2018 Van Deun Reproducible Measurements of Muscle
2018 Van Deun Reproducible Measurements of Muscle
2018 Van Deun Reproducible Measurements of Muscle
tone, the precision to find subtle changes in muscle proper- and by reliability parameters, according to the question
ties, which is indispensable in research, is lacking. that should be answered. Agreement parameters assess
Although muscle tone is commonly defined as the how close the results of the repeated measurements are,
central mediated resistance to passive movement, periph- by estimating the measurement error in repeated mea-
eral components such as changes in biomechanical muscle surements, whereas reliability parameters assess whether
properties (such as elasticity and stiffness) may also play participants can be distinguished from each other, despite
an important role.1,4 Recently, a noninvasive device known measurement errors.15
as the MyotonPRO, which combines the assessment of Besides the effect of aging, we hypothesize that parato-
peripheral biomechanical muscle properties with muscle nia will have an influence on muscle tone and biomechani-
tone in 1 single measurement, was introduced. Studies in cal properties measured by MyotonPRO. Therefore, the
healthy participants as well as in individuals with stroke aims of the present study were to (1) compare muscle tone,
or Parkinson’s disease have shown a moderate to very elasticity, and stiffness between 3 different subpopulations
high reliability of the MyotonPRO for measuring muscle of young and old healthy adults and individuals with para-
properties.5-10 Importantly, however, biomechanical muscle tonia, and (2) investigate the intra- and interrater reproduc-
properties can be characteristically different in each neu- ibility of MyotonPRO measurements of the biceps brachii
rological condition. Therefore, the reliability of these mea- (BB) muscle in each subpopulation.
surements may vary between patient populations. Hence,
these previous findings, from diverse neurological condi- METHODS
tions, cannot necessarily be generalized from one patient
group to another. Participants
To date, the MyotonPRO device has been tested in To enlarge the contrast between individuals with and
patients with Parkinson’s disease8 and stroke9,11 but, to the without paratonia, we targeted 3 different subpopulations
best of our knowledge, not yet in patients suffering from (purposive sampling): (1) healthy young adults (n = 18),
paratonia. According to Hobbelen et al, paratonia is a (2) healthy older adults (n = 20), and (3) older adults with
form of hypertonia with an involuntary variable resistance dementia and paratonia (n = 16). For the healthy adults, the
during passive movement. The degree of resistance varies exclusion criteria were presence of any neurological disease
depending on the speed of movement and is proportional and/or usage of medication with impact on muscle tone.
to the amount of force applied. The resistance to passive They were recruited using an informative leaflet, distrib-
movement is in any direction and there is no clasp-knife uted both among staff of the department of Rehabilitation
phenomenon. Moreover, paratonia increases with progres- Sciences and Physiotherapy of the Ghent University, and in
sion of dementia.12 Although the presence of paratonia can a senior’s leisure club in Ghent. The individuals with para-
have an enormous impact on daily care and comfortable tonia were recruited from 2 nursing homes. All of them
positioning especially in the more advanced stages,13 reli- had a diagnosis of dementia, and presence of paratonia
able evidence-based interventions in this population are was evaluated with the Paratonia Assessment Instrument.
challenging.14 To comply with clinical guidelines, the effects The Paratonia Assessment Instrument is a diagnostic tool
of any intervention should be assessed in perspective of the for paratonia, in which the 4 limbs of the participant are
levels of the International Classification of Functioning, moved passively, both slowly and rapidly; the presence of
Disability, and Health model. The levels of activities and paratonia is estimated by criteria based on the consensus
participation of this model are essential in individuals with definition.16 Medication usage and neurological comorbidi-
paratonia. However, as paratonia frequently accompanies ties were recorded. The study was approved by the Ethical
dementia, self-reporting and understanding of guidelines Committee of the Ghent University Hospital, and all partic-
and commands of any testing are hampered for validity, ipants (or legal representative) signed an informed consent.
