NUTRITION
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RESEARCH ARTICLE
Association between malnutrition, clinical
parameters and health-related quality of life
in elderly hospitalized patients with
Parkinson’s disease: A cross-sectional study
Maria Theresa Gruber 1 , Otto W. Witte
1,2 , Julian Grosskreutz
1,2 , Tino PrellID
1,2*
1 Department of Neurology, Jena University Hospital, Jena, Germany, 2 Center for Healthy Ageing, Jena
University Hospital, Jena, Germany
Abstract
Objective
This study aimed to explore the association between malnutrition, clinical parameters, and
health-related quality of life in elderly hospitalized patients with Parkinson’s disease (PD).
Methods
Cross-sectional study of 92 hospitalized elderly patients with PD (mean age 73.6 ± 6.7 years) without dementia. The Mini Nutritional Assessment (MNA) was used to evaluate
nutritional status. Motor impairment and non-motor symptoms burden (Movement Disorder
Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale [MDS-
UPDRS], Non-Motor Symptoms Questionnaire, and Hoehn & Yahr staging), depression
(Becks Depression Inventory-II), and health-related quality of life (PD quality of life Ques-
tionnaire-39) were assessed.
Results
Every second patient was malnourished or at risk of malnutrition. In the multivariable analy-
sis, male gender, longer disease duration, higher Hoehn & Yahr and depression were asso-
ciated with total MNA score. Besides non-motor symptoms and motor impairment,
malnutrition was an independent predictor of poor health-related quality of life. In the multi-
variate analysis, malnutrition had a statistically significant effect on emotional well-being,
mobility, social support, stigmatization, and cognition. The strongest association was found
between malnutrition and emotional well-being.
Conclusion
Elderly male persons with longer PD duration and higher disease stages are more likely to
be malnourished or at risk for malnutrition. Malnutrition was mainly associated with poor
emotional well-being, suggesting that treatment of depression and anxiety beside diet and
physical activity can help improving nutrition status in these subjects. The MNA should not
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OPEN ACCESS
Citation: Gruber MT, Witte OW, Grosskreutz J,
Prell T (2020) Association between malnutrition,
clinical parameters and health-related quality of life
in elderly hospitalized patients with Parkinson’s
disease: A cross-sectional study. PLoS ONE 15(5):
e0232764. https://doi.org/10.1371/journal.
pone.0232764
Editor: John Duda, Philadelphia VA Medical Center,
UNITED STATES
Received: February 21, 2020
Accepted: April 21, 2020
Published: May 4, 2020
Copyright: © 2020 Gruber et al. This is an open access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: The authors received no specific funding
for this work.
Competing interests: The authors have declared
that no competing interests exist.
be used independent of other measures of cognition and depression in people with
advanced PD.
Background
Parkinson’s disease (PD) is a common neurodegenerative disorder characterized by motor
impairment and a plethora of non-motor symptoms. People with PD are at a high risk of malnutri-
tion [1]. In PD, malnutrition and risk of malnutrition were associated with motor impairment, dis-
ease duration, and several non-motor symptoms, such as constipation and depression [2, 3]. There
are several reasons and mechanisms how clinical factors can contribute to malnutrition. Besides
reduced food intake due to dysphagia, loss of smell, slow gastric emptying, side effects of drug ther-
apy may also play a role [4]. As the disease progresses, people with PD increasingly need help with
daily activities due to an increase of motor impairments (e.g. gait disturbances, falls) and the occur-
rence of neuropsychological problems (e.g. dementia) [5]. Therefore, in the course of the disease
many patients have to be treated in hospital to optimize medical and non-medical treatment.
A gold standard for the optimal definition of malnutrition is still lacking [1]. The European
Society for Clinical Nutrition and Metabolism (ESPEN) recommends, among others, the Mini
Nutritional Assessment (MNA) for screening malnutrition and the risk of developing malnu-
trition. It includes physical and mental aspects that frequently affect the nutritional status
among elderly people in home-care programs, nursing, homes and hospitals [6]. The MNA
detects the risk of malnutrition when albumin levels and BMI are still normal. The score is
derived from six items—reduced food intake in the preceding 3 months; weight loss during
the preceding 3 months; mobility; psychological stress or acute disease in the preceding 3
months; neuropsychological problems; and body mass index. The MNA is highly predictive
for adverse health outcome, social functioning, length of hospital stay and mortality [7].
