Clinical examination and diagnosis

Section Three  Adult brachial plexus palsies

CHAPTER

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14 

Clinical examination and diagnosis Aymeric Y.T. Lim FRCS (Glas), Sandeep J. Sebastin , MCh (Plast)

SUMMARY BOX 1. A brachial plexus injury can be defined by four elements, which are analogous to the four dimensions of space: breadth (number of roots involved), length (level), depth (severity), and time. 2. The two basic clinical presentations are a partial lesion (C5,6/C5,6,7) and a complete lesion (C5,6,7,8T1). 3. The evolution of brachial injuries has three important milestones. These are at immediate presentation, at completion of Wallerian degeneration (three weeks), and at onset of muscle degeneration (six months). 4. The history obtained from the patient should include questions relating to the energy of injury, the nature of the pain, the presence of reinnervation, and the social circumstances. 5. The examination of the patient is targeted to determine the extent of the injury (partial or complete); the level of the injury (condition of proximal muscles); the severity of the injury (avulsion or different grades of rupture); and the time related changes (reinnervation and atrophy).

Introduction The surgical treatment of brachial plexus injuries is relatively straightforward, once an accurate diagnosis is made. The assessment of brachial plexus injuries is fundamentally clinical and investigations serve essentially to confirm the clinical diagnosis. These injuries therefore need a clinician familiar with the anatomy. The complexity of this anatomic structure and the difficulty in remembering how to examine the more significant of the 59 muscles (this includes all the intrinsics and the diaphragm) supplied by the plexus are daunting to most specialists in the fields of hand, orthopedic, plastic, and neurosurgery. Most surgeons are therefore reluctant © 2012, Elsevier Inc DOI: 10.1016/B978-1-4377-0575-1.00014-9

6. The extent of injury is most easily determined by examining sensory dermatomes. 7. The level of injury is determined by testing muscles. The signs of avulsion include absent diaphragmatic function, absent serratus anterior and rhomboid function, and Horner’s syndrome. 8. An assessment of C7 root is important as it influences treatment decisions. This is done by assessing the C7 sensory dermatome and wrist extensor function (extensor carpi radialis brevis and longus). 9. A progressive Tinel’s sign and the tender muscle sign are indicators of reinnervation. 10. Regular and consistent documentation of follow-up visits is imperative. A good standard is measuring medical research council (MRC) grades, scapulohumeral angle for shoulder function, kilograms weights for elbow function, and range of motion for wrist and finger function.

to treat brachial plexus injuries. This chapter aims to make the assessment of these injuries less intimidating and to simplify the process of making an accurate clinical diagnosis. All that is required are three things; a revision of the anatomy of the plexus, revision of the technique of examining specific muscles, and a chart to document the result of the clinical examination. There is no simpler way to revise the anatomy than to read the paper by George Edwards (Figure 14.1).1 Muscle examination has been summarized well in section 4 of Tubiana et al.’s classic book Examination of the hand and wrist.2 Most charts3,4,5 are box based, and although they give valuable information as to the root levels of the muscles affected, they are difficult to use for someone who

Section Three  Adult brachial plexus palsies

is not familiar with brachial plexus anatomy. We use a chart based on the branches of the plexus. (Figure 14.2). Another concept we have found useful, when trying to describe a brachial plexus injury, is to relate it to the four dimensions of space (Figure 14.3).6 The first dimension to consider is the breadth of the lesion, which indicates the number of roots involved, the extent of the injury. The next dimension is length, which corresponds to the level of injury indicating whether the injury occurred at the roots, trunks or cords. The third dimension is the depth of the lesion, which refers to the severity of the injury, and this is understood in terms of the grades of nerve injury as classified by Sunderland.7 Time, the fourth dimension unmasks the true extent of the injury by allowing the recovery of partially injured roots, and can reveal reconstructive options.

STEP 1 (left side)

STEP 2

DS

STEP 3

6 7 8

LP

SS

C5

MC

Lateral cord

LT

Posterior cord USS TD LSS Medial cord

T1

M

Ax R

MP MBC MABC

U

Figure 14.1  How to draw a brachial plexus in 15 seconds (or less).

Brachial Plexus Injury - Sensory Assessment Chart Name: No.: Sex: Male / Female Date of birth: Date of injury: Side injured: Right / Left

C3 C4

C3 C4

C5

C5

T2

Horners: Present / Absent Tinels sign: Present / Absent Location Nature: Static / Advancing Deep pain: Supraspinatus: Present / Absent Deltoid: Present / Absent Biceps: Present / Absent

T2

C6

T1

T1

C6 MRC grading S0: No sensation S1: Deep pain S2: Superficial pain & some touch S3: S2 without over-response S3+: S2 with some 2 PD S4: Normal sensation

C6 C7

C8

Palmar Date:

Examiner:

A Figure 14.2  (A) Chart for sensory assessment of brachial plexus injuries. 174

C6 C8 C7

Dorsal

Clinical examination and diagnosis

14

Brachial Plexus Injury - Motor Function Assessment Chart Trapezius (XI Cr n.) Diaphgragm (Phrenic n.)

2 C5 C5

Levator scapulae (3,4,5)

4 Dorsal scapular n.

Rhomboides maj. & min. (4,5) 5 Suprascapular n.

C6 C6 Uppe

r trun

C7 C7

Middle

C8 C8 Low

Supraspinatus (4,5,6) Infraspinatus (5,6)

era

run

k

9 Medial pectoral n. 3 Pectoralis maj. (5,6) Pectoralis maj. Lmin. (6,7,8,1) Pectoralis (8,1) Long thoracic n. Pectoralis min. (7,8,1) Med. cut. n. arm Serratus ant. (5,6,7,8) Med. cut. n. forearm Subscapularis. (5,6,7) Latissimus dorsi (5,6,7) Teres major (5,6,7)

Po

ste

Medial

subscapular n. 8 Upper Upper subscapular n. Thoracodorsaln.n. 7 Thoracodorsal Lower subscapular n. 8 Lower subscapular n.

cor

d

rd

6 Axillary n.

Teres min. (5,6) Deltoid (5,6)

Radial n. 11

cord

13 Ulnar n.

PB (8,1) ADM (8,1) ODM (8,1) FDM (8,1) FPB (8,1) Dorsal interossei (8,1) Palmar interossei (8,1) Adductor pollicis (8,1) Lumbrical 3 & 4 (8,1)

0: No contraction 1: Palpable, no movement 2: Movement with gravity eliminated A. <50% of normal range B. >50% of normal range 3. Movement against gravity A. <50% of normal range B. >50% of normal range 4. Movement against resistance A. <50% of normal range B. >50% of normal range 5. Normal

