Background
Although intradural exploration of the brachial plexus had been reported in 1911 [[1 ]] and surgical repair of an intraspinal plexus lesion had been performed in 1979
[[2 ]], directly implanting avulsed roots into the spinal cord stimulated the interest
of surgeons for a short period of time before falling into disrepute. The fact is,
following avulsion of the nerve roots off the spinal cord, successful recovery of
function depends on several factors [[3 ],[4 ]]. Firstly, new nerve fibers have to grow along a trajectory consisting of central
nervous system growth-inhibitory tissue in the spinal cord as well as peripheral nervous
system growth-promoting tissue in nerves. Secondly, local segmental spinal cord circuits
have to be reestablished. Thirdly, a large proportion of motoneurons die shortly after
the injury. Schwann cells are one of the major sources of neurotrophic factors, particularly
those relating to the survival of motoneurons, such as ciliary neurotrophic factor
(CNTF) and brain-derived neurotrophic factor. In root avulsions, the loss of peripheral
connection leads to loss of this local source of trophic support and subsequent apoptosis,
but ischaemic cell death might also occur.
Nevertheless, regrowth of motoneuron axons into neighboring ventral nerve roots after
lesions was proven in the pioneering studies by Ramon y Cajal [[5 ]] and later confirmed in several other experimental studies [[6 ],[7 ]]. The scar tissue within the spinal cord was shown to be conducive to regeneration
[[3 ]]. Clinically, interest in direct cord implantation was rekindled in 1995, when Carlstedt
et al. [[8 ]] described the implantation of a ventral nerve root and nerve grafts into the spinal
cord in a patient with brachial plexus avulsion injury. Results of surgery were reported
in several other studies [[3 ],[8 ],[9 ],[10 ],[11 ]].
Although the technique is expected to solve the problem of multiple root avulsions,
it has found only limited application among brachial plexus surgeons. The fact is,
current surgical approaches for direct cord implantation provide only limited exposure
either to the brachial plexus or to the cervical cord, cause much tissue damage and
lack extensibility. Using a single stage combined anterior (first) posterior (second)
approach, we describe a technique that provides adequate exposure to the brachial
plexus and to the cervical cord, causes minimal tissue damage, is extensible and allows
for ample placement of nerve grafts along the cervical cord and roots, trunks and
cords of the brachial plexus.
Methods
Patients
5 patients suffering from complete traumatic brachial plexus palsy, 4 adults and 1
obstetric case, were operated upon from 2005 up to 2006 and followed up for 2 years.
At the time of surgery, the ages of the adult subjects ranged from 27 up to 45 years
with a median of 37 years; all were male. 2 adult patients suffered from a (C5,6 rupture
C7,8T1 avulsion), 2 were (C5,6,7,8T1 avulsions); all were operated upon within 1 year
after injury. The obstetric case was a (C5,6,7,8T1 avulsion) and was operated upon
at 1 year of age. The demographic data, clinical and operative findings and operative
procedures are presented in [Table 1 ].
Table 1
The demographic data of the patients, lesion types, operative procedures, preoperative
cocontractions and deformities and the pre- and postoperative evaluation scores
Pt
Age (yrs) sex
Type of injury
Time of surgery after injury (mths)
Procedure
Nerve grafts
Associated injuries
Deformities
Shoulder score Narakas (N), Gilbert (G)
Elbow score Waikakul (W). Gilbert (G)
Hand score Raimondi (R)
1
27 M
C5,6,7,8T1 avulsion lt. brachial plexus; retraction of the brachial plexus to the
deltopectoral groove
8
Direct cord implantation
Both surals
Retroclaclavicular CSF sac; neglected rupture of subclavian artery; delayed union
of fracture of the lt. humerus
Volkmann’s ischaemic contracture
Ngood
Wgood
R0
2
40 M
C5,6,7,8T1 avulsion rt. brachial plexus; retraction of the brachial plexus to the
deltopectoral groove
12
Direct cord implantation
Both surals
grafted subclavian artery
-
Ngood
Wgood
R0
3
45 M
C5,6 rupture C7,8T1 avulsion rt. brachial plexus; retraction of the brachial plexus
to the outer border of scalenus anterior muscle
8
C5,6 grafting to superior trunk, C7,8T1: direct cord implantation
Medial cutaneous nerve of forearm, superficial radial nerve, supraclavicular nerves
-
-
Nexcellent
Wexcellent
R3
4
30 M
C5,6 rupture C7,8T1 avulsion lt. brachial plexus; retraction of the brachial plexus
to the clavicle
8
C5,6 grafting to superior trunk, C7,8T1: direct cord implantation
Medial cutaneous nerve of forearm, superficial radial nerve, supraclavicular nerves
-
-
Nexcellent
Wexcellent
R3
5
1 M
C5,6,7,8T1 avulsion rt. brachial plexus; retraction of the brachial plexus to the
clavicle; obstetric palsy
12
Direct cord implantation
Medial cutaneous nerve of forearm, superficial radial nerve
Ngood, G3
Ggood
R4
Patient evaluation
All patients were evaluated pre- and postoperatively (every 2 months) for deformities,
muscle function and cocontractions. To limit intraobserver and interobserver variability,
testing for deformities, muscle function and cocontractions was recorded by digital
photography on both normal and healthy sides. The normal side was recorded to ensure
the patient had complied with the examiner’s instructions. Electromyographic studies
were performed preoperatively. Although CT cervical myelography is more accurate than
magnetic resonance imaging in evaluating root avulsions [[12 ]], patients accepted magnetic resonance imaging more readily. Magnetic resonance
imaging was reported to have a 81% sensitivity in detecting root avulsions [[13 ]]. Thus, root avulsions were evaluated by magnetic resonance imaging and confirmed
intraoperatively [[14 ]].