reliability, and meaningfulness, due to the cognitive dete-
rioration in these patients. For this reason, an objective Device
technical metric assessment at the level of impairment (eg, The MyotonPRO is a small, noninvasive hand-held appa-
muscle tone), without the requirement of understanding ratus that provides objective measurements of mechanical
commands, could significantly improve the evaluation and muscle properties expressed on a continuous scale. After
therapeutic contribution of an intervention. the device probe is positioned on the skin surface above
In addition, despite the valuable research into the psy- the muscle being measured, and thereby slightly compress-
chometric properties that was conducted, some important ing subcutaneous superficial tissue, it exerts a light quick-
gaps still remain. First of all, most intrarater reliability released mechanical impulse. The subsequent dampened
studies focused on test-retest reliability within the same oscillation of the muscle is recorded by an accelerometer
day.5-9,11 However, for the assessment of an intervention and numeric values of muscle parameters are calculated,
effect or process, between-day reliability should not be representing the muscle tone, and biomechanical properties
neglected. Second, reliability does not necessarily represent (http://www.myoton.com/en/Technology). F [Oscillation
the total aspect of reproducibility. According to de Vet Frequency (Hz)] indicates the state of intrinsic tension
et al,15 reproducibility can be described both by agreement or muscle tone in a passive resting state, without any
voluntary contraction. The higher the oscillation frequency, always feasible, and this could thereby affect the muscle
the higher the muscle tone. Frequency increases with con- tone measurements.
traction or muscle stretch. D [Logarithmic Decrement of The measuring point was determined centrally on the
the muscle’s natural oscillation] represents the muscle’s BB muscle belly, at about one-third of the total muscle
elasticity, indicating how much mechanical energy dissi- length (starting distally). The measuring point was marked
pates into the muscle tissue during a single oscillation cycle. and the distance to the cubital fossa was registered to locate
Elasticity is inversely proportional to the decrement (the a reproducible site over the muscle belly in both testing ses-
smaller the value of D, the higher the muscle’s elasticity). sions. The used measurement mode was multiscan (10 taps)
It quantifies the muscle’s ability to recover its initial shape with a tap time of 15 milliseconds and 2 consecutive series
after removal of the external force. S [Dynamic Stiffness of 10 taps were conducted. If the coefficient of variation
(N/m)] is a biomechanical muscle property that depicts (CV) in a series of 10 taps was 3% or more, the measure-
the resistance to contraction from an external force trying ment was repeated until all CV values were less than 3%,
to deform its initial shape. Myotonometric measurement as recommended in the MyotonPRO user’s manual.
of muscle tone, elasticity, and stiffness has been described On each day, measurements were performed on both
as reliable, valid, and responsive outcome measures for left and right BB muscles by 2 raters subsequently. The rat-
muscle property assessment in stroke rehabilitation.11 In ers had little experience with the device (1 training session),
individuals with Parkinson’s disease, a significant correla- and the measurements were performed independently but
tion has been found between myotonometric measurement using the same measurement point. The retesting took
of BB muscle belly stiffness and clinical rating of parkinso- place on the same day of the following week. Participant
nian rigidity.8 characteristics–age, length, and weight—were recorded if
available. In individuals with paratonia, muscle tone of
Procedure the left and right elbow flexor and extensor muscles was
MyotonPRO measurements were performed in supine estimated using the MAS. The sum of these 4 MAS scores
position, elbows flexed in 90° with hands supported on (MAS sum) provides a global view of the severity of para-
the abdomen (Figure 1). This position was chosen to avoid tonia in each individual.14,17,18
discomfort in the individuals with paratonia because their
full range of motion during elbow extension was not
Statistical Analysis
MyotonPRO data were imported and analyzed using
Statistical Package for the Social Sciences version 22
(SPSS 22). The data were checked for normality using the
Shapiro-Wilks test.
To compare muscle properties of the different subpopu-
lations, analysis of variance (ANOVA)/Welch and post hoc
tests were performed and boxplots were used to display
data graphically. Intrarater reliability (between series and
between days) and interrater reliability were analyzed
through the intraclass correlation coefficient (ICC), using
a 2-way mixed model with absolute agreement and single
measures ICC.
