246e251

recommend further focus for early detection for nutritional risk The patients were recruited in the waiting room before their
among COPD patients [20], however the outpatient setting is not clinical consultation. The investigator approached the patients and
mentioned in this statement. Not all patients with COPD need gave oral and written information about the study. If the patients
nutritional intervention and since nutritional screening, assess- wanted to participate in the study, they signed the statement of
ment and intervention are time-consuming tasks that require consent, and thereafter the questionnaire was completed along
specific knowledge, we find it relevant to identify the prevalence with the measurements of height and weight. The patients either
of UWL and whether UWL may be used as initial indicator for completed the questionnaire by themselves or the investigator sat
further nutritional screening in the COPD outpatient clinic. next to them and helped fill it out based on the patients informa-
According to The Danish Association for Pulmonary Diseases, tion. The database “Clinical suite” was used to access the patients’
2019, 160.000 Danish patients are diagnosed with COPD and it is medical records by the investigator afterwards.
assumed that the double amount remain undiagnosed. Patients
are followed in general practice when stable, and unstable pa- 2.3. Questionnaire
tients, as well as patients confined to oxygen therapy are mainly
followed in the outpatient clinic. There are no numbers for The questionnaire was developed by last author and it was
nutritional risk in COPD patients in outpatient clinics, and no tested in prior studies [21,22]. In total, there were five questions.
recommendations for screening patients for disease-related The first questions were the background questions: Gender (male,
malnutrition in Danish outpatient clinics. Screening patients for female or other), age (years), weight (kg), height (cm) and educa-
malnutrition may enable nurses or dieticians when available, to tion level (none, shorter courses, vocational, short, medium or long
initiate an early nutritional effort in patients at risk of negative education). Thereafter, 2. UWL (yes or no), if yes then the amount
outcomes related to malnutrition. In the outpatient clinic, clini- of weight loss (kg), 3. Reduced food intake (RFI) within the last
cians (nurses and doctors) have a very short time for contacts week (yes or no), 4. Intended weight loss (yes or no), if yes then the
with patients and therefore tools used for screenings must be amount of weight loss (kg). 5. Nutrition impact symptoms (NIS)
targeted and not take too long to use. In Denmark dieticians are (nausea and/or worries and/or appetite and/or shortness of breath
rarely represented in the pulmonary outpatient clinics, which and/or lack of help for cooking/shopping and/or pain and/or
may be due to this lack of numbers for the prevalence of swallowing problems and/or constipation and/or discomfort in
malnutrition risk. the mouth and throat and/or do not like eating alone). The pa-
Therefore, the aim of this study was to examine the prevalence tients were able to apply more than one answer at question 5.
of UWL within the past three months among patients affiliated to a UWL was defined as a minimum of two kilos of stable weight loss
COPD outpatient clinic, and to identify if UWL may be a relevant (disregarding day to day change) within three months [23,24]. RFI
indication used as initial indicator for further nutritional screening was defined as an estimated intake less than 75% compared to
in the outpatient clinic. Furthermore, the second aim was and to usual [16,25].
identify possible nutritional risk factors for UWL among patients.
2.4. Statistical analysis
2. Materials and methods
REDCap (Research Electronic Data Capture) was used for data
This study was a cross-sectional study based on a patient management and STATA (version STATA/MP 16.1 for Windows) was
questionnaire as well as data collected from medical records. We used to complete the statistical analysis. Chi2 tests and simple lo-
consecutively included the entire sample of COPD patients affili- gistic regression analysis were performed regarding associations
ated to the COPD outpatient clinic at a Danish University Hospital. between UWL and the independent variables. A significance level
Inclusions were made during a period of six months, from of 0.05 was used (p < 0.05). Reference group was chosen as the
November 2020 to May 2021. Data collection was extended due to group with the highest number of records.
COVID-19. Missing data were excluded from the analysis. For descriptive
statistics, number of filled-in replies (N) and percent (%),
2.1. Sample mean ± standard deviation (SD) or median ± range were pre-
sented. As the patients could give more than one answer at
The COPD outpatient clinic is organized and physically placed question 5, some of the included patients seem duplicated in the
within the Department of Pulmonary Diseases. The COPD popula- descriptive statistics. UWL was used as the only dependent vari-
tion visiting the outpatient clinic is a quite heterogeneous popu- able. Independent variables were: Sex, age, BMI, Gold stage, RFI,
lation. This COPD outpatient clinic currently follows 218 patients, NIS, asthma, emphysema, hospitalization, smoking, education
and we aimed to include all patients, in order for the study to be level and civil status. All independent variables were assumed
representative of our population, and to meet the sample of Mete potential risk factors for UWL. BMI was categorized regarding to
et al. [13]. Most patient past the age of 65 are furthermore affiliated the WHO-definition [26]. To describe severity of COPD, data of
to a community COPD database, for which they measure and enter forced expiratory volume (FEV-1) were categorized by Global
their weight weekly. These community data are not associated with Initiative for Chronic Obstructive Lung Disease (GOLD) grading
the hospital patient records. system as used in former studies [27].

