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Neurophysiological and clinical study of Brunnstrom recovery stages in the

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DOI: 10.3109/02699052.2010.506860 · Source: PubMed

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Brain Injury, October 2010; 24(11): 1372–1378

ORIGINAL ARTICLE

A neurophysiological and clinical study of Brunnstrom recovery

stages in the upper limb following stroke

SOOFIA NAGHDI1, NOUREDDIN NAKHOSTIN ANSARI1, KOROSH MANSOURI2, &

SCOTT HASSON3
1
Faculty of Rehabilitation, Tehran University of Medical Sciences, Tehran, Iran, 2Medical School, Iran University of
Medical Sciences, Iran, and 3Physical Therapy Department, Angelo State University, San Angelo, TX, USA

(Received 19 January 2010; revised 1 June 2010; accepted 5 July 2010)

Abstract
Primary objective: To determine the extent to which the Brunnstrom recovery stages of upper limb in hemiparetic stroke
patients are correlated to neurophysiological measures and the spasticity measure of Modified Modified Ashworth
Scale (MMAS).
Research design: A concurrent criterion-related validity study.
Interventions: Not applicable.
Methods and procedures: Thirty patients (15 men and 15 women; mean  SD ¼ 58.8  11.5 years) with upper limb spasticity
after stroke were recruited. Wrist flexor spasticity was rated using the MMAS. The neurophysiological measures were Hslp/
Mslp ratio, Hmax/Mmax ratio and Hslp.
Main outcomes and results: There was a significant moderate correlation between the Brunnstrom recovery stages and the
neurophysiological measures. The Brunnstrom recovery stages were highly correlated to the MMAS scores (r ¼ 0.81,
p < 0.0001).
Conclusions: The Brunnstrom recovery stages are moderately correlated with neurophysiological measures and highly
correlated with the MMAS regarding the evaluation of motor recovery in stroke patients. The Brunnstrom recovery stages
can be used as a valid test for the assessment of patients with post-stroke hemiplegia.

Keywords: The Brunnstrom recovery stages, spasticity, H-reflex, Modified Modified Ashworth Scale

Introduction Spasticity has been classically defined as an

Stroke is the leading cause of disability in the adult
population, which affects more than four million
people in the US [1]. The data from the World
Health Organization (WHO) have shown that stroke
affects 15 million people in the world annually and
approximately one-third will live with permanent
disability, inflicting a burden on the patient, family
and the community [2]. Patients with hemiplegia
after stroke are left with impaired motor activity,
abnormal synergies, spasticity and muscle weakness
leading to functional disability.
increased resistance to a passive stretch. The
increased resistance is a result of a velocity-depen-
dent increase in tonic stretch reflexes that occurs
from hyper excitability of the stretch reflex which is
one component of the upper motor neuron syn-
drome [3]. This definition implies an increase in
reflex excitability in patients with upper motor
neuron lesions including stroke. A recent study
demonstrated a velocity-dependent EMG response
to stretch in patients with stroke, compared with an
absence of EMG activity in control participants at
any of the target velocities [4].

Correspondence: Dr Soofia Naghdi, Faculty of Rehabilitation, Tehran University of Medical Sciences, Enghelab Ave, Pitch-e-Shemiran, Zip: 11489,
PO Box 11155-1683, Tehran, Iran. Tel: þ98 21 77535132. Fax: þ98 21 77882009. E-mail: naghdi@sina.tums.ac.ir
ISSN 0269–9052 print/ISSN 1362–301X online  2010 Informa UK Ltd.
DOI: 10.3109/02699052.2010.506860