B

rior

Brachialis (5,6) Coracobrachialis (6,7)

l co

FCU (7,8,1) FDP RF & LF (7,8,1)

Modified MRC Grading

Date:

10 Musculocutaneous n. Biceps Brachii (5,6)

9 Lateral Lateralpectoral pectoraln.n. Pectoralismaj. maj.U.(5,6) Pectoralis (5,6,7)

trunk

Lat

er t

T1 T1

k

Triceps (6,7,8,1) Brachioradialis (5,6) ECRL (5,6,7,8) ECRB (5,6,7,8) ECU (6,7,8) EDC (6,7,8) EDM (6,7,8) EPL (6,7,8) EIP (6,7,8)

12 Median n.

APL (6,7,8) EPB (6,7,8) Anconeus (7,8) Supinator (5,6) Brachialis (5,6)

PT (6,7) FCR (6,7,8) PL (7,8,1) FDS (7,8,1) FPL (7,8,1) FDP IF & MF (7,8,1) PQ (7,8,1) APB (6,7,8,1) OP (6,7,8,1) FPB sup. (6,7,8,1) Lumbrical 1&2 (7,8,1)

Examiner:

Figure 14.2, Continued  (B) Chart for motor assessment of brachial plexus injuries.

Clinical presentation

Figure 14.3  Relating a brachial plexus injury to the four dimensions of space.

There are two basic presentations, partial or complete. Partial lesions affect C5 and C6 roots, or C5, C6, and C7 roots, whereas the complete lesion affects all roots. Partial lesions affecting only the inferior roots are uncommon. The diagnostic picture may be complicated by incomplete recovery of certain muscles, but the basic picture is always partial or complete, and the surgeon will have to differentiate between these two clinical pictures. A surgeon may not be involved in the treatment of the patient from the onset. However, he needs to be aware of the three important milestones in the evolution of a brachial plexus injury. These milestones influence the clinical assessment, and determine treatment options. One should note however that there is an increasing body of evidence in favor of early exploration. 175

Section Three  Adult brachial plexus palsies

1. Immediate presentation is almost always in the context of an open injury or an avascular limb. There is usually no opportunity for a clinical assessment and a diagnosis is made based on intra-operative findings and stimulation of the cut ends of any severed nerves. A closed plexus injury may also be seen primarily by the treating surgeon. In such cases, a thorough clinical examination can be done, but one must resist the temptation to order nerve conduction studies and/or imaging studies like MRI/CT myelograms at this point. It takes time (2–3 weeks) for denervation fibrillation potentials to appear or a pseudo-meningocele to form.8 2. The next juncture occurs at three weeks and is defined by a biological event, namely, Wallerian degeneration, and its effect on previously innervated muscles. At this juncture, although the breadth (extent) and length (level) of the injury remains unchanged, radiological and nerve studies become valuable in defining depth (severity) of the lesion and unmasking time related features like re-innervation before they become clinically apparent. Recovery potentials appear before the return of perceptible contractions in the muscle (Grade 1).9 If the radiological investigation shows pseudo-meningocele formation, one would diagnose an avulsion type injury and consider early surgical intervention. On the contrary, if the nerve study shows evidence of muscle recovery (nascent potentials, a decrease in number of fibrillation potentials, or the appearance of an increased number of motor unit potentials), one would choose to observe. 3. The next critical stage is at six months and beyond. This indicates the end of the ‘golden period’10 for primary brachial plexus surgery (primary repair/grafting/nerve transfers etc.) and the key biological event is muscle degeneration.11 At this stage, neurotization is usually no longer indicated and treatment options are limited to tendon or free functioning muscle transfers or joint fusion. 176

Diagnosis History There are four main points to be acquired: 1. 2. 3. 4.

The The The The

energy and thus the severity of the injury nature and the radiation of the pain presence of reinnervation patient’s social circumstances

The objective of determining the events surrounding the accident is to establish the depth or severity of the injury. In developing nations, motorcycle accidents are the cause of a brachial plexus injury in 82% of cases, as in Songcharoen’s series of 520 cases.12 In developed countries, the causes are varied and sports related injuries are more common. ‘Burners’ or acute traction injuries caused by stretching of the upper plexus roots when tackling or falling affects up to 50% of football players.13 A high speed motorcycle accident on a highway is more likely to cause a severe nerve lesion than a scooter collision with a pedestrian on a city road. The energy transfer in an injured football player would be even less. The presence of associated injuries suggests high energy trauma. Associated injuries can be divided into two groups: peripheral and central. Peripheral injuries include limb fractures, rib fractures and hemothorax. Central injuries are neurological. They range from spinal cord injuries to cranial hematomas. They may result from avulsion of the ventral and dorsal rami of the roots of the spinal nerves. The pain that patients feel is neuralgic and is caused by interruption of the nerve. It is commonly described as burning or stabbing and distresses them greatly. Severe pain is often a sign of avulsion.14 Patients can be surprisingly specific about the radiation of this pain, and can even refer it to a dermatomal distribution. This symptom is an accurate indicator of the breadth of the lesion, or the root involvement. A C5/C6 avulsion injury will manifest in neuralgic pain in the lateral aspect of the arm, forearm, and thumb. It is important to ask the patient regarding any evidence of reinnervation. The patient will be able to tell you about a twitch in a muscle before you can see it and assign grade 1 power to it. Similarly it helps to teach a patient about Tinel’s sign. This is something that they can easily monitor. It involves them and motivates them in the process of recovery.

Clinical examination and diagnosis

Finally, the surgeon must try to understand the patient and evaluate their social support. The patient has just sustained a devastating injury and the loss of a limb. Their prognosis is based not just on the severity of injury, but on the patient’s outlook and his/her social circumstances. One needs to assess the patient’s motivation, their family support and job/financial constraints. Much of the pre- and post-operative care of patients with brachial plexus injuries involves practical and social counseling and the management of pain.

Physical examination It is at this stage that the physician confirms his diagnosis and sets a treatment plan. The clinical examination of a patient with a brachial plexus injury is targeted towards answering four questions. 1. What is the extent of the injury? (Is it partial or complete?) 2. What is the level of the injury? (Is the proximal musculature preserved?) 3. What is the severity of the injury? (Is it an avulsion or a rupture?) 4. What are the time-related changes? (Has there been any recovery?) This sequence of thought is repeated through two cycles, once during the process of inspection, and again during muscle examination.