Range of motion and deformities
The range of elbow flexion was measured as the angle formed between the long axis
of the arm and the forearm. The range of abduction was recorded by measuring the angle
formed between the arm axis and parallel to the spinal cord axis. External rotation
was measured with the patient standing with the shoulder fully internally rotated
and forearm placed transversally over the abdomen. Any rotation from this position
was measured and noted as the range of external rotation [[15 ]].
In all adult patients, the shoulders and elbows were flail. The wrist and fingers
were stiff in extension in 2 patients, while 1 patient presented with a Volkmann’s
ischaemic contracture of the forearm and hand ([Table 1 ]).
Muscle function
Muscle function was assessed using the system described in the report of the Nerve
Committee of the British Medical Council in 1954 and previously used by other authors
[[16 ]]. The anterior, middle and posterior deltoid were tested separately [[17 ]]. The subscapularis was tested by the lift-off test and the lift-off lag sign [[18 ],[19 ],[20 ]]. The supraspinatus was tested using Jobe’s empty can test. The infraspinatus integrity
is tested by the external rotation lag (dropping) sign, by Hornblower’s sign and by
the drop arm sign. These tests were modified to test for muscle power. Although all
of the above tests were reliable, the most sensitive test was the drop arm test [[18 ]]. Some reports questioned its sensitivity, however [[20 ]]. In the current study, when the patient could actively abduct his shoulder, the
drop arm sign was used, as it was the most sensitive; otherwise, the other two tests
were used. In testing finger flexors and extensors, both elbows and wrists were immobilized
on a board.
Evaluation for cocontractions
Cocontractions were evaluated by asking the patient to abduct the shoulder without
actively flexing, internally or externally rotating it and without actively moving
the elbow, forearm, wrist or fingers [[21 ]]. He was observed if he could abduct the shoulder independently of other movements.
The same procedure was repeated for shoulder flexion, elbow flexion and extension,
forearm pronation and supination, wrist and finger flexion and extension.
Functional scoring
Shoulder function was graded using the scale proposed by Narakas [[15 ],[21 ],[22 ],[23 ]] (poor: no abduction movement and feeling of weightlessness in the limb (motor power
grade 0); fair: stable shoulder without any subluxation but no active movement (motor
power grade 1); good: active abduction of < 60 degrees (motor power grade 3) and active
external rotation of < 30 degrees; excellent: active abduction of > 60 degrees (motor
power grade 4) and active external rotation of > 30 degrees).
Elbow function was graded using the scale proposed by Waikakul et al. [[15 ],[24 ]] (excellent: ability to lift 2 kg weight from 0 to 90 degrees of elbow flexion more
than 30 times successively; good: ability to lift 2 kg weight from 0 to 90 degrees
of elbow flexion, but less than 30 repetitions successively; fair: motor power more
than grade 3 but unable to lift a 2 kg weight; poor: motor power less than grade 3).
The paediatric case was evaluated using the Gilbert shoulder and elbow scales [[21 ],[22 ]] (shoulder scale: Grade 0: completely paralysed shoulder or fixed deformity; Grade
1: abduction = 45 degrees, no active external rotation; Grade 2: abduction < 90 degrees,
bioactive external rotation; Grade 3: abduction = 90 degrees, active external rotation
< 30 degrees; Grade 4: abduction < 120 degrees, active external rotation 10–30 degrees;
Grade 5: abduction > 120 degrees, active external rotation 30–60 degrees; Grade 6:
abduction > 150 degrees, active external rotation > 60 degrees). The Gilbert elbow
scale included the following items: flexion (1: no or minimal muscle contraction,
2: incomplete flexion, 3: complete flexion); extension (0: no extension; 1: weak extension;
2: good extension); flexion deformity (extension deficit) (0: 0–30 degrees, -1:30–50
degrees, -2:> 50 degrees). Evaluation was as follows: 4–5 points: good regeneration;
2–3 points: moderate regeneration; 0–1 points: bad regeneration.
The Raimondi hand evaluation scale [[21 ],[22 ]] comprised the following grades: Grade 0: complete paralysis or minimal useless
finger flexion; Grade 1: useless thumb function, no or minimal sensation, limitation
of active long finger flexors; no active wrist or finger extension, key-grip of the
thumb; Grade 2: active wrist extension; passive long finger flexors (tenodesis effect);
Grade 3: passive key-grip of the thumb (through active thumb pronation), complete
wrist and finger flexion, mobile thumb with partial abduction, opposition, intrinsic
balance, no active supination; Grade 4: complete wrist and finger flexion, active
wrist extension, no or minimal finger extension, good thumb opposition with active
intrinsic muscles (ulnar nerve), partial pronation and supination; Grade 5: as in
Grade 4 in addition to active long finger extensors, almost complete thumb pronation
and supination.
Pain
In adults, the presence or absence of pain and its degree were assessed on a visual
analogue scale from 1 to 5.
Operative procedure
Draping of the patient
The patient was prepared and draped in the lateral position, the affected side up.