The clinical measures for the assessment of muscle
spasticity are the Ashworth scales and the Tardieu
scales [5–9]. The Modified Modified Ashwoth Scale
(MMAS) is a modified version of the Bohannon-
Smith Modified Ashwoth Scale (1987) for clinical
assessment of spasticity [6, 10]. The MMAS
removed the ‘1þ’ and re-defined the grade ‘2’.
This measure has been shown to be reliable and valid
in the measurement of spasticity in different spastic
muscle groups [11–15].
The H-reflex is a useful tool in evaluating reflex
pathways. The ratio of the maximum size of the
H-reflex (Hmax) to the maximal size of the M
response (Mmax) is the conventional indicator for
evaluating reflex excitability and spasticity [16].
Another method using H-reflexes and M-responses
is the ratio of the developmental slope of the H-reflex
(Hslp) to the slope of the M-response (Mslp)
[17, 18]. The Hslp/Mslp ratio has been suggested
as a preferred index for assessing the motoneuron
pool excitability and the degree of motor recovery
after stroke, because it excludes alterations in
peripheral factors from influencing H-reflex ampli-
tude [17–19].
There are several motor measures defining the
recovery stages for patients with stroke [20–23].
The motor recovery defined by Brunnstrom classifies
the recovery process into six stages (Table I). This
classification established from clinical observations of
a large number of hemiplegic patients is based on the
degree of spasticity, synergies and voluntary
movement. While this classification has face validity,
it has never been assessed for reliability and validity.
This study was therefore aimed to determine the
validity of the Brunnstrom recovery stages with
Table I. Brunnstrom recovery stages.
Stages Description
Stage 1 Flaccidity is present and no movements of the limbs
can be initiated.
Stage 2 The basic limb synergies or some of their components
may appear as associated reactions or minimal
voluntary movement responses may be present.
Spasticity begins to develop.
Stage 3 The patient gains voluntary control of the movement
synergies, although full range of all synergy compo-
nents does not necessarily develop. Spasticity is
severe.
Stage 4 Some movement combinations that do not follow the
synergies are mastered and spasticity begins to
decline.
Stage 5 More difficult movement combinations are possible as
the basic limb synergies lose their dominance over
motor acts.
Stage 6 Spasticity disappears and individual joint movements
become possible.
Study of Brunnstrom recovery stages 1373
neurophysiological measures and the Modified
Modified Ashworth Scale.
Methods and procedures
Participants
This study was approved by the research council
of Rehabilitation Faculty, Tehran University of
Medical Sciences. Informed consent was obtained
directly or via a care-giver. Thirty adult patients with
first ever stroke were recruited who met the following
inclusion criteria: clinically detectable increase in
muscle tone; able to comply with the study proce-
dure; and not taking anti-spastic drugs.
Procedure
The stage of motor recovery was determined using
the criteria described by Brunnstrom. The assess-
ment of Brunnstrom recovery stage was always
carried out first. The wrist flexors spasticity was
graded according to the MMAS. A single physio-
therapist experienced in neurological rehabilitation
assessed motor recovery and muscle spasticity.
These measurements were followed by H-reflex
measurements. All neurophysiological measurements
were also performed by the same trained physiother-
apist. The measurements were made in a same
session. Demographic data pertaining to the patients
were also recorded.
Outcome measures
The outcome measures were the Brunnstrom recov-
ery stages, MMAS for the clinical assessment of
spasticity and the neurophysiological measures of
Hslp/Mslp ratio, Hmax/Mmax and Hslp.
Brunnstrom recovery stages. The motor recovery of
patients was assessed clinically with Brunnstrom
recovery stages (Table I). This test describes the
sequences of motor recovery after stroke based on
the degree of spasticity and the appearance of
voluntary movement.
The Modified Modified Ashworth Scale. Spasticity of
the wrist flexors was assessed using a 5-point
MMAS, in which the score is graded as follows:
0 ¼ No increase in muscle tone; 1 ¼ Slight increase
in muscle tone, manifested by a catch and release
or by minimal resistance at the end of the range of
motion when the affected part(s) is moved in flexion
or extension; 2 ¼ Marked increase in muscle tone,
manifested by a catch in the middle range and
resistance throughout the remainder of the range
of motion, but affected part(s) easily moved;
