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384 Journal of Neurology, Neurosurgery, and Psychiatry 1990;53:384-387

Laboratory testing of muscle function in the

management of neuromuscular disease
C M Wiles, Y Karni, J Nicklin

Abstract this work was given to the Association of

A laboratory was set up to assess muscle British Neurologists.7
weakness and physical disability in
patients with peripheral neuromuscular
diseases. Muscle strength was mainly Methods
measured with a hand held dyn- a) Techniques
amometer and results were expressed in Muscle strength is measured using a handheld
relationship to a "guideline" range for electrodynamometer (Penny and Giles Ltd)
sex: disability was expressed in terms of applied to standard anatomical points89 (see
ordinal data with a performance score table). In brief, the examiner holds the dyn-
and as interval data with simple timed amometer on the body part and applies
tests. Of 17 patients with polymyositis on sufficient counter force to overcome (and
immunosuppressive medication fol- thereby lengthen) the muscle group under test
lowed for a mean of 2-9 years (range 1 1- during the patient's best voluntary effort: the
4-7 years) only eight became stronger force recorded as the examiner overcomes the
one of whom died. Assessment of weak- patient's contraction is taken as the peak force.
ness (the major impairment), disability, When a muscle group is tested against gravity
body weight, creatine kinase and the we prefer to add the weight of the limb
patient's subjective view of their state (weighed on the dynamometer) to the force
were essential to obtaining a clear view recorded'0 although difficulties with patient
of progress. relaxation sometimes make this difficult to
measure accurately. In practice an examiner
The traditional neurological examination is can apply a counter force of up to 250-300
primarily directed towards establishing an newtons but some muscle groups"' 2 yield
accurate diagnosis. For the motor system, the higher forces and the technique is therefore
history, the distribution of weakness between inappropriate for monitoring near normal
various muscle groups together with changes in strength in some individuals. Knee extension
tone, coordination and reflexes establish the strength is measured using a special muscle
differential diagnosis. For this application testing chair in which the patient makes a
many muscle groups are examined rapidly and maximum contraction against a fixed strap."3
annotated using a manual muscle testing sys- Handgrip and pinch grip are assessed on a
tem such as the MRC scale,' which subdivides separate dynamometer (MIE Medical
strength into ordinal categories. Functional Research Ltd). In some patients a test of
testing such as sitting from supine, or walking shoulder abduction fatiguability" is also util-
up and down stairs provides essential informa- ised.
tion for management but its grading is not of The purpose of measuring strength is to
primary importance in diagnosis. relate it to some estimate of "normal" and to
By contrast, follow up clinical assessment record change over time. We therefore establi-
should include measures of the major impair- shed "guideline" ranges for each of the muscle
ment caused by the disease (that is, muscle groups tested in groups of 30 healthy subjects
Departments of weakness in most cases of muscle disease), a of each sex none of whom undertook regular
Clinical measure of disability such as the ability to sit, muscle strengthening exercises (table).
Neurophysiology and stand, walk, swallow and some indication of Functional assessments consisted of a
Physiotherapy, The how this disability is perceived by and affects
National Hospital for modified version of a scoring system"5 of 0 to 2/
Nervous Diseases, the patient, that is, handicap.2 3 for ventilation, swallowing, use of arms,
Queen Square, The advantages of interval data over ordinal truncal movements and ambulation: the scores
London scales"' for strength measurements include a
C M Wiles were summed to give a performance score of 0
Y Karni clearer relationship of any particular value and to 58. In addition, the patient was timed
J Nicklin the normal range, accuracy and sensitivity over walking 30 m (with one turn) and the number of
Correspondence to: the whole range of values, valid proportionate paces counted: they were also timed up and
Dr C M Wiles
Department of Neurology, changes6 and ease of statistical handling. down 13 stairs and asked to make a vital
University of Wales College What follows is a brief description of the capacity manoeuvre using a "Vitalograph"
of Medicine, Heath Park,
Cardiff CF4 4XN, United methods used in a "muscle function" spirometer. Swallowing was assessed for the
Kingdom. laboratory established at the National Hospital, time it takes to drink 150 ml water when this
Received 8 April 1989 and in Queen Square in 1981 with illustrative exam- can be done safely. Height and weight are
revised form 26 September
1989. ples taken from a group of patients with recorded and the patient rated their strength on
Accepted 18 October 1989 polymyositis. A preliminary report of some of a 10 cm visual analogue scale ("very weak" to
 Downloaded from http://jnnp.bmj.com/ on April 6, 2015 - Published by group.bmj.com

