An acute onset of an unusually severe and relentless pain in the neck, shoulder and / or arm regions is very characteristic of the disorder and occurs in 96% of all patients. It often (61%) wakes patients in the middle of the night or early morning, and usually increases to maximum severity in a few hours. Then it has almost invariably become very severe, and unlike anything the patient experienced before (unless he or she had a previous attack). Instructing the patient to grade the pain on a scale of 0 to 10 (0 being no pain and 10 the most severe pain imaginable) is an illustrative way of making this clear, because initially 60% and subsequently 90% of the patients will have such a NRS (Numerical Rating Scale) score of 7 or more, and the median NRS is 8 at onset and 9 at maximum intensity. The pain can also have a stuttering onset, and it can take up to two weeks or more for paresis to develop. Pain is usually worse at night and 94% of the patients cannot sleep because of it. Typically attempts to mitigate it by assuming certain postures or using acetaminophen or NSAIDs provide no relief whatsoever, and patients often tell that the pain had them up all night sitting on the couch with their arm pressed tightly against their body, or even had them crawling desperately on the floor not knowing what to do anymore. It is a story not lightly forgotten once heard, and the next patient will probably be recognized by it too, making it a useful diagnostic tool.
Once the acute stage of an attack is over, i.e. the initial pain has subsided and a patchy paresis and atrophy have become evident, 77% of the patients will go on to suffer from one or two additional types of pain. First the damaged nerves in the plexus can give rise to an increased mechanical sensitivity, eliciting shooting or radiating neuropathic pain in the affected nerves’ territory by putting strain on them through extension, abduction or elevation of the arm (a “Lasegue sign of the arm”). This hypersensitivity usually dissipates after weeks to months. Additionally many patients also develop musculoskeletal-type pain localized to the origin or insertion of the paretic — or compensating — muscles, especially in the periscapular, cervical and occipital regions. This pain may be particularly therapy-resistant and can sometimes become almost as incapacitating as the residual paresis itself. The main risk for developing it seem to be probably scapular instability caused by a paresis of the serratus anterior, rhomboids or trapezius. One the one hand this can lead to local myalgia and muscle strain in the trapezius and levator scapulae if they have to compensate for a downward and laterally displaced scapula. Often it is maximally felt at the points where these muscles attach to the occiput, cervical spine or shoulder blade, and can radiate further to the forehead — resembling tension-type headache — or interscapular region. Myalgia and pain at the attachment sites frequently also arises in paretic periscapular muscles that (also) serve a postural function. It is most often found in the serratus anterior region, extending from the medial scapular edge via the subscapular region and axilla to the midaxillary chest wall where the muscle inserts onto the ribs. This pain can be so bothersome that it even prevents normal breathing, because chest wall movement will further increase it. Obviously this complication can be even more impairing when the patient also has concomitant phrenic nerve dysfunction. Besides in the serratus anterior region it may occur in the area of any paretic muscle in NA. And finally, pain can result from glenohumeral joint pathology such as rotator cuff impingement or capsular irritation, developing as a consequence of the altered shoulder biomechanics in NA (see below).
Motor and sensory symptoms
The second typical feature of NA, that can at the same time make it difficult to recognize by clinicians, is the patchiness of the motor and sensory symptoms. Histological studies have already shown that the pathologic, presumably inflammatory, process can cause very focal damage to one or a few of the fascicles that make up a brachial plexus trunk or cord or a peripheral nerve, while simultaneously scatteredly affecting several parts of the plexus as a whole [2
]. This is reflected clinically by a wide variety in the possible distribution — and severity — of paresis and sensory deficits. Any part of the brachial plexus, and clinically any muscle or skin area can be involved, in all sorts of combinations. Sensory symptoms or pain tend not to correlate with the localisation of the paresis. [1
] It is precisely the recognition of this patchiness that is a very important clue to the diagnosis of the plexopathy in NA.
There are several overall patterns of paresis that occur more frequently than others. An upper brachial plexus distribution — the periscapular and perihumeral muscles — is most common, and occurs in 71% of the patients, either with (50%) or without (21%) involvement of the long thoracic nerve that leads to an unstable or winged scapula. Women have symptoms in a middle or lower brachial plexus distribution twice as often (23%) as men (11%), including symptoms that mainly affect the interosseus anterior nerve, with reduced pinch grip strength due to weakness of the long thumb and index finger flexors. Almost 80% of the patients have sensory deficits on examination, and NA can also present with pain and sensory symptoms only, frequently in the distribution of the lateral cutaneous antebrachial nerve [18
]. In 15% of the attacks there are signs of distal autonomic nervous system dysfunction (e.g. hand oedema, vasomotor instability). Additionally, nerves outside the distribution of the brachial plexus can also be involved, and this occurs in 56% of the attacks in HNA patients and in 17% of the attacks in the idiopathic form. They usually involve the lumbosacral plexus (usually in a lumbar trunk distribution), phrenic nerve or recurrent laryngeal nerve, but occasionally more ‘exotic’ structures such as the facial or abdominal nerves may be affected too.