1374 S. Naghdi et al.
3 ¼ Considerable increase in muscle tone, passive
movement difficult; and 4 ¼ Affected part(s) rigid in
flexion or extension [10]. Spasticity was measured at
the wrist joint with the patient in the supine position.
With forearm in neutral position, the physiotherapist
stabilized the forearm just proximal to the wrist joint
and the other hand grasped the patient’s palm. The
wrist was moved from maximum possible flexion to
maximum possible extension over a duration of 1
second (by counting one thousand one). Very good
inter-rater reliability of MMAS (weighted
kappa ¼ 0.92, p < 0.0001) has been shown for wrist
flexors in patients with hemiplegia [11].
Measurements of H-reflex and M-response. This
study performed the technique used in previous
studies [13, 24, 25]. Maximum H-reflex and max-
imum M-response were assessed. The measures
were made with the forearm in supination. The
MytoII EMG machine (Italy) was used to obtain the
H-reflex and the M-response. The bandpass filter
was set at 5 Hz to 3 kHz, sweep rate at 5 ms/div, and
sensitivity at 500 mV to 2 mV/div were used.
Rectangular electric pulses with a duration of 1 ms
were repeated every 5 seconds and the output ranged
from 0–100 mA. The median nerve was stimulated
at the elbow crease using a bipolar ball electrode.
The recording electrodes were placed over the
muscle belly of Flexor Carpi Radialis (FCR).
Paired surface electrodes (Ag/AgCl) were used.
Active electrode was placed on the belly of FCR at
one third of the proximal distance between the
medial epicondyl of humerus and the radial styloid.
The electrical resistance between the two electrodes
was less than 10 k
. The ground was attached to the Results
skin between stimulating and recording electrodes.
H-reflexes and M-response were recorded during
stepwise increases in stimulus intensity from below
threshold for the H-reflex to that eliciting a maximal
M-response. The intensity of pulses was gradually
increased with 0.5 mA steps.
Recruitment curves
The procedure reported was followed and used
elsewhere to collect data and produce recruitment
Table II. Results of H-reflex tests for Brunnstrom recovery stages in the affected arm.
Stages Frequency Hslp/Mslp, M (SD), range
Stage 2 2 2.02 (0.63), 1.582.46
Stage 3 8 1.70 (1.4), 0.183.90
Stage 4 6 1.21 (0.5), 0.571.74
Stage 5 9 0.72 (0.64), 0.121.81
Stage 6 5 0.52 (0.33), 0.171.03
curves [13, 17, 19, 24, 25]. At each stimulus
intensity, the mean of three pulses were calculated.
The amplitudes of the H-reflexes and M-response
were measured from the largest peak of the positive
to the largest peak of the negative deflections from
the baseline. The mean of the three H-reflexes and
M-response obtained at each stimulus intensity
was expressed as a percentage of the maximal
M-response. The mean Mmax was calculated from
all maximal M-waves evoked at the highest stimulus
intensity. Stimulus intensity was presented as the
ratio to the threshold of the M-response (Mth).
Hmax was defined as the highest mean amplitude of
three H-reflexes. The slope of the regression line
of the H-reflex and M-response was obtained as
Hslope (Hslp) and Mslope (Mslp). Data were
analysed by using the Hslp/Mslp ratio and the
Hmax/Mmax ratio.
Statistical analysis
The Spearman’s rho test was used to establish
relationships between the Brunnstrom recovery
stages and H-reflex indices and MMAS scores.
Additionally, the correlation between the MMAS
scores and H-reflex indices were calculated using
Spearman’s rho test. The strength of correlations
was interpreted as follows: low (0.00–0.39), moder-
ate (0.40–0.59), moderately high (0.60–0.79), high
(0.80–1.00) [26]. The alpha level for the determi-
nation of statistical significance was p < 0.05. The
statistical analyses were performed using an SPSS
11.5 software package.
Thirty right hand-dominant patients with hemiplegia
after stroke (15 men and 15 women) and a mean
(standard deviation, range) age of 58.8 years (11.5,
37–75) participated. The mean (standard deviation,
range) time since the stroke onset was 23.23 (13.63,
2–60) months. Twenty patients had left hemiplegia.
Table II demonstrates the frequency of the
Brunnstrom recovery stages and the H-reflex indices
values taken on the affected arm. Most patients were
in the higher Brunnstrom recovery stages (4, 5 or 6)
Hmax/Mmax, M (SD), range Hslp, M (SD), range
0.72 (0.06), 0.680.77 96.6 (15.78), 85.44107.76
0.60 (0.31), 0.131.00 196.71 (145.65), 25.92434.90
0.54 (0.19), 0.280.77 113.77 (22.48), 73.33130.27
0.32 (0.25), 0.090.73 72.74 (66.07), 11.94191.47
0.27 (0.13), 0.110.41 30.83 (12.66), 18.2345.70
 Study of Brunnstrom recovery stages 1375