2.2. Procedure 2.5. Ethical considerations

Inclusion criteria were 1.
18 years of age and 2. willing to sign The study was forwarded to the ethical committee, who found
an informed consent after written and oral information in Danish that further approval was not required according to the Danish
or English. Patients were excluded if did not want to be weighed, legislation. The North Jutland data protection agency approved the
could not clearly report a weight measured within the past week, study, application ID 2020e119. The study was performed accord-
did not want to have height measured or could not clearly report ing to the Helsinki declaration of 2013 [28]. Patients gave written
their height measured within the past year. informed consent at inclusion.

247
T. Christensen, S. Mikkelsen, L. Geisler et al. Clinical Nutrition ESPEN 49 (2022) 246e251

3. Results Table 2
Nutritional status and weight loss.

3.1. Demographic data Variable N (%)/median Total ¼ n

(range)
In this study 200 patients affiliated to a Danish University BMI Groups, kg/m2 (n (%)) 200
Hospital COPD outpatient clinic were included. Eighteen patients Underweight <18.5 27 (13.5)
were not included in the study, which gave a response rate of 92%. Normal weight 18.5e24.9 57 (28.5)
Pre-obesity 30.0e34.9 47 (23.5)
Of these, eight patients did not want to be weighed or did not know
Obesity
35 69 (34.5)
or want to share information about current weight, three could not Unintended weight loss, yes (n (%)) 43 (21.5) 200
oversee participation, two were not able to provide informed Unintended weight loss, kg (median, range) 3.5 (1e16) 42
written consent, and five were missed while the investigator was Reduced food intake, yes (n (%)) 44 (22.0) 200
Unintended weight loss þ 17 (39.5) 44
measuring other patients. Demographic data are presented in
reduced food intake, yes (n (%))
Table 1. Intended weight loss, yes (n (%)) 7 (3.5) 200
Intended weight loss, kg (median, range) 2.5 (1e6) 6
3.2. Nutritional status and weight loss

Within the included patients, a few were underweight (BMI Table 3

<18.5 kg/m2), and more than one third had a BMI of 30 or above. We Nutrition impact symptoms.
found that 21.5% of the patients reported UWL within the past three Variable, N ¼ 183 N (%)
months with a median weight loss of 3.5 kg (2e16 kg). Almost one
Experience nutrition impact symptoms, es (n (%)) 84 (42.0)
fourth suffered RFI in the past week, and many of the patients with
UWL also had RFI. Intended weight loss within the past three Which nutrition impact symptoms? yes (n (%))
Shortness of breath 52 (61.9)
months was only seen in few. Data are presented in Table 2.
Reduced appetite 36 (42.9)
NIS were seen among 42% of patients. Shortness of breath, Nausea 21 (25.0)
reduced appetite and nausea were the most pronounced NIS. Data Swallowing problems 14 (16.7)
are presented in Table 3. Pain 11 (13.1)
Worries 11 (13.1)
Constipation 5 (6.0)
3.3. Lung function and COPD related variables
Oral problems (pain, mouth sores, fungus) 4 (4.8)
Do not like eating alone 4 (4.8)
Among the included patients, close to one third were catego- Lack of help for cooking/shopping 2 (2.4)
rized with moderate COPD severity and a little more with severe
COPD according to GOLD stage. Asthma-COPD overlap syndrome
(ACOS) was found common and many had emphysema. Within the Table 4
past three months, 12.6% of the patients had been hospitalized Lung function and hospitalizations.
caused by COPD exacerbation, and a little less had been hospital- Variable N (%) Total ¼ n
ized for other reasons than COPD. COPD municipality rehabilitation
Gold stage, FEV1 (%) (n (%)) 164
was noted in 196 of patient records. Of these, 155 were offered Mild >80 14 (8.5)
municipality rehabilitation. Between these, 49 refused, four did not Moderate 50-80 51 (31.1)
take the whole program, 73 completed the entire program and 29 Severe 30-50 60 (36.6)
accepted rehabilitation but no information was provided on status Very Severe <30 39 (23.8)
Lack of Alfa-1-antitrypsin, yes (n (%)) 13 (6.6) 197
for completion. Data about lung function and diagnose related
Asthma-COPD overlap syndrome, yes (n (%)) 51 (26.7) 191
variables are presented in Table 4. Emphysema (hyperinflation), yes (n (%)) 118 (60.2) 196
Hospitalization COPD exacerbation 25 (12.6) 199
3.4. Associations related to unintended weight loss in the last 3 months, yes (n (%))
Hospitalization other reasons in 21 (10.6) 199
the last 3 months, yes (n (%))
A significant association was found between UWL and BMI, RFI Non-invasive ventilation at home, yes (n (%)) 12 (6.0) 199
and NIS. Patients who were underweight had higher OR for UWL.