A pad helped elevate the head. The sterilization area included: the front and back
of the neck, the front and back of the chest up to the midline and the whole affected
upper limb ([Figs. 1a ] and [1b ]). Both lower limbs served as donor sites for sural nerve grafts and were sterilized.
Figure 1 . The sterilization area includes: the front and back of the neck, the front and back
of the chest up to the midline and the whole affected upper limb. Next the patient
is turned into the usual supine position for anterior exploration of the brachial
plexus. To help extend the shoulders, a sterile pad is placed posteriorly between
them (yellow arrow). A head pad supports the head. The head is turned to the contralateral
side.
Turning the patient into the supine position
Next the patient was turned into the usual supine position for anterior exploration
of the brachial plexus. To help extend the shoulders, a sterile pad was placed posteriorly
between them. A head pad supported the head. The head was turned to the contralateral
side ([Figs. 1c ] and [1d ]).
Conventional anterior exploration of the brachial plexus
After that, the brachial plexus was explored anteriorly as usual. We preferred to
explore it through a transverse supraclavicular incision with a deltopectoral extension,
yet without clavicular osteotomy [[14 ]]. After cutting the clavicular head of the sternomastoid and the insertion of scalenus
anterior muscle medially, and the clavicular and part of acromial insertion of the
trapezius muscle laterally [[25 ],[26 ]], exploration of the brachial plexus proceeded as described elsewhere [[14 ],[27 ],[28 ],[29 ]].
In Cases 1, 2, 5 (C5,6,7, 8T1 avulsions), aiming at direct cord implantation and using
the principle of closed loop of end-to-side side-to-side grafting neurorrhaphy [[30 ]], one nerve graft was looped through the superior and middle trunks and lateral
and posterior cords and another nerve graft was looped through the inferior trunk,
medial cord and medial root of median nerve. In Cases 3 and 4 (C5,6 ruptures C7,8
T1 avulsions) the closed loop technique of end-to-side side-to-side grafting neurorrhaphy
[[30 ]] was used to graft the ruptured C5,6 roots to the superior trunk of the brachial
plexus. Next, aiming at direct cord implantation, one nerve graft was looped through
the middle trunk and posterior cord and another was looped through the inferior trunk,
medial cord and medial root of median nerve ([Figs. 2 ] and [3a, b ]).
Figure 2 . The inset shows the position of the patient and the incision line.
Figure 3 . It also shows the technique of closed loop grafting as explained in [Fig. 2 ]. In (C5,6,7, 8T1 avulsions), one nerve graft is looped through the superior and
middle trunks and lateral and posterior cords and another nerve graft is looped through
the inferior trunk, medial cord and medial root of median nerve. In (C5,6 ruptures
C7,8 T1 avulsions) the closed loop technique of end-to-side side-to-side grafting
neurorrhaphy is used to graft the ruptured C5,6 roots to the superior trunk of the
brachial plexus. Next, one nerve graft is looped through the middle trunk and posterior
cord and another is looped through the inferior trunk, medial cord and medial root
of median nerve.
Turning the patient into the lateral position again
The sterile pad between the shoulders was removed and the patient was turned again
into the lateral position. Contrary to conventional fascicular epiperineurial neurorrhaphy,
closed looping provided a stable graft recipient junction, which allowed turning the
patient again into the lateral position to approach the cervical cord posteriorly
Exposing the cervical cord through a conventional posterior cervical laminectomy
Through a midline skin incision extending from the occiput to the posterior process
of T1, and using the midline intermuscular plane of the posterior neck muscles, the
cervical laminae were exposed. A cervical laminectomy was carried out.
Retrieving the nerve graft loops into the posterior laminectomy
Through the posterior incision and using a submuscular plane, a right-angled dissection
forceps was inserted along the posterior aspect of C7 transvserse process, and entered
into the anterior incision. It was used to hold the proximal free ends of the graft
loops and pull them gently into the posterior laminectomy incision ([Fig. 4 ])
Figure 4 . The dura has been incised. The grafts have been passed through the dural incision
and placed in an end(graft)-to-side(cord) and side(graft)-to-side(cord) fashion for
about 4 cms along the anterior cord close to the midline sulcus in a subpial plane.
They are held in place by placing them anterior to C4 intradural cervical nerve root
proximally and T1 intradural nerve root distally. In 5 minutes, they adhere to the
cord. The dura is closed using 3/0 prolene continuous sutures. The inset shows the
position of the patient.
Opening the dura
The dura was next opened posteriorly using a 11-scalpel blade. Its edges were kept
open by means of 3/0 prolene sutures. A dural dissector was used to cut the dentate
ligaments and clear the pia mater off the anterior cord from C4 up to C7. The avulsed
roots were explored intradurally. Thus extending the laminectomy by a partial facetectomy
on the injured side of the brachial plexus to fully expose every root and provide
adequate working space for the subsequent repair was avoided lest the spine should
be destabilized.
Inserting the proximal ends of the graft into the anterior cord
The grafts were passed through the dural incision and placed in an end(graft)-to-side(cord)
and side(graft)-to-side(cord) fashion for about 4 cms along the anterior cord close
to the midline sulcus in a subpial plane ([Figs 3 ] and [5 ]). They were held in place by placing them anterior to C4 intradural cervical nerve
root proximally and T1 intradural nerve root distally. In 5 minutes, they adhered
to the cord. The dura was closed using 3/0 prolene continuous sutures.
