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International Journal of Nursing Practice 2014; ••: ••–••

CLINICAL PAPER

Factors contributing to malnutrition in patients

with Parkinson’s disease
Sung R Kim RN PhD
Assistant Professor, College of Nursing, Chonbuk National University, Jeonju, Korea

Sun J Chung MD PhD

Associate Professor, Department of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

Sung-Hee Yoo RN PhD

Assistant Professor, College of Nursing, Chonnam National University, Gwangju, Korea

Accepted for publication November 2014

Kim SR, Chung SJ, Yoo SH. International Journal of Nursing Practice 2014; ••: ••–••
Factors contributing to malnutrition in patients with Parkinson’s disease

Our objective in this study was to evaluate the nutritional status and to identify clinical, psychosocial, and nutritional
factors contributing to malnutrition in Korean patients with Parkinson’s disease. We used a descriptive, cross-sectional
study design. Of 102 enrolled patients, 26 (25.5%) were malnourished and 27 (26.5%) were at risk of malnutrition based
on Mini-Nutritional Assessment scores. Malnutrition was related to activity of daily living score, Hoehn and Yahr stage,
duration of levodopa therapy, Beck Depression Inventory and Spielberger’s Anxiety Inventory scores, body weight, body
weight at onset of Parkinson’s disease, and body mass index. On multiple logistic regression analysis, anxiety score,
duration of levodopa therapy, body weight at onset of Parkinson’s disease, and loss of body weight were significant factors
predicting malnutrition in Parkinson’s disease patients. Therefore, nutritional assessment, including psychological evalu-
ation, is required for Parkinson’s disease patients to facilitate interdisciplinary nutritional intervention for malnourished
patients.
Key words: malnutrition, nutritional status, Parkinson’s disorder.

INTRODUCTION Malnutrition is generally defined as an underweight

Parkinson’s disease (PD) is the second most common
neurodegenerative disorder characterized by dopaminer-
gic neuronal loss.1 Patients with PD experience not only
neurological motor symptoms including tremor, rigidity
and bradykinesia but also health-related problems includ-
ing depression, dementia, fatigue and constipation.2 Mal-
nutrition has also been recognized as an important problem
in PD patients.2,3
Correspondence: Sung-Hee Yoo, College of Nursing, Chonnam
National University, 160 Baekseo-ro, Dong-gu, Gwangju 501-746,
Korea. Email: shyoo@jnu.ac.kr
BMI less than 18.50 kg/m2 in adults, according to the
WHO classification.4 Previous studies have shown that PD
patients have a lower body weight and body mass index
(BMI) than healthy controls5–7 and also are at increased
risk of developing malnutrition than age-matched con-
trols.8 The prevalence of malnutrition in PD patients has
been reported to range from 0 to 24%, and the malnutri-
tion risk from 3 to 60% based on various nutritional
parameters and definitions.8–11 Although the true extent of
malnutrition in the PD population remains unclear, a not
inconsiderable proportion of patients have a nutritional
problem.

