Journal of Alzheimer’s Disease 78 (2020) 1615–1637 1615

DOI 10.3233/JAD-200691
IOS Press

Paratonia in Dementia: A Systematic

Review
Hans Drentha,b,∗ , Sytse Zuidemac , Ivan Bautmansd , Lucio Marinellie,f ,
Galit Kleinerg,h and Hans Hobbelena,c
a Research group Healthy Ageing, Allied Health Care and Nursing, University of Applied Sciences Groningen,
Groningen, the Netherlands
b ZuidOostZorg, center for Elderly Care, Drachten, the Netherlands
c Department of General Practice and Elderly Care Medicine, University of Groningen, University Medical

Center Groningen, Groningen, the Netherlands

d Frailty in Ageing Research Group and Gerontology Department, Vrije Universiteit Brussel, Brussels, Belgium
e Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, University

of Genoa, Genoa, Italy

f Department of Neuroscience, IRCCS Ospedale Policlinico San Martino, Genoa, Italy
g Department of Medicine, Division of Neurology, University of Toronto, Toronto, ON, Canada
h Jeff and Diane Ross Movement Disorders Clinic, Baycrest Center for Geriatric Health, Toronto, ON, Canada

Handling Associate Editor: Teresa Liu-Ambrose

Accepted 2 October 2020

Abstract.
Background: Paratonia is a dementia-induced motor abnormality. Although paratonia affects virtually all people with
dementia, it is not well known among clinicians and researchers.
Objective: The aim of this study was to perform a systematic review of the literature on the definition, pathogenesis, diagnosis,
and intervention of paratonia as well as to propose a research agenda for paratonia.
Methods: In this systematic review, the Embase, PubMed, CINAHL, and Cochrane CENTRAL databases were searched
for articles published prior to December 2019. Two independent reviewers performed data extraction and assessed the risk
of bias of the studies. The following data were extracted: first author, year of publication, study design, study population,
diagnosis, assessment, pathogenesis, therapy and interventions.
Results: Thirty-five studies met the inclusion criteria and were included. Most studies included in the review mention clinical
criteria for paratonia. Additionally, pathogenesis, method of assessment, diagnosis, and paratonia severity as are interventions
to address paratonia are also discussed.
Conclusion: This systematic review outlines what is currently known about paratonia, as well as discusses the preliminary
research on the underlying mechanisms of paratonia. Although paratonia has obvious devastating impacts on health and
quality of life, the amount of research to date has been limited. In the last decade, there appears to have been increased
research on paratonia, which hopefully will increase the momentum to further advance the field.

Keywords: Dementia, motor disorders, motor skills disorders, paratonia, systematic review

INTRODUCTION
∗ Correspondence to: Hans Drenth, Research Group Healthy
Ageing, Allied Healthcare and Nursing, Hanze University of
According to the 5th edition of the Diagnostic
Applied Sciences, PO Box 3109, 9701 DC, Groningen, the Nether- and Statistical Manual of Mental Disorders (DSM
lands. Tel.: +31 622663466; E-mail: [email protected]. V), dementia is a major neurocognitive disorder

ISSN 1387-2877/20/$35.00 © 2020 – IOS Press and the authors. All rights reserved
This article is published online with Open Access and distributed under the terms of the Creative Commons Attribution Non-Commercial License (CC BY-NC 4.0).
1616 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

that affects 6 distinctive cognitive domains [1]. The

effects of dementia on the perceptual-motor domain
in particular highlight the fact that motor impairments
are correlated with cognitive impairments in demen-
tia. Motor decline in dementia has been demonstrated
over decades [2] but still lacks widespread recogni-
tion as a major cause of disability and dependency
in dementia. Often, movement disorders are present
prior to detectable cognitive changes. Studies have
shown that gait speed starts declining up to 12 years
prior to the development of mild cognitive impair-
ments (MCI) and up to 7 years prior to the clinical
onset of dementia [3, 4]. The extent of motor impair-
ment varies depending on the type of dementia
[5, 6].
One manifestation of motor abnormalities obser-
ved in dementia is paratonia (Fig. 1). Paratonia was
first described and observed by Friedlander [7] in
1828 and later observed by Dupré [8] in 1910; they
characterized paratonia as “an inability to relax mus-
cles in the setting of cognitive impairment”. In 1927,
Kleist [9] observed a hypertonic response to pas-
sive movement in late-stage dementia and called it
“Gegenhalten” (i.e., counter pull). In 1949, Kral [10]
described facilitory paratonia as a form of pathologic
assistance (i.e., actively assisting passive movement
or involuntary cooperation). Both types of parato-
nia have been shown to be associated with cognitive
impairment or mental disorders [11, 12]. Involun-
tary resistance to passive movement, also called
“oppositional paratonia”, has been estimated to be
Fig. 1. Typical (fetal) posture of patient with advanced paratonia
present in 5% of patients with MCI and in up to with flexion and adduction of the extremities.
100% of patients with advanced dementia [13, 14].
In advanced dementia, paratonia may lead to fixed
postures (contractures). Fixed postures may lead to paratonia in the clinical setting as well as to propose
skin breakdown, infection, and pain upon movement, a research agenda on paratonia for future work.
thereby reducing comfort and quality of life. Some
of the consequences of paratonia include difficulties METHODS
with washing, dressing, feeding, and providing gen-
eral care to the patient as well as increased caregiver The PRISMA (Preferred Reporting Items for
burden and stress [15]. Systematic Reviews and Meta-Analyses) guidelines
Despite the fact that paratonia eventually affects were adopted [17]. A checklist is provided as Sup-
virtually all people with dementia and leads to dev- plementary Table 1.
astating health consequences and poor quality of life
[16], this condition is not well known among clin- Search strategy
icians and researchers. Additionally, research-based
data are scarce, and clinical guidelines are lacking. The Embase, PubMed, CINAHL, and Cochrane
Therefore, the aim of this study is to perform CENTRAL databases were searched for articles pub-
a systematic review of the literature on the defi- lished prior to December 2019. Search terms were
nition, pathogenesis, diagnosis, and intervention of both employed as free text words and mapped to
paratonia. With this overview of the existing scien- subject headings terms with explosion when feasi-
tific evidence, we aim to increase the awareness of ble. We utilized all possible relevant terminology
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1617

Table 1
Key words regarding dementia, paratonia/hypertonia and older people used in the search string
Entry Keywords
Dementia “Dementia” OR “Alzheimer Disease” OR “Alzheimer” OR “Lewy Body Disease” OR “Lewy Bod” OR
“Parkinson Disease” OR “Parkinson” OR “Dementia, Vascular”
AND
Paratonia/hypertonia “Muscle Rigidity” OR “Muscle Hypertonia” OR “Paratonia” OR “Gegenhalten” OR “Facilitory Paratonia”
OR “Mitgehen” OR “Muscle Rigidit” OR “Counterpull” OR “Motor negativism” OR “Hypertonia” OR
“Hypertonie d’opposition” OR “Muscle resistance” OR “Motor resistance” OR Muscle ton∗ OR “Muscle
stiffness” OR “Motor Abnormalities”
AND
Older people “Adult” OR “Middle Aged” OR “Aged” OR “Aged, 80 and over” OR “Frail Elderly” OR “Adult” OR
“Elder” OR “Senior” OR “Geriatric” OR “Nursing home”

regarding dementia, paratonia/hypertonia and older Data extraction and study quality
people using the PICO process [18]. For detailed
information on the search terms, see Table 1. Bibli- The data were independently extracted by two
ographies from identified articles were reviewed for reviewers. A standardized data extraction form was
additional references. utilized in the review of each study, and the following
data were extracted: first author, year of publication,
study design, study population (age, gender, and type
Study selection of dementia) and content/context regarding parato-
nia (i.e., definition and clinical criteria, diagnosis and
Initially, abstracts and titles were screened inde-
assessment, pathogenesis, and therapy and interven-
pendently by two reviewers using the online program
tions). The methodological quality of each study was
Rayyan [19]. Any disagreements were solved by dis-
assessed to determine to what extent each publica-
cussion until a consensus was reached.
tion addressed the possibility of bias in its design.
Critical appraisal tools were used to examine the
Inclusion criteria study design to ensure that the criteria were met [20].
The tools determined whether a criterion was met,
All types of study designs and all articles written whether it was unclear if the criterion was met, or
in English, Dutch, French, or German were eligi- whether that criterion was not applicable. One point
ble for inclusion when paratonia or its synonyms was allocated when a criterion was met. The number
(i.e., Gegenhalten, mitgehen, oppositional paratonia, of points was summed and compared to the maximum
facilitory paratonia, counterpull, motor negativism, number of points possible. If an item was not applica-
hypertonie d’opposition) were described. Studies ble, the maximum number of points was reduced by
were also included if they described a direct rela- one (Table 2). The assessment of bias was performed
tionship between dementia, muscle stiffness, or range independently by two reviewers. Disagreements
of motion (i.e., extrapyramidal signs, muscle rigidity, were resolved by discussion until a consensus was
stiffness, hypertonia, contractures, muscle resistance, reached.
motor resistance, variable muscle tone, muscle tone
disorder, muscle stiffness, or movement disorder).
RESULTS
Exclusion criteria
Search results and study quality
Studies related to stroke or Parkinson’s disease
(PD), Lewy body dementia, or studies that used the After duplicates were eliminated, 1,573 publica-
Unified Parkinson Disease Rating Scale (UPDRS) tions were identified using key words. After an initial
were excluded from the systematic review, as stroke- screening of titles and abstracts, 1,499 studies were
and PD-related motor impairments (spasticity and excluded because they did not meet the inclusion cri-
Parkinsonian rigidity) have different clinical pre- teria, and the full texts of 74 studies were reviewed.
sentation and other pathophysiological origin than An examination of the available reference lists of
dementia-related motor impairments. these 74 studies did not reveal additional studies.
 Table 2
Data extraction Table