Table 1 Furthermore, patients who experienced RFI and NIS had higher OR
Demographic data. for UWL. No significant association was shown between UWL and
Variable N (%), median (range), Total ¼ n
gender, age, GOLD Stage, asthma, emphysema, smoking, hospitali-
mean ± SD zation related to COPD, hospitalization for other reasons, education
level or civil status. Results are presented in Table 5.
Sex, woman (n (%)) 111 (55.5) 200
Age, years (mean ± SD) 68.7 (11.2) 200
BMI, kg/m2 (median (range)) 26.7 (12.9e61.3) 200
Education (n (%))
4. Discussion
Non or shorter courses 87 (43.5) 200
Short or Vocational (1e3 years) 90 (45.0) This cross-sectional study accepted the hypothesis of high
Medium long or long (>3 years) 23 (11.5) prevalence of UWL in COPD outpatients, and NIS and RFI as char-
Civil status (n (%)) 200
acteristics associated with UWL. Shortness of breath, reduced
Live alone 90 (45.0)
Cohabitant 110 (55.0) appetite and nausea were the most common NIS. In this study, we
Smoking (n (%)) 197 examined the prevalence of UWL as an initial indicator for disease
Never smokes 7 (3.6) related malnutrition in COPD patients in an outpatient clinic. We
Former smoker 156 (79.2) found that 21.5% of the included patients suffered UWL within the
Smoker 34 (17.3)
past three months, with a median weight loss of 3.5 kg. The
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T. Christensen, S. Mikkelsen, L. Geisler et al. Clinical Nutrition ESPEN 49 (2022) 246e251