A

14

Inspection With the patient’s torso completely exposed, the examiner looks for wasting, the muscle desolation wrought by the nerve injury. He assesses the extent by systematically scanning myotomal sectors. The C5 sector includes supraspinatus, infraspinatus and the deltoid; the C6 sector, the biceps, and C7, the triceps and the forearm extensors. C8 and T1 lesions are apparent when the hand is flail and digital flexor or intrinsic function is absent. Skip lesions in plexus injuries almost never occur and sparing of a myotomal sector only occurs at the cranial or caudal end of the roots. It is difficult to precisely define the level of the lesion by inspection. However the presence of proximal musculature is a good indicator that the lesion is at or beyond the cords. It is important to understand that a nerve root avulsion does not indicate just the level of the injury, but also the severity. This has profound implications for reconstruction, both in terms of timing and options. Avulsion of the upper roots (C5/C6 and/or C7) is manifested in scapular winging and wasting of the trapezius, whereas avulsion of the lower roots (C8/T1) is revealed by a Horner’s sign. If a patient presents with a flail upper limb, winging of the scapula and a Horner’s sign, it is evident that he has an avulsion injury of all the roots (Figure 14.4 A and B). Another indicator of

B Figure 14.4  (A) Total palsy front view. (B) Total palsy back view. 177

Section Three  Adult brachial plexus palsies

avulsion is cervical scoliosis, following disruption of the posterior branches of the spinal nerve going to the cervical paravertebral muscles (Figure 14.4B).15 The moisture of the skin can also give useful information about the lesion. Dry skin in an anaesthetic area suggests a post-ganglionic lesion; on the contrary, a normal moist skin suggests a pre-ganglionic lesion. Sliding a plastic pen over the skin of the affected limb and comparing it to the normal side can be used to test sweating function of the skin.16 Other indicators of a severe lesion are associated injuries and scars. Finally, the way the patient is able to cope with the paralysis, take on or off his/her clothes and deal with normal activities is important to note (Video 1: patient coping with ADL’s). The older the lesion, the easier it is to make a complete diagnosis just by inspecting the patient.

Palpation The examination should always start by testing dermatomes. This is the easiest way to determine the extent of the lesion and gives important and reliable information. The key to remembering the dermatomal map is that the middle finger is supplied by the middle root that is C7. The rest of the map can then be worked out quite logically by working ones way, cranially and caudally. C6 supplies the thumb, C5 the lateral arm and forearm, C8 supplies the little finger and T1, the medial forearm (Figure 14.2A). There are four notes of caution. The medial aspect of the arm is supplied by T2, the inter-costobrachial nerve. The index finger is usually supplied by C7, as donor morbidity from cross C7 transfers has demonstrated.17 Incomplete nerve lesions or lesions affecting C5 may not give complete anesthesia of the dermatome. Over time, adjacent neuro­ tization may blur the edges of the dermatomal territories. Once the extent of the injury has been determined, the next step is to determine the level of the injury. This is done by muscle examination. The medical research council (MRC) grading has been the standard for assessment of motor power.18 Though it is simple, each MRC grade represents a wide range, and one cannot quantify a difference between muscles in the same grade or an improvement in the same muscle on

178

follow-up.19 We have modified the MRC grade for use in our practice (Figure 14.2B). In addition, we found it difficult to use the standard manual muscle strength testing techniques in brachial plexus patients, especially in the shoulder girdle muscles. We therefore modified the techniques to make it more suitable for use in brachial plexus patients, and to enable a major part of the examination in the sitting position. Although palpation of the muscle being tested is not required for assessment of motor grades 2–5, it is prudent to assess activity in the muscle being tested at all times. Narakas describes five levels: the roots; the anterior branches of the spinal nerves, the primary trunks, the secondary cords and the peripheral nerves.20 More practically, there are two important levels: avulsions and ruptures. Avulsions can only be treated with nerve transfers, whereas with ruptures, the option of nerve repair with grafting exists. There are many muscles to test and all muscles have more than one root origin.21 A consistent sequence of examination is thus necessary. Intuitively, it makes sense to ‘walk’ the nerves (Figure 14.5). This is only possible if there is a clear picture of the anatomy in one’s head. In the beginning, it is always helpful to have a diagram at hand and record the findings in a chart (Figure 14.2B). It is logical to begin by ‘walking’ the C5 root, the most cranial and proximal part of the plexus. The first branch is the phrenic nerve. The clinical test for a raised hemidiaphragm is percussion of the chest wall in inspiration and expiration. There should be an additional two intercostal spaces of resonance with inspiration. This test is hard to administer accurately, and a quick glance at the chest X-ray will usually give the required information accurately and more efficiently (Figure 14.6). The next branch of C5 is the long thoracic nerve, which also receives contributions from C6, C7, and occasionally C8. These branches arise very proximal, near the foramina. Paralysis or weakness of the serratus anterior, supplied by this nerve is strongly indicative of an avulsion of one or all of the roots of supply. It is impossible to test the serratus anterior in brachial plexus patients in the conventional manner by asking them to push against a wall. To overcome this, one has to use a modified test. The test is performed in a sitting position with both arms outstretched on a table in front

Clinical examination and diagnosis

14

1 Sensory examination 2 Phrenic n. Diaphgragm

4 Dorsal scapular n. Rhomboides maj & min (4,5)

C5

5 Suprascapular n. Supraspinatus (5,6) Infraspinatus (5,6)

C6

Uppe r trrun k

C7 C8

Middle

T1

unk

al

9 Medial pectoral n. Pectoralis maj. (5,6) Pectoralis min. (8,1)

r co

rd

Med

co

erio

10 Musculocutaneous n.

6 Axillary n. Teres min. (5,6) Deltoid (5,6)

ter

Pos t

3 Long thoracic n. Serratus ant. (5,6,7)

Lateral pectoral n. Pectoralis maj. (5,6)

La

Low er tr

9

trunk

rd

11 Radial n.

ial c

ord

8 Upper and lower subscapular n. 7 Thoracodorsal n. Subscapularis. (5,6,7) Latissimus dorsi (5,6,7) Teres major (5,6)

13 Ulnar n.

12 Median n.

1 Sensory examination 2 Phrenic n. (Diaphragm)

4 Dorsal scapular n. (Rhomboides major and minor) 3 Long thoracic n. (Serratus anterior)

5 Suprascapular n. (Supraspinatus and infraspinatus) Thoracodorsal n. 7 (Latissimus dorsi) 6 Axillary n. (Teres minor and deltoid)

9 Medial and lateral pectoral n. (Pectoralis major and minor)

11 Radial n.

13 Ulnar n.

12 Median n. 8 Upper and lower subscapular n. (Subscapularis and teres major)

10 Musculocutaneous n. (Biceps brachii)

Figure 14.5  Walking the nerves. Top: Order of examination of various muscles innervated by the brachial plexus. Bottom: Simplified path.