Malnutrition is associated with poor health-related quality of life (QoL) and differentially
influences distinct domains of health-related QoL, especially well-being and mobility domains
[3, 8, 9]. However, in previous studies the investigated patients with and without malnutrition
showed relevant differences in terms of clinical parameters, which also influence health-related
QoL, such as age, disease duration, and non-motor symptoms burden [8–10]. After correction
for these cofactors, mainly depression, more severe motor symptoms and more advanced dis-
ease stage remained significant predictors of poorer nutritional status in non-hospitalized
patients with PD [8, 9, 11]. However, fewer data are available for elderly subjects without cog-
nitive deficits as well as for hospitalized patients. Given that hospitalization is more frequently
necessary in advanced disease stages, we assumed that malnutrition-related factors differ in
hospitalized and non-hospitalized patients with PD. With the current study, we aimed to close
this gap and to answer the following three questions:
• What is the prevalence of malnutrition in hospitalized elderly patients with PD?
• To what extent does malnutrition predict health-related QoL in elderly patients with PD?
• Which domains of health-related QoL are mainly affected by malnutrition?
Methods
Participants and assessments
This cross-sectional study was approved by the local ethics committee of the Jena University
Hospital (4572-10/15), and all patients gave their written informed consent. Data were
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collected from patients with PD at the beginning of their stay (day 1–3) in the neurological
ward of the Department of Neurology at the Jena University Hospital (Germany). All the
patients were hospitalized because of the worsening of motor function or complications (dys-
kinesia, falls, and medication side effects). All received a multimodal treatment by specialized
therapists and medication modifications during their stay in the hospital (German Multimo-
dale Komplexbehandlung bei Morbus Parkinson) [12]. Inclusion criteria were as follows: 60
years or older and PD diagnosis according to the Movement Disorder Society (MDS) diagno-
sis criteria. Exclusion criteria were as follows: PD dementia, cerebrovascular disorders, delir-
ium, deep brain stimulation, levodopa/carbidopa enteral infusion, apomorphine infusion,
unable to complete a questionnaire, special diets (calorie restriction and low protein), and
gastroenterological (surgical procedure, malabsorption, and inflammatory bowel disease) or
renal disorders (nephritis and severe kidney failure) in medical history. All tests were con-
ducted during the medication ON phase.
Several clinical variables were recorded, including the MDS-sponsored revision of the Uni-
fied Parkinson’s Disease Rating Scale III (MDS-UPDRS III) to assess motor function, the
revised Non-Motor Symptoms Questionnaire (NMS-Quest), Hoehn and Yahr staging (H&Y),
and levodopa equivalent daily dose (LEDD). Cognition was assessed using the Montreal Cog-
nitive Assessment (MoCa); PD dementia was defined as MoCa < 21 [13]. Beck’s Depression
Inventory-II (BDI) was used to quantify depressive mood. Health-related QoL was assessed
with the German version of the 39-item PD QoL questionnaire (PDQ-39), which is commonly
used to assess eight domains: mobility, activities of daily living, emotional well-being, stigma,
social support, cognition, communication, and bodily discomfort. The PDQ-39 Summary
Index (PDQ-39SI) summarized the eight dimensions as one score. A maximum score of 100
represents the worst condition. The short form Mini Nutritional Assessment (MNA) question-
naire was applied to evaluate nutritional status (www.mna-elderly.com). It was specifically
designed for the elderly and is recommended by the European Society for Clinical Nutrition
and Metabolism. It consists of six questions about dietary regime in the last 3 months, weight
loss, immobility, recent stress period, neuropsychological disorders (depression and demen-
tia), and body mass index (BMI) or calf circumference (MNA scores of 12–14 indicate normal
nutritional status, 8–11 at risk of malnutrition, and 0–7 malnutrition) [14, 15].
Epidemiological factors, the MDS-UPDRS III, NMS-Quest, H&Y, LEDD, MoCa and dis-
ease duration were derived from the medical records. The BDI and PDQ-39 were self-reports.
The MNA was assessed by MT. After exclusion of 8 people with missing data in the BDI or
PDQ-39, the data from 92 subjects were used for the following analyses.
Statistical analysis
The SPSS statistical computer package (version 25.0; IBM Corporation, USA) was used for all
statistical analyses. Values are given as mean and standard deviation or median and interquar-
tile range (IQR). Categorical variables are presented as numbers or percentages.
Multiple linear regression analysis was subsequently performed to ascertain the indepen-
dent predictors of the MNA. The clinical parameters / independent variables were derived
from the literature and included: age, gender, disease duration, H&Y, MDS-UPDRS III,
NMS-Quest, BDI, and LEDD [2, 8–11, 16–18]. The significance level for variables entering the
linear regression model was set at 0.2 and for removing from the model at 0.4.