One of the main pitfalls in the diagnostic phase is that the patients tend to complain about that part of their shoulder or arm that is most impaired by either pain or paresis, but hardly notice or give attention to other, lesser impairments in strength or sensory loss. About a third of the attacks have bilateral involvement that usually is asymmetrical in its severity, so here too one side can easily get overlooked. As a clinician one should be aware of this, and supplement the history by a meticulous physical examination that specifically pays attention to those muscles or skin areas the patient doesn’t mention. Omitting this increases the chance of either diagnostic errors (e.g. making the clinical diagnosis of a mononeuropathy or radiculopathy instead of a plexus lesion) or difficulty in correctly explaining certain symptoms, such as mistaking an unstable and downwardly displaced scapula for atrophy of the trapezius muscle, or its subsequent inability to move the arm overhead for a deltoid paresis.
For most clinicians the biomechanics of shoulder and arm movements are not part of daily practice. However, a little knowledge about the anatomical relations between the scapula, chest wall and humerus will greatly facilitate the understanding of why damage to certain parts of the plexus or peripheral nerves gives rise to impaired movements or joint complications that cannot be explained by paresis only.
It is important to realize that the scapula, through its glenoid cavity and acromial extension, forms half of the glenohumeral joint, i.e. the socket. [20
] For fluent movements of the arm it is necessary that the other half, the humeral head, remains approximately centered in its socket during the whole range of motion. This is normally achieved through two simultaneous mechanisms: rotation of the scapula to optimize the position of the glenoid cavity, and the action of several muscles that lift, depress or rotate the humeral head during abduction to ensure its optimal position (Figs. and ; reproduced with kind permission of K. van Nugteren from “Orthopedische Casuïstiek”). These two mechanisms must be able to work in a well-coordinated fashion because otherwise the humeral head will become impinged against the acromion, initially compressing elements of the interposed rotator cuff and subsequently making further movement mechanically impossible due to collision of both joint surfaces. The rotator cuff is made up of the brachii supraspinatus, subscapularis, teres minor and biceps tendons. At rest, the humeral head is also kept in place by the action of the deltoid muscle. Weakness < MRC 3 of this muscle can lead to sagging of the humeral head, creating a dynamic subluxation that depends on the residual strength and fatigue of this muscle. Vice versa if the deltoid is unaffected but the other cuff muscles are weak it can also lead to a dynamic impingement because of unopposed cranial elevation of the humeral head during deltoid contraction (Fig. ). The downward and lateral displacement of the scapula on the chest wall in case of serratus weakness also leads to an altered position of the glenoid and acromion at rest which makes the humeral head protrude — or subluxate — anteriorly, increasing the chance of impingement.
Transversal plane schematic of muscles keeping the humeral position optimized against the scapula
Coronal plane schematic of muscles that keeping the humeral position optimized against the scapula
For fluent abduction of the arm at a level of more than 80° elevation scapular support of the humeral head is indispensable. [16
] The arm has to be tilted up and outward by contraction of the supraspinatus and deltoid, which can only be fully achieved when the rotated humeral head is supported from below by the scapular socket to be moved further up and out. This means that when scapular movement is impaired, e.g. when the serratus anterior is < MRC 3, abduction and elevation will automatically be impaired above this level, even when the deltoid supplying the force for this movement is intact. When in doubt whether insufficient scapular movement or paresis of the deltoid is responsible for decreased arm abduction, one can attempt to fixate the scapula by compressing it against the chest while exerting counterpressure with the other hand placed underneath the patients arm anteriorly on the chest. In a case of pure serratus weakness the patient should now be able to lift the arm more easily to maximally 110° (to complete this motion to 170° elevation scapular movement is required).