Figure 14.6  CXR to show phrenic nerve palsy.

179

Section Three  Adult brachial plexus palsies

(Figure 14.7A). The examiner uses his thumb and fingers to track the movement of the scapula and feel the serratus (Figure 14.7A). The patient is asked to project his entire extremity forward and the examiner feels for the movement of the scapula away from the midline (protraction)(Figure 14.7B). If the patient is able to move, it indicates M2 grade (movement with gravity eliminated). If he is unable to move, the examiner feels for a palpable contraction under his fingers (M1), and no contraction would indicate M0. If the patient has M2 power, the examiner offers resistance with his free arm over the anterior aspect of the shoulder to determine M4 (some movement with resistance) or M5 (normal) (Figure 14.7C). If the patient is unable to move against resistance, he needs to be examined in the

supine position. The examiner supports his upper limb with one hand and feels the scapula with his other hand. The patient is again asked to move his limb forward, and if he is able to do, it indicates M3 (movement against gravity)(Figure 14.7D). There are many subtleties to winging, and paralysis of the trapezius and/or the rhomboids can also cause winging. In a serratus anterior palsy, the inferior angle of the scapula is separated from the thorax and pulled backwards to the spine (Figure 14.7E). On the other hand, in trapezius palsy, the scapula moves outwards and forwards (Figure 14.7F). When both muscles are paralysed, the entire medial border is lifted up. The last branch from the C5 root is the dorsal scapular nerve and this innervates the rhomboids

Long thoracic nerve to serratus anterior C5-C7 C5 C6 C7 C8 T1

Serratus anterior

A Figure 14.7  Assessment of serratus anterior. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with long thoracic nerve highlighted in red. Bottom left: Origin and insertion of serratus anterior. Bottom right: Relation of examiners hand to the scapula. 180

Clinical examination and diagnosis

B

14

C

Figure 14.7, Continued  (B) Examination for motor grades 0, 1 and 2. (C) Examination for motor grades 4 and 5. (D) Examination for motor grade 3 in supine position. (E) Winging caused by serratus anterior palsy. (F) Winging caused by trapezius palsy.

D

E

and the levator scapulae. The ventral primary ramii of both C4 and C5 contribute towards this nerve. The rhomboides major arises from the spinous processes of the T2 to T5 vertebrae, and it inserts on the medial border of the scapula, from the level of the scapular spine to the scapula’s inferior angle. It is a difficult muscle to test as it lies deep to the trapezius. The classically described test for the rhomboids involves placing the patient’s palm

F

facing outwards on his lower back and asking the patient to push outwards against resistance. We have found it difficult to place the palm in the above position in patients with brachial plexus injury. The rhomboids are antagonists of the serratus anterior, and therefore tested by resisting retraction of the scapula. We perform a test in the sitting position with the patients shoulder abducted to 90 degrees, elbow flexed to 90 degrees, and 181

Section Three  Adult brachial plexus palsies

palm facing downwards. This position is maintained by a table of appropriate height kept on the side to be examined (Figure 14.8A). In order to relax the trapezius, the test is performed with the neck extended and laterally flexed toward the tested side, and the face turned toward the opposite side.22 The examiner’s thumb is placed on the medial border of the scapula at the level of the spine. The patient is then asked to push his arm/ shoulder backward and the examiner feels for the movement of the scapula towards the midline (retraction). The examiner’s thumb can feel the contraction of the rhomboids and the scapula slips medially under the thumb (Figure 14.8B). If the patient is able to move, it indicates M2 grade (movement with gravity eliminated). If he is unable to move, the examiner feels for a palpable contraction under his thumb (M1), and no contraction would indicate M0. If the patient has M2 power, the examiner offers resistance with his free arm over the posterior aspect of the shoulder to determine M4 (some movement with resistance) or M5 (normal)(Figure 14.8C). If the patient is unable to move against resistance, he needs to be

examined in the prone position. The patient is asked to lie down with his arms by his side and palms facing upwards. He is then asked move his shoulder backwards and the examiner feels the medial border of the scapula for movement (Figure 14.8D). If movement is felt, it indicates M3 (movement against gravity). The serratus anterior and rhomboids are difficult muscles to test. The most direct way of testing these or any muscle is to grade the effect that they have on the bone upon which they are inserted. Thus, just as triceps function is assessed by its effect on the ulna, the serratus anterior and rhomboid functions are best assessed by their effect on the scapula. Proceeding distally, the C5 root joins the C6 root to form the upper trunk and the first branch from the upper trunk is the suprascapular nerve. It receives contributions from both roots, and supplies the supraspinatus and infraspinatus. It is not uncommon for this nerve to be injured at two levels, and at this stage it costs nothing to percuss the nerve from Erb’s point (junction of C5 and C6) to the scapular notch (Figure 14.9A). Abnormal

Dorsal scapular nerve to rhomboids C5 C5 C6 C7 C8 T1

A

Trapezius Upper

Levator scapluae

Middle Lower

Rhomboid minor Rhomboid major

Figure 14.8  Assessment of the rhomboids. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with dorsal scapular nerve highlighted in red. Bottom left: Origin and insertion of trapezius and rhomboides. Bottom right: Relation of examiners hand to the scapula. 182

Clinical examination and diagnosis

B

C

D

Figure 14.8, Continued  (B) Examination for motor grades 0, 1 and 2. (C) Examination for motor grades 4 and 5. (D) Examination for motor grade 3 in prone position.

Supraspinatus

14

Suprascapular nerve To Suprapinatus C5-C6

C5 C6 C7 C8 T1

Superior transverse scapular ligament Supraspinatus muscle (cut)

Suprascapular nerve

Suprascapular artery Scapular notch Acromion Inferior transverse scapular ligament Teres minor muscle Quadrangular space Deltoid muscle

Infraspinatus muscle (cut) Triangular space

A

Teres major muscle

Triceps hiatus Long head, triceps brachii Lateral head, triceps brachii

Figure 14.9  Assessment of supraspinatus. (A) Top left: Origin and insertion of supraspinatus. Top right: Brachial plexus with suprascapular nerve highlighted in red. Bottom left: ‘X’ marking likely points of nerve compression or injury. Bottom right: Anatomy of the suprascapular nerve. 183

Section Three  Adult brachial plexus palsies

B

C

D

E

Figure 14.9, Continued  (B) Position of patient and examiner. (C) Examination for motor grade 3. (D) Examination for motor grades 4 and 5. (E) Examination for motor grades 0, 1, and 2.