doi:10.1111/ijn.12377 © 2014 Wiley Publishing Asia Pty Ltd

2 SR Kim et al.
Nutritional assessment can be performed by assessing
hematologic parameters such as albumin or prealbumin
levels, anthropometric parameters such as body mass
index (BMI) and body weight, and using nutritional assess-
ment tools to assess dietary habits and general status.12
The mini-nutritional assessment (MNA) tool is one of
the most widely used tools for nutritional assessment in
clinical and research settings, because it can evaluate
neuropsychological health and morbidity as well as
anthropometric parameters and dietary habits, and has
been validated in elderly patients.13 Therefore, nutritional
assessment using this validated tool is essential for PD
patients.
Several factors might contribute to the high prevalence
of malnutrition in PD patients. The first factor is related
to motor symptoms. Bradykinesia, rigidity and gait dis-
turbance cause some patients to experience difficulty in
performing the activities of daily living (ADL) such as
shopping, preparing and eating or swallowing food inde-
pendently11,14 These types of disabilities might also be
caused by levodopa-related motor complications such
as dyskinesia.7,8,15 The second factor is related to psycho-
social and cognitive factors. Depression, anxiety and
dementia have been found to contribute to lowered food
intake and weight loss in the elderly,16–18 and such symp-
toms are present at a higher incidence in PD patients than
in controls.19,20 The last factor is related to medications
that are used to manage PD, which can have side effects
such as nausea, vomiting, loss of appetite and change of
taste.8,21–23
Although multiple factors might contribute to malnu-
trition in PD patients, only a few of these factors have
been examined in previous studies.5,7,9,10,23 Therefore, a
comprehensive study examining all potential factors is
needed to identity factors that significantly affect malnu-
trition in PD patients. Because malnutrition leads to
poorer quality of life and worse health outcomes, such as
higher mortality and prolonged length of hospital stay,8
evaluation of the nutritional status of PD patients and
determination of the factors that contribute to malnutri-
tion in PD patients are particularly relevant.
Aims
Our aims in the current study were to describe the nutri-
tional status of Korean patients with PD and to identify
clinical, psychosocial and nutritional factors that predicted
malnutrition in these patients.
© 2014 Wiley Publishing Asia Pty Ltd
METHODS
Design
This was an observational study with a cross-sectional
design.
Participants
Subjects were recruited from a single tertiary university
hospital in Seoul, Korea, and convenience sampling was
used to select subjects.
We included patients (i) who were over 20 years of
age, (ii) who had PD based on the United Kingdom Par-
kinson’s Disease Society Brain Bank criteria as the primary
diagnosis,24 and (iii) who had no other major health prob-
lems that could influence nutritional status such as active
cancer, infection, inflammation, liver failure, or renal
failure. We excluded patients with atypical Parkinsonism
or secondary Parkinsonism. We enrolled a total of 102
patients in the current study.
Measurement of nutritional status
Mini-Nutritional Assessment (MNA)
Nutritional status was measured using the MNA tool.25
The MNA is widely used to assess nutritional status and
has been validated in various settings,13 including in
elderly Korean patients.26 MNA is highly sensitive (96%)
and specific (98%).13,27 The MNA is an 18-item question-
naire comprising anthropometric measurements, general
status including swallowing function, dietary habits and
self-perception of health and nutrition states.13 MNA
scores range from 0 to 30 points; a higher score indicates
a healthier nutritional status. Based on the final MNA
scores, we classified the nutritional status of subjects
‘good’ (≥ 24 points), at ‘risk of malnutrition’ (17–23.5
points), or ‘malnourished’ (< 17 points).13,25 In this study,
we defined patients with a good nutritional status and
those at risk of malnutrition into the non-malnutrition
group, whereas malnourished patients were defined to the
malnutrition group.
Beck Depression Inventory (BDI)
Depression was measured using the Beck Depression
Inventory (BDI) with self-rating scales,28,29 which is one of
the most commonly used tools for assessment of depres-
sion.30 Its reliability and validity have been validated in
Korean patients.30,31 The BDI includes 21 questions and