Figure 5 . Conventional anterior dissection (anterior bifurcated black arrow) provides access
to the roots, trunks and cords of the brachial plexus. Approaching the cervical cord
through a conventional laminectomy (posterior bifurcated black arrow) provides adequate
exposure and allows for lateral retraction of the paraspinal musculature, thus preserving
their segmental nerve and vascular supply. Through the posterior incision and using
a submuscular plane, a right-angled dissection forceps is inserted along the posterior
aspect of C7 transvserse process, and entered into the anterior incision (bright green
line). It is used to hold the proximal free ends of the graft loops and pull them
gently into the posterior laminectomy incision. The red line shows the path of the
nerve grafts.
Wound closure
The wound was closed in layers.
Postoperative immobilization
The patient’s neck was immobilized postoperatively in a soft collar for 6 weeks. [Figure 6 ] shows a postoperative picture illustrating the incision lines of the combined approach
Figure 6 .
Donor nerves
Both sural nerves, the superficial radial nerve and the medial cutaneous nerve of
the forearm and the supraclavicular nerves served as nerve grafts.
Results
Technical advantages
Anterior exposure
As both supraclavicular and infraclavicular parts of the brachial plexus were explored,
the extent of the injury could be estimated. Cases 1, 2 and 5 were C5,67,8T1 avulsions;
the brachial plexus was retracted to the deltopectoral groove in Cases 1 and 2 and
to the clavicle in Case 5. Cases 3 and 4 were C5,6 ruptures C7,8T1 avulsions
The brachial plexus was retracted to the outer border of scalenus anterior in Case
3 and to the clavicle in Case 5.
Posterior exposure
As the whole cervical cord was explored adequately, the extent of root avulsions could
be determined accurately. It was used to confirm the findings obtained from MRI and
anterior exposure.
Complications of surgery
None of our patients lost neurologic function, had CSF leak or developed myelitis
as a result of cord manipulation. None suffered from cervical pain or developed cervical
instability as a result of the laminectomy. The paediatric case complained of mild
hyperextension of the neck as a result of contracture of the posterior laminectomy
scar.
Motor power
Improvements in motor power are shown in Table 2 [see [additional file 1 ]].
Motor power in C5,6 ruptures C7,8T1 avulsions
In Cases 3 and 4, the biceps and anterior deltoid improved from Grade0 to Grade5;
the lateral and posterior deltoid, the supra- and infraspinatus, the subscapularis,
pectoral and clavicular heads of pectoralis major, latissimus dorsi, triceps improved
from Grade 0 to Grade 4. The pronator teres, extensor carpi ulnaris, flexor digitorum
profundus and flexor pollicis longus improved from Grade 0 to Grade 3. The flexor
digitorum superficialis improved from Grade 0 to Grade 2.
Motor power in C5,6,7,8T1 avulsions
In Cases 1 and 2, the biceps and anterior, lateral and posterior deltoid, the supraspinatus,
the subscapularis, pectoral and clavicular heads of pectoralis major, latissimus dorsi,
improved from Grade 0 to Grade 4. The infraspinatus, triceps and pronator teres improved
from Grade 0 to Grade 3.
In Case 5, the biceps and anterior deltoid improved from Grade0 to Grade5; the lateral
and posterior deltoid, the supraspinatus, the subscapularis, pectoral and clavicular
heads of pectoralis major, latissimus dorsi, triceps improved from Grade 0 to Grade
4. The infraspinatus, pronator teres, extensor carpi ulnaris, extensor carpi radialis
longus and brevis, flexor carpi ulnaris, flexor carpi radialis, thumb and finger extensors,
flexor digitorum profundus and superficialis, flexor pollicis longus improved from
Grade 0 to Grade 3. The intrinsic muscles of the hand improved from Grade 0 to Grade
2.
Cocontractions
C5,6 ruptures C7,8T1 avulsions
No cocontractions were recorded in Cases 3 and 4.
C5,6,7,8T1 avulsions
In Cases 1 and 2 cocontractions occurred between the lateral deltoid and biceps on
active shoulder abduction.
In Case 5, cocontractions occurred between the lateral deltoid, biceps and finger
extensors on active shoulder abduction.
Functional Score
Shoulder score
- C5,6 ruptures C7,8T1 avulsions:
Cases 3 and 4 achieved a Narakas score of excellent
- C5,6,7,8T1 avulsions:
Because of weak shoulder external rotation, Cases 1, 2, and 5 achieved a Narakas score
of good. Case 5 achieved also a Grade3 Gilbert score.
Elbow score
- C5,6 ruptures C7,8T1 avulsions:
Cases 3 and 4 achieved a Waikakul score of excellent
- C5,6,7,8T1 avulsions:
Cases 1 and 2 achieved a Waikakul score of good.
Case 5 achieved a Gilbert score of good.
Hand score
- C5,6 ruptures C7,8T1 avulsions:
Cases 3 and 4 improved from a Raimondi score of 0 to a score of 3.
- C5,6,7,8T1 avulsions:
Cases 1 and 2 remained with a Raimondi score of 0.
Case 5 improved from a Raimondi score of 0 to a score of 4.
Pain
In adult total avulsions (Cases 1 and 2), pain persisted and had a grade of 4. In
C5,6 ruptures C7,8T1 avulsions, pain disappeared, but patients complained of a sensation
of tingling on combined shoulder flexion and elbow extension.