(n ¼ 20). No patient was in stage 1. Figure 1 depicts The results have been shown in Table IV. The
the mean of H-reflex indices in each of the correlation between the Brunnstrom recovery stages
Brunnstrom recovery stages. There was a significant and MMAS scores was statistically significant
moderate correlation between the Brunnstrom (r ¼ 0.81, p < 0.0001) (Table III).
recovery stages and the H-reflex indices (Table III). The mean of H-reflex indices for MMAS scores
Most patients were scored ‘2’ and ‘3’ based on are reported in Table V. The MMAS had a
the MMAS (n ¼ 17). In the low Brunnstrom recovery significant correlation with the H-reflex indices
stages (1, 2 or 3) patients were scored ‘2’ or ‘3’ on the (Table III). The Brunnstrom recovery stages,
MMAS (n ¼ 10). In the higher Brunnstrom recovery MMAS and H-reflex indices were correlated to
stages, patients were mostly scored ‘0’ or ‘1’ (n ¼ 13). each other (Table III).

Discussion
(a) 2.5
Hslp/Mslp In this study, 30 patients with hemiplegia due to
stroke were examined to evaluate the validity of the
Hmax/Mmax
2.0 Brunnstrom recovery stages by using neurophysio-
Mean of H-reflex tests

logical measures and clinical Modified Modified

Ashworth Scale. The findings revealed that the
1.5
Brunnstrom’s 6-stages of motor recovery are valid
for assessing motor impairment in patients with
1.0 stroke resulting in hemiplegia.
To the best of the authors’ knowledge, this is the
first report on the validity of the Brunnstrom
0.5 recovery stages in patients with hemiplegia. While
Brunnstrom recovery stages have been used as a
0.0 standard against which to study the validity of newly
2.00 3.00 4.00 5.00 6.00 developed methods [18, 27–29], no reports existed
Brunnstrom recovery stages in the literature on the psychometric properties of
this recovery staging system. The Brunnstrom stag-
(b) 300
ing system is based on muscle spasticity and limb
synergies of hemiplegic patients. Appearance of
individual limb movement is associated with the
decline in muscle spasticity and the control over limb
200 synergies. The synergies have been associated with
Mean of Hslp

spasticity in hemiparetic stroke patients and patients

whose movements are restricted to the synergies also
would exhibite spasticity [30]. In this study, the
100
Hslp/Mslp ratio as well as the traditional index of
Hmax/Mmax in accordance with the Brunnstrom’s
notion of recovery decreased with progression of
stages. This finding indicates that the motoneuron
pool excitability tends to decline with control over
0 voluntary movement.
2.00 3.00 4.00 5.00 6.00
The spasticity measured on the MMAS also
Brunnstrom recovery stages
showed that the degree of spasticity decreased as
Figure 1. The mean H-reflex indices of (a) Hmax/Mmax and the recovery stages progressed. In Brunnstrom
Hslp/Mslp and (b) Hslp in Brunnstrom recovery stages. recovery stage 3 classically defined as ‘Spasticity is

Table III. Spearman’s  correlation coefficients of Brunnstrom recovery stage, MMAS and H-reflex indices.

MMAS Hslp/Mslp Hmax/Mmax Hslp

Brunnstrom recovery stage 0.81, p < 0.0001 0.51, p ¼ 0.004 0.54, p ¼ 0.002 0.54, p ¼ 0.002
MMAS 0.42, p ¼ 0.02 0.39, p ¼ 0.03 0.47, p ¼ 0.009
Hslp/Mslp 0.64, p < 0.0001 0.70, p < 0.0001
Hmax/Mmax 0.71, p < 0.0001
1376 S. Naghdi et al.