tenderness or a positive Tinel’s sign at the notch would be an indication for distal exploration. The difficulty in examining the supraspinatus lies in the fact that its location and function are masked by two large muscles, the trapezius and the deltoid respectively. The upper and middle fibers of the trapezius completely cover the supraspinatus. In order to relax the trapezius, the patent is examined with neck extended and laterally flexed toward the tested side, and the face turned toward the oppo­ site side.22 The supraspinatus initiates abduction, whereas the deltoid continues and maintains it. It is thus tested by preventing the initiation of abduction. The patient is examined in a sitting position with his elbow flexed and arms internally rotated and by his sides (Figure 14.9B). He is then asked to 184

attempt abduction as the examiner palpates the supraspinatus (Figure 14.9C). If he is able to move the limb, he is graded as M3 (no resistance, but movement against gravity). The examiners then offers resistance over the dorsum of the elbow with his free hand to determine, if the patient has M4 (some movement with resistance) or M5 (normal) power (Figure 14.9D). If the patient is unable to move, he is put into the supine position, with his arm by his side, supported by the bed. He is then asked to abduct his shoulder and graded M2 if he is able to move it, M1 if he is unable to move it but a palpable contraction is felt, and M0 if no contraction is felt (Figure 14.9E). The other muscle innervated by the suprascapular nerve is the infraspinatus. It is the more powerful

Clinical examination and diagnosis

14

Suprascapular nerve To Infraspinatus C5-C6

C5 C6 C7 C8 T1

A

Infraspinatus Teres minor

B

C

D

Figure 14.10  Assessment of the infraspinatus and teres minor. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with suprascapular nerve highlighted in red. Bottom left: Origin and insertion of infraspinatus and teres minor. (B) Examination for motor grade 3. (C) Examination for motor grades 4 and 5. (D) Examination for motor grades 0, 1 and 2 in prone position.

of the two external rotators of the humerus, the other being the teres minor (innervated by the axillary nerve). It is not possible to test these muscles separately, and therefore the external rotators are tested as a group. The patient is examined in the sitting position with the shoulder abducted to 90 degrees, elbow flexed to 90 degrees, and palm

facing downwards. This position is maintained by a table of appropriate height kept on the side to be examined (Figure 14.10A). The examiner stands besides the patient, palpates the infraspinatus using his fingers over the body of the scapula below the spine in the infraspinous fossa, and the teres minor on the inferior margin of the scapula along the 185

Section Three  Adult brachial plexus palsies

axillary border of the scapula using his thumb. The patient is then asked to move his forearm upward through the range of external rotation. If the patient is able to move, it indicates M3 grade (movement against gravity) (Figure 14.10B). If the patient has M3 power, the examiner offers resistance with his free arm over the dorsum of the wrist to determine M4 (some movement with resistance) or M5 (normal) (Figure 14.10C). If he is unable to move, the patient is put into the prone position with the head turned to the test side, trunk at the edge of the bed, the limb hanging loosely from the shoulder in neutral rotation, and palm facing the bed (Fig. 14.10D). The patient is asked to attempt external rotation of the shoulder as the examiner palpates the infraspinatus and teres minor. If the patient is able to move, it indicates M2 grade (movement with gravity eliminated). No movement, but a palpable contraction would indicate M1, whereas no contraction would indicate M0. The examiner then logically walks to the posterior cord, to complete the examination of the axillary nerve by testing the deltoid. The key to testing the deltoid is to eliminate the action of the supraspinatus. The patient is in the sitting position with the shoulder abducted 90 degrees, elbow extended, and palm facing downwards. This position is maintained by a table of appropriate height kept on the side to be examined (Figure 14.11A). The anterior, middle, and posterior portions of the deltoid have to be tested separately. The examiner palpates the respective potions of the deltoid with one hand and offers resistance/support (as needed) with the other hand. The anterior portion is tested first. The examiner stands besides the patient, puts the patients shoulder into a position of forward flexion and asks him to abduct the shoulder (Figure 14.11B). If the patient is able to move, it indicates M3 grade (movement against gravity). If the patient has M3 power, the examiner offers resistance with his free arm over the lateral aspect of the elbow to determine M4 (some movement with resistance) or M5 (normal) (Figure 14.11C). If he is unable to move, the patient is asked to lie on his unaffected side and the examiner supports the patients arm with his free hand (Figure 14.11D). The patient is again asked to attempt abduction of the shoulder. If the patient is able to move, it indicates M2 grade (movement with gravity eliminated). No movement, but a palpable contraction would indicate M1, while no contraction would indicate M0. The middle portion of the 186

deltoid is examined in a similar manner except that there is no forward flexion of the shoulder to determine grades 3, 4 and 5, (Figure 14.11, E and F) and the patient is examined in supine position to determine grades 2, 1 & 0 (Figure 14.11G). The posterior portion of the deltoid is examined in the same position as the middle portion, but instead of abduction, the patient is asked to slide his arm backwards. If the patient is able to do so, it indicates M2 grade (movement with gravity eliminated). The examiners then offers resistance to this backward movement with his free hand at the elbow to determine M4 (some movement with resistance) or M5 (normal) (Fig. 14.11H & Fig. 14.11I). If the patient is unable to move, but a palpable contraction is felt, it indicates M1 grade and the absence of contraction would mean M0 grade. Movement against gravity (M3) is assessed in the prone position with the forearm hanging down (Figure 14.11J). Reinnervation occurs first in the posterior portion, then the lateral and finally the anterior portion.23 The examination of the posterior cord is completed by testing the subscapularis, latissimus dorsi, and the teres major. All of them adduct and internally rotate the arm. In addition, the latissimus dorsi and teres major also extend the shoulder. The subscapularis is examined with the patient is examined in the sitting position with the shoulder abducted to 90 degree supported by a table, and the forearm hanging over the edge of the table with the palm facing backwards (Figure 14.12A). The patient is asked to move his arm backwards and upwards. If he is able to do so, it indicates M3 grade (movement against gravity) (Figure 14.12B). The examiner then offers resistance against the volar side of the forearm just proximal to the wrist with one hand, and counterforce is applied at the elbow with his other hand to determine M4 grade (some movement with resistance) and M5 (normal) (Figure 14.12C). If he is unable to do so, the patient is examined in the prone position with the entire arm hanging freely by the side of the patient and the palm facing the patient. The examiner palpates the tendon of the subscapularis deep in the central area of the axilla and asks the patient to internally rotate his arm so that the palm faces away from him (Figure 14.12D). If he is able to do so, it indicates M2 grade (movement with gravity eliminated). No movement, but a palpable contraction would indicate M1, whereas no contraction would indicate M0.