Laboratory testing of muscle function in the management of neuromuscular disease 385

Table Muscle strength and timed activity in normal subjects
maintaining an indication of the "guideline"
Muscle strength (N) Males Females range.
or
Timed activity (S) Mean (SD) Mean (SD)
Group Results
a Neck flexion supine 139 (37) 68 (13) Illustrative examples
b Neck flexion sitting 176 (39) 95 (19)
c Shoulder abduction 232 (39) 151 (28) We compared the initial and most recent as-
d Elbow flexion 254 (27) 184 (31) sessment of 17 patients (six male, 11 female)
e Elbow extension 161 (30) 117 (20)
f Grip 405 (66) 236 (34) with poly- or dermato-myositis treated with
g Pinch grip 86
h First dorsal interosseous 45
(14)
(8)
58
35
(15)
(6) immunosuppression whose follow up was
i
j
Abductor pollicis Br.
Abductor digiti minimi
50
27
(9) 34 (7) longer than a year (mean 2-94 years, range
k Hip flexion 233
(5)
(40)
22
172
(5)
(35) 1*1-4.7). In addition creatine kinase (CK)
l Hip abduction 263 (37) 218 (31) measurements were extracted from the case
m Knee extension-R 443 (119) 292 (82) notes.
-L 421 (122) 287 (81)
n Walking 30 m-(s)
-paces
13
32
(2) 15 (3) Eight patients were stronger at the end of the
o Stairs 13 (s) 6
(4)
(2)
39
8
(5)
(2)
follow up period: all had a mean increase in
p Swallow 150 ml (s) 5 (2) 8 (3) strength of more than 20% of the lower limit of
Positions for muscle testing (for others see ref 9)
the normal range (46&7-130-7 %LLN). All
Subject position Myometer rated themselves as being stronger: timed 30 m
Small hand muscles
First DIO, ADM
Sitting: elbow/forearm No applicator walk was quicker and performance score
supported: forearm, hand Lateral aspect proximal inter increased in all but one patient who had gained
pronated, fingers extended phalangeal joint
Abductor pollicis br. As above No applicator 15 kg in weight. Although all showed a decline
Thumb abducted 90' from palm. in creatine kinase this did not correlate with
Interphalangeal joint
Grip Sitting, elbow support flex. 45°, Grip bars of myometer
semipronated forearm, hand
change in strength and was minimal in three
usually unsupported (1,240 to 948, 355 to 325, 90 to 65 iu/l). One
Pinch grip As above, thumb and index
extended at interphalangeal
Bars squeezed by index and thumb patient in this group died of cardiac complica-
joints tions of polymyositis.
Table groups
Five patients were essentially unchanged in
Sex Mean age (years) Range
a, b M 39 19-77 strength (mean change + 14-5 to -13% LLN)
c, d, e, k, 1
F 37 16-78 but three rated themselves as improved. One
M 34 20-61
F 34 19-57 walked more quickly and had increased perfor-
f, g M 38 20-60 mance score from 33 to 36 in association with
F 36 19-62
h, i, j M 40 19-63 13 5 kg weight loss. Creatine kinase concentra-
m, n, o, p
F 35 19-63 tions declined significantly in four patients but
M 42 17-66
F 42 was lower (median 126, range 22-910 iu/l) at
21-66
the start of the follow up period than in the
group which improved (median 1,815, range
"very strong"). "Guideline" values for walk- 90-10,175 iu/l). Two patients in this group
ing time and paces and drinking 150 ml in 30 died because of infective complications related
healthy subjects for both sexes are shown in the to immunosuppression or carcinoma.
table. Four patients were weaker (mean change
-20 to -50 8% LLN) of whom two rated
themselves as stronger at the end of the follow
b) Data collection and presentation up. Despite being weaker one walked faster
Muscle groups were selected by a physio- after a 15 kg weight reduction and one whose
therapist guided by diagnosis, pattern of weak- strength had declined by 51% LLN had main-
ness and disability: measurements were made tained performance score and walking speed
without reference to previous values obtained after a 14-5 kg weight reduction.
and took about 30 minutes. Data was stored on Patients who were unchanged or
a microcomputer sequentially in columns using deteriorated over the follow up period (on
a spreadsheet programme. Reports based on average similar to those who improved) had
the first and the last four assessments were had symptoms for longer (median 1 141 days,
generated with summary graphs when range 12-12 962), than those who improved
appropriate and a written conclusion appen- (median 149 days, range 40-420) though this
ded. was not statistically significant: only one
Reports composed of many columns of data patient in the group which improved was first
are indigestible and a summarising procedure assessed more than one year after the onset of
was adopted. Strength data was reviewed to see symptoms. The group which improved were
which groups were weak (> 2 sd below weaker (unpaired t test, p < 0.02), lighter
"guideline" mean) and whether all these (p < 0'01) and had higher CK values (In CK,
groups were following the same general trend. p < 0-01) at the beginning of monitoring than
The data for selected muscle groups were then those who deteriorated or were unchanged
expressed as a percentage of the value two during the follow up period.
standard deviations below the mean "guide-
line". The mean value for several muscle Example 1 (fig 1)
groups, thus expressed, was then displayed This patient aged 36 years had subacute
graphically provided that this did not obviously polymyositis. When first seen she was indepen-
conceal major disparities in trend between dently mobile but could not sit up from supine,
muscle groups. This data reduction procedure balance on one leg nor climb stairs easily: she
clarifies the trend of strength changes whilst made light of her symptoms but several major
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386 Wiles, Karni, Nicklin