1618
First Design Population, n = age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Bautmans RCT n = 15, age range: Form of hypertonia characterized Presenting paratonia with altered – Cervical spine 10/13
et al. 77–98, male n = 6, by an active unintentional neck posture (cervical mobilization,
(2008) severe AD resistance against passive antero-position, extension or caused by postural
[28] movement. Based on consensus kyphosis) and known dysphagia. head and cervical
definition by Hobbelen et al. 2006 neck changes due
[47]. to paratonia, to
improve
swallowing

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

capacity.
Benassi Cross-sectional n = 398, age range: Primitive reflex. Limp placement maneuver, Cortical – 3/7
et al. 67–87, dementia examiner passively lifts the patients disinhibition sign.
(1990) (n = 27, male n = 14) arm with the instruction to relax.
[33] When the arm stays elevated this
indicates paratonia.
Bennet Cohort, 5.8 years n = 77, age range: – – Frontal system – 8/9
et al. 60–86, male n = 58, dysfunction.
(2002) VaD
[32]
Beversdorf Cross-sectional n = 25, age mean: Alteration of tone to passive Subjective impressions of both Frontal lobe – 3/7 Score on Test
and and test 70.1(8.7), male n = 9, movement, divided into assistance and resistance offered to dysfunction. accuracy
Heilman AD (n = 20), FTD oppositional paratonia passive flexion and extension about appraisal; 7/9
(1998) (n = 2), LBD (n = 1), (Gegenhalten) and facilitory the elbow versus Modified Kral
[11] pseudodementia paratonia. procedure; With this procedure the
(n = 1), isolated patient is in seated position. The
memory impairment examiner will flex and extend the
(n = 1) right arm between full flexion and
90 degrees of extension three times
with the patient instructed to relax
completely. At the end of the third
cycle, the patient’s arm will be
released at the level of the patient’s
leg and the examiner’s hand
withdrawn. The patient’s response
must be scored as follows: 0 = no
movement; 1 = right arm flexes, but
insufficiently to raise the hand off
of the leg; 2 = right arm flexes,
lifting the arm off of the leg but less
than halfway to full
flexion;3 = right arm flexes at least
halfway, but not fully; 4 = right arm
flexes fully, or repeated cycles of
flexion and extension occur.
 Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Critchley Narrative review – Gegenhalten. A uniform resistance – Cerebrovascular – 5/6
(1956) to passive manipulations, especially degeneration.
[22] in limbs and the neck. Often with a
“mental” component, i.e., rigidity
may vary directly with the amount
of force used by the examiner or

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

the subject is not relaxing.
Damasceno Cross-sectional n = 174, AD (n = 30, Primitive reflex, Gegenhalten. Subjective impressions of Cortico- – 5/7
et al. age: mean 70.9 (9.1), resistance to passive, irregular subcortical
(2005) male n = 11 extension and flexion of arms and neuronal loss.
[34] legs.
Drenth Prospective study, n = 152, age: mean Form of hypertonia with an MyotonPro (handheld device Peripheral – 10/10
et al. 6 months on 83.5 (8.2), dementia involuntary variable resistance objectively measuring muscle biomechanical
(2017) psychometric during passive movement. Based properties) versus MAS-P, PAI, muscle changes
[40] properties test on consensus definition by passive movement of extremities. due to AGEs.
Hobbelen et al. 2006 [47]. Following criteria must be met;
-An involuntary variable resistance
during passive movement
-No clasp-knife phenomenon
-Resistance to passive movement is
in any direction
-Resistance must be felt in either
one limb in two movement
directions or in two different
limbs
-Degree of resistance correlates
with the speed of movement (e.g.,
a low resistance to slow
movement and a high resistance
to fast movement).
Drenth Cohort, one-year n = 144, age: mean Form of hypertonia characterized PAI; passive movement of Peripheral Preventing or 9/9
et al. 80.7 (7.7), AD or by an active unintentional extremities (see above) MAS-P. biomechanical postponing
(2017) AD/VaD resistance against passive muscle changes paratonia by
[30] movement. Based on consensus due to AGEs. decreasing AGE
definition by Hobbelen et al. 2006 formation and
[47]. accumulation
through glycemic
control (physical
activity, diet)

1619
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Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Duret et al. RCT n = 14, age: range Rigidity, extrapyramidal sign. Modifies Columbia rating scale for Lewy bodies, – 11/13
(1989) 56–83, male n = 6, rigidity. neuronal loss or
[29] dementia gliosis in
substantia nigra.
Rigidity in AD
differs

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

pharmacologically
from Parkinson
rigidity.
Franssen Cross-sectional n = 135, age: mean Primitive reflex. Paratonic rigidity Graded with the amount of passive Cortical inhibition – 6/7
et al. 72.6 (9.5), male defined as stiffening of a limb in force necessary to elicit stiffening. loss.
(1991) n = 45, no memory response to contact with the
[35] impairment n = 27, examiner’s hand and an involuntary
mild cognitive resistance to passive changes in
impairment n = 20, position and posture.
AD n = 88
Franssen Case series n = 56, age: mean 74.6 Primitive reflex, paratonic rigidity Resistance elicited with sudden Frontal lobe – 89
et al. (9.6), male n = 16, AD or Gegenhalten. Defined as a passive changes in position and/or pathology.
(1993) sudden increase in muscle tone of speed and regularity of movement
[46] an extremity in reaction to an of the upper extremity.
external perturbation of that
extremity, resulting in an
involuntary resistance to passive
movement.
Hobbelen Pilot RCT n = 15, age: range Oppositional paratonia a form of Middelveld-Jacobs criteria; passive – - Passive 11/13
et al. 70–9, male n = 1 hypertonia in late stage dementia. movement of extremities, trunk and movement therapy
(2003) head. Following criteria must be -Stabilizing
[25] met: cushions
-Increase in muscle tone during
passive movement of the
extremities, head or trunk
-Occurring at flexion and
extension, independent of the
starting position of the joints
-Increasing with rapid movement
-Decreasing slow movement
-Ranging from light tovery fierce.
MAS-P.
 Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Hobbelen Delphi procedure – Paratonia is a form of hypertonia – – – 6/6
et al. for consensus with an involuntary variable
(2006) definition resistance during passive

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

[47] movement. The nature of paratonia
may change with progression of
dementia (e.g., from active
assistance to active resistance). The
degree of resistance depends on the
speed of movement.The degree of
paratonia is proportional to the
amount of force applied and
increases with progression of
dementia. The resistance to passive
movement is in any direction and
there is no clasp-knife
phenomenon.
Hobbelen Cross-sectional on Phase 1: n = 79, age: Consensus definition Hobbelen PAI passive movement of – – 6/6
et al. psychometric range 67–99, male et al. 2006 [47]. extremities (see above).
(2008) properties test in 3 n = 17, AD/VaD
[42] phases (n = 57), VaD (n = 17),
LBD (n = 4), other
(n = 1)
Phase 2: n = 86, age:
range 65–96, male
n = 26, AD/VaD
(n = 60), VaD (n = 22),
LBD (n = 2), other
(n = 2)
Phase 3: n = 24, age:
range 78–95, male
n = 4, AD/VaD
(n = 16), VaD (n = 6),
other (n = 1)

1621
 1622
Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Hobbelen Cohort, one year n = 204, age: mean Consensus definition Hobbelen PAI passive movement of Unclear – 10/10
et al. 79.8 (7.5), male et al. 2006 [47]. extremities (see above). -Frontal lobe
(2011) n = 93, AD (n = 91), pathology
[14] VaD (n = 50), -Substantia nigra
AD/VaD (n = 36), pathology
LBD (n = 14), other -Peripheral

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

(n = 13) biomechanical
changes
-Anti psychotic
medication may
induce
paratonia-like
rigidity.
-Diabetes and
vascular damage
are risk factors
Hobbelen RCT n = 102 (intervention Consensus definition Hobbelen PAI passive movement of – Passive movement 12/13
et al. n = 48, control n = 54), et al. 2006 [47]. extremities (see above). MAS-P. therapy.
(2012) age: range 67–98,
[26] male n = 19, AD
(n = 64), VaD (n = 18),
AD/VaD (n = 11),
LBD (n = 4), other
(n = 5)
Jenkyn Cross-sectional n = 76, age: range Primitive reflex, Gegenhalten. Passive extension and flexion of the Cerebral – 7/7
et al. 16–80, male n = 43, Paratonia can be differentiated limbs. dysfunction,
(1977) cognitive impaired; from the full range, regular rigidity, An irregular opposition to the cortical inhibition
[21] mild (n = 25), or cog-wheeling of Parkinsonism examiner’s movementsafter loss.
moderate (n = 23), and theclasp-knife phenomenon of instructions to relax resulted in a
marked (n = 10), no spasticity. ‘catching’sensation is considered
impairment (n = 18) abnormal.
Limp placement maneuver,
examiner passively lifts the patients
arm with the instruction to relax.
Any delay in dropping of the arm
was considered abnormal after
Parkinsonian rigidity and spasticity
had been excluded.
 Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Kleiner- RCT n = 10 (intervention Increasing muscle resistance PAI passive movement of Originate in the Botulinum toxin 12/13
Fisman n = 5, control n = 5 reflexively when a limb is moved extremities (see above). Severity by central nervous injection
et al. with crossover), age: passively (severity can fluctuate joint range of motion. system.