BDI scores range from 0 to 63. Higher scores indicate
greater depression. Cronbach’s alpha value for the BDI
was 0.90 in the current study.
Malnutrition in patients with PD
Spielberger’s Anxiety Inventory (SAI)
Anxiety was measured using the Korean version of
SAI.32,33 This is a well-established scale that has been used
extensively in research and clinical practice.34,35 SAI
includes 20 questions and SAI scores range from 20 to 80.
Higher scores indicate greater anxiety. Cronbach’s alpha
value for the SAI was 0.95 in the current study.
Mini-Mental State Examination (MMSE)
Korean version of the MMSE (K-MMSE) was used to
measure the cognitive function of patients.36 Sensitivity
for detecting dementia with the K-MMSE has been
reported to range from 0.70 to 0.83.37 K-MMSE scores
range from 0 to 30. Higher scores indicate greater cogni-
tive function.
Other variables
We examined various clinical and nutritional variables
using a structured questionnaire. The clinical characteris-
tics of age of onset of PD, disease duration, duration of
levodopa therapy, daily levodopa equivalent dose (LED),
presence of motor fluctuation and dyskinesia, Hoehn and
Yahr stage, and the Schwab and England ADL score were
assessed.
We assessed nutritional characteristics in detail includ-
ing MNA; anthropometric parameters such as current
body weight, body weight at onset of PD, weight loss and
body mass index (BMI); biochemical parameters such as
serum albumin and total protein; and presence of symp-
toms potentially affecting oral intake by PD medication
such as constipation, nausea and vomiting, and dyspepsia.
Current body weight and BMI were measured using an
automatic fatness measuring system (G-tec, G-tec Inter-
national, Uijungbu, South Korea). Subjects were assigned
to one of four categories based on BMI values according to
WHO recommendations for Asian populations.38 Weight
loss was calculated as the difference between weight at
onset of PD and current weight based on a review of
electronic medical records. In addition, serum protein
and albumin levels were assessed as biochemical param-
eters. Serum total protein was classified based on a cut-off
of 6.2 g/dL and serum albumin on a cut-off of 3.5 g/
dL.39 We defined constipation as bowel action less than
three times weekly,40 whereas we defined dyspepsia as
gastrointestinal discomfort after taking PD medication
based on subjective sensations of bloating, burning and gas
in the bowels.22
3
Data collection
Between March and September 2012, we enrolled sub-
jects who provided written informed consent. Subjects
were informed of the aims and procedures of the current
study by clinical nurse specialists. Patients who agreed to
face-to-face interviews had their body weight and BMI
measured and were administered a structured question-
naire that they completed together with a spouse or family
member. Following the interviews, we confirmed patient
information using medical records.
Analysis
Statistical analyses were conducted using SPSS version
20.0 (IBM SPSS Statistics, SPSS Inc., Chicago, IL). All
data are expressed as numbers (percentages), means ± SD
(standard deviations), or medians (ranges). To compare
clinical, psychosocial and nutritional characteristics
between the malnutrition and non-malnutrition group,
we used the chi-square test, t-test or Mann–Whitney
U-test as appropriate, and we used the Kolmogorov–
Smirnov test to analyze the normality of continuous vari-
ables. To identify independent predictors of malnutrition,
we performed multiple logistic regression analysis and
calculated odds ratios (ORs) and 95% confidence intervals
(CIs). Hosmer–Lemeshow test was used to assess
goodness-of-fit. A two-tailed P value less than 0.05 was
considered statistically significant.
Ethical considerations
The current study was approved by the Institutional
Review Board (IRB) of Asan Medical Center in Korea.
We obtained written informed consent from all subjects
or their legal representatives. Subjects were allowed to
voluntarily withdraw their informed consent and their
personal data were kept strictly confidential throughout
the study.
RESULTS
Demographic, clinical and
psychosocial characteristics
Of the 102 patients included in this study, 57 (55.9%)
were female. Age ranged from 31 to 81 years
(mean ± SD, 61.2 ± 10.1 years), and the median disease
duration was 9 years (range, 1–24 years). Median Hoehn
and Yahr stage was 2 (range, 0–5). Mean K-MMSE, BDI,
and SAI scores were 25.7 ± 3.7, 14.7 ± 10.8, and
44.6 ± 11.1, respectively.
© 2014 Wiley Publishing Asia Pty Ltd
4 SR Kim et al.