Figure I Creatine kinase Example 2 (fig 2)

(iu/l), muscle strength (0% This patient, aged 28 years at presentation, had
LLN,female), a waddling gait, could only get upstairs holding
performance score (max
58), and alternate day onto a rail, but could not get up easily from a
prednisolone dose are low chair or sit from supine. Although her CK
shown over a six year fell promptly on prednisolone and azathioprine
period.
it was some months before she improved in
strength. Her CK remained high (1,000-2,000
Creatine kinase(IU/1) iu/l) as her strength increased. During pred-
nisolone reduction she hastened the decline in
200 T
* Cyclophosphamide dose covertly and strength was found to have
dropped markedly although she did not com-
150 Mean strength (%LLN-female) plain of new symptoms. With increased pred-
nisolone her strength improved by September
100
1985. As she still complained of significant
Performance score (max 58)
disabilities, her strength was not in the normal
50
range, and her CK remained elevated she was
started on oral low dose cyclophosphamide
Pred. (mg/alt day) which, together with a further transient
12/12/1981 12/12/1983 11/12/1985 11/12/1987 increase in prednisolone dosage, resulted in a
further increase in strength and decline in CK.
proximal muscle groups were reduced in stren- Although CK remained elevated throughout
gth to about 50% of the lower limit of normral this patient's illness log CK showed a strong
for her sex, and were estimated as MRC grades inverse correlation with strength (r = -0 9,
4 to 4-. She responded to prednisolone and p < 0-001). Changes in performance score
her CK fell to normal. As prednisolone was were small and at the top end of the scale but
reduced in early 1983 she became weaker again, appeared to correlate with strength so that, for
this being anticipated by a steep rise in CK, but example, ability to sit from supine was reliably
there was no change in functional ability and predicted by increased strength. The changes
she denied feeling worse. She did not tolerate in this patient's strength were such that they
azathioprine and was started on oral cyclophos- were all encompassed by MRC grade 4. The
phamide and increased prednisolone to which patient herself found it helpful to see her
she responded. In early 1985 her strength again progress objectively recorded and this
declined but there was no concomitant rise in facilitated compliance.
CK and she had few complaints. Her strength
subsequently improved with a moderate Example 3 (fig 3)
increase in prednisolone dosage and remains in This patient, aged 63 years, was first seen after
the "guideline" range. three months of symptoms when he was
Thus strength measurements were more profoundly weak, unable to swallow and
sensitive to the progress of polymyositis than required positive pressure ventilation. He was
either symptoms, performance criteria or CK. grossly wasted with a low CK considering the
The patient never regained the strength she rapidity of his polymyositis. He responded to
had in her original remission although she was prednisolone but this had to be temporarily
able to lead an active and full life. Her CK did discontinued because of side effects resulting in
not predict her second relapse. Strength
changes were large in comparison to the
2000T I
changes in performance score.
1600o-
Figure 2 Creatine kinase 5000
(iu/l), muscle strength (% 1200or
LLN,female), 4000
performance score (max
58) and daily prednisolone 800o-
3000
dose are shown over a four Creatine kinase ((U/Il
year period. 4010
2000
reatine kinase (U/I)