Discussion
Six issues have to be addressed in this work: 1. approaching the brachial plexus surgically
for purpose of cord implantation; 2. side-to-side end-to-side grafting neurorrhaphy
between the recipient brachial plexus and the distal aspect of the nerve graft conduits;
3. side-to-side end-to-side grafting neurorrhaphy between the donor anterior aspect
of the cervical cord and the proximal ends of the nerve graft conduits; 4. the role
of direct cord implantation in complete avulsions; 5. the role of direct cord implantation
in incomplete avulsions; 6. shortcomings of the technique and future directions; 7.
limitations of the study.
Approaching the brachial plexus surgically for purpose of cord implantation
Approaching the brachial plexus surgically for purpose of cord implantation is the
first issue we have to address.
Conventional anterior approaches to the brachial plexus [[14 ],[27 ],[28 ],[29 ]] afford good exposure to the anterior structures. Yet, a facetectomy, foraminotomy
or hemilaminectomy cannot be performed through them. Juergens-Becker et al. [[31 ]] performed a diagnostic foraminotomy through a posterior approach as a first stage.
At a second stage, anterior exploration of the brachial plexus was carried out.
Using the posterior subscapular approach [[32 ],[33 ]] ([Fig. 7 ]), Carlstedt [[8 ]] was able to approach the laminae, facet joints and avulsed root stumps present
within the spinal canal. He was not able to reach those roots avulsed out of the spinal
canal and migrated distally [[8 ]]. In the posterior subscapular approach [[32 ]], the trapezius muscle was divided longitudinally away from its nerve supply, the
levator scapulae, the rhomboideus minor and major muscles were exposed and divided
away from the edge of the scapula. Thus, the posterior chest wall was exposed. The
ribs were then palpated, the first rib was located and removed extraperiosteally,
from the costotransverse articulation posteriorly to the costoclavicular ligament
anteriorly. The posterior and middle scalene muscles were released from their origin
from the transverse spinous processes. After removal of these muscles superiorly,
the roots of spinal nerves and the trunks of the brachial plexus were exposed and
traced back to the spine. Some elevation and retraction of the paraspinous muscle
mass exposed the lateral posterior spine overlying the intraforminal course of the
spinal nerves.
Figure 7 . The anterior plane of dissection is developed by disinserting the levator scapulae,
the posterior and middle scalene muscles and retracting them anteriorly and superiorly
(anterior black arrow); this provides only limited exposure to the brachial plexus.
The posterior plane of dissection is developed by medial retraction of the paraspinal
muscles (posterior black arrow). The latter muscles are too bulky to be retracted
medially adequately. Besides, medial retraction damages their nerve and vascular supply.
From that description, it is evident, that this approach affords little exposure to
the anterior structures, namely the trunks, cords and divisions of the brachial plexus,
the subclavian vessels and their branches. This approach affords also limited exposure
to the posterior structures, namely the cord and intradural nerve roots. Furthermore,
it lacks extensibility. As it does not pass through proper intermuscular-internervous
planes, it produces damage to the muscles and their vascular supply.
The lateral approaches to the crevical spine provide only a partial answer to this
problem [[34 ],[35 ],[36 ]]. To expose the upper cervical spine, Crockard et al. [[37 ]] placed the patient in the lateral position, entered the cervical spine posterior
to the sternomastoid, the levator scapulae and splenius cervicis muscles. Later on,
Carlstedt used the extreme-lateral approach [[3 ]] ([Figs. 8 ] and [9 ]) to access both the intra-and the extraspinal parts of the plexus. The patient was
placed in a straight lateral position. The head was held in a Mayfield clamp with
the neck slightly flexed laterally to the opposite side. A skin incision was made
in the region of the sternoclavicular joint and continued in the posterior triangle
of the neck in a lateral and cranial direction, toward the spinous processes of C4-5.
The accessory nerve was identified and protected as it emerged from the dorsal aspect
of the cranial part of the sternocleidomastoid muscle. The extraspinal portion of
the plexus was next dissected. The transverse processes of C4-7 were approached through
a connective tissue plane between the levator scapula and the posterior and medial
scalenus muscles. The longissimus muscle had to be split longitudinally to approach
the posterior tubercles of the transverse processes. The paravertebral muscles were
dissected free from the hemilaminae and pushed dorsomedially. After performing a hemilaminectomy,
the dura mater was incised longitudinally.
Figure 8 .
Figure 9 . To approach the cord posteriorly, the transverse processes of C4-7 are approached
through a connective tissue plane between the levator scapula and the posterior and
medial scalenus muscles. The longissimus muscle has to be split longitudinally to
approach the posterior tubercles of the transverse processes (black arrow). As mentioned
before, the paraspinal muscles are too bulky to be retracted medially adequately.
Besides, medial retraction damages their nerve and vascular supply.
Thus, lateral approaches to the spine not only suffer from the same disadvantages
described previously, but they also afford little exposure to the cord and intradural
nerve roots, thus limiting the area of side neurotization to the cord.
For our part, we described an extended anterior and posterior approach to the brachial
plexus [[25 ]]. The brachial plexus was exposed through a standard L-shaped incision with a deltopectoral
extension as described by other authors [[14 ],[27 ],[28 ],[29 ]].