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

(2014) mean 85.3 (8.0), male depending on level of relaxation),
[27] n = 1, AD (n = 9), FTD unto constant muscle contraction in
(n = 1) advanced stages.
Kurlan Narrative review/ – In paratonic rigidity, there is – – – 6/6
et al. Viewpoint resistance to passive movement of a
(2000) limb whereby the degree of
[12] resistance varies depending on the
speed of movement. Resistance
increases when the limb is moved
more rapidly and decreases or even
disappears when it is moved more
slowly. Cogwheeling can occur
with parkinsonian or paratonic
rigidity and does not help to
distinguish the two types of
rigidity. The presence of mitgehen
suggests that the quality of rigidity
is paratonic.
Marinelli Cross-sectional on n = 10, age: range Oppositional (Gegenhalten) with Paratonia scale; subjective Defective – 8/10
et al. psychometric 63–84, male n = 6, resistance to passive movement or impressions of both assistance and response
(2017) properties test MCI (n = 7), AD facilitory (mitgehen) occurring resistance offered to passive flexion inhibition
[43] (n = 1), AD/VaD when the action is in the same and extension about the elbow. associated with
(n = 1), Fld (n = 1) direction of passive movement. Modified Kral procedure (see frontal lobe
above) versus electromyography. lesions.
O’Keeffe Cross-sectional n = 110, age: mean 78 Primitive reflex Presence or absence of Frontal lobe – 6/7
et al. (5) Paratonic rigidity (Gegenhalten). Gegenhalten noted during irregular pathology
(1996) AD (n = 55, male passive extension and flexion of the Extrapyramidal
[36] n = 21) Control elbow and wrist joints. neural loss.
(n = 55)

1623
 1624
Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Paulson Narrative review n = 85, age: mean 62.3 Primitive reflex. – Central nervous – 5/6
and (?), dementia Increase in rigidity in both the degeneration by
Gottlieb motor and psychological areas. age and disease.
(1968) Paratonic rigidity (Gegenhalten).
[23] Marked increase in tone which the

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

examiner may think is voluntary,
but usually is not consciously
determined.
Hypertonus is accentuated by rapid
passive movements of the limb and
distinguished it from spasticity
(clasp-knife) as well as from
cogwheel rigidity of Parkinsonism.
Peralta and Narrative review AD Gegenhalten. Catatonia like sign. – – – 6/6
Cuesta. Motor abnormality of severe
(2017) mental disorder.
[50]
Pauc and Narrative review Dementia Involuntary resistance to passive – Neuronal loss – 3/6
Young movement (Gegenhalten). occurring with
(2012) A primitive reflex occurring normal ageing and
[48] naturally in neonates which should the onset of
disappear as the brain develops. dementia.
Ries Narrative review AD, VaD, AD/VaD, Consensus definition Hobbelen PAI passive movement of – Facilitating the 6/6
(2018) LBD, PDD, FTD et al. 2006 [47]. extremities (see above). movement by
[49] giving some
counterpressure in
the direction of
the movement that
the patient must
move into
Risse et al. Cohort until death n = 28, male n = 28, Resistance to movement with – No – 4/9
(1990) (probable) AD increased muscle tone throughout neuro-pathologic
[31] the range of motion while not on (substantia nigra
antipsychotic drugs. Gegenhalten, neural loss)
patient appears to be actively evidence for
resisting passive movement in any Parkinson disease.
direction.
 Table 2
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total
publication items
Souren Narrative review AD Type of rigidity that occurs on Moving passively an extremity Symptom of Paratonia serves 6/6
et al. contact. Changing resistance to (usually the forearm) repeatedly, congenital or as a physiologic
(1997) passive alterations in position and first slowly and evenly, and, acquired diffuse and psychological
[16] posture. The degree of paratonia subsequently in a more rapid, brain damage. stabilizing
increases when the patient is brusque and irregular fashion. Resembles mechanism,

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

repeatedly urged to relax. Can be primitive reflex in protecting the
elicited or augmented by state of healthy infants, patient against
anxiety, anger and agitation. therefore can be overwhelming
considered as the external stimuli.
return of an Approach and
infantile behavioral advice
stabilization reflex are given, such as
mechanism, gentle
parallel to the movements, eyes
patient’s motor and voice contact
function decline. to reduce anxiety
and agitation.
Active physical
activity to prevent
or postpone
contractures.
Tyrell and Cross-sectional n = 10, age; range Paratonic rigidity (Gegenhalten) an Rigidity detected on passive – – 3/7
Rossor. 53–82, male n = 2, AD increase in muscle tone which movement of the limb, occurring in
(1988) (n = 4), AD/VaD occurs in response to passive absence of cogwheeling or a spastic
[38] (n = 1), Progressive movement, proportional in degree catch, that is not exacerbated by
dyspraxia (n = 3), to the stimulus applied. movement in the contralateral fist.
CVD (n = 2) Limb placement maneuver (see
above).
Tyrell et al. Cross-sectional n = 20, age: mean 59.1 Extrapyramidal sign, rigidity. – No evidence for – 4/7
(1990) (8.5), AD dopaminergic
[37] nigrostriatal
dysfunction.
Van Deun Cross-sectional on n = 16, age: mean 85.5 Consensus definition Hobbelen PAI passive movement of – – 9/10
et al. psychometric (6.8), male n = 3, et al. 2006 [47]. extremities (see above).MAS-P.
(2016) properties test dementia with MyotonPro (handheld device
[41] paratonia objectively measuring muscle
properties).

1625
 Table 2

1626
Continued
First Design Population, n=, age, Definition/Clinical criteria Diagnosis and assessment Pathogenesis Therapy and Critical appraisal
author/ gender and dementia interventions score Items
year of type positive/total items
publication
Van Deun Survey Physiotherapists in Consensus definition Hobbelen et al. – – Positioning and soft 7/9
et al. nursing homes (n = 242) 2006 [47]. passive
(2018) [45] mobilization were
most applied.
Key points for
paratonia approach
were relaxation,

H. Drenth et al. / Paratonia in Dementia: A Systematic Review

positioning, active
movement
stimulation.
Van Deun Cross-sectional Healthy control (n = 60, Consensus definition Hobbelen et al. PAI passive movement of extremities – – 7/8
et al. age: mean 82.07 (5.53), 2006 [47]. (see above).
(2018) [39] male n = 30). Mild MyotonPro (handheld device
dementia (n = 31, age: objectively measuring muscle
mean 80.48 (4.87), properties).
male n = 15). Moderate
dementia (n = 31, age:
mean 87.81 (4.94),
male n = 3)
Van Deun CT with AB/BA n = 22, age: mean 84.8 Consensus definition Hobbelen et al. PAI passive movement of extremities – -Harmonic 6/9
et al. crossover (7.3), AD (n = 10), VaD 2006 [47]. (see above). movement
(2019) [44] (1), FTD (n = 1), other MAS-P. techniques.
(n = 10) MyotonPro (handheld device -Supporting
objectively measuring muscle tone). cushions
Vahia et al. Prevalence study n = 80, age: mean 75.5 External stimulus dependent increase Graded with the amount of passive Disorder of frontal – 4/9
(2007) [13] (7.0), male n = 17, AD in muscle tone that is absent at rest. force necessary to elicit stiffening. lobe origin.
Villeneuve Cross-sectional n = 155, Organic brain Primitive reflex. Gegenhalten, a Any resistance of the forearm to Central nervous – 5/8
et al. syndrome (including particular form of rigidity, also called passive movement from the examiner degeneration by age
(1974) [24] dementia) (n = 56), age: negativism or opposition hypertonia. is considered as a hypertonic and disease (frontal
mean 76 (7.2), male The marked increase in tone is not manifestation. lobe, metabolic,
n = 56, Functional consciously determined and is vascular cerebral,
psychoses (n = 51), age: accentuated when a rapid movement deep coma)
mean 70.9 (5.8), male is imparted to a limb. It is different
n = 33, Schizophrenia form spasticity (clasp-knife) and from
(n = 16), age: mean 76.3 cogwheel rigidity of Parkinsonism.
(8.8), male n = 0,
Healthy controls
(n = 32), age: mean 83.2
(4.9), male n = 11
AD, Alzheimer Disease; AGE, advanced glycation end-products; CVD, cardiovascular disease; FTD, frontotemporal dementia; LBD, Lewy body dementia; MAS-P, Modified Ashworth Scale for
paratonia severity; MCI, mild cognitive impairment; PAI, Paratonia Assessment Instrument; PDD, Parkinson’s disease dementia; RCT, randomized controlled trial; VaD, vascular dementia.
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1627

Fig. 2. Flowchart of selection process.