The periscapular — serratus anterior, trapezius, rhomboid — muscles are not just important for abduction and elevation of the arm. They also serve an important postural function in stabilizing the scapula to provide a fixed support for any arm and hand movements in front of or behind the trunk. In this capacity they are activated in any body posture except lying supine. This means that even sitting or walking will cause symptoms when these muscles are paretic, especially when the arms own weight cannot be supported. When scapular instability and impaired motion is present patients often subconsciously attempt to compensate and increase stability by adducting the shoulder through contraction of the trapezius, in addition with lateroflexion of the trunk to the contralateral side to elevate the affected shoulder further and facilitate abduction by helping tilt the humeral head anteriorly. Although in itself at least partially effective, this strategy frequently leads to myalgia in the trapezius and paraspinal muscles due to strain.
Physical examination and pitfalls
Because NA attacks frequently involve the proximal or upper parts of the brachial plexus and therefore often influences shoulder biomechanics, there are some issues that merit special attention during the physical examination. It is convenient to start out with inspection of the shoulder blades, assessing their respective position on the chest wall. In case of serratus anterior or — much less frequently — trapezius weakness the shoulder blade sags a few centimeters downward (because of the weight of the arm attached) and in serratus palsy is usually also laterally displaced with the lower border medially rotated at rest. Winging, or a scapula alata, can be observed at rest but becomes more prominent with arm movement. If the affected shoulder appears to be higher than the unaffected side it is usually because the patient is compensating the downward scapular sagging by tensing the trapezius muscle; after testing the following relaxation will often show the downward displacement at rest.
In case of severe serratus anterior weakness the whole shoulder and arm can slide off the chest wall to a more caudal and anterior position. If one is unaware of this type of paresis, it can easily be mistaken for atrophy of the trapezius muscle because the edge of the shoulder is lower on that side. Sometimes we found the aberrant position of the scapula in combination with supraspinatus atrophy had given rise to the impression that a tumour protruded from the shoulder blade, while in fact it was the crest of the scapular spine.
Besides testing all the individual muscles or muscle groups for strength grading, it is also useful to inspect the so-called scapulothoracic and glenohumeral rhythm in NA patients. The first can be done by having the patient slowly abduct and elevate the arm in a coronal plane to the maximum of 170 degrees and then moving it downward in the sagittal plane, and vice versa. The normal scapular motion outwards and inwards during this movement should be fluent, but when impaired it becomes jerky, indicating weakness of the serratus, or less often also the rhomboids or trapezius. To test the glenohumeral joint for impingement, the patients flexed arm can gently be lifted to maximum abduction in the coronal plane by the examiner while keeping the other hand on the acromion and humeral head; there should be no crepitation, restriction of movement or local pain in part of the arc and the humeral head should not luxate (if necessary keep it fixed with your fingers to prevent this). Restricted capsular movement can be tested by passive arm exorotation, comparing the range of excursions to that of the contralateral side. During the previous tests it is also possible to note any mechanical or stretch-sensitivity of the affected nerves (a ‘Lasegue sign of the arm’).
As many patients experience musculoskeletal-type pain in both affected and compensating muscles in the months to years following an attack, which can sometimes be difficult to differentiate from the neuropathic pains occurring in NA, it is useful to differentiate these paintypes by palpating the bulk and attachments of these muscles to detect atrophy, hypertrophy and tenderness that points to strain. The levator scapulae (a part of which can be palpated just anterior to the trapezius at the point where the neck changes into the shoulder), its insertion on the occiput and scapular crest, and the insertion of the pectoralis minor on the coracoid process are often especially painful when the serratus anterior is weak.
Another pitfall we came across was the impression of deltoid or biceps weakness in cases with scapular instability. To avoid this influencing strength grading in these muscles, one may test the deltoid at about 70– 80 degrees lateral elevation, and have the patient firmly adduct the flexed elbow against the chest for resistance testing the of biceps, thereby limiting the role of scapular stability in these movements.
Because the phrenic nerve is involved in 7% (INA) to 14% (HNA) of the patients it is also useful to inspect the diaphragm for paradoxical breathing, i.e. the in- and upward movement of the abdominal wall during deep inspiration instead of the normal down- and outward displacement. When present this is strongly suggestive of (hemi-) diaphragmatic paralysis, and this could be confirmed by having the patient bend over or lie down supine to see if there is orthopnoea (which occurs due to even further restriction of the lung volume by upward movement of the abdominal contents in these positions).
As sensory deficits in NA are often restricted to relatively small skin areas, it is useful to compare pinprick sensation of both sides in both shoulders, arms and hands. Proprioceptic loss is very rare in NA, but one can find signs of vasomotor instability indicating focal autonomic system dysfunction in the forearm and hands of some 15% of the patients.