Clinical examination and diagnosis

14

Middle Anterior

Posterior

A

C5 C6 C7

Axillary nerve To Deltoid (C5-C6)

C8 T1

B Figure 14.11  Assessment of the deltoid. (A) Top left: Position of patient and examiner for testing mid portion of deltoid. Top right: Origin and insertion of three portions of deltoid. Center left: Position for examination of anterior portion of deltoid. Center right: Testing of posterior portion of deltoid. Bottom left: Brachial plexus with axillary nerve highlighted in red. (B) Examination of anterior portion of deltoid for motor grade 3.

187

Section Three  Adult brachial plexus palsies

C

D

E

F

G

H

I

J

Figure 14.11, Continued  (C) Examination of anterior portion of deltoid for motor grades 4 and 5. (D) Examination for anterior portion of deltoid for grades 0,1, and 2 in lateral position. (E) Examination of middle portion of deltoid for motor grade 3. (F) Examination of middle portion of deltoid for motor grades 4 and 5. (G) Examination of middle portion of deltoid for motor grades in supine position for grades 0, 1, and 2. (H) Examination for posterior portion of the deltoid for grades 3. (I) Examination for posterior portion of the deltoid for grades 4 and 5. (J) Examination of the posterior portion of the deltoid in prone position for motor grades 0, 1, and 2.

188

Clinical examination and diagnosis

14

C5 C6 C7 C8 T1

Subscapular nerve (Upper) To Subscapularis C5-C6

A

Subscapularis

B

C

D

Figure 14.12  Assessment of the subscapularis. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with upper subscapular nerve highlighted in red. Bottom: Origin and insertion of subscapularis. (B) Examination for motor grade 3. (C) Examination for motor grades 4 and 5. (D) Examination for motor grades 0, 1, and 2.

189

Section Three  Adult brachial plexus palsies

C5 C6 C7 C8 T1

Thoracodorsal nerve To Latissimus dorsi C6-C8 A

Teres major Latissimus dorsi

B Figure 14.13  Assessment of the latissimus dorsi. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with thoracodorsal nerve highlighted in red. Bottom: Origin and insertion of latissimus dorsi and teres major. (B) Examination for motor grade 3.

The latissimus dorsi is examined in the sitting position with the patients arm hanging freely by his side and the palm facing backwards. The muscle is palpated on the lateral aspect of the thoracic wall just above the waist (Figure 14.13A). The patient is asked to extend and adduct his arm. If he is able to do so, it indicates M3 grade (movement against gravity) (Figure 14.13B). The examiner then offers resistance on the volar aspect of the forearm against the direction of extension (Figure 14.13C). Some movement against resistance would indicate M4 grade and M5 would be normal. If the patient is unable to move, he is asked to lie on his unaffected side, with his 190

arm at his side and palm facing backwards. He is then asked to extend his arm, keeping his shoulder adducted. The examiner supports his arm with one hand, and palpates the latissimus dorsi with his other hand. If the patient is able to move his arm, it indicates M2 (movement with gravity eliminated). No movement, but a palpable contraction would indicate M1, whereas no contraction would indicate M0 (Figure 14. 13D). The teres major is palpated on the lateral border of the scapula just below the axilla and forms the lower posterior rim of the axilla (Figure 14.14). It is difficult to test the teres major in isolation from the subscapularis and the

Clinical examination and diagnosis

14

D

Figure 14.13, Continued  (C) Examination for motor grades 4 and 5. (D) Examination for motor grades 0, 1 and 2 in prone position.

C

C5 C6 C7 C8 T1

Lower Subscapular nerve To Teres major C5-C6

Teres major

Figure 14.14  Assessment of the teres major. Top left: Position of patient and examiner. Top right: Brachial plexus with lower subscapular nerve highlighted in red. Bottom: Origin and insertion of teres major. 191

Section Three  Adult brachial plexus palsies

C5

Lateral Pectoral nerve to clavicular part of pectoralis major C5-C6

C6 C7 C8 T1

A

Medial Pectoral nerve to sternocostal part of pectoralis major C6-T1

Pectoralis major

B

C

Figure 14.15  Assessment of the pectoralis major. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with medial and lateral pectoral nerves highlighted in red. Bottom: Origin and insertion of pectoralis major. (B) Examination of the upper portion for motor grades 0, 1, and 2. (C) Examination of the upper portion for motor grades 4 and 5.

192

Clinical examination and diagnosis

D

F

latissimus dorsi, and its function is best felt when testing for these two muscles (Figure 14.14). This completes the examination of the posterior cord. The integrity of the medial and lateral cords is verified by testing the pectoral muscles, and the biceps. The upper (clavicular) portion of the pectoralis major is innervated by the lateral pectoral nerve (branch of lateral cord), whereas the lower (sternal) portion is innervated by the medial pectoral nerve (branch of medial cord). Both portions of the pectoralis major muscle should be tested separately, because they have different nerve root innervations. The upper portion of the pectoralis major is tested with the patient in the sitting position with the shoulder abducted 90 degree, elbow partially flexed, and palm facing downwards. This position is maintained by a table of appropriate height kept on the side to be examined (Figure 14.15A). The examiner palpates the clavicular fibres of the pectoralis major under the medial half of the clavicle, and asks the patient to move his arm horizontally across the table (Figure 14.15B). If he is able to do so, it indicates M2 grade (movement with gravity eliminated). The examiner then

14

E

Figure 14.15, Continued  (D) Examination of the upper portion for motor grade 3 in supine position. (E) Examination of the lower portion for motor grades 0, 1, and 2. (F) Examination of the lower portion for motor grades 4 and 5.

offers resistance on the volar aspect of the elbow against the direction of movement (Figure 14.15C). Some movement against resistance would indicate M4 grade and M5 would be normal. No movement, but a palpable contraction would indicate M1, whereas no contraction would indicate M0. If the patient is unable to move against resistance, he needs to be examined in the supine position with the examiner supporting his arm to determine if he has M3 grade (movement against gravity) (Figure 14.15D). The lower (sternal) portion of the pectoralis major is also tested in the sitting position. The sternal portion of the muscle is palpated on the upper aspect of the chest wall just medial to the shoulder joint. The patients arm is supported on a table with the shoulder in 75–90 degrees abduction and slight forward flexion with the elbow flexed (Figure 14.15E). The patient is asked to move his hand diagonally down and in towards the opposite hip (Figure 14.15E). If he is able to do so, it indicates M2 grade (movement against gravity). The examiner then offers resistance against the volar aspect of the direction of movement (Figure 14.15F). Some movement 193

Section Three  Adult brachial plexus palsies

C5 C6 C7 C8 T1

A

Medial Pectoral nerve to sternocostal part of pectoralis major C6-T1

B Pectoralis minor

Figure 14.16  Assessment of the pectoralis minor. (A) Top left: Position of patient and examiner. Top right: Brachial plexus with medial pectoral nerve highlighted in red. Bottom: Origin and insertion of pectoralis minor. (B) Examination for motor grades 0, 1, and 2.