Nine studies were excluded because they used the studies were included in this systematic review (Fig. 2
UPDRS, and 34 studies were excluded because they and Table 2). For detailed information on the critical
did not meet the inclusion criteria. Additionally, two appraisal, see Supplementary Table 2.
studies [21, 22] were included on recommendation
by external experts and examination of those refer- Data extraction
ences yielded in two more studies [23, 24]. Thus, 35 The extracted data is summarized in Table 2.
1628 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

Study design One study [25] defined oppositional paratonia as

“a form of hypertonia in late stage dementia”. Two
The study designs included randomized controlled studies [11, 43] stated that paratonia can be divided
trials (RCTs) [25–29] (n = 5), cohort studies [14, into two separate entities: “facilitory paratonia”, in
30–32] (n = 4), cross-sectional studies [11, 21, 24, which the patient moves along with the examiner
33–39] (n = 10), studies on the psychometric prop- (keeping control of the movement, or inability to
erties of measurement instruments [40–43] (n = 4), relax), and “oppositional paratonia”, in which the
a clinical trial with crossover [44] (n = 1), a preva- subject appears to resist the passive movement of the
lence study [13] (n = 1), a survey [45] (n = 1), a case examiner.
series [46] (n = 1), a Delphi procedure [47] (n = 1), Five studies [12, 21, 23, 24, 47] distinguish Parkin-
and narrative review [12, 16, 22, 23,48–50] (n = 7). sonian rigidity from paratonia by noting that in
paratonia the resistance increases when the limb is
moved more rapidly and decreases or even disappears
Definition and clinical criteria of paratonia when the limb is moved more slowly. Furthermore,
Kurlan et al. [12] describes that the presence of
With the exception of one study [32], all studies “oppositional” paratonia suggests that the quality of
gave a definition of paratonia and/or described the rigidity is paratonic and that cogwheeling can occur
clinical criteria. with parkinsonian or paratonic rigidity and cannot
Two studies [22, 38] published a definition of para- be used to distinguish the two types of rigidity. Four
tonia based on the study by Kleist [9]; they defined studies [21, 23, 24, 47] state that paratonia is differ-
paratonia as “an increase in muscle tone which occurs ent form spasticity (clasp-knife) and from cogwheel
in response to passive movement, proportional in rigidity of Parkinsonism.
degree to the stimulus applied”. Vahia et al. [13] Risse et al. [31] further specified that “paratonia is
extended this definition to include that an “external resistance to movement with increased muscle tone
stimulus-dependent increase in muscle tone is absent throughout the range of motion while not on antipsy-
at rest”. chotic drugs”. Souren et al. [16] noted that “paratonia
Two publications [29, 37] reported that dopamin- occurs on contact and can be elicited or augmented
ergic nigrostriatal dysfunction was present in PD; the by a state of anxiety, anger and agitation”.
authors further hypothesized that dementia-related One study [50] described paratonia as “a cata-
rigidity was an “extrapyramidal sign”. tonia like sign and a motor abnormality of severe
In seven studies [21, 23, 24, 33, 34, 36, 48], the mental disorder”. Catatonia is a neuropsychiatric psy-
presence of paratonia was described as paratonic chomotor syndrome characterized not only by a broad
rigidity (Gegenhalten) associated with the appear- range of movement disorders but also by affectiv-
ance of other primitive reflexes, such as snout, suck, ity disturbance and complex behaviors, including the
palmomental, grasp and glabellar reflexes, which disturbance of will. Paratonia is usually suggested to
are normally present in infancy and disappear as occur with other catatonic symptoms, such as auto-
the nervous system matures. Two studies [23, 24] matic obedience, motor perseveration, echopraxia
emphasized that this perceived increase in tone is and primitive reflexes.
not consciously determined by the patient. Franssen Thirteen studies [14, 26, 45, 47, 49, 27, 28, 30,
et al. [35] also described paratonic rigidity (Gegen- 39–42, 44] included the consensus definition of para-
halten) as a primitive reflex and further defined it as tonia that was proposed by Hobbelen et al. [47] in
“the stiffening of a limb in response to contact with 2006. This definition was derived using a Delphi pro-
the examiner’s hand and an involuntary resistance to cess with 8 international experts.
passive changes in position and posture”. Another The Delphi panel agreed on the following defini-
study [46] defined paratonia as “a sudden increase in tion of Paratonia:
muscle tone of an extremity in reaction to an external
perturbation of that extremity, resulting in an involun- “a form of hypertonia with an involuntary vari-
tary resistance”. The flexed posture with contractures able resistance during passive movement. The
of the extremities, which is seen in the last stage of nature of paratonia may change with progression
dementia is described by Paulson and Gottlieb [23] as of the dementing illness (e.g., active assistance)
a related phenomenon to paratonic rigidity, occurring is more common early in the course of degener-
over time after an initial phase of Gegenhalten. ative dementias, whilst active resistance is more
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1629

common later in the course of the disease). The and extension, independent of the starting position
degree of resistance varies depending on the of the joints, and a rapid movement must show an
speed of movement (e.g., a low resistance to slow increase of tone and a slow movement a decrease.
movement and a high resistance to fast move- One study [28] described paratonia when there was an
ment). The degree of paratonia is proportional to altered neck position (cervical antero position, exten-
the amount of force applied. Paratonia increases sion or kyphosis) in patients with severe dementia.
with progression of dementia. Furthermore, the The psychometric properties were not reported for
resistance to passive movement is in any direction the abovementioned described procedures.
and there is no clasp-knife phenomenon” [47]. Ten studies [14, 26, 30, 39–42, 44, 49, 54] used
the validated Paratonia Assessment Instrument (PAI),
With this operational definition of paratonia, the based on the consensus definition of Hobbelen et al.
distinction between paratonia, spasticity and Parkin- in 2006 [47]. With this assessment instrument, an
sonian rigidity is possible. The distinction between examiner can establish the presence (or absence) of
(oppositional) paratonia and stroke-spasticity is paratonia by successively moving all four limbs pas-
based upon two factors; 1) the absence of a catch/ sively in flexion and extension while the participant
clasp-knife response and 2) that resistance to move- is in a sitting position (Fig. 3) or supine in bed. The
ment in paratonia can be in any direction in contrast PAI is a tool to confirm the presence of paratonia and
to a hemiplegic unilateral, focal, upper motor neu- distinguish it from other forms of increased tone, but
ron pattern resistance in stroke spasticity [51]. The it has not been validated to determine whether it cap-
distinction between (oppositional) paratonia and tures change over time or grades the magnitude of the
Parkinsonian rigidity is based upon the velocity severity of paratonia. The PAI has only expert valid-
dependency of paratonia. In Parkinsonian rigidity the ity and face validity. In a three-stage study examining
resistance is not dependent on the speed of the move- 87, 97, and 24 participants with an established form
ment (lead pipe phenomenon) [52]. of dementia, interobserver reliability as measured by
Cohen’s kappa ranged from 0.63 to 1.
Diagnosis of paratonia Facilitory paratonia can be diagnosed with the
paratonia scale, which establishes the subjective
We identified 25 studies [11, 13, 29, 30, 33–36, 38– impressions of both assistance and resistance offered
41, 14,42–44, 46, 49, 16, 21, 24–28] that described to passive flexion and extension about the elbow [11,
the process of diagnosing a patient with paratonia. 43]. Facilitory paratonia can also be diagnosed with
The subjective impression of resistance (oppositional the modified Kral procedure as described by Bevers-
paratonia) to sudden, irregular passive changes in dorf and Heilman [11].
position and/or speed in the extension and flexion Marinelli et al. [43] validated a quantitative me-
of arms and legs was described in 7 studies [16, 21, thod to assess and visualize facilitory and opposi-
24, 34–36, 46]. Three studies [23, 24, 38] expanded tional paratonia in elbow flexor and extensor muscles
this description with that resistance occurs in the using surface electromyography (EMG) and metro-
absence of cogwheeling or a spastic catch. Tyrrell and nome-controlled passive movements. In a group of
Rossor [38] supplemented this with that the resistance outpatients with cognitive impairment (n = 10), the
is not exacerbated by movement in the contralat- researchers found that facilitory paratonia was more
eral fist. Three studies [21, 33, 38] describe the prevalent than oppositional paratonia and had a
limb placement maneuver, whereby the examiner higher amplitude in elbow flexors than in extensors.
passively lifts the patient’s arm with the instruction Both facilitory and oppositional paratonia increased
to relax. When the arm remains elevated or shows over time during continuous passive flexion and
any delay in dropping, this indicates paratonia. Vahia extension elbow movements, differently from discon-
et al. [13] indicated paratonia to be the amount of tinuous movements, underlining the role of move-
passive force necessary to elicit stiffening. The mod- ment repetition in increasing paratonia. Information
ified Columbia rating scale for rigidity to identify on the psychometric properties is absent in the men-
rigidity in patients with dementia was used by Duret tioned procedures.
et al. [29]. In 2003, Hobbelen et al. [25] used spe- Two studies [40, 41] investigated a device called
cific criteria [53] for diagnosing paratonia; during the MyotonPro to objectively assess the presence
passive movement of the extremities, trunk and head and severity of paratonia. The MyotonPro is a small
an increase in muscle tone must occur at flexion handheld device that measures mechanical muscle
1630 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