To determine the most appropriate number of taps
needed for an objective measurement, interrater reliabil-
ity and intrarater reliability between days were calculated
twice: first using the mean of 2 series (mean of 20 taps),
and second using the mean of only the first series (mean of
10 taps). For interpretation of the ICC values, the criteria of
Domholdt were used: 0.90 or more = very high, 0.89 to 0.7
= high, 0.69 to 0.5 = moderate, 0.49 to 0.26 = low, and
0.25 or less = poor.19 For the agreement estimation, stan-
dard error of measurement (SEM) was calculated as SEM
= SD × √(1 − ICC), where SD is standard deviation for all
observations for the parameter concerned in the given sub-
population. SEM% represents the relative amount of mea-
surement error and is calculated as SEM% = (SEM/mean)
× 100. In this formula, “mean” indicates the mean of all
measurements for the corresponding parameter for each
Figure 1. Illustration of measurements with the MyotonPRO subpopulation. SEM% of less than 10% was arbitrarily
device. considered to be small.20 To estimate the clinical relevance,
196 Volume 41 • Number 4 • October-December 2018
Copyright © 2018 The Academy of Geriatric Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited.
Research Report
the minimal detectable change (MDC) was calculated. MDC with paratonia (P = .986). Subpopulation differences are
is the minimum difference between 2 measurements that is graphically displayed in Figure 2.
necessary to indicate 95% confidence of a real difference
between the true scores of a single individual, and is defined Intrarater Reproducibility Between Series
by MDC = 1.96 × SEM × √2.21 MDC% is calculated as Intrarater reliability and agreement between series are
MDC% = (MDC/mean) × 100. MDC% interpretation is displayed in Table 3. Intrarater reliability between the con-
arbitrary, although Chuang et al9 suggested that MDC% secutive series was very high in healthy young and older
smaller than 10% can be considered excellent, and MDC% adults and moderate to high in individuals with paratonia.
smaller than 30% can be considered acceptable. For all In the healthy subpopulations, intrarater agreement
reproducibility analysis data from left biceps were used, for between series was good; all SEM% were less than 10%,
intrarater between series and interrater reproducibility data and MDC% varied from excellent (<10%) to acceptable
from day 1 were used, and for intrarater reproducibility (<30%), whereas in individuals with paratonia SEM%
data from rater 1 were used. These were chronologically exceeded 10% for muscle tone and for stiffness and all
the first conditions in the test procedure and thereby not MDC% exceeded 10% or even 30%.
affected by previous measurements. Moreover, by using
the data of the left arm (this was mostly the nondominant Intrarater Reproducibility Between Days
arm in the healthy subpopulations; in the individuals with Intrarater reproducibility between days is represented
paratonia dominance was unknown), we tried to reduce the in Table 4. Reliability ranged from moderate to high in
influence of foregoing physical activity. For all analyses, a healthy young adults, and from low to moderate in healthy
significance threshold was set at P < .01. older adults, regardless of the amount of series used. In
individuals with paratonia, intrarater reliability between
days ranged from poor to moderate when using only
RESULTS 1 series (10 taps), and from poor to low when using 2 series
Participants of taps (20 taps).
In total, 54 persons participated in this study: 18 healthy Intrarater agreement between days differed between
young adults (mean age 28.4 years), 20 healthy older the subpopulations. In healthy young adults, all SEM%
adults (mean age 79.6 years), and 16 older adults with were less than 10%, and MDC% ranged from acceptable
paratonia (mean age 85.5 years). Participant characteristics (<30%) to excellent (<10%). In healthy older adults only
are presented in Table 1. In individuals with paratonia, for muscle tone, SEM% was less than 10% and MDC%
the presence of neurological comorbidities and medication less than 30%. In individuals with paratonia, all SEM%
usage were recorded. From this subpopulation, 3 partici- exceeded 10% and all MDC% exceeded 30%.
pants had a history of stroke or transient ischemic attack,
and 6 of them used medication with possible influence on Interrater Reproducibility
muscle tone. Influence of medication and/or neurological In Table 5, interrater reproducibility is presented. In
comorbidities on muscle parameters was assessed without healthy young adults, interrater reliability was high; in
yielding significant effects. healthy older adults, interrater reliability ranged from
high to very high. In individuals with paratonia, inter-
Muscle Tone and Mechanical Properties rater reliability ranged from low to high when 2 series
Parameter characteristics and variance analysis statistics were used, and from low to moderate when only 1 series
are displayed in Table 2. For all parameters ANOVA/ was used.