0li
1000
12

10

10 .. Average strength % LLN-(8 muscles)

$0
410 Performance (max 58)

0 , r-v!- Prednisolone (mg/alt day)

0~~~~1/1195
7/10/1984 1 1/11/1985 1/219
16/12V1986
Date

Figure 3 Creatine kinase (iu/l), muscle strength (%

LLN, male), performance score (max 58), and alternate
Date day prednisolone dose are shown over a three year period.
 Downloaded from http://jnnp.bmj.com/ on April 6, 2015 - Published by group.bmj.com

Laboratory testing of muscle function in the management of neuromuscular disease 387

a decline in strength in mid 1985 and a rapid Summed ordinal scores need caution in inter-
rise in CK. Prednisolone was eventually pretation. Although a very wide range of "fun-
resumed together with low dose oral cyclo- ctional" ordinal scales are available for scoring
phosphamide and he improved and was even- neurological disabilities we believe that there
tually able to walk with one stick. He continued would be advantages to measuring disabilities
to have mild muscle weakness. where possible in terms of interval units such as
time or distance and to relate these to the
specific impairments relevant to the disease
Discussion process in question. Thus walking is commonly
While it may be obvious that a patient can abnormal in muscle disease, multiple sclerosis
improve in days, or even minutes, as in the case and Parkinson's disease and the degree of
of a tensilon test for myasthenia, both clinician disability may be represented by the time taken
and patient can lose the perspective of change to walk a specific distance, the number of paces
in the longer term. We quite regularly notice or the stride length: this may be preferred for
discrepancies between the subjective analogue some purposes to having disease specific dis-
score of wellbeing and measures of strength ability scales. For clinical trials, notably in
and performance. Duchenne muscular dystrophy,'6 techniques of
It is uncommon for patients to insist that strength measurement and/or manual muscle
they are well when the indicators of disease testing are essential. Objective strength
progress are worsening (for example, fig 1) but measurements appear statistically more power-
the converse is more common. Reports from ful than functional testing'7 or manual muscle
the laboratory of stability or improvement in testing'8 and may easily and routinely be
condition may be misleading for several applied to adult neuromuscular disease as a
reasons. Firstly, a new impairment not covered means of clarifying progress.
by testing emerges or progresses (for example,
sensory loss in a neuropathy, pain, ataxia, We are grateful to The National Fund for
depression). Strength monitoring is inap- Research into Crippling Diseases (Action
propriate and misleading if the major disability Research) for the initial funding of this work
is due to an impairment other than weakness. A and to Dr R Willison (Department of Clinical
widening disparity between functional perfor- Neurophysiology) for helpful advice and criti-
mance and strength usually indicates the cism. Dr D Short performed some of the
presence of another impairment as illustrated measurements.
by the influence of body weight on perfor-
mance, a point commonly emphasised in the 1 Medical Research Council: Aids to examination of the
management of wasting diseases. peripheral nervous system. Memorandum no 45. London:
HMSO, 1976.
Secondly, the patient's impression and the 2 The International Classification of Impairments, Dis-