Fig. 3. The PAI procedure: The examiner starts with a slow movement of the limb, after which the movement is accelerated. A construct
of five criteria allows a categorical diagnosis of paratonia, i.e., paratonia can only be diagnosed when all five criteria are present; 1) an
involuntary variable resistance; 2) a degree of resistance that varies depending on the speed of the movement (e.g., a low resistance to slow
movements and a high resistance to fast movement; 3) resistance to passive movement can be felt in any direction (no distinct pattern);
4) no clasp-knife phenomenon; and 5) resistance is present in 2 movement directions in 1 limb or in 2 different limbs. With permission
from Cambridge University Press reprinted from; Diagnosing paratonia in the demented elderly: reliability and validity of the Paratonia
Assessment Instrument (PAI) [42].

properties and can differentiate between muscle tone resistance during passive movement and rated on a
and biomechanical properties (stiffness, elasticity, 5-point scale ranging from 0 to 4, (0 = no resistance
and viscoelasticity). Van Deun et al. [41] reported to passive movement, 1 = slight resistance, 2 = more
low-to-high interrater reliability (ICC: 0.43–0.73), marked resistance, 3 = considerable resistance, and
moderate-to-high between-series intrarater reliabil- 4 = severe resistance) [55].
ity (ICC: 0.57–0.86), and poor-to-moderate intrarater The severity of paratonia can also be assessed by
reliability and agreement (ICC = 0.23–0.47) in a the MyotonPro device [40, 41]. The MyotonPro is
group of patients with paratonia (n = 16). Validity, able to record changes over time in patients with
reliability and responsiveness were studied by Drenth paratonia, and the minimal detectable change (MDC)
et al. [40] in a cohort of people with dementia and minimal detectable important change (MDIC)
(with paratonia n = 70, without n = 82). In the total were calculated (Supplementary Table 3) [40]. The
population of their study, they found evidence that MDIC was established with an anchor-based method
MyotonPro is able to differentiate between people in which longitudinal changes in the MyotonPRO
with and without paratonia (area under the curve outcomes after six months were related to an external
ranging from 0.60 to 0.67), with sensitivity esti- criterion for important change (the “anchor”), and the
mates ranging from 70%–60%, specificity estimates worsening of movement opposition during activities
ranging from 54%–61% and moderate to high inter- of daily living (ADL) was measured with the Clinical
and intrarater reliability (ICC: 0.57–0.75 and ICC: Global Impression (CGI) of change scale. Because
0.54–0.71, respectively). the MDC values surpassed the MCID, the ability to
detect small relevant changes in this population is
Assessment of paratonia severity complicated [40].

Beversdorf an Heilman [11] published the first Pathogenesis

semiquantitative paratonia rating scale, thus enabling
researchers to rate oppositional or facilitory parato- Central nervous system (CNS)
nia. In 1999, a modified Ashworth scale (MAS-P) Five studies [14, 22, 27, 35, 48] suggested that
was validated and found to be reliable for assessing the pathogenesis of paratonia is related to damage to
the severity of oppositional paratonia (intrarater reli- cortical and subcortical motor structures. Impaired
ability, Kendall’s Tb 0.62–0.80; interrater reliability, response inhibition associated with frontal lobe
Kendall’s Tb 0.72–0.77) [55]. Six studies [25, 26, 30, lesions was suggested in 10 studies [11, 13, 21, 23,
40, 41, 44] used the MAS-P to assess the severity of 24, 32, 33, 36, 43, 46]. One study [16] hypothesized
paratonia (after being identified with the PAI). With that paratonia may be a re-manifestation of an infan-
the MAS-P, muscle tone is assessed by the perceived tile stabilization reflex mechanism. In these studies,
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1631

however, these possible pathways were only briefly Interventions

mentioned, and no scientific data that described
the relationship between paratonia and changes in Five studies [25–28, 44] addressed therapeutic
specific brain areas were presented. Although the interventions to treat paratonia.
involvement of the basal ganglia and possibly the Hobbelen et al. [25] performed a pilot study of
substantia nigra in the pathogenesis of paratonia was 15 nursing home residents with dementia and para-
mentioned in 4 studies [29, 31, 36, 37], there was no tonia to investigate the effects of stabilizing cushions
evidence that dopaminergic nigrostriatal dysfunction and passive movement therapy (PMT). Subjects were
is a mechanism for the pathophysiologic substrate of randomized to one of three groups: group 1 received
paratonia. PMT 3 times a week, group 2 used stabilizing cush-
ions only, and group 3 was a control group receiving
standard care. The results showed a modest short-
Peripheral biomechanical changes term (15 minutes after one treatment) benefit of
Peripheral biomechanical changes induced by cushions in the arms and positive short-term effects
advanced glycation end-products (AGEs) contribut- of PMT. However, the long-term effects (after three
ing to the etiology of paratonia were described in 2 weeks) were positive only in the control group. This
studies [14, 30]. AGEs are mediated by the nonenzy- pilot study provided the groundwork for a larger
matic condensation of a reducing sugar with proteins multicenter randomized clinical trial of PMT [26]
(especially collagen tissue) and are spontaneously in which 101 nursing home residents with demen-
produced in human tissues which increases with tia and moderate-to-severe paratonia were randomly
aging [56]. In many age-related diseases, the accu- assigned to either a PMT group or a control group.
mulation of AGEs is a significant contributing factor The PMT group received PMT 3 times a week over
in degenerative processes, especially in cardiovascu- 4 weeks. The main outcomes were the severity of
lar diseases, diabetes mellitus (DM), and Alzheimer’s paratonia as measured by the MAS-P and caregiver
disease (AD) [56, 57]. burden as measured by the modified patient-specific
Hobbelen et al. [14] hypothesized that AGEs complaint score list. The study showed that PMT
could be involved in the development of paratonia increased the severity of paratonia and did not reduce
by the formation of cross-links in muscle colla- caregiver burden.
gen due to DM, resulting in tissue stiffness. In a Bautmans et al. [28] used a randomized controlled
one-year follow-up study in people with early, mod- crossover design to study gentle cervical spine mobi-
erate and severe dementia (n = 174), they found that lization in elderly nursing home residents with altered
after adjusting for several known confounders people neck posture (cervical antero-position, extension, or
with dementia and DM (n = 39) had a significantly kyphosis) due to paratonia and known dysphagia
higher risk (OR = 10.7; 95% CI: 2.2–51.7) of devel- (n = 15). Patients were randomized into 2 groups:
oping paratonia than people those with dementia but group one started with one week of cervical spine
without DM. mobilization, followed by one-week of wash-out and
Drenth et al. [30] published a one-year longitudi- one week of control treatment (i.e., socializing vis-
nal study examining the relationship between AGEs its). The other group started with one week of control
and paratonia in people with early-stage dementia treatment, followed by one-week of wash-out and one
(n = 118). After adjusting for several known con- week of cervical spine mobilization. The primary out-
founders, they found that AGE levels were associated come measures were feasibility (attendance, hostility
with the presence (OR = 3.47, 95% CI: 1.87–6.44, to therapy, and complications) and dysphagia limit
p < 0.001) and severity (␤=0.17, 95% CI: 0.11 –0.23, (maximal volume of water that can be swallowed
p < 0.001) of paratonia. The authors hypothesized that in a single movement (0–20 ml)). The results show
AGE-induced impaired skeletal muscle function, due that gentle cervical spine mobilization was feasible
to collagen cross-linking and intramuscular inflam- and improved swallowing capacity after one session
mation, causes perceived resistance during passive (p = 0.01) and after one week of treatment (p = 0.03).
movement in early-stage paratonia; these findings Kleiner-Fishman et al. [27] used a blinded, ran-
indicate that these peripheral biomechanical changes domized, placebo-controlled crossover design to
play a role in initiating movement stiffness in the early study the application of botulinum toxin in patients
stages, whereas CNS pathology accelerates paratonia with advanced cognitive impairment and paratonia
as dementia progresses. (n = 10). Patients were randomized to one of two
1632 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