Nutritional status and characteristics In the malnutrition group, the age of onset of PD was
Nutritional characteristics are summarized in detail in significantly higher than that in the non-malnutrition
Table 1. Twenty-six (25.5%) of the 102 patients were group (55.6 ± 9.5 years vs. 49.6 ± 11.8 years, respec-
categorized as malnourished whereas 27 (26.5%) patients tively) (P = 0.020), and Schwab and England ADL
were considered at risk of malnutrition based on the score was significantly lower in the malnutrition group
MNA results. Fifty-eight (56.8%) patients had experi- (P < 0.001). However, the duration of levodopa therapy
enced weight loss. Mean BMI of all PD patients was was significantly shorter in the malnutrition group
23.2 ± 3.7 kg/m2 and seven patients (6.9%) were under- (P = 0.038). Hoehn and Yahr stage was significantly cor-
weight (BMI < 18.5 kg/m2). Mean serum total protein related with the degree of malnutrition according to MNA
and albumin levels were 6.6 ± 0.5 and 4.0 ± 0.4 g/dl score (P = 0.017).
(range, 5.3–7.7 g/dl and 3.0–5.9 g/dl), respectively. BDI and SAI scores were significantly higher in the
malnutrition group than the non-malnutrition group
Demographic, clinical, psychosocial, (P = 0.009 and P < 0.001, respectively).
and nutritional characteristics Among nutritional parameters, body weight, body
related to malnutrition weight at disease onset, and BMI were significantly lower
Differences in demographic, clinical, psychosocial, and in the malnutrition group than the non-malnutrition
nutritional characteristics between the two groups are group (P < 0.001, P = 0.009, and P < 0.001, respec-
presented in Table 2. tively), whereas weight loss was higher in the malnutri-
tion group than the non-malnutrition group (P < 0.001).
Table 1 Nutritional characteristics of PD patients (n = 102)
Moreover, we found a significant correlation between
malnutrition and nausea and vomiting (P = 0.048) and
Variables n (%) or Range
dyspepsia (P = 0.001) related to anti-PD medication.
mean ± SD
However, clinical factors such as sex, age, disease dura-
tion, daily levodopa equivalent dose (LED), motor fluc-
MNA 21.4 ± 6.2 4.5–29.0
Good status (≥ 24) 49 (48.0%)
tuation, dyskinesia, K-MMSE score, and levels of visceral
Risk of malnutrition (17–23.5) 27 (26.5%) proteins such as serum total protein and albumin were not
Malnutrition (< 17) 26 (25.5%) related to malnutrition.
Body weight (kg) 58.7 ± 9.4 40.5–83.0
Body weight at disease onset (kg) 61.7 ± 9.4 42.0–93.8 Factors predicting malnutrition in
Weight loss 58 (56.9%) patients with PD
7.2 ± 4.7 1.0–20.0 Multiple logistic regression analysis revealed that anxiety
BMI (kg/m2) 23.2 ± 3.7 14.4–34.2 score (OR = 1.124, 95% CI: 1.003–1.261, P = 0.044),
< 18.5 7 (6.9%) duration of levodopa therapy (OR = 0.666, 95% CI:
18.5 ≤ BMI < 23 44 (43.1%) 0.460–0.962, P = 0.030), body weight at onset of PD
23 ≤ BMI < 27.5 40 (39.2%) (OR = 0.709, 95% CI: 0.544–0.925, P = 0.011), and
≥ 27.5 11 (10.8%)
weight loss (OR = 2.972, 95% CI: 1.366–6.464,
Protein (g/dl), (n = 98) 6.6 ± 0.5 5.3–7.7
P = 0.006) were significant factors predicting malnutri-
< 6.2 21 (21.4%)
≥ 6.2 77 (78.6%)
tion (Table 3).
Albumin (g/dl), (n = 98) 4.0 ± 0.4 3.0–5.9
< 3.5 8 (7.8%) DISCUSSION
≥ 3.5 90 (88.2%) The results of our study indicate that the prevalence of
Constipation 55 (53.9%) malnourishment in patients with PD is high, and that the
Nausea & vomiting 12 (11.8%) psychological factor of anxiety, as well as duration of
Dyspepsia 16 (15.7%) levodopa treatment, initial weight at diagnosis, and
weight change after PD onset are independent predictors
PD, Parkinson’s disease; SD, standard deviation; MNA, mini- of malnutrition. A strength of our study is that we
nutritional assessment; LED, levodopa equivalent dose; K-MMSE, examined all potential contributing factors, including
Korean mini mental status examination; BMI, body mass index. nutritional symptoms related with anti-PD medication,