Welch revealed statistically significant differences (P < In healthy young and older adults, all SEM% were less
.001) between the 3 subpopulations. Post hoc tests were than 10% and MDC% were less than 30%. In individuals
all significant (P < .001), except for muscle dynamic with paratonia, all SEM% values exceeded 10% and all
stiffness between healthy older adults and individuals MDC% exceeded the benchmark of 30%.
Table 1. Mean, Standard Deviation, and Range of Participant Characteristics by Subpopulation
Young Adults (n = 18) Older Adults (n = 20) Individuals With Paratonia
(4 Male/14 Female) (7 Male/13 Female) (n = 16) (3 Male/13 Female)
Participant Characteristics Mean (SD) Range Mean (SD) Range Mean (SD) Range
Age, y 28.4 (3.5) 24-34 79.6 (5.6) 66-87 85.5 (6.8) 70-98
Length, cm 170.4 (9.1) 155-192 163 (8.8) 150-180 N/A (N/A) N/A
Weight, kg 63.5 (8.5) 48-80 68.1 (10.6) 50-85 N/A (N/A) N/A
BMI, kg/m2 21.8 (1.9) 18.7-25.8 25.3 (3.0) 19.1-31.2 N/A (N/A) N/A
MAS sum N/A (N/A) N/A N/A (N/A) N/A 10.9 (3.2) 6-16
Abbreviations: BMI, body mass index; MAS, Modified Ashworth Scale; N/A, information not available; SD, standard deviation.
Table 2. Parameter Characteristics, ANOVA/Welch and Post Hoc Test of Tone, Elasticity, and Stiffness of the Biceps Brachii Muscle of
Healthy Young and Older Adults and Individuals With Paratonia
Parameter Characteristics Young Adults Older Adults Individuals With Paratonia
Tone, Hz
Mean (SD) 11.80 (0.84) 14.02 (1.83) 15.01 (2.81)
Range (min-max) 4.47 (10.34-14.81) 15.29 (10.50-25.79) 19.98 (10.51-30.49)
ANOVA/Welch P < .001
Tukey post hoc
Young adults / P < .001 P < .001
Older adults P < .001 / P < .001
Individuals with paratonia P < .001 P < .001 /
Elasticity (log decrement)
Mean (SD) 1.47 (0.19) 1.84 (0.37) 1.71 (0.43)
Range (min-max) 0.99 (1.05-2.05) 1.82 (1.00-2.82) 2.15 (0.90-3.05)
ANOVA/Welch P < .001
Tukey post hoc
Young adults / P < .001 P < .001
Older adults P < .001 / P < .001
Individuals with paratonia P < .001 P < .001 /
Stiffness, N/m
Mean (SD) 199.84 (20.14) 273.89 (53.03) 273.20 (70.86)
Range (min-max) 91.80 (148.70-240.50) 533.80 (166.80-700.60) 510.3 (129.90-640.20)
ANOVA/Welch P < .001
Tukey post hoc
Young adults / P < .001 P < .001
Older adults P < .001 / P = .986
Individuals with paratonia P < .001 P = .986 /
Abbreviations: ANOVA, analysis of variance; SD, standard deviation.
Figure 2. Boxplot visualization of (A) tone, (B) elasticity, and (C) stiffness of biceps brachii muscle between healthy young
adults, healthy older adults, and individuals with paratonia.
domain refolding. However, further fundamental research MyotonPRO results remains however unclear and should
is needed to clarify this hypothesis. be investigated in future studies.
When comparing healthy older adults with healthy
young adults, higher muscle tone, lower elasticity, and Intrarater Reproducibility Between Series
higher stiffness as well as a broader range in each of these Intrarater reliability between series was very high for all
parameters can be observed in the older subpopulation. parameters in the healthy subpopulations, which is in
Potentially, structural changes in the individual aging accordance with previous studies.5-7,10 ICC values were
muscles may be responsible for these findings.25-28 remarkably lower in individuals with paratonia (Table
Compared with previous studies in healthy adults 3). We argue this might be due to the susceptibility of
using MyotonPRO, our values of muscle tone were individuals with paratonia for external influences. For
lower, while elasticity and stiffness were higher.5-7 A example, a sudden noise during one of the series of taps
possible explanation for this deviating findings might be might remain unnoticed by the rater but can affect muscle
the difference in elbow flexion angle (and thereby differ- tone in individuals with paratonia. Also, due to the muscle
ent elongation of the BB muscle) in the supine position. tone fluctuations in individuals with paratonia, it was
To avoid discomfort in individuals with paratonia, all often necessary to repeat several testing series to obtain
our participants were tested in 90°, versus 10° to 15° a CV less than 3% (as recommended in the MyotonPRO
in previous studies.5-7 The influence of elbow angle on user’s manual).