A second linear regression was used to study the association between PDQ-39SI (dependent
variable) and MNA and variables known to influence health-related QoL in PD (age, disease
duration, NMS-Quest, BDI, MDS-UPDRS III, and H&Y) [19, 20]. Before regression analyses,
autocorrelation (Durbin–Watson) and multicollinearity (variance inflation factor and
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tolerance) were excluded. A multivariate analysis of variance (MANOVA) and MANCOVA
were used to study the association between MNA total score and the eight PDQ-39 domains.
Anonymized data from this study are available as supplementary material.
Results
Malnutrition: Prevalence and association with clinical parameters
The detailed clinical characteristics are given in Table 1. According to the MNA, every second
patient was malnourished or at risk for malnutrition (Fig 1A). The histogram of the MNA sum
score is shown in Fig 1B. Most patients reported weight loss (MNA item B), followed by neuro-
psychological problems (MNA item E) and declined food intake (MNA item A) (Fig 2).
In the linear regression analyses male gender, longer disease duration, higher H&Y stage,
and higher BDI were found to be associated with malnutrition (Table 2).
Association between malnutrition and health-related QoL
In the next step, we aimed to answer if malnutrition is associated with overall health-related
QoL (PDQ-39SI) after controlling for known factors that influence PDQ-39 (age, gender,
NMS-Quest, BDI, MDS-UPDRS III, and H&Y) [19, 20]. In the regression analysis, the
NMS-Quest, MNA, MDS-UPDRS III, and BDI were found to be independent predictors of
the PDQ-39SI (Table 3).
Table 1. Characteristics of the cohort (n = 92).
Mean SD
Age 73.6 6.7
Disease duration (years) 7.9 5.7
MDS-UPDRS III (motor examination) 28.1 15.1
MDS-UPDRS IV 4.5 5.1
NMS-Quest 11.5 4.8
LEDD 670 436
Number of drugs per day 6.2 3.0
BDI total 13.7 7.6
BMI (kg/m 2 ) 25.7 3.4
median IQR
Hoehn and Yahr stage 3.0 1.0
MNA sum score 12.0 3.0
n %
Gender Female 40 43.5
Male 52 56.5
Marital status Married 70 76.1
Single/divorced/widowed 22 23.9
Nutrition status malnutrition 6 6.5
risk of malnutrition 36 39.1
normal nutrition 50 54.3
IQR, interquartile range; MNA, Mini Nutritional Assessment Short Form; MDS-UPDRS, Movement Disorder
Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale; NMS-Quest, revised Non-Motor
Symptoms Questionnaire; LEDD, levodopa equivalent daily dose; MoCa, Montreal Cognitive Assessment; BDI, Beck
Depression Inventory; BMI, Body mass index (BMI).
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Fig 1. Malnutrition in patients with Parkinson’s disease according to the Mini Nutritional Assessment (MNA). (A) Prevalence of different
nutritional status (n = 92). (B) Frequency of different MNA sum scores in the cohort.
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Fig 2. Detailed prevalence of pathological items in the Mini Nutritional Assessment (MNA). All values (%) refer to the total number of 92 subjects. BMI, body mass
index.
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Given that malnutrition impacts the PDQ-39SI, we then analyzed the relationship between
nutrition status and the PDQ-39 domains. A MANOVA was used to study the association
between malnutrition and the eight PDQ-39 domains. The MANOVA revealed a significant
multivariate main effect for the MNA total score on the eight PDQ-39 subdomains (p = 0.016; Wilk’s Λ = 0.799, partial η2 = 0.20). However, significant univariate main effects for MNA were only found on emotional well-being (p < 0.001, partial η2 = 0.15), mobility (p = 0.004, partial η2 = 0.09), stigmatization (p = 0.003, partial η2 = 0.1), and social support (p = 0.043, par- tial η2 = 0.05). As indicated by the partial η2, the strongest association was found between mal- nutrition and emotional well-being. The MANCOVA was conducted to examine whether
these findings could be accounted for by other medical covariates (age, disease duration,
NMS-Quest, and MDS-UPDRS III). Here, disease duration (Wilks’ λ = 0.75, p = 0.006, partial η2 = 0.25), NMS-Quest (Wilks’ λ = 0.43, p < 0.001, partial η2 = 0.57), and MDS-UPDRS III (Wilks’ λ = 0.59, p < 0.001, partial η2 = 0.41), but not age (p = 0.13), were significant in the model. In addition, the results did not change after controlling for these variables, as there
remained a significant main effect of MNA on the emotional well-being (p < 0.001, partial η2 = 0.23), mobility (p = 0.003, partial η2 = 0.11), stigmatization (p = 0.001, partial η2 = 0.13), social support (p = 0.02, partial η2 = 0.07), and in addition cognition (p = 0.02, partial η2 = 0.07).