© 2014 Wiley Publishing Asia Pty Ltd

Malnutrition in patients with PD 5

Table 2 Comparison of clinical, psychosocial, and nutritional characteristics between the malnutrition group and the non-malnutrition
group

Variables Malnutrition Non-malnutrition t or z or χ2 P value

(n = 26) (n = 76)

Clinical characteristics
Sex (Female) 18 (69.2%) 39 (51.3%) 0.169 0.112
Age (years) 64.5 ± 8.6 60.1 ± 10.4 1.968 0.052
Age at onset (years) 55.6 ± 9.5 49.6 ± 11.8 2.360 0.020*
Disease duration (years) 8.7 ± 5.3 10.6 ± 6.2 −1.338 0.114†
Hoehn & Yahr stage 13.463 0.017*
0 0 2 (2.6%)
1 3 (11.5%) 5 (6.6%)
2 10 (38.5%) 46 (60.5%)
3 5 (19.2%) 16 (21.1%)
4 5 (19.2%) 7 (9.2%)
5 3 (11.5%) 0
ADL (%) 63.9 ± 26.1 84.7 ± 11.9 −3.930 < 0.001**
Duration of levodopa Therapy (years) 6.5 ± 4.4 9.3 ± 6.1 −2.468 0.038†*
LED (mg/day) 614.1 ± 311.9 788.5 ± 497.7 −1.643 0.384†
Motor fluctuation (n = 25) (n = 76) 0.849 0.654
No 9 (36.0%) 22 (28.9%)
Yes, but not disabling 8 (32.0%) 32 (42.1%)
Yes, disabling 8 (32.0%) 22 (28.9%)
Dyskinesia (n = 25) (n = 76) 0.004 0.998
No 9 (36.0%) 27 (35.5%)
Yes, but not disabling 11 (44.0%) 34 (44.7%)
Yes, disabling 5 (20.0%) 15 (19.7%)
K-MMSE 24.4 ± 3.6 26.1 ± 3.6 −2.036 0.083†
Psychosocial characteristics
Depression 23.7 ± 10.6 11.6 ± 9.1 4.682 0.009†*
Anxiety 52.3 ± 12.3 42.2 ± 9.6 3.654 < 0.001**
Nutritional characteristics
Body weight (kg) 50.8 ± 6.3 61.4 ± 8.8 −5.629 < 0.001**
Body weight at PD onset (kg) 57.5 ± 8.5 63.1 ± 9.3 −2.655 0.009*
BMI (kg/m2) 20.2 ± 2.6 24.3 ± 3.4 −5.612 < 0 .001**
< 18.5 6 (23.1%) 1 (1.3%) 27.951 < 0.001**
18.5 ≤ BMI < 23 17 (65.4%) 27 (35.5%)
23 ≤ BMI < 27.5 3 (11.5%) 37 (48.7%)
≥ 27.5 0 11 (14.5%)
Weight loss (kg) 22 (84.6%) 36 (47.4%) 10.957 0.001*
7.4 ± 5.0 3.1 ± 4.6 3.992 < 0.001†**
Protein (g/dl) 6.6 ± 0.4 6.6 ± 0.5 −0.161 0.873
Albumin (g/dl) 4.0 ± 0.6 3.9 ± 0.3 0.629 0.401†
Constipation 14 (53.8%) 41 (53.9%) 0.000 0.993
Nausea & vomiting 6 (23.1%) 6 (7.9%) 4.302 0.048*
Dyspepsia 10 (38.5%) 6 (7.9%) 13.686 0.001**

* P < 0.05; ** P < 0.001; †Mann–Whitney U-test. ADL, activities of daily living; LED, levodopa equivalent dose; K-MMSE, Korean-
mini mental status examination; BMI, body mass index.