Table 5 had higher odds for UWL (p < 0.05). Existing evidence found that
Associations related to UWL. underweight and weight loss contribute to the risk of exacerbations
Unintended weight loss (yes) and progress stage of COPD [15,30], and RFI may lead to loss of body
OR [95% CI] p-value
weight [9]. In the present study, patients with a GOLD stage <30
had higher OR of having UWL, although the association was not
Sex 0.963
statistically significant. Mete et al. found an association between
Women Reference
Men 0.98 [0.50; 1.94] FEV1 and Medical Research Council Dyspnoea Scale (MRC) and
Age 0.932 malnutrition measured by Mini nutritional assessment (MNA)
<60 0.96 [0.37; 2.53] among 105 patients [12]. We however did not use full screening, as
60e69 0.78 [0.34; 1.80]
our approach was to use a tool likely to implement by nurses in the
70e79 Reference
>79 1.03 [0.37; 2.83] clinical setting. Therefore, an association might have been found if
BMI 0.000* we had used full nutrition screening and other indicators for COPD
Underweight <18.5 8.22 [2.77; 24.38]* severity. A firm association was found between RFI and UWL
Normal weight 18.5e24.9 3.46 [1.31; 9.13]* (p < 0.05). These results are consistent with previous studies
Pre-obesity 30.0e34.9 1.55 [0.51; 4.75]
[9,15,30]. In this study, we did not investigate, for how long the
Obesity >35 Reference
GOLD Stage 0.656 patients had the disease diagnosis, and a few were yet in the
Mild >80 1.5 [0.34; 6.56] investigation phase. This may affect the results regarding the
Moderate 50-80 1.0 [0.35; 2.84] prevalence of patients, that had experienced an UWL, as patients
Severe 30-50 Reference
especially seem to lose weight around the time of diagnosis and on
Very severe <30 1.8 [0.63; 5.12]
Reduced food intake 0.003*
times of exacerbations and other disease events [31e33]. This was
No Reference not shown in the associations between UWL and hospitalizations
Yes 3.15 [1.50; 6.59] (p > 0.05), although patients with one or more hospitalizations
Nutrition impact symptoms 0.002* within the past three months had higher OR of having UWL,
No Reference
however not statistically significant.
Yes 2.96 [1.47; 5.95]
Asthma 0.983 This study found a great variation of BMI, mean 26.7 (12.9e61.3)
No Reference kg/m2 [26]. Among the included patients, 34.5% of the patients
Yes 1.01 [0.46; 2.20] were obese (BMI
30 kg/m2), but there were no significant associ-
Emphysema 0.331
ation between UWL and the obesity group. The very high preva-
No Reference
Yes 1.42 [0.69; 2.91]
lence of obesity indicates that obesity may require consideration
Smoking 0.851 upon physiological risk factors among those caring for COPD pa-
Never smokes 0.58 [0.07; 4.95] tients. Obesity is known to contribute to respiratory illness, such as
Former smoker Reference sleep apnea, asthma and pulmonary embolism [34,35]. Further-
Smoker 0.89 [0.36; 2.23]
more, obesity in COPD patients has been associated with increased
Hospitalization related to COPD, last 3 months 0.195
No Reference risk of development of comorbidities including diabetes, metabolic
Yes 1.87 [0.75; 4.68] syndrome and cardiovascular disease even increasing the risks of
Hospitalization for other reasons than COPD, last 3 months 0.068 the general population [36e38]. Furthermore, sarcopenic obesity
No Reference may influence pulmonary as well as physical function [39]. In that
Yes 2.51 [0.97; 6.53]
Education level 0.216
view, early recognition of the need for a thorough nutritional
Non or shorter courses 0.59 [0.28; 1.25] assessment and intervention are not only important looking at the
Short or Vocational (1e3 years) Reference risks of negative associated consequences for COPD patients who
Medium long or long (>3 years) 1.35 [0.49; 3.71] are underweight but also for COPD patients with obesity. We did
Civil status 0.108
not investigate how patients with an intended weight loss lost
Living alone 1.74 [0.88; 3.44]
Cohabitant Reference weight e.g., by dietetic guidance, training as for instance in pul-
monary rehabilitation programs or cutting down on foods, but it is
* Statistical significance.
certain that weight loss in patients with inflammatory diseases
such as COPD, should be guided by professionals like trained di-
eticians, in order not to lose muscle mass. Results of this study
prevalence of UWL in this study is consistent with the results from highlights the necessity for early recognition of UWL as well as
previous studies regarding various settings, where 10e45% of the increasing obesity among COPD patients, in order to enhance
COPD patients were found malnourished [12,15]. Since one out of optimal pulmonary function, and maybe even reduce further ex-
five in this study experienced UWL and 13.5% were underweight, acerbations and development of comorbidities.
and the prevalence is confirmed by former studies from other
settings and countries, we find it realistic to assume that risk of 4.1. Study strengths and limitations
malnutrition would also be found by screening among the majority
of patients identified by UWL. Nutritional screening does not take In this study, some data is missing due to the lack of possibility
place in the outpatient clinic, and even though some COPD mu- to find sufficient data in all patients’ medical records. Therefore, a
nicipality rehabilitation programs take care of nutritional screening few associations related to UWL were not calculated on full cases
and intervention when relevant, this is inconsistent, and even and eventual patterns in missing data may have affected the results.
more, our data showed that less than half our patients completed Questionnaires were based on patient reported data, providing the
municipality rehabilitation [29]. Aiming at early intervention risk of recall bias for those who were not weighed on sight but
before the onset of sarcopenia and cachexia (2, 4, 10, 12), we claimed to be sure of their current weight. However, the majority of
therefore find there is a need to have focus on early identification of patients who are past 65 years of age, measure and enter weight
nutritional risk among COPD patients in the outpatient clinics. data in the community database weekly. These data are reported
We also investigated possible characteristics among the COPD every Monday morning, and since the COPD outpatient clinic is
patients with UWL. COPD patients that were already underweight confined to Mondays, the weight was measured and reported on
249
T. Christensen, S. Mikkelsen, L. Geisler et al. Clinical Nutrition ESPEN 49 (2022) 246e251

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