against resistance would indicate M4 grade and M5 would be normal. No movement, but a palpable contraction would indicate M1, whereas no contraction would indicate M0. If the patient is unable to move against resistance, he needs to be examined in the supine position with the examiner supporting his arm to determine if he has M3 grade (movement against gravity). Although testing both portions of the pectoralis major is sufficient to evaluate the medial and lateral pectoral nerves, it is useful to assess the function of the pectoralis minor separately. This may enable its use as a tendon transfer or ensure success of a medial pectoral nerve transfer. The tendon of the muscle can be palpated over the anterior aspect of the shoulder joint under the pectoralis major muscle. The pectoralis minor muscle is tested in the sitting position with the patient’s arm hanging freely by his side (Figure 14.16A). The patient is asked to thrust his shoulder forward with the arm at his side (Figure 14.16B). If he is able to do so, it indicates M2 grade (movement with gravity eliminated). No movement, but a palpable contraction 194

would indicate M1, whereas no contraction would indicate M0. The examiner then offers resistance on the anterior aspect of the shoulder, downwards against the direction of movement (Figure 14.16C). Some movement against resistance would indicate M4 grade and M5 would be normal. If the patient is unable to move against resistance, he needs to be examined in the supine position with his arms by his side to determine if he has M3 grade (movement against gravity) (Figure 14.16D). The lateral cord examination is completed by examining the biceps to evaluate the musculocutaneous nerve. The examiner is then left with examination of the peripheral nerves and the radial, median and ulnar nerves are examined in turn.

Signs of reinnervation It is the passage of time, more than the most exhaustive examination or the most sensitive investigation that confirms the extent, level and the severity of a lesion. Evidence of steady recovery is an excellent prognostic sign, whereas a silent and flail arm is the

Clinical examination and diagnosis

14

advance of the regenerating axons down the nerve can be followed by studying the advance of the Tinel sign. There is an element of unreliability as some of these regenerating axons are not on their way to any target. In general, a strongly positive Tinel sign over a lesion soon after injury indicates rupture or severance. If a nerve repair is going to be successful, the centrifugally moving Tinel sign is persistently stronger than that at the suture line, and if the repair is going to fail, the Tinel sign at the suture line remains stronger than that at the growing point. A failure of distal progression of the Tinel sign in a closed lesion indicates rupture or other lesion impeding regeneration.25 Although the Tinel sign is difficult to interpret in brachial plexus lesions, Landi et al.26 have enumerated the value of Tinel sign as follows:

C

D Figure 14.16, Continued  (C) Examination for motor grades 4 and 5. (D) Examination for motor grade 3 in supine position.

expression of a deep and an extensive injury. The return of motor and sensory function is the con­ clusion of reinnervation. This is preceded by two important signs that are particularly useful when assessing return of function after neurotization. The first is Tinel’s sign. This was described separately by Tinel and Hoffman in 1915.24 Tinel sign is elicited by lightly percussing along the course of the affected nerve from distal to proximal. When the finger percusses over the zone of regenerating fibers, the patient will announce the sensation of pins and needles, which may be quite painful, into the cutaneous distribution of the nerve. The

1. No response at all implies preganglionic damage to the injured root assessed. 2. Local pain implies that there is an underlying cervical plexus lesion that is recovering, or that there is residual contrast medium in a pseudomeningocoele. 3. Pure Tinel sign means that that the lesion is in anatomic continuity and sequential recordings can demonstrate progression of recovery. Roots C5 and C6 are the most superficial and Tinel sign can easily be elicited. C7, C8 and T1 are deeper and difficult to assess. 4. The neuroma sign is positive when pain is elicited in the distribution of the nerve when tapped. This sign means disruption of continuity of the whole nerve. The second and less well recognized sign is the tender muscle sign. This tenderness is elicited by squeezing the muscle that is being examined. The pain felt is distinctive and is different from a skin sensation. It is feels like a deep ache and always produces a characteristic wince in the patient. This pain can be differentiated by doing a similar squeeze on the normal side (Video 2: tender muscle sign). It is not dissimilar to the pain experienced when having a muscle cramp. Early on, it may be referred to the neurotizing area, i.e. chest wall after intercostals to biceps transfer. It follows a Tinel sign that has progressed into a muscle and appears before evidence of grade 1 power. There are three clearly defined phases during the process of nerve and muscle recovery. In the first phase, one follows the Tinel sign down the course 195

Section Three  Adult brachial plexus palsies

of a nerve, into the muscle. In the second phase, once the axons reach the muscle and establish a connection with the brain, one can elicit the tender muscle sign. The third phase is observing for the various grades of the MRC score. For the purposes of documenting recovery of a lesion, spontaneous or after nerve transfer or a functional muscle reconstruction, it is better to use more precise measures. These are, for the shoulder, scapulohumeral angle; for the elbow, kilogram weights, and for the wrist and fingers, ranges of motion.

Inventory of reconstructive options A final part of the examination is the cataloging of reconstructive options. Scars in the intercostal spaces from chest tube insertion would preclude the use of that intercostal nerve for neurotization. A well recovered latissimus dorsi or a good long head of the triceps give options for the reconstruction of elbow flexion.27 The best reconstruction for elbow flexion is the Oberlin nerve transfer.28 It gives the best results, has the least morbidity and can even be done as a day surgery procedure. However, the presence of a good ulnar nerve is required before an Oberlin transfer can be considered. This is most reliable when the C7 root is intact, as patients with avulsion of C5,6,7 are likely to present with grade 2 or grade 3 lesion of the C8T1 roots.29 It is thus important to ascertain the quality of the C7 root. First check the C7 sensory dermatome by assessing the sensation in the middle finger. Next check the C7 myotome. This is made difficult as there are more than 20 muscles with shared innervations from the C7 root. The most reliable way of confirming an intact C7 root is to look at proximally innervated muscles, which are not innervated beyond the C6 root. These are the deltoid, biceps and brachioradialis. If these are absent in the presence of wrist extensors (extensor carpi radialis brevis and longus), then the partial lesion that is present probably involves only C5 and C6 roots. If these are absent along with absence of wrist extensors, then C7 root is likely to be involved and one should be cautious about using the Oberlin procedure.29

Measuring results Accuracy and reproducibility of results is vital. Despite its drawbacks, the MRC classification of muscle recovery and sensory loss is standard. Its 196

primary drawback is its lack of sensitivity. This has been eloquently elaborated by Narakas ‘the power of a muscle to lift the arm against gravity is much more than that to move a finger.’ However in the absence of a better system, one must use the MRC system in a consistent manner. There is no place for the commonly used plus or minus suffixes as they are not reproducible and vary widely from examiner to examiner, especially in the rather subjective region of power grip from 3+ to 4-. We have modified the MRC system in our practice to log an improvement in the range of motion (Figure 14.2B). This also allows for an accurate assessment of reinnervation, and the available reconstructive options.