treatment cycle protocols: active drug then placebo the authors proposed the use of behavioral interven-
vs placebo followed by active drug. Each treatment tions intended to reduce anxiety and agitation, such
cycle lasted for 16 weeks to allow for the complete as gentle movements, eye contact and soothing voice,
washout of toxin. Patients received up to 300 units of and physical activity to prevent or delay contrac-
incobotulinumtoxin A in the upper extremities. The tures. Ries [49] suggested the use of counterpressure
primary outcome measure was the modified Carer movements as an additional strategy to reduce para-
Burden Scale and the secondary outcome measure tonia. Drenth et al. [30] postulated that AGE-induced
was joint passive range of motion (PROM) as mea- impairments in muscle function contributed to para-
sured by a goniometer. The results demonstrated that tonia. Thus, they hypothesized that interventions to
botulinum toxin was safe and efficacious in reducing decrease AGE formation and accumulation could
caregiver burden (p = 0.02) and increasing the PROM be viable for preventing and reducing paratonia;
around different joints (p = 0.02 to < 0.001). such interventions could be achieved by optimizing
Van Deun et al. [44] used a crossover design to glycemic control through physical activity and diet.
study the short-term effects of supporting cushions
(SC) and harmonic techniques (HT) in nursing home
residents with moderate-to-severe paratonia (n = 22). DISCUSSION
The primary outcome measure was muscle tone as
measured by the MyotonPro. The other outcome General
measures were elbow and knee PROM, which were
measured by a goniometer, and pain, which was mea- This systematic review indicates that there has
sured by a validated instrument to assess pain in been promising research activity and progress in
nonverbal people with dementia (the PACSLAC-D) the field of paratonia. Although the literature search
and by the visual analog scale (VAS) to assess the yielded only 35 articles from the last 64 years (the
comfort of the respondent. The HT intervention con- oldest article was from 1956), 13 studies were from
sisted of pulsating/oscillating movements applied to the last 10 years and were written by 4 different
the upper limbs, lower limbs, and trunk. To max- research groups (Italy, Canada, Belgium, and the
imize the harmonic oscillating effect of the HT, Netherlands). It is unclear why there appears to be a
balloons were placed under the limbs of the par- lack of scientific interest in paratonia despite the fact
ticipant to provide additional movement resonance. that paratonia has a devastating effect on the quality
The results demonstrated short-term improvement in of life of people with late stage dementia. We hypoth-
PROM after both SC and HT interventions (p = 0.028 esize that in the four countries in which research on
to p < 0.001) and decreased upper limb muscle tone paratonia has been performed in the last decade, there
after the SC intervention (p = 0.028). However, upper is greater intersection between geriatric care and sci-
limb muscle tone increased after the HT interven- entific research with infrastructure in place making it
tion (p = 0.032). Improvements in pain (p = 0.003) more feasible to perform studies in this population.
and caregiver-reported VAS (p = 0.001 to p = 0.019) Further, scientific research in the field of dementia is
were observed after the HT intervention. often focused on pre-clinical or early stage disease
Four other studies [16, 30, 45, 49] outlined current where paratonia is absent or mild. There has been
practices to address paratonia or examined poten- limited focus on late stage disease targeting palliative
tial beneficial interventions. A survey among Belgian approaches to reduce suffering and enhance quality
long-term care (LTC) facilities assessed the cur- of life.
rent standard of care for paratonia in late-stage We excluded 9 articles that used the UPDRS to
dementia [45]. It highlighted that the most com- diagnose rigidity or paratonia in people with demen-
mon interventions being utilized in Belgian LTC tia. It is important to highlight this, as diagnosing
facilities included stabilizing cushions, multisensory paratonia in dementia with an instrument that is devel-
stimulation (snoezelen), pulsation/rocking, active oped to assess the motor aspects of PD may mislead
physical activity, active and passive mobilization clinicians to diagnose parkinsonism and to use inter-
techniques (PMTs), stretching, casting, heat applica- ventions that target PD rather than paratonic rigidity;
tion, massage and relaxation baths. Souren et al. [16] these diseases have different underlying etiologies
hypothesized that paratonia served as a physiologic and therapies. The UPDRS should not be used for
and psychological stabilizing mechanism that pro- people with dementia other than people with Lewy
tected against overwhelming external stimuli. Thus, body dementia or PD dementia.
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1633

Definition, diagnosis, and assessment of severity paratonia to differentiate facilitory from opposi-
tional paratonia [43]. Surface electromyography is
Most recent studies in this review used the consen- the most appropriate way of demonstrating muscle
sus definition of paratonia that was proposed in 2006. activation, as it provides optimal temporal resolu-
This working definition led to additional research, tion, the possibility to distinguish among muscle
including the creation of the PAI, which is a standard- groups and the agonist-antagonist interplay. In a
ized, validated method to clinically identify paratonia pilot study, [43] demonstrated that paratonic activity
and differentiate it from other forms of increased can be quantitatively measured and that its opposi-
muscle tone, such as parkinsonian rigidity and spas- tional and facilitory features can be distinguished.
ticity [42]. Quantitative analysis confirmed that paratonia is a
One study [50] described paratonia as a catatonia- velocity-dependent phenomenon and that it increases
like symptom. Cognitive factors that affect muscle following movement repetition, which is the underly-
tone when a catatonic posture is assumed (i.e., per- ing premise of the PAI [42]. Interestingly, paratonia is
severation of limb placement) are mentioned in the the only known condition in which movement repeti-
literature, but are differentiated from paratonia [21, tion induces an increase in muscle activation. In fact,
22]. Muscle tone in catatonia requires further char- in spasticity, repetitive muscle stretching induces a
acterization as it is difficult to determine whether the gradual reduction in muscle reflex activation, while in
alteration of muscle tone occurs only during passive parkinsonian rigidity, the activity remains the same.
movements, or whether it persists when the exam- The contrast between paratonia and these other forms
iner is no longer manipulating the limb. For example, of hypertonia can be used to clearly distinguish oppo-
“waxy flexibility” is found when the patient main- sitional paratonia from spasticity and parkinsonian
tains a posture imposed by the examiner, which is not rigidity.
considered a feature of paratonia. Further research is
necessary to determine whether the limb placement
maneuver detects paratonia or detects a catatonic Pathogenesis
posture.
Studies of the MyotonPro indicated that this device Although a CNS-based etiology of paratonia seems
can be used to objectively quantify paratonia severity. likely in severe paratonia, additional research on the
However, because of the inherent variability in move- relation between the development of paratonia and
ment resistance in paratonia, the authors suggested AGEs indicates that a peripheral biomechanical com-
that the outcomes from the MyotonPRO should be ponent cannot be ruled out. It can be hypothesized that
interpreted with care [40, 41]. The promising results several central and peripheral pathways take place
of the MyotonPRO studies provide optimism for fur- simultaneously and reinforce or interact with each
ther study. It is conceivable that the MyotonPro could other. It is currently assumed that facilitory parato-
be used in the clinical diagnosis of paratonia. The nia is the first stage of paratonia and that at some
MyotonPro may be used as an alternative for the sub- stage, a transition into oppositional paratonia occurs.
jective MAS-P; however, future studies should focus However, it is not known whether facilitory and
on additional guidelines for MyotonPro measure- oppositional paratonia are two aspects of the same
ments, such as multiple measurements. This could phenomenon or even if the two types of paratonia
possibly allow for adjustment for diurnal variation in share the same neural mechanisms.
paratonia and increase the clinical interpretation and There may be several risk factors for parato-
improve reproducibility [40]. nia: The longitudinal study of Hobbelen et al. [14],
Until objective measuring instruments are avail- demonstrated that in 51 participants that developed
able to measure the presence and severity of para- paratonia, those with Vascular Dementia had the
tonia, it is recommended that, subsequent studies highest Hazard Ratio (3.1). The severity of cognitive
on clinal correlations, causes and consequences of decline and the presence of DM were statistically sig-
paratonia, should include multiple outcome measures nificant risk factors for developing paratonia. Drenth
such as motor function, ADL, pain, behavior, and et al. [30] showed that the level of AGE accumulation
diurnal variation of paratonia. is also a risk factor for developing paratonia.
One possible objective strategy for the diagnosis An increase in tissue stiffness due to AGE cross-
and quantification of paratonia involves record- linking is associated with a loss of viscoelasticity;
ing electromyographic muscle activation related to the tissue becomes stiffer, and after contraction, the
1634 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

