Introduction
It is well known that shoulder subluxation in hemiplegics is one of the disabling
factors encountered in rehabilitating patients. The causative factors may include
the pull of gravity on the paralyzed shoulder [[1]], peripheral nerve lesions [[2]] or tear in the rotator cuff [[3]]. Hemiplegic extremities are usually recognized as being flaccid during the early
stage following cerebrovascular accident, and this may cause migration of the humeral
head in the shoulder joint leading to overstretching of the capsule, tendons and ligaments
along with the brachial plexus [[4],[5],[6]]. The mechanism of the palsy appears to involve a stretch injury. The hemiplegic
patient without complications most commonly shows a course in which flaccidity is
followed by spasticity, and in which return of function and muscle tone proceeds from
proximal to distal muscle groups [[7],[8]].
An axillary nerve lesion caused by prolonged stretching, can be expressed by numbness
over part of the outer shoulder, difficulty in lifting objects with the sore arm and
in raising it above the head. These symptoms will blur the successful results of the
rehabilitation after stroke if the axillary nerve is involved.
The aim of the study was to prove the probability of axillary nerve lesion after shoulder
injury due to hemiplegia and so, to improve preventive and corrective measures for
this difficult condition, knowing that even in case of complete recovery from hemiplegia,
a disability will remain as a result of this lesion.
Methods
The study was a retrospective analysis of data on patients hospitalized in our rehabilitation
department between the years 2003 and 2006. We routinely perform nerve conduction
tests on all stroke patients who have flaccid paralysis in the upper limb [[9]]. Twenty-two inpatients suffered from hemiplegia after first-time stroke, included
8 men and 14 women, were tested. Their mean age was from 50 to 90 years (mean 72.5
± 9.5 years) and the duration of the hemiplegia at the time of examination varied
from 25 to 87 days (mean = 43 ± 12 days, and median = 43 days). Eleven patients had
right hemiplegia and the remaining eleven, left hemiplegia. All patients were right
hand dominant. The causes of hemiplegia were cerebral infarction in 16 patients, cerebral
hemorrhage in 4 patients and cerebral hemorrhage inside infarction in 2 patients.
Selection criteria were paralysis of upper limb after first-time stroke, flaccidity
and atrophy of shoulder girdle muscles in the involved side and one or more fingers
breadths in the upper part of the gleno-humeral joint space of the paralyzed shoulder
([Figure 1]). All patients had no previous history of trauma or peripheral nerve injury in the
paralyzed upper extremities. All patients who had flaccid paralysis after a second
or later stroke, were excluded from the study.
Figure 1
One or more fingers breadths in the upper part of gleno-humeral joint space, between
the acromion and the humeral head of the paralyzed shoulder.
Nerve conduction studies were performed by the first author in a closed room in which
the temperature was maintained at 22–24° Celsius, while the patient was placed in
a sitting position, on his wheelchair, with the arm at 45 degrees abduction. All patients
were studied on a Nicolet Viking III P, Madison Wisconsin, USA electromyography machine.
Electrical nerve stimulation of 200 Volts, well tolerated by the patients, was given
at the Erb’s point, slightly above the upper margin of the clavicle and lateral to
the clavicular head of the sternocleidomastoid muscle. Stimulator pulse duration of
the square wave was 0.1 msec. A coaxial needle for registration was inserted into
the middle deltoid muscle, 4 cm directly beneath the lateral border. The ground electrode
was placed between the stimulating and the pick-up electrode [[10]]. The latency was measured from the stimulus artifact to the CAMP onset point and
the amplitude was determined from baseline to the highest negative peak [[11],[12]].
Results of the paralyzed shoulder were compared to those obtained in the sound shoulder.
We had to take into consideration that there was an asymmetry between the shoulders,
due to muscular atrophy in the paralyzed side. Due to technical disorders, skin temperature
was measured only in few patients.
Statistical analysis
A descriptive statistical study of the quantitative parameters of mean and standard
deviation was performed, and the Wilcoxon signed rank sum test was used to compare
the quantitative data presented as latencies and amplitudes between the healthy and
the paralyzed sides (assumption of normal distribution could not be held for differences).