© 2014 Wiley Publishing Asia Pty Ltd

6 SR Kim et al.
Table 3 Predictors of malnutrition in PD patients
Variables Odds 95% CI P value
ratio
Anxiety 1.124 1.003–1.261 0.044*
Duration of levodopa therapy 0.666 0.460–0.962 0.030*
Body weight at onset of PD 0.709 0.544–0.925 0.011*
Weight loss 2.972 1.366–6.464 0.006*
* P < 0.05, Hosmer–Lemeshow goodness-of-fit test showed
χ2 = 1.56 (P = .980). PD, Parkinson’s disease; CI, confidence
interval.
clinical and psychological factors, and various nutritional
parameters, to determine independent predictors of
malnutrition.
The prevalence of malnutrition was 25.5% and the risk
of malnutrition was 26.5%, indicating that more than half
of the subjects (52%) had nutritional problems. This
result is largely consistent with those reported in previous
studies based on MNA assessment.8,23 Our results indicate
that PD patients are therefore more likely to be under-
nourished than hemodialysis patients (56.5%)41 or
patients with other chronic diseases, such as chronic
obstructive pulmonary disease (30.7%).42 This result
highlights the necessity of performed nutritional assess-
ments in all PD patients, given that patients at risk of
malnutrition might become malnourished.43
We found that although K-MMSE scores were lower
in the malnutrition group than in the non-malnutrition
group (24.4 ± 3.6 vs. 26.1 ± 3.6, respectively), these
scores were not statistically correlated with malnutrition,
a finding similar to that reported in previous studies.7,8
However, because cognitive function has been shown to
be associated with malnutrition in other populations,44
including Alzheimer’s disease patients,45 further studies
are warranted to elucidate the correlation between cog-
nitive function and nutritional status in patients with PD.
Because PD is a neurodegenerative disorder, disease
duration and disease severity are positively associated with
each other, and both might be negatively associated with
nutritional status. We found an association between mal-
nutrition and a higher Hoehn and Yahr stage, as described
in previous studies,6,8 but no association between malnu-
trition and PD duration. It is therefore unclear whether
PD duration is associated with malnutrition, because pre-
vious studies have reported findings that conflict with
© 2014 Wiley Publishing Asia Pty Ltd
those of the current study;6,7,23 further studies are needed
to address this issue. Our results suggest that disease
severity might be a more important factor than disease
duration for predicting malnutrition in PD patients.
It is well known that depression and anxiety are
psychological factors associated with malnutrition,16,18
consistent with our results. In particular, we found that
anxiety was an independent predictor of malnutrition
after adjusting for all other factors in our study. Anxiety is
a frequent emotional symptom in PD patients and is asso-
ciated with motor symptoms, such as severe gait prob-
lems, dyskinesia, and off symptoms.46 Anxiety might
worsen nutritional status through exacerbated neurologic
symptoms and might affect appetite and food intake. Until
recently, medication was the main treatment strategy in
patients with high levels of anxiety.47 However, cognitive
behavior therapy and exercise are gaining popularity as
effective approaches to treat anxiety in PD patients.48,49
Thus, a multi-dimensional intervention strategy might
alleviate anxiety and improve nutritional status in PD
patients.
Other nutritional parameters were also significantly
different between the malnutrition and non-malnutrition
groups. We used albumin as a biochemical parameter to
investigate cross-sectional nutritional state in PD patients,
not temporal changes, because albumin is known to be a
good predictor of poor clinical outcomes in various dis-
eases50,51 and has a longer half-life than prealbumin or
transferrin. However, the albumin results did not reflect
the MNA results in our study. This was consistent with
previous findings that the serum albumin was not a reli-
able indicator for nutritional assessment in patients with
chronic diseases.52 In addition, we also measured the BMI
as an anthropometric parameter, but the proportion of
underweight individuals according to the WHO BMI clas-
sification showed a discrepancy with the incidence of mal-
nutrition according to the MNA. It was also consistent
with previous findings performed in elderly patients and
patients with cancer.53–55 We believe that these results
might be due to each nutritional parameter (such as
anthropometric, biochemical, and global assessment
tools) reflecting a different clinical process.56 Neverthe-
less, the MNA considers various nutritional parameters
including food intake by appetite or swallowing difficulty,
anthropometric measurements including weight loss, and
physical and mental functions, and malnutrition and non-
malnutrition groups classified by the MNA showed a dif-
ference in clinical and psychological factors reported in
Malnutrition in patients with PD
previous studies, symptoms affecting oral intake, and
other nutritional factors excluding biochemical param-
eters. Therefore, we believe that the MNA is a useful tool
for nutritional assessment in patients with PD as a chronic
disease.
We recommend assessing the nutritional state of PD
patients using a validated tool and identifying risk factors
for poor nutrition. Moreover, for patients at risk of mal-
nutrition, as well as those with malnutrition, various
individual interventions such as diet modification and
nutritional supplements, education, stress relief, regula-
tion of symptoms affecting poor oral intake, and dietary
consultation should be considered in both research set-
tings and clinical practice.
CONCLUSIONS
Our study revealed that more than half of patients with
PD had nutritional problems, and that anxiety, duration of
levodopa therapy, body weight at onset of PD, and weight
loss were factors that contributed significantly to the
development of malnutrition in PD patients.
Therefore, appropriate nutritional assessment, includ-
ing psychological evaluation, should be conducted regu-
larly in PD patients, and a multidisciplinary approach
involving various nutritional interventions should be con-
sidered for undernourished patients.
ACKNOWLEDGEMENTS
No research funding or any other financial support was
received for this study. None of the authors have any
conflicts of interest to declare.
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