Discussion
Malnutrition is a highly relevant condition in elderly people with PD that favors loss of auton-
omy, lower quality of life, higher frequency of hospital admissions, and untimely higher mor-
tality. The prevalence of malnutrition and risk of malnutrition we observed in hospitalized
elderly patients with PD was higher than previous studies using the MNA as an outcome mea-
sure in community-dwelling elderly people [2, 8, 17, 18]. In a systematic review the prevalence
of malnutrition in PD according to the MNA was between 0% and 2%, while 20% to 34% were
at risk of malnutrition [18]. Most common symptom related to malnutrition was weight loss.
This agrees with other studies reporting weight loss in PD [21]. Weight loss may predate diag-
nosis and tend to continue during PD stages [22].
In our cohort of elderly patients with PD (without dementia) malnutrition was associated
with male gender, longer disease duration, higher H&Y and depressive mood. Three recent
Table 2. Linear regression model: Predictors of the MNA total score.
Coefficient Standard error Standardised β p Adjusted R2
Constant 12.436 0.792 0.14
Gender (female) -0.15 0.431 0.339 0.029
Disease duration -0.074 0.037 0.273 0.050
H&Y (stage 1,2,3) 0.902 0.495 0.229 0.072
BDI -0.062 0.041 0.134 0.158
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Table 3. Linear regression model: Predictors of the PDQ-39SI.
Coefficient Standard error Standardised β p Adjusted R2
Constant 20.859 7.862 0.52
NMS-Q 1.710 0.251 0.684 <0.001
MNA -1.752 0.529 0.161 0.001
MDS-UPDRS III 0.208 0.074 0.117 0.006
BDI 0.374 0.233 0.038 0.113
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studies also investigated the association between MNA and clinical parameters. Fereshtehnejad
et al. investigated 150 patients with PD (men age 60.8 ± 10.8) and found in their multivariate linear model that depression, UPDRS total score, LEDD and patients’ sex were significantly
associated with the total MNA score [8]. Ongun studied 112 patients with PD (mean
age = 63.7 ± 6.4) and in the multiple logistic regression analysis depression, UPDRS total score, and male gender were independently related to malnutrition [9]. The cohort studied by
Tomic et al. (n = 107, mean age 70.2 ±8.6) is comparable to our cohort in terms of age, how- ever, here only group comparisons (abnormal vs. normal nutrition) or univariate correlations
between MNA and clinical parameters (age, H&Y scale, UPDRS part III, ‘off’ periods and
depression) were reported and no multivariable analyses were performed [3]. In contrast to
the studies of Fereshtehnejad et al. and Ongun, we did not observe an association between
LEDD, NMS-Quest and malnutrition. However, from a methodological point these studies
differed from our study when different measures were used (UPDRS instead of MDS-UPDRS)
and the patients were younger. In summary, our and these studies show that relevant motor
impairments/higher disease stages and depression are the main factors for malnutrition in PD.
We found that malnutrition is an independent predictor of the PDQ-39SI in elderly sub-
jects with PD after controlling for other known predictors of health-related QoL, namely NMS
which have large impact on QoL in elderly patients [10, 23–25]. The impact of malnutrition on
health-related QoL is in line with previous studies in younger cohorts [8, 9]. In particular,
emotional well-being, mobility, social support, and stigmatization were negatively influenced
by malnutrition in our study. Health-related QoL was in addition studied by Fereshtehnejad
et al. and Ongun using the PDQ-39. Ongun and Fereshtehnejad et al. performed univariate
comparisons of the PDQ-39 domains between patients with normal and abnormal nutritional
status and found higher PDQ-39 scores in all [9] or most [8] PDQ-39 domains. In contrast to
other studies, we observed the strongest association between emotional well-being and malnu-
trition and not between mobility and malnutrition [8, 9, 26]. One has to take into account that
in the studies of Ongun and Fereshtehnejad et al., significant differences of the PDQ-39
domains were observed between the poor-nutrition and normal-nutrition groups [8, 9]. How-
ever, in these two studies, both groups also significantly differed in terms of disease duration
and motor and non-motor impairment, which also influence QoL. In particular, longer disease
duration and higher non-motor burden might contribute to poorer health-related QoL in mal-
nourished patients in these studies. This and the higher age in our cohort might explain these
different results. The emotional well-being domain is related to symptoms of depression and
long-standing anxiety [27]. Patients with depression are more likely to exhibit loss of appetite
and decreased food intake, which can favor malnutrition [16, 21]. As demonstrated in our and
former studies, depression and malnutrition seem to be associated in PD [11, 28, 29].