Additionally, 11 patients having right shoulder paralysis were compared with 11 patients
having right healthy shoulders and separately, another 11 patients having left shoulder
paralysis were compared with 11 having healthy left shoulders, using the Mann-Whitney
test. P values below 0.05 were taken to indicate statistical significance. SPSS for
Windows version 11.5 (Chicago, IL) was used for the statistical analysis.
Results
The mean latency time to the deltoid was 8.49 ms, SD = 4.36 in the paralyzed shoulder and 5.17 ms, SD = 1.35 in the sound shoulder (Wilcoxon signed rank test, p < 0.001, 1-sided).
The mean compound muscle action potential (CMAP) amplitude was 2.83 mV, SD = 2.50 in the paralyzed shoulder and was 7.44 mV, SD = 5.47 in the sound shoulder (Wilcoxon signed rank test, p < 0.001, 1-sided), ([Table 1]).
Table 1
CMAP latency and amplitude recorded in the deltoid muscle
|
Sound shoulder
|
Paralyzed shoulder
|
p-value
|
|
CMAP latency
|
5.17 ± 1.35
|
8.49 ± 4.36
|
< 0.001, 1-sided
|
|
CMAP amplitude
|
7.44 ± 5.47
|
2.83 ± 2.50
|
< 0.001, 1-sided
|
The same tendencies were found significant when this comparison was done separately
for patients with a right paralyzed shoulder (N = 11) and for patients with left paralyzed
shoulders (N = 11). Patients with right paralyzed shoulder compared to patients with
right sound shoulder (p < 0.001, 1-sided for latency; p = 0.003, 1-sided for amplitude), and patients with left paralyzed shoulder compared
to patients with left sound shoulder (p = 0.011, 1-sided for latency, p = 0.001, 1-sided for amplitude), support the same outcomes.
The mean latency time to the deltoid in patients tested up to 43 days after stroke
breakout was 9.3 ms (SD = 4.55) in the paralyzed shoulder and 5.3 ms (SD = 1.5) in the sound shoulder (Wilcoxon signed rank test, p = 0.007, 1-sided). The mean CMAP amplitude in patients tested up to 43 days after
stroke breakout was 2.8 mV, SD = 2.4 in the paralyzed shoulder and 6.5 mV, SD = 5.1 in the sound shoulder (Wilcoxon signed rank test, p = 0.001, 1-sided) ([Table 2], [Table 3]).
Table 2
CMAP latency and amplitude recorded in the deltoid m. up to 43 days after stroke onset
|
Sound shoulder
|
Paralyzed shoulder
|
p-value
|
|
CMAP latency
|
5.3 ± 1.5
|
9.3 ± 4.55
|
0.007, 1-sided
|
|
CMAP amplitude
|
6.5 ± 5.1
|
2.8 ± 2.4
|
0.001, 1-sided
|
Table 3
CMAP latency and amplitude recorded in the deltoid m. over 43 days after stroke onset
|
Sound shoulder
|
Paralyzed shoulder
|
p-value
|
|
CMAP latency
|
5.07 ± 1.2
|
7.55 ± 4.15
|
0.02, 1-sided
|
|
CMAP amplitude
|
8.5 ± 5.98
|
2.88 ± 2.7
|
0.005, 1-sided
|
Discussion
Electrophysiological investigations of shoulder subluxation in hemiplegic patients
has been well documented in several reports [[7],[9],[13],[14]]. Milanov [[15]] who evaluated the motor conduction in median, ulnar, peroneal and tibial nerves,
found that the mean M-wave amplitudes were significantly decreased for each nerve
study, in both upper and lower limbs of the paralyzed limbs, compared with the healthy
side. In contrast, the mean motor conduction velocities were not reduced in the involved
limbs compared to the unaffected limbs. Their patients were with long-term spastic
hemiplegia after stroke. In our study, both the motor latency and the M-wave amplitude
were significantly reduced in the paralyzed side, taking into consideration that our
patients had in contrast, short-term flaccid hemiplegia.