Extending the horizontal limb of the L-incision posteriorly, the trapezius muscle
was disinserted from the clavicle and acromion process. Extending the vertical limb
of the L-incision horizontally along the superior nuchal line, the origin of the the
trapezius muscle from the superior nuchal line and the external occipital protuberance
was cut and the spinal accessory nerve was followed to its motor point into the trapezius
muscle. Next, the muscle itself was reflected posteriorly to expose the levator scapulae
muscle anteriorly and the splenius capitis muscle posteriorly. This done, the splenius
capitis and semispinalis capitis musles were disinserted from the occiput and reflected
posteriorly as well. The plane posterior to the following muscles was located: the
levator scapulae, the iliocostalis cevicis and the longissimus capitis and cervicis.
Anterior retraction of these muscles and medial retraction of the semispinalis cervicis
and multifidus muscles allowed us to expose the facet joints and perform a facetectomy
([Figs. 10 ] and [11 ]).
Figure 10 . Extending the horizontal limb of the L-incision posteriorly, the trapezius muscle
is disinserted from the clavicle and acromion process. Extending the vertical limb
of the L-incision horizontally along the superior nuchal line, the origin of the trapezius
muscle from the superior nuchal line and the external occipital protuberance is cut
and the spinal accessory nerve followed to its motor point into the trapezius muscle.
Next, the muscle itself is reflected posteriorly to expose the levator scapulae muscle
anteriorly and the splenius capitis muscle posteriorly. This done, the splenius capitis
and semispinalis capitis musles is disinserted from the occiput and reflected posteriorly
as well.
Figure 11 . Anterior retraction of these muscles and medial retraction of the semispinalis cervicis
and multifidus muscles allows exposure of the facet joints and performing a facetectomy
(posterior black arrow).
The problems we met with in this approach were sloughing of the fat pad covering the
brachial plexus due to its extensive dissection; sloughing of the tip of the skin
flap at the medial end of the lower horizontal skin incision; bleeding from the vertebral
artery; bleeding from the cranial vessels, which lay between the semispinalis capitis
and the semispinalis cervicis; CSF leakage from meningoceles.
A two stage combined posterior (first) anterior (second) approach was introduced [[38 ]] that provided adequate exposure to the brachial plexus and to the cervical cord.
These advantages were undermined by operating in two stages. In the first stage, one
end of the harvested sural nerve graft was implanted into the ventral lateral aspect
of the spinal cord; the other end was identified with a small segment of Foley catheter
and radioopaque marker hemoclips and inserted carefully into the paraspinal muscles
toward the anterior suprascapular region. Several days later, and through an anterior
supraclaviclar approach, the Foley catheter segment was dug out with or without fluoroscopic
guidance, removed and the nerve graft anastomosed to the trunk level of the brachial
plexus. Thus, extensive tissue damage might occur by having to identify the sural
nerve grafts through the paraspinal muscles several days later. Also, as the grafts
were invariably inserted into the anterior suprascapular region to be anastomosed
several days later to the trunk level of the brachial plexus, no account was taken
of the severity of the brachial plexus lesion itself, which might lead to retraction
of the avulsed roots up to the deltopectoral or axillary areas (e.g. Cases 1 and 2
in this study), necessitating tailoring grafts to extend to the latter sites. Although
Juergens-Becker et al. [[31 ]] performed a diagnostic foraminotomy through a posterior approach as a first stage,
the presence or absence of root avulsions or ruptures, the degree of retraction of
the brachial plexus, the extension of fibrosis and scarring along the brachial plexus
are all determinants which can only be properly estimated after anterior (first) exploration
of the brachial plexus. Root avulsions could be confirmed after that through a posterior
laminectomy. Preoperative investigations to determine root avulsions merely help the
surgeon devise the operative technique.
These complications prompted us to devise a single stage combined anterior (first)
posterior (second) approach for purpose of direct cord implantation. Both approaches
passed through anatomical planes and were extensible. The anterior approach afforded
good exposure to the roots, trunks, divisions and cords of the brachial plexus, while
the posterior approach provides good exposure to the cervical cord and roots of the
brachial plexus. The patient was prepared and draped in the lateral position, the
affected side up. A pad helped elevate the head. The sterilization area included:
the front and back of the neck, the front and back of the chest up to the midline
and the whole affected upper limb. Next the patient was turned into the usual supine
position for anterior exploration of the brachial plexus and the brachial plexus explored
anteriorly as usual; ruptures were grafted. Nerve grafts were looped into the recipient
avulsed nerves. This done, the patient was turned again into the lateral position
and the cervical cord exposed just like a conventional cervical laminectomy. Through
the posterior incision and using a submuscular plane, a right-angled dissection forceps
was inserted along the posterior aspect of C7 transvserse process, and entered into
the anterior incision. It was used to hold the proximal free ends of the graft loops
and pull them gently into the posterior laminectomy incision.
Side-to-side end-to-side grafting neurorrhaphy between the recipient brachial plexus
and the distal aspect of the nerve graft conduits
Side-to-side end-to-side grafting neurorrhaphy between the recipient brachial plexus
and the distal aspect of the nerve graft conduits is the second issue we have to consider.
In a previous clinical study [[30 ]], we introduced several end-to-side side-to-side grafting neurorrhaphy techniques.
In the intranervous closed loop technique nerve grafts were passed (looped) into slits
made into the distal nerve stumps and side grafted to them. Contrary to conventional
fascicular epiperineurial neurorrhaphy, this created a stable recipient-graft junction
and allowed for an increased contact area between the grafts and the recipient nerves.