The best agreement was found in healthy young adults, 30%; this indicates that small changes within a group
with small SEM% and excellent MDC%.9,20 In healthy of individuals could be effectively detected using the
older adults, SEM and MDC values were slightly higher MyotonPRO.9,20 In healthy older adults, only for muscle
than in healthy young adults, nevertheless SEM% were tone SEM% less than 10% and MDC% less than 30%
small and MDC% were acceptable to excellent.9,20 In were obtained. The higher agreement for healthy young
individuals with paratonia, SEM and MDC values were adults compared with older adults is in line with findings
higher than in the healthy subpopulations, indicating lower of Agyapong-Badu et al.10 In individuals with paratonia, all
agreement; for muscle tone and stiffness, SEM% exceeded SEM% and MDC% exceeded largely the proposed thresh-
10% and MDC% exceeded 30%. The SEM and MDC olds. This might suggest this device would—in the given
values of the healthy subpopulations in the present study protocol—be less suitable to detect small changes over time.
are somewhat higher than the values reported in previ- On the other hand, up to now there is no valuable alterna-
ous studies.6,7,10 Possibly this difference may be caused tive device that provides this specific information. Besides,
by participant characteristics. In the previous studies all the fluctuating nature of paratonia is a real challenge for
participants were males.6,7,10 However, a possible gender any assessment tool. Moreover, we consider that appropri-
relationship is not investigated yet. ate consideration of additional outcome parameters such
as pain and difficulties in daily care could provide further
Intrarater Reproducibility Between Days insight into the effects of an intervention for paratonia.
Also for intrarater reliability between days, differences were Obviously, intrarater reproducibility between days is
found between the subpopulations (Table 4). The highest lower than intrarater reproducibility between series (ie,
reliability (ie, moderate to high) was found in healthy young within the same day). That is not surprising, because when
adults. Again, the lowest reliability (poor to moderate) was comparing measurements from 2 different days, more fac-
found in individuals with paratonia. In the present study, tors such as fluctuations in measurement circumstances
for all parameters intrarater between-day reliability was (eg, room temperature and background noise) and muscle
substantially higher in healthy young adults than in healthy conditions of the participants (eg, related to physical activ-
older adults. In a previous study, this could only be estab- ity previous to the testing moment, mood changes, and
lished for muscle tone and stiffness but not for elasticity.10 exact timing of medication intake) could have affected
In healthy young adults, all intrarater between-day our results. The described reproducibility should be inter-
SEM% were less than 10% and MDC% were less than preted as a combination of reproducibility of the device
(measuring a muscle in exactly the same condition on Interrater reliability ranged from high to very high in
both occasions) and the variability in muscle condition. the healthy subpopulations (Table 5), whereas in indi-
Notwithstanding our efforts, this variability could not be viduals with paratonia interrater reliability ranged from
completely excluded, which may have been of importance low (muscle tone) to moderate (elasticity and stiffness)
especially for persons with paratonia. Apart from that, our when 1 series of taps was used, and from low (muscle
method of (re)locating the point of measurement might tone) to moderate (elasticity) and high (stiffness) when 2
have also added more variability in our between-day series of taps were used. A plausible assumption for the
results, especially in older individuals. More specifically, lower interrater reliability in individuals with paratonia
the muscle belly of older adults is often less voluminous, compared with the healthy subpopulations is again the
and the location of the middle of the BB muscle belly might variable and sensitive nature of paratonia, enhancing
be situated some more medially and distally.5,6 This is why possible variability within subsequent measurements.