muscle may not return to its original baseline tone. A Intervention

decrease in elasticity suggests that the tissue becomes
weak and that is has difficulty returning to its original An important practical question for managing peo-
form after deformation. If we assume that a smaller ple with paratonia in daily clinical practice is “what
dissipation of mechanical energy (which was regis- are effective interventions to reduce muscle tone in
tered in the MyotonPro studies) is associated with a order to decrease caregiver burden, reduce or delay
higher elasticity in the tissue, it is plausible that when contractures, and improve quality of life?”
tissue stiffness and intrinsic tension increase due to Our findings are very limited:
AGE crosslinking, the mechanical energy increases
(similar to a tightly tensioned spring), as in passive 1. In severe paratonia: One pilot study [25] (n = 5)
movement. It remains unclear in what way AGEs showed a positive effect of stabilizing cushions
cause motor decline in early-stage dementia. on muscle tone, and one study [44] (n = 22)
In patients suffering from paratonia, hypertonia showed a positive effect of harmonic techniques
and active opposition during ADL can vary and on range of motion. Both studies had important
may fluctuate. Although factors such as aggression, methodological shortcomings. One study [28]
agitation, anxiety, pain, confusion and sudden exter- showed promising results with the use of cer-
nal stimuli (e.g., light, sound) have been reported vical spine mobilization to improve swallowing
to potentially influence the severity of paratonia in capacity, but the sample size for this study was
observational studies [13, 16], further research is nec- also small (n = 15); therefore, it is not possi-
essary to investigate the exact relationship of these ble to make definitive recommendations at this
factors and their impact on paratonia. In addition time until methodologically rigorous studies are
to memory loss, other cortical functions decline in conducted.
dementia, including impaired sensory input [58]. This 2. In moderate paratonia, promising results were
could elicit primitive fight/flight responses, which shown in a randomized placebo-controlled pilot
include increased muscle tone. It has been hypoth- using botulinum toxin to reduce involuntary
esized that in people with dementia, the loss of postures due to paratonia [27]. This method
the sense of proprioception is compensated for by has the potential to be a significant palliative
extreme joint positions and an increase in muscular treatment for reducing complications due to
tension to gain additional tactile sensory information paratonia, including contractures and pressure
[59]. Although aging is generally associated with a ulcers if the results of the pilot trial can be repro-
decline in the sense of proprioception [60], no studies duced in large-scale trials that are in progress
have been published addressing the impact of demen- (personal communication).
tia on proprioception. 3. No research has been published regarding how
Another putative theory to explore regarding the to prevent paratonia. Intensive glycemic con-
origin of paratonia is the age-associated increase trol and reducing oxidative stress by nutrition
in the coactivation of antagonist muscles. Some and physical activity may be key methods for
studies have demonstrated that aging results in the decreasing AGE formation [62] and potentially
heightened activation of antagonist muscles during prevent paratonia. Physical inactivity has been
voluntary movements [61]. The activation of agonist found to be associated with high AGE levels in
and antagonist muscle pairs is postulated to be orga- older people [63]. The mechanism of how exer-
nized around a dual system of cortically and spinally cises modulate the development of AGEs, para-
mediated reciprocal inhibition that is affected by age. tonia is an important research avenue to pursue.
It could be hypothesized that reciprocal inhibition is
also modified or augmented with increasing cognitive Strength and limitations
impairment as dementia progresses. This could be an
explanation for the perceived resistance to movement, A limitation of this study is that we only found
especially when considering the inability to relax. To 35 studies. The wide variety of different types of
our knowledge, however, the only study using EMG research into paratonia prevented us from pooling the
recordings in paratonia [43] did not reveal the coac- data and performing a meta-analysis. Further, much
tivation of agonist and antagonist muscles. Further of the data available were of low quality, and there
neurophysiological studies could shed light on the were very few randomized placebo-controlled tri-
role of cortical and spinal circuitry. als. On the other hand, we performed an extensive
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1635

literature search using all possible search terms ACKNOWLEDGMENTS

to identify studies of paratonia, and we found
1,577 studies. We also diligently adhered to the This work, performed by the International Joint
PRISMA guidelines in performing this review to Research Group ‘Move in Age’ was supported by
avoid potential biases. The fact that so few studies regular funds of the Research Group Healthy Age-
with varying designs were eligible for our review ing, Allied Healthcare and Nursing, Hanze University
indicates that there is still little research on parato- Groningen, the Department of General Practice and
nia. This study indicates that high-quality research is Elderly Care Medicine, University Medical Center
urgently needed to allow for definitive conclusions Groningen, the Frailty in Ageing Research Group and
regarding the pathophysiology of paratonia and to Gerontology Department, Vrije Universiteit Brussels
develop possible preventive and therapeutic interven- and ZuidOostZorg, Organisation for Elderly Care,
tions to alleviate the effects of paratonia. Drachten.
This comprehensive review highlights the fact that Authors’ disclosures available online (https://
paratonia is poorly recognized and health profes- www.j-alz.com/manuscript-disclosures/20-0691r1).
sionals lack clear guidance as to management. In
future, creating a practical and operational decision
tree in the management of paratonia might be help- SUPPLEMENTARY MATERIAL
ful for help professionals to refer to; in the interim
the PAI as part of the general assessment in people The supplementary material is available in the
with dementia should be encouraged for use in rec- electronic version of this article: https://dx.doi.org/
ognizing paratonia as it is a valid and reliable tool to 10.3233/JAD-200691.
differentiate paratonia from Parkinson’s rigidity and
spasticity [42].
REFERENCES
Future directions of research
[1] American Psychiatric Association (2013) Diagnostic and
We propose a paratonia research agenda compris- statistical manual of mental disorders (DSM-5), Washing-
ton, DC.
ing 3 main topics: 1) Delineation of the pathogenesis [2] Scarmeas N, Hadjigeorgiou GM, Papadimitriou A, Dubois
of paratonia; 2) Validation and refinement of instru- B, Sarazin M, Brandt J, Albert M, Marder K, Bell K, Honig
ments and techniques to capture and measure the LS, Wegesin D, Stern Y (2004) Motor signs during the
course of Alzheimer disease. Neurology 63, 975-982.
severity of paratonia that can detect changes due to
[3] Dumurgier J, Artaud F, Touraine C, Rouaud O, Tavernier
trial interventions; and 3) Methodologically rigorous B, Dufouil C, Singh-Manoux A, Tzourio C, Elbaz A
clinical trials of therapeutics. (2017) Gait speed and decline in gait speed as predictors
Research on paratonia needs to bridge several of incident dementia. J Gerontol A Biol Sci Med Sci 72,
655-661.
research questions, areas, techniques and disciplines. [4] Buracchio T, Dodge HH, Howieson D, Wasserman D, Kaye
To improve the quality of life of people with demen- J (2010) The trajectory of gait speed preceding mild cogni-
tia, intensive collaboration between different fields of tive impairment. Arch Neurol 67, 980-986.
research is imperative. [5] Mc Ardle R, Morris R, Wilson J, Galna B, Thomas AJ,
Rochester L (2017) What can quantitative gait analysis tell
us about dementia and its subtypes? A structured review. J
Conclusion Alzheimers Dis 60, 1295-1312.
[6] Kueper JK, Speechley M, Lingum NR, Montero-Odasso M
This systematic review of the literature on parato- (2017) Motor function and incident dementia: A systematic
review and meta-analysis. Age Ageing 46, 729-738.
nia outlines what is currently known about paratonia [7] Friedlander LH (1828) Arznygelahrtheit. Allg Lit Zeiting,
with respect to defining, detecting, and treating it. pp. 257-258.
There was also preliminary research to suggest the [8] Dupré E (1910) Débilité mentale et débilité motrice
underlying mechanisms of paratonia. Although para- associées. Rev Neurol (Paris) 20, 54-56.
[9] Kleist K (1927) Gegenhalten (motorischer Negativismus)
tonia has obvious devastating impacts on health and Zwanga greifen und Thalamus Opticus. Monatschr Psychiat
quality of life, the amount of research to date has been Neurol 65, 317.
limited. However, in the last decade, there appears [10] Kral VA (1949) Ueber eine iterative bewegunsstörung bei
stirnhirnläsionen. Monatsschr Psychiatr Neurol 118, 257-
to have been increased research on paratonia, which
272.
hopefully will increase the momentum to further [11] Beversdorf DQ, Heilman KM (1998) Facilitory paratonia
advance the field. and frontal lobe functioning. Neurology 51, 968-971.
1636 H. Drenth et al. / Paratonia in Dementia: A Systematic Review