The MNA is widely used and is available in multiple languages and many studies in various
settings used this tool. A large body of evidence underlines the usefulness of the MNA as
screening tool in elderly people. However, despite these benefits of MNA, the sensitivity of the
MNA is still debated because it has been related to a high risk of overdiagnosis of malnutrition
[30–32]. Moreover, in our opinion a relevant shortcoming of the MNA in PD is lumping
dementia and depression together under the term ´neuropsychological problems´. Given the
high prevalence of PD dementia and depression in PD this might cause relevant bias. More-
over, the ´neuropsychological problems´ are not well operationalized in detail. In two studies
among older hospitalized patients, the ´neuropsychological problems’ have operationalized
based on the results of Mini Mental Status Examination and the Geriatric depression score.
However, both studies found different cut-offs to categorize patients into the different catego-
ries of the MNA item ´neuropsychological problems´ (no problems; mild dementia; severe
depression or dementia) [33, 34]. We also observed disagreement when some patients were
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classified as having ´mild dementia´ in the MNA but the MoCa did not indicate PD dementia.
In our study the MNA and MoCa were assessed by independent persons. The assessment of
the MNA item was based on the examiner’s assessment at the time the MNA was collected on
the patient and not on the basis of other medical information in the medical record. Therefore,
persons with subjective memory complaints can be categorized as ´mild dementia´ in the
MNA although the MoCa indicates no relevant objective cognitive deficits. There are also mis-
matches for depression. For example, one person was scores as having ´depression´ in the
MNA, but the BDI was normal. This may be due to the fact that we only recorded depression
using a self-report and not using the gold standard, the interview based on DSM or ICD-10
criteria. Therefore, the MNA has limitations in some patients with PD when it is assessed inde-
pendent of other measures (i.e. depression, cognition). Given the limitations when the MNA
was assessed by medical staff, we assume that a MNA that is patient completed has only limited
value to screen for malnutrition in advanced PD. However, our data underline that also the
MNA that was completed by the nursing staff needs additional geriatric comprehensive assess-
ment to be valid.
Our study has some more limitations. The analysis of health-related QoL and malnutrition
was restricted to hospitalized patients without dementia, limiting the generalizability of our
results. Moreover,—as in the other studies [8–10]—we did not perform detailed assessment of
dysphagia which might have also a relevant influence on malnutrition. We restricted the analy-
sis to the screening part of the MNA, and we cannot fully rule out that the results would differ
if the full MNA would have been used. On the other hand, the sensitivity and specificity of the
short form MNA are almost identical to the original MNA, confirming that the short form is
valid and compares well against the full MNA [14, 15].
Conclusion
The predictors of malnutrition and the impact on health-related QoL in our cohort of elderly
hospitalized patients differ from the existing studies in younger patients. We found that elderly
male persons with longer disease duration and higher disease stages are more likely to be mal-
nourished or at risk for malnutrition. Malnutrition was mainly associated with poor emotional
well-being. Further studies in elderly patients with PD should therefore answer if the treatment
of depression and anxiety beside diet and physical activity can help to improve nutrition status
in these subjects. The MNA should not be used independent of other measures of cognition
and depression in people with advanced PD.
Supporting information
S1 Data.
(SAV)
Author Contributions
Conceptualization: Maria Theresa Gruber, Tino Prell.
Data curation: Maria Theresa Gruber, Julian Grosskreutz.
Formal analysis: Maria Theresa Gruber, Tino Prell.
Investigation: Maria Theresa Gruber.
Methodology: Maria Theresa Gruber, Tino Prell.
Project administration: Tino Prell.
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Supervision: Otto W. Witte.
Validation: Maria Theresa Gruber.
Visualization: Maria Theresa Gruber.
Writing – original draft: Maria Theresa Gruber.
Writing – review & editing: Maria Theresa Gruber, Otto W. Witte, Julian Grosskreutz, Tino
Prell.
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