severe’, all patients had severe spasticity as assessed
by the MMAS (scores of 2 and 3). As the recovery
stage progressed, the frequency of patients with
severe spasticity decreased. In Brunnstrom recovery
stage 6, classically defined as ‘Spasticity disappears’,
all patients scored low grades of spasticity as assessed
by the MMAS (scores of 0 and 1). In Brunnstrom
recovery stage 2, classically defined as ‘Spasticity
begins to develop’, patients scored 3 (Considerable
increase in muscle tone, passive movement difficult)
on the MMAS. One would expect to have mild
spasticity in stage 2. Furthermore, the spasticity did
not disappear clinically even in stage 6, even though
the motoneuron pool excitability indices were in the
normal range. The higher degree of spasticity in
stage 2 could be because of the changes in the
muscles. The evidence indicates an intrinsic change
in the passive mechanical properties of spastic
muscle [31]. The MMAS used in this study grades
a relaxed limb’s resistance to passive movements.
The severe spasticity scored in the patients with
stage 2 might be due to structural changes in the
muscle and increased reflex activity. However, these
patients also had very high motoneuron pool excit-
ability reflected in the abnormal Hslp/Mslp (2.2 and
0.82) and Hmax/Mmax (0.68 and 0.77). In this study,
a significant correlation existed between the MMAS
scores and the neurophysiological tests (p < 0.05).
Also, the mean of these tests increased accordingly
with the degree of MMAS, confirming the results of
previous study that the MMAS is a valid ordinal level
scale of muscle spasticity [13].
Table IV. The frequency of Modified Modified Ashworth Scale
(MMAS) scores in each of Brunnstrom recovery stages obtained
from the affected arm.
MMAS grades
Recovery
stages 0 1 2 3 Total
2 0 0 0 2 2
3 0 0 3 5 8
4 0 1 3 2 6
5 2 5 2 0 9
6 1 4 0 0 5
Total 3 10 8 9 30
In Brunnstrom recovery stage 6, only one out of
five patients scored ‘0’ on the MMAS. The presence
of spasticity in stage 6 could be that in the
Brunnstrom approach the speed tests for spasticity
is not based on isolated fast passive stretches in
relaxed patients. Instead, the patients carry out the
movements actively as fast as possible [20]. The
response to stretch differs in the passive and active
conditions. Reflexes have different roles in passive
and active states [32] and reflexes elicited under
active conditions are functionally relevant [33]. In
the facilitation-based approach of Brunnstrom, the
spasticity has been assumed as a direct cause of
disordered movement in hemiparetic patients [34].
In active situations, factors other than spasticity may
also be associated with voluntary movement distur-
bance such as lack of strength and dexterity [35–38],
disrupted inter-joint coordination related to distur-
bances of central planning [39], abnormalities in
electromyographic output [40], insufficient activa-
tion of the muscle [41] and abnormal passive
stiffness of the muscles [42–44]. Therefore, it is
possible for a patient in Brunnstrom recovery stage 6
to demonstrate spasticity measured as resistance to
passive movement.
The Brunnstrom recovery stages showed a signif-
icant negative correlation with H-reflex tests. The
Hslp/Mslp and Hmax/Mmax decreased as the stages
progressed. However, the peak of Hslp occurred
in Brunnstrom recovery stage 3 and decreased with
stage progression. The Hslp was the neurophysio-
logical variable that had the highest correlation with
the Brunnstrom recovery stages as well. The Hslp
has been considered as the ‘reflex gain’ being an
effective tool for evaluation of motoneuron pool
excitability [17]. The Brunnstrom six-stages scale
describes the recovery based on spasticity and the
Hslp compared with the other neurophysiological
variables was best matched with Brunnstrom stages.
Furthermore, the MMAS was correlated with the
H-reflex tests. The values of the indices increased
with the severity of MMAS. Again, the Hslp had a
higher correlation with MMAS than the Hslp/Mslp
and the Hmax/Mmax. Therefore, although all
neurophysiological measures of H-reflex used in
this study can be applied for objective examination
of spasticity, the Hslp seems to be a better tool for

Table V. Results of H-reflex indices for MMAS grades in the affected arm.

MMAS Frequency Hslp/Mslp, M (SD), range Hmax/Mmax, M (SD), range Hslp, M (SD), range

0 3 0.69 (0.44), 0.21.03 0.17 (0.06), 0.120.23 29.58 (16.01), 11.9443.19

1 10 0.75 (0.57),0.171.81 0.41 (0.2), 0.110.73 75.9 (62.37), 18.23191.47
2 8 1.02 (1.28), 0.123.90 0.49 (0.36), 0.090.94 111.49 (97.73), 15.29321.19
3 9 1.81 (0.88), 0.683.50 0.58 (0.23), 0.281.00 168.73 (125.89), 25.92434.9

assessment in terms of motor recovery stages and
spasticity in patients after stroke.
Conclusion
According to the results of the present investigation,
it is concluded that the Brunnstrom recovery stages
are moderately correlated with the H-reflex indices
and highly correlated to the Modified Modified
Ashworth Scale concerning the evaluation of motor
recovery in stroke patients. Being a convenient
measure, it can be applied as a valid test for the
assessment of patients with hemiplegia.
Acknowledgements
This research was supported by Tehran University
of Medical Sciences and health Services (Grant-87-
8263). We would like to thank all patients who
participated in this study.
Declaration of interest: The authors report no
conflicts of interest. The authors alone are respon-
sible for the content and writing of the paper.
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