In that study, we also introduced the principle of single donor to multiple recipient
neurotization. Success of that procedure depended upon choosing a donor with high
axonal count [[14 ],[39 ],[40 ]], on increasing the number of grafts and on increasing the recipient-graft and graft
donor contact areas [[30 ],[41 ]]. Only through this could several muscles reach motor power greater than Grade 3
without cocontractions.
In the present work, closed looping provided a stable graft recipient junction, which
allowed turning the patient again into the lateral position to approach the cervical
cord posteriorly; it also allowed retrieving of the proximal ends of the grafts fom
the anterior to the posterior field. In C5,6,7, 8T1 avulsions and using the principle
of closed loop of end-to-side side-to-side grafting neurorrhaphy [[30 ]], one nerve graft was looped through the superior and middle trunks and lateral
and posterior cords and another nerve graft was looped through the inferior trunk,
medial cord and medial root of median nerve. In C5,6 ruptures C7,8 T1 avulsions, after
grafting ruptures, one nerve graft was looped through the middle trunk and posterior
cord and another was looped through the inferior trunk, medial cord and medial root
of median nerve.
Side-to-side end-to-side grafting neurorrhaphy between the donor anterior aspect of
the cervical cord and the proximal ends of the nerve graft conduits
Side-to-side end-to-side grafting neurorrhaphy between the donor anterior aspect of
the cervical cord and the proximal ends of the nerve graft conduits is the third issue
we have to address..
After root avulsion from the spinal cord, there is degeneration of sensory and motor
axons of spinal motoneurons, loss of synapses, deterioration of local segmental connections,
nerve cell death and reactions among non neuronal cells with scar formation [[4 ]]. Nevertheless, motoneurons are able to regenerate; new nerve fibers grow along
a trajectory consisting of central nervous system (CNS) growth-inhibitory tissue in
the spinal cord as well as peripheral nervous system PNS growth-promoting tissue in
nerves [[4 ]]. Several theories have been advanced to account for the limited regenerative capacity
of the central nervous system.: the physical characteristics of the glial scar, inhibitory
cell surface or extracellular matrix molecules (such as axon growth-inhibitory proteoglycan
NG2 [[42 ]]), a lack of suitable guidance channels and substrates, the presence of myelin associated
growth-inhibiting molecules, an absence of growth-promoting neurotrophic molecules
and the cell intrinsic growth potential motoneurons [[43 ]].
Nonetheless, avulsed nerve roots could be reimplanted into the spinal cord [[44 ],[45 ],[46 ],[47 ],[48 ],[49 ],[50 ],[51 ]]. It was concluded that central nervous tissue axons might grow through scar tissue
that had a persistent defect in the blood-brain barrier [[52 ]]. Blood borne cells such as macrophages and T cells invaded the scar, and through
their release of interleukins tumor necrosis factor, interferon gamma and prostaglandins
contributed to upregulation by astrocytes of neurotrophins and extracellular matrix
molecules, such as laminin, and neurotrophins [[3 ]]. After ventral root avulsion, mRNAs for receptors or receptor components for neurotrophin-3
(NT-3), ciliary neurotrophic factor (CNTF) and leukemia inhibitory factor (LIF) were
strongly downregulated, while receptors for glial cell line-derived neurotrophic factor
(GDNF) and laminins were profoundly upregulated [[53 ]]. Both laminin-2 (alpha2beta1gamma1) and laminin-8 (alpha4beta1gamma1) were important
for axonal regeneration after injury [[54 ]]. The production of nerve growth factor by the astrocytes, was shown to attract
leptomeningeal cells to participate in the formation of a trabecular scar. These leptomeningeal
cells, in turn, were shown to express the low affinity neurotrophin receptor p75 [[3 ]].
However, neurons could not elongate across the peripheral (PNS)-central nervous system
(CNS) transitional zone. The astrocytic rich central nervous system part of the spinal
nerve root prevented regeneration even of nerve fibers from transplanted embryonic
ganglion cells. Regeneration of severed nerve fibers into the spinal cord occurred
when the transition zone was absent as in the immature animal [[55 ]]. Thus to reestablish spinal cord to peripheral nerve connectivity, the transitional
region should be deleted and severed ventral or dorsal roots directly implanted into
the spinal cord [[55 ],[56 ]]. This procedure formed a kind of side neurotization between the donor cord side
to the end and side of the recipient nerve graft. Interestingly, the same procedure
also seemed to have an attenuating effect on the pain that developed in cases with
a combined dorsal root avulsion [[56 ]].
Nevertheless, problems in nervous regeneration such as non directional growths and
unspecific reinnervation of target organs led to unpredictable sensorimotor activity
and conspired against a useful recovery of function [[4 ]]. After ventral nerve root implantation, different functional pools of motor neurons
were attracted to regrow axons on the implanted root as judged by their position in
the ventral horn [[3 ]]. However, neurons normally supplying an antagonist muscle, such as the triceps
muscle, might participate in the innovation of the biceps muscle, thus leading to
cocontractions among antagonistic muscles. Strategies improving the number of motor
fibers regenerating into the reimplanted ventral roots and possibly extending regeneration
to distal musculature include: the placement of peripheral nerve grafts, the grafting
of fetal neurons or of olfactory ensheathing cells [[57 ],[58 ]] (neural transplantation), the application of growth factors or Schwann cells to
the area of the spinal lesion, the blockade of inhibitory molecules [[43 ]], or the genetic modification of peripheral nerve grafts to overexpress outgrowth-promoting
proteins [[59 ],[60 ],[61 ],[62 ]]. However, high levels of neurotrophic factors in the ventral horn might prevent
directional growth of axons of a higher number of surviving motoneurons into the implanted
root [[63 ]].