laboratory measurements may diverge because abilities and Handicaps: a manual of relating to the
consequences of disease. Geneva: WHO, 1980.
muscle groups relevant to the progressive dis- 3 MacKenzie CR, Charlson ME. Standards for the use of
ability are not assessed; particularly common ordinal scales in clinical trials. Br Med J 1986;292:40-3.
4 Forrest M, Anderson B. Ordinal scales and statistics in
are the failure to monitor bulbar and res- medical research. Br Med J 1986;292:537-8.
piratory muscle function, truncal muscle weak- 5 Andres PL, Hedlund W, Finison L, Conlon T, Felmus M,
Munsat TL. Quantitative motor assessment in amyotro-
ness and hip abduction weakness. Because of phic lateral sclerosis. Neurology 1986;36:937-41.
the selective nature of muscle involvement in 6 van der Ploeg RJO, Oosterhuis HJGH, Reuvekamp J.
Measuring muscle strength. JNeurol 1984;231:200-3.
many disorders, it is necessary to identify the 7 Wiles CM, Karni Y, Nicklin J. Muscle function testing in
sources of disability and the impairment polymyositis. J Neurol, Neurosurg Psychiatry
1988;51:1363.
accurately. When reporting muscle strength 8 Scott OM, Hyde SA, Goddard C, Dubowitz V. Quantitation
measurements we pay close attention to serial of muscle function in children: a prospective study in
Duchenne muscular dystrophy. Musck Nerve
changes within individual groups and not 1982;5:291-301.
(initially) to trends in the average values of 9 Wiles CM, Karni Y. The measurement of muscle strength in
patients with peripheral neuromuscular disorders. J
many muscle groups. When data are reduced Neurol, Neurosurg Psychiatry 1983;46:100-13.
for the purposes of a summary chart a mislead- 10 Bohannon RW. Correspondence. J Neurol, Neurosurg Psy-
chiatry 1987;50:1562-3.
ing graph may arise (for example, one which 11 Young A, Stokes M, Crowe M. The size and strength of the
minimises average strength changes) if dis- quadriceps muscles of old and young men. Clin Physiol
1985;5:145-54.
ability is the result of very selective muscle 12 Bassey EJ, Bendall MJ, Pearson M. Muscle strength in
involvement. We therefore highlight changes triceps surae and objectively measured customary walking
activity in men and women over 65 years of age. Clinical
in individual muscle groups if these are per- Science 1988;74:85-9.
ceived as relevant to functional performance 13 Edwards RHT, Young A, Hosking GP, Jones DA. Human
skeletal muscle function: description of tests and normal
whatever the average change is. values. Clinical Science and Molecular Medicine
Serial measurements of strength and perfor- 1977;52:283-90.
14 Nicklin J, Kami Y, Wiles CM. Shoulder abduction
mance allow some validation of this particular fatiguability. J Neurol, Neurosurg Psychiatry 1987;50:
423-7.
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16 Florence JM, Pandya S, King WM, et al. CIDD group:
be noted when the average strength in diffuse Clinical trials in Duchenne muscular dystrophy. III
or proximal myopathy drops to below about Standardisation and reliability of evaluation procedures.
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 Downloaded from http://jnnp.bmj.com/ on April 6, 2015 - Published by group.bmj.com

Laboratory testing of muscle function in the

management of neuromuscular disease.
C M Wiles, Y Karni and J Nicklin

J Neurol Neurosurg Psychiatry 1990 53: 384-387

doi: 10.1136/jnnp.53.5.384

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