[12] Kurlan R, Richard IH, Papka M, Marshall F (2000) Move- paratonia in early stage Alzheimer disease. J Am Med Dir
ment disorders in Alzheimer’s disease: More rigidity of Assoc 18, 636.e7-636.e12.
definitions is needed. Mov Disord 15, 24-29. [31] Risse SC, Lampe TH, Bird TD, Nochlin D, Sumi SM,
[13] Vahia I, Cohen CI, Prehogan A, Memon Z (2007) Prevalence Keenan T, Cubberley L, Peskind E, Raskind MA (1990)
and impact of paratonia in Alzheimer disease in a multiracial Myoclonus, seizures, and paratonia in Alzheimer disease.
sample. Am J Geriatr Psychiatry 15, 351-353. Alzheimer Dis Assoc Disord 4, 217-225.
[14] Hobbelen JHSM, Tan FE, Verhey FR, Koopmans RT, de [32] Bennett HP, Corbett AJ, Gaden S, Grayson DA, Kril JJ,
Bie RA (2011) Prevalence, incidence and risk factors of Broe GA (2002) Subcortical vascular disease and functional
paratonia in patients with dementia: A one-year follow-up decline: A 6-year predictor study. J Am Geriatr Soc 50,
study. Int Psychogeriatr 23, 1051-1060. 1969-1977.
[15] Gilhooly KJ, Gilhooly MLM, Sullivan MP, McIntyre A, [33] Benassi G, D’Alessandro R, Gallassi R, Morreale A,
Wilson L, Harding E, Woodbridge R, Crutch S (2016) A Lugaresi E (1990) Neurological examination in subjects
meta-review of stress, coping and interventions in dementia over 65 years: An epidemiological survey. Neuroepidemi-
and dementia caregiving. BMC Geriatr 16, 106. ology 9, 27-38.
[16] Souren LE, Franssen EH, Reisberg B (1997) Neuromotor [34] Damasceno A, Delicio AM, Mazo DFC, Zullo JFD, Scherer
changes in Alzheimer’s disease: Implications for patient P, Ng RTY, Damasceno BP (2005) Primitive reflexes and
care. J Geriatr Psychiatry Neurol 10, 93-98. cognitive function. Arq Neuropsiquiatr 63, 577-582.
[17] Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Pet- [35] Franssen EH, Reisberg B, Kluger A, Sinaiko E, Boja C
ticrew M, Shekelle P, Stewart LA (2015) Preferred reporting (1991) Cognition-independent neurologic symptoms in nor-
items for systematic review and meta-analysis protocols mal aging and probable Alzheimer’s disease. Arch Neurol
(PRISMA-P) 2015: Elaboration and explanation. BMJ 350, 48, 148-154.
g7647. [36] O’Keeffe ST, Kazeem H, Philpott RM, Playfer JR, Gosney
[18] Schardt C, Adams MB, Owens T, Keitz S, Fontelo P (2007) M, Lye M (1996) Gait disturbance in Alzheimer’s disease:
Utilization of the PICO framework to improve searching A clinical study. Age Ageing 25, 313-316.
PubMed for clinical questions. BMC Med Inform Decis Mak [37] Tyrrell PJ, Sawle G V, Ibanez V, Bloomfield PM, Leen-
7, 16. ders KL, Frackowiak RS, Rossor MN (1990) Clinical and
[19] Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A positron emission tomographic studies in the “extrapyra-
(2016) Rayyan—a web and mobile app for systematic midal syndrome” of dementia of the Alzheimer type. Arch
reviews. Syst Rev 5, 210. Neurol 47, 1318-1323.
[20] Joanna Briggs Institute, Critical Appraisal Tools. [38] Tyrrell P, Rossor M (1988) The association of gegenhal-
https://joannabriggs.org/critical-appraisal-tools ten in the upper limbs with dyspraxia. J Neurol Neurosurg
[21] Jenkyn LR, Walsh DB, Culver CM, Reeves AG (1977) Clini- Psychiatry 51, 995-997.
cal signs in diffuse cerebral dysfunction. J Neurol Neurosurg [39] Van Deun B, Van Den Noortgate N, Van Bladel A, Palmans
Psychiatry 40, 956-966. T, Cambier D (2019) The impact of paratonia on fine and
[22] Critchley M (1956) Neurologic changes in the aged. J gross motor function in older adults with mild and moderate
Chronic Dis 3, 459-477. dementia. Alzheimer Dis Assoc Disord 33, 54-61.
[23] Paulson G GG (1968) Developmental reflexes: The reap- [40] Drenth H, Zuidema SU, Krijnen WP, Bautmans I, van der
pearance of foetal and neonatal reflexes in aged patients. Schans C, Hobbelen H (2018) Psychometric properties of
Brain 91, 37-52. the MyotonPRO in dementia patients with paratonia. Geron-
[24] Villeneuve A, Turcotte J, Bouchard M, Côté JM, Jus tology 64, 401-412.
A (1974) Release phenomena and iterative activities in [41] Van Deun B, Hobbelen JSM, Cagnie B, Van Eetvelde B, Van
psychiatric geriatric patients. Can Med Assoc J 110, Den Noortgate N, Cambier D (2018) Reproducible mea-
147-153. surements of muscle characteristics using the MyotonPRO
[25] Hobbelen JHSM, de Bie RA, van Rossum E (2003) Het device: Comparison between individuals with and without
effect van passief bewegen op de mate van paratonie. Een paratonia. J Geriatr Phys Ther 41, 194-203.
partieel geblindeerde gerandomiseerde klinische trials. Ned [42] Hobbelen JSM, Koopmans RTCM, Verhey FRJ, Habraken
Tijdschr Fysiother 6, 132-137. KM, de Bie RA (2008) Diagnosing paratonia in the
[26] Hobbelen JHSM, Tan FES, Verhey FRJ, Koopmans RTCM, demented elderly: Reliability and validity of the Parato-
de Bie RA (2012) Passive movement therapy in severe nia Assessment Instrument (PAI). Int Psychogeriatr 20,
paratonia: A multicenter randomized clinical trial. Int Psy- 840-852.
chogeriatr 24, 834-844. [43] Marinelli L, Mori L, Pardini M, Beversdorf D, Cocito
[27] Kleiner-Fisman G, Khoo E, Moncrieffe N, Forbell T, Gryfe L, Curra A, Fattapposta F, Ghilardi MF, Abbruzzese G,
P, Fisman D (2014) A randomized, placebo controlled pilot Trompetto C (2017) Electromyographic assessment of para-
trial of botulinum toxin for paratonic rigidity in people with tonia. Exp Brain Res 235, 949-956.
advanced cognitive impairment. PLoS One 9, e114733. [44] Van Deun B, Van Den Noortgate N, Van Bladel A, De
[28] Bautmans I, Demarteau J, Cruts B, Lemper J-C, Mets T Weerdt K, Cambier D (2019) Managing paratonia in persons
(2008) Dysphagia in elderly nursing home residents with with dementia: Short-term effects of supporting cushions
severe cognitive impairment can be attenuated by cervical and harmonic techniques. J Am Med Dir Assoc 20, 1521-
spine mobilization. J Rehabil Med 40, 755-760. 1528.
[29] Duret M, Goldman S, Messina D, Hildebrand J (1989) Effect [45] Van Deun B, Van den Noortgate N, Cinthia S, Van Bladel A,
of L-dopa on dementia-related rigidity. Acta Neurol Scand Dirk C (2018) Paratonia in Flemish nursing homes: Current
80, 64-67. state of practice. Am J Alzheimers Dis Other Demen 33,
[30] Drenth H, Zuidema SU, Krijnen WP, Bautmans I, van der 205-214.
Schans C, Hobbelen H (2017) Advanced glycation end- [46] Franssen EH, Kluger A, Torossian CL, Reisberg B (1993)
products are associated with the presence and severity of The neurologic syndrome of severe Alzheimer’s disease.
 H. Drenth et al. / Paratonia in Dementia: A Systematic Review 1637

Relationship to functional decline. Arch Neurol 50, 1029- [56] Rahmadi A, Steiner N, Munch G (2011) Advanced glycation
1039. endproducts as gerontotoxins and biomarkers for carbonyl-
[47] Hobbelen JSM, Koopmans RTCM, Verhey FRJ, Van Peppen based degenerative processes in Alzheimer’s disease. Clin
RPS, de Bie RA (2006) Paratonia: A Delphi procedure for Chem Lab Med 49, 385-391.
consensus definition. J Geriatr Phys Ther 29, 50-56. [57] Gasser A, Forbes JM (2008) Advanced glycation: Implica-
[48] Pauc R, Young A (2012) Paratonia and gegenhalten in child- tions in tissue damage and disease. Protein Pept Lett 15,
hood and senescence. Clin Chiropr 15, 31-34. 385-391.
[49] Ries JD (2018) Rehabilitation for individuals with demen- [58] Scherder E (2016) Aging and dementia. Neuropsychology,
tia; facilitating success. Curr Geriatr Rep 7, 59-70. motor skills, and pain, VU University Press, Amsterdam.
[50] Peralta V, Cuesta MJ (2017) Motor abnormalities: From [59] Rakt J van der (1997) The development of a fetal position in
neurodevelopmental to neurodegenerative through “func- psychogeriatric patients; a hypothesis. Fysiother Ouderen-
tional” (neuro)psychiatric disorders. Schizophr Bull 43, zorg, pp. 2-6.
956-971. [60] Verschueren SMP, Brumagne S, Swinnen SP, Cordo PJ
[51] Thibaut A, Chatelle C, Ziegler E, Bruno M-A, Laureys (2002) The effect of aging on dynamic position sense at
S, Gosseries O (2013) Spasticity after stroke: Physiology, the ankle. Behav Brain Res 136, 593-603.
assessment and treatment. Brain Inj 27, 1093-1105. [61] Hortobagyi T, Devita P (2006) Mechanisms responsible for
[52] Shahed J, Jankovic J (2007) Motor symptoms in Parkinson’s the age-associated increase in coactivation of antagonist
disease. Handb Clin Neurol 83, 329-342. muscles. Exerc Sport Sci Rev 34, 29-35.
[53] Middelveld-Jacobs IM, Boogerd van den MECP (1986) [62] Magalhães PM, Appell HJ, Duarte JA (2008) Involvement of
Paratonie een vorm van hypertonie in het psychogeriatrisch advanced glycation end products in the pathogenesis of dia-
verpleeghuis. Ned Tijdschr Fysiother 96, 85-87. betic complications: The protective role of regular physical
[54] Hobbelen JSM, Verhey FRJ, Bor JHJ, de Bie RA, Koop- activity. Eur Rev Aging Phys Act 5, 17-29.
mans RTCM (2007) Passive movement therapy in patients [63] Drenth H, Zuidema SU, Krijnen WP, Bautmans I, Smit AJ,
with moderate to severe paratonia; study protocol of a ran- Schans C van der, Hobbelen H (2018) Advanced glycation
domised clinical trial (ISRCTN43069940). BMC Geriatr end-products are associated with physical activity and phys-
7, 30. ical functioning in the older population. J Gerontol A Biol
[55] Waardenburg H, Elvers JWH, van Vechgel F, Oosten- Sci Med Sci 73, 1545-1551.
dorp RAB (1999) Is Paratonie Betrouwbaar te meten? Een
betrouwbaarheid onderzoek voor het meten van paratonie
met de VAS en de gemodificeerde tonusschaal van Ash-
worth. Ned Tijdschr Physiother 2, 30-35.