Conclusion The surgical problem in a brachial plexus reconstruction is not dissimilar to the strategy required in a chess end-game. There are only a limited number of options for reconstruction, intra-plexal neurotization, and nerve transfers. For complete lesions, a maximum of 4 or 5 transfers are possible. In incomplete lesions, there are more possibilities and an active and accurate search must be performed to detect intact or recovering nerves. With a limited number of options, a useful result must be obtained for the patient. It is thus vital to establish the presence and quality of these options. That is the main purpose of clinical examination.

References 1. Edwards Jr GS. How to draw a brachial plexus in 15 second (or less). ASSH Correspondence Newsletter:103, 1991. (http://www.assh.org/Members/GetInvolved/ Lending%20a%20Hand/Documents/How_to_Draw_ Brachial_Plexus.pdf) 2. Tubiana R, Thomine JM, Mackin E. Examination of the Hand & Upper Limb. 2nd ed. London: Martin Dunitz; 1998. p. 286–327. 3. Alnot JY. Indications and therapeutic perspectives. In: Alnot JY, Narakas A, editors. Traumatic brachial plexus injuries. 1st ed. Paris: Expansion Scientifique Francaise; 1996. p. 94–109. 4. Boome RB. General discussion on the brachial plexus. In: Boome RB, editor. The brachial plexus (Hand and upper extremity series), New York: Churchill Livingstone; 1997. p. 1–8. 5. Brunelli G. Proposal of a new synoptic evaluation chart for brachial plexus lesion. In: Alnot JY, Narakas A, editors. Traumatic brachial plexus injuries. 1st ed. Paris: Expansion Scientifique Francaise; 1996. p. 65–67.

Clinical examination and diagnosis 6. Einstein A, Grossmann M. Entwurf einer verallgemeinerten Relativitätstheorie und eine Theorie der Gravitation. Zeitschrift für Mathematik und Physik 1913;62:225–261. 7. Sunderland SS. Brachial plexus lesions due to compression, stretch and penetrating injuries. Nerves and Nerve Injuries. 2nd ed. Edinburgh: Churchill Livingstone; 1978. p. 870–900. 8. Moran SL, Steinmann SP, Shin AY. Adult brachial plexus injuries: mechanism, patterns of injury, and physical diagnosis. Hand Clin 2005;21:13–24. 9. Highet WB, Sanders FK. The effect of stretching nerves after sutures. Br J Surg 1943;30:355–369. 10. Chuang DC. Nerve transfers in adult brachial plexus injuries: My methods. Hand Clin 2005;21:71–78. 11. Aird RB, Naffziger HC. The pathology of human striated muscle following denervation. J Neurosurg 1953;10:216–227. 12. Songcharoen P. Brachial plexus injury in Thailand: a report of 520 cases. Microsurgery 1995;16:35–39. 13. Clancy Jr WG, Brand RL, Bergfeld RA. Upper trunk brachial plexus injuries in contact sports. Am J Sports Med 1977;5:209–216. 14. Bonnard C, Narakas AO. Supraclavicular traction injuries in adults. In: Boome RB, editor. The brachial plexus (Hand and upper extremity series). New York: Churchill Livingstone; 1997. p. 1–8. 15. Bufalini C, Pescatori G. Posterior cervical electromyography in the diagnosis and prognosis of brachial plexus injuries. J Bone Jt Surg 1969;51B: 627–631. 16. Ozkan T, Aydin A. Physical examination. In: Gilbert A, editor. Brachial Plexus Injuries. London: Martin Dunitz; 2001. p. 17–29. 17. Songcharoen P, Wongtrakul S, Mahaisavariya B, et al. Hemi-contralateral C7 transfer to median nerve in the treatment of root avulsion brachial plexus injury. J Hand Surg 2001;26A:1058–1064. 18. Seddon HJ, editor. Peripheral nerve injuries. Medical Research Council Special report series, No. 282. London: Her Majesty’s Stationery Office; 1954. p. 3–4.

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19. Bhardwaj P, Bhardwaj N. Motor grading of elbow flexion – is the Medical Research Council grading good enough? J Brachial Plex peripher Nerve Inj 2009;4:3. 20. Narakas A, Bonnard C. Anatomopathological lesions. In: Alnot JY, Narakas A, editors. Traumatic brachial plexus injuries. 1st ed. Paris: Expansion Scientifique Francaise; 1996. p. 73–91. 21. Mesulam MM, Brushart TM. Transganglionic and anterograde transport of horseradish peroxidase across dorsal root ganglia: a tetramethylbenzidine method for tracing central sensory connections of muscles and peripheral nerves. Neuroscience 1979;4:1107–1117. 22. Kendall FP, McCreary EK, Provance PG, et al. Muscles: Testing and function with posture and pain. 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2005. p. 314. 23. Narakas A, Bonnard C. Clinical examination. In: Alnot JY, Narakas A, editors. Traumatic brachial plexus injuries. 1st ed. Paris: Expansion Scientifique Francaise; 1996. p. 53–64. 24. Davis EN, Chung KC. The Tinel sign: A historical perspective. Plast Reconstr Surg 2004;114: 494–499. 25. Birch R, Bonney G, Wynn Parry CB. Clinical aspects of nerve injury. In: Birch R, Bonney G, Wynn Parry CB, editors. Surgical disorders of the peripheral nerves. Edinburgh: Churchill Livingstone; 1998. p. 71–86. 26. Landi A, Copeland S. Value of the Tinel sign in brachial plexus lesions. Ann Royal Coll Surg Eng 1979;61:470–471. 27. Haninec P, Szeder V. Reconstruction of elbow flexion by transposition of pedicled long head of tricep brachii muscle. Acta Chir Plast 1999;41:82–86. 28. Oberlin C, Beal D, Leechavengvongs S, et al. Nerve transfer to biceps muscle using part of ulnar nerve for C5-6 avulsions of the brachial plexus. J Hand Surg 1994;19A:232–237. 29. Oberlin C, Ameur NE, Teboul F, et al. Restoration of elbow flexion in brachial plexus injury by transfer of ulnar nerve fascicles to the nerve to the biceps muscle. Tech Hand Up Extrem Surg 2002;6:86–90.

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