our methodology focused on the proximodistal distance The best interrater agreement was found in healthy
and determined the exact mediolateral testing site by sub- young adults, with SEM% less than 10% and MDC%
jectively palpating the muscle belly. Only the proximodistal less than 30%. This better agreement in healthy young
distance was recorded, and as a result, this could have adults compared with older adults for all parameters is
added some (mediolateral) variation when retracing the in line with a previous study.5 Although all SEM(%) and
location of the measurement in the retest. MDC(%) values were higher in older than in younger
adults, still nearly all SEM% of healthy older adults were
Interrater Reproducibility less than 10% and MDC% were less than 30%. In indi-
In the present study, for all 3 parameters, interrater reliabil- viduals with paratonia, all SEM% exceeded 10% and all
ity was the highest in healthy older adults. Agyapong-Badu MDC% exceeded 30%.
et al5 described this tendency only for elasticity whereas Notably, in the present study the reliability and
for muscle tone and stiffness the highest ICC values were agreement show different tendencies when comparing the
reported in young adults. 2 healthy subpopulations; although reliability was higher in
Journal of GERIATRIC Physical Therapy 201
Copyright © 2018 The Academy of Geriatric Physical Therapy, APTA. Unauthorized reproduction of this article is prohibited.
Research Report
the oldest, agreement was higher in the youngest individu- time-effectiveness of this assessment. In previous studies
als. This finding supports the importance of investigating the amount of taps was very diverse. Aird et al29 found
both aspects of reproducibility and highlights the strength higher reliability and agreement in MyotonPRO measure-
and novelty of our study design. On one hand, reliability ments of quadriceps muscles of older males when using
is about distinguishing individuals from each other despite the mean of 2 series of 10 taps than using only 1 series.
measurement errors and therefore will be facilitated if In this study we performed 2 series of 10 taps and repro-
variability between individuals is high, which is frequently ducibility was calculated both using 1 and 2 series. When
the case in older adults. On the other hand, for agreement comparing the results, we found interesting dissimilarities
between repeated measures, measurement error is more between the subpopulations. In general, in all subpopula-
determinant. It is possible that in our results, this measure- tions reproducibility was higher when the mean of 2 series
ment error was increased in the older adult subpopulation was used. However, the increase in reproducibility by add-
due to body composition characteristics of our partici- ing a second series was higher in individuals with paratonia
pants. For example, lower muscle mass due to aging, high than in healthy adults. When performing MyotonPRO
body mass index, and/or high subcutaneous fat percentage measurements in healthy participants therefore, one should
could impede appropriate muscle palpation and thereby consider whether it is worth the effort of performing a
jeopardize precise localization of the measuring point and second series to increase reproducibility. On the other
increase measurement errors in the collection data. hand, in individuals with paratonia, the added value of this
additional series is apparent. This finding could provide
Number of Series Used additional guidelines to improve experimental designs of
In our study design, we included 2 different protocols to studies using MyotonPRO.
calculate intrarater between days (Table 4) and interrater
reproducibility (Table 5). This was done purposefully to Study Limitations
determine the most appropriate number of taps needed Apart from the difficulties in standardizing the exact
for an objective measurement without compromising the location of the measuring point on the BB muscle, some
other limitations of the present study should be taken into 3. Biering-Sorensen F, Nielsen JB, Klinge K. Spasticity-assessment: a review.
Spinal Cord. 2006;44(12):708-722.
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5. Agyapong-Badu S, Aird L, Bailey L, et al. Interrater reliability of muscle
body temperature, blood flow, alcohol consumption, and tone, stiffness and elasticity measurements of rectus femoris and biceps
the degree of foregoing physical activity levels, were not brachii in healthy young and older males. Working Pap Health Sci.
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was not available even though we assume body composi- symmetry and within-session reliability using the MyotonPRO. J Neurol
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mentioned that although all participants were very col- mechanical properties of biceps brachii muscles in healthy young adult males
using the MyotonPRO device. Working Pap Health Sci. 2013;1(3):1-11.
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repeated if not comply with a CV less than 3%, which was myotonometric measurements of hemiparetic arms in patients with stroke.
often challenging. Furthermore, because of practical rea- Arch Phys Med Rehabil. 2013;94(3):459-466.
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ACKNOWLEDGMENT minimally detectable change and minimally important change. Health Qual
The authors sincerely thank all participants who vol- Life Outcomes. 2006;4:54.
22. Hobbelen JS, Tan FE, Verhey FR, Koopmans RT, de Bie RA. Prevalence,
unteered for this study. Our special thanks to Helga incidence and risk factors of paratonia in patients with dementia: a one-year
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