The muscular tone in the paralyzed upper limb of our patients remained flaccid for
more then several weeks. In the flaccid stage of stroke, the shoulder is prone to
inferior subluxation and vulnerable to soft-tissue damage; weakness in the shoulder
girdle muscles and gravitational pull tend to result in inferior subluxation [[16],[17],[18]].
Does a downward subluxation may produce traction on the axillary nerve as it winds
around the surgical neck of the humeral shaft?
Injury to the axillary nerve in stroke patients may result from a traction force.
In the present study, the latency time to the deltoid muscle showed delayed latency
values and the CMAP amplitude showed reduced values in the axillary nerve on the paralyzed
side.
There is sufficient biomechanical evidence that the peripheral nerve under tension
undergoes strain and glides within its interfacing tissue [[19]]. The weight of the unsupported arm may also cause traction damage to various nerves
including the axillary nerve [[20]], the suprascapular nerve [[21]] and the brachial plexus [[1]]. Ring et al [[9]] found that among 6 stroke patients that manifested certain deterioration of their
gleno-humeral alignment, 5 had an electromyographic feature of axillary nerve damage.
The most common zone of injury is just proximal to the quadrilateral space [[22]]. Ring et al [[14]] suggested that downward subluxation is able to produce traction on the axillary
nerve as it winds around the surgical neck of the humeral shaft. The presence of an
atypical pattern including flaccidity and atrophy of the supraspinatus, infraspinatus,
deltoid and biceps muscles in the impaired upper extremity, in the presence of increased
muscle tone or movement in the distal muscles, should alert caregivers to the possibility
of complicating brachial plexus lesion [[7]].
We must also take into consideration that the prolonged latency registered after giving
an electrical stimulation of the axillary nerve in the paralyzed shoulder, may be
related also to the lowering of the skin temperature in the affected limbs. In chronic
hemiplegia a decrease in temperature may result from inactivity of the limbs and reduced
circulation [[23]].
Wasting of muscles in the shoulder girdle, among them the deltoid muscle, in patients
after lesions of the upper motor neuron, can be a cause of reduced conduction velocity
[[24]]. McComas et al [[25]] described a possible mechanism for muscle atrophy following upper motoneuron lesions.
We believe that a decreased diameter of the nerve fiber as a result or cause of muscle
atrophy, could lead to a decreased nerve conduction velocity.
We believe that continuous traction of the axillary nerve, as in the hypotonic shoulder,
may affect the electro-physiological properties of the nerve. It most probably results
from subluxtion of the head of the humerus, causing demyelinization and even axonopathy.
Myelin loss results in slowing of the nerve conduction through the area involved.
When traction is severe, an axonal damage, expressed by reduction of CMAP amplitude,
may occur. We cannot disregard the fact that slowing of the conduction velocities
of the axillary nerve in the paralyzed shoulders may be related also to the lowering
of the skin temperature in the same limbs.
The difference between the mean latency time and CMAP amplitude in the paralyzed compared
to the sound shoulder, tested up to 43 days after stroke breakout, was statistically
significant. Rehabilitation of stroke patients with hemiplegia takes place generally
in the first two or three months of the disease, meaning that the onset of axillary
nerve lesion in the paralyzed side is early, and happens generally during the rehabilitation
period.
Most stroke patients with hemiplegia will experience shoulder injury and pain [[26]]. Nerve lesions secondary to subluxation or dislocation may retard or be detrimental
for muscle recovery and limb function [[9]].
Conclusion
The initial flaccidity of the hemiplegic shoulder can result in the axillary nerve
lesion associated with shoulder subluxation. It is advocated that electrophysiological
studies of the shoulder girdle be carried out, several weeks after stroke breakout,
to assess the severity of peripheral nerve involvement, so early preventive measures
for shoulder subluxation and subsequent nerve damage can be applied. We are not able
to propose the exact mechanism of lower motor neuron degeneration, but our findings
are compatible with myelin changes in motoneurons followed by axonal involvement.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
AT performed all the examinations on the patients, wrote the manuscript and collected
the references. HR proposed the initial design.