In a previous clinical study [[30 ]], we introduced several end-to-side side-to-side grafting neurorrhaphy techniques.
In the long length contact technique, we used both of the cut end and side of contralateral
C7 to neurotize the lateral, medial and posterior cords of the brachial plexus simultaneously.
Recovery was marked by being associated with cocontractions and by being differential
in nature, some muscles recovering better than others, agonists recovering better
than antagonists, proximal muscles recovering better than distal muscles. Achieving
functional motor power in several muscles without cocontractions depended upon choosing
a donor with high axonal count [[14 ]], on increasing the number of grafts and on increasing the recipient-graft and graft
donor contact areas [[30 ],[41 ]].
Current approaches used for direct cord implantation afford little exposure to the
cord and intradural nerve roots, thus limiting the area of side neurotization to the
cord.
In the present work, the dura was opened posteriorly using a 11-scalpel blade. Its
edges were kept open by means of 3/0 prolene sutures. A dural dissector was used to
clear the pia mater off the anterior cord from C4 up to C7. The grafts were passed
through the dural incision and placed in an end(graft)-to-side(cord) and side(graft)-to-side(cord)
fashion for about 4 cms along the anterior cord close to the midline sulcus in a subpial
plane. They were held in place by placing them anterior to C4 intradural cervical
nerve root proximally and to T1 intradural nerve root distally. These procedures allowed
for side neurotization between the donor cord and the nerve grafts along a broad surface
area. This became only possible because of the adequate exposure and extensibility
provided by the posterior cervical laminectomy.
The role of direct cord implantation in complete and incomplete avulsions
The role of direct cord implantation in complete and incomplete avulsions are the
fourth and fifth issues we have to consider. This was carried out experimentally on
monkeys, cats and rats [[64 ],[65 ],[66 ],[67 ]]. The C5-C8 ventral roots were avulsed in Macaca fascicularis monkeys and reimplanted
into the ventrolateral part of the spinal cord either immediately or after a delay
of 2 months. There was substantial recovery of function especially after immediate,
less so after delayed spinal cord implantation. Cocontractions occurred [[64 ],[65 ]]. Clinically, motor function significantly improved after re-implanting avulsed
spinal roots directly to the spinal cord [[3 ],[8 ],[9 ],[10 ],[11 ],[68 ]]. Motor function might be restored throughout the arm, forearm and hand when 1 or
2 avulsed roots were reimplanted into the cord, while the others were intact [[9 ]]. Motor function might even be restored in the intrinsic muscles of the hand when
surgery was performed in the paediatric age group [[10 ]]. However, cocontractions of agonist and antagonist muscle groups were reported
to occur clinically. Spontaneous contractions of limb muscles in synchrony with respiration,
the “breathing arm” might also ensue [[3 ],[8 ],[9 ],[10 ],[68 ]]. Clinically, pain intensity was significantly correlated with the number of roots
avulsed prior to surgery; surgical repairs were associated with pain relief. Sensory
recovery to thermal stimuli was observed, mainly in the C5 dermatome. Allodynia to
mechanical and thermal stimuli was observed in the border zone of affected and unaffected
dermatomes. Pain and sensations referred to the original source of afferents as well
as “wrong-way” referred sensations (e.g. down the affected arm while shaving or drinking
cold fluids) might occur [[69 ]]. Early repair was more effective than delayed repair in the relief from pain and
there was a strong correlation between functional recovery and relief from pain [[70 ]].
In the current series, Cases 1 and 2 were complete avulsions in patients, in whom
surgery was performed within 1 year after injury. The biceps and anterior, lateral
and posterior deltoid, the supraspinatus, the subscapularis, pectoral and clavicular
heads of pectoralis major, latissimus dorsi, improved from Grade 0 to Grade 4. The
infraspinatus, triceps and pronator teres improved from Grade 0 to Grade 3. Thus there
was nearly complete improvement in shoulder and elbow functions; improvement extended
even into the forearm. Cocontractions were recorded.
Because of weak shoulder external rotation, Cases 1 and 2 achieved a Narakas and a
Waikakul score of good; they remained with a Raimondi score of 0..
Cases 3 and 4 were C5,6 ruptures C7,8T1 avulsions. The biceps and anterior deltoid
improved from Grade0 to Grade5; the lateral and posterior deltoid, the supra- and
infraspinatus, the subscapularis, pectoral and clavicular heads of pectoralis major,
latissimus dorsi, triceps improved from Grade 0 to Grade 4. The pronator teres, extensor
carpi ulnaris, flexor digitorum profundus and flexor pollicis longus improved from
Grade 0 to Grade 3. The flexor digitorum superficialis improved from Grade 0 to Grade
2. Thus there was almost complete improvement in shoulder and elbow functions; improvement
extended even into the forearm and hand. No cocontractions were recorded. Both cases
achieved a Narakas score of excellent, a Waikakul score of excellent. and improved
from a Raimondi score of 0 to a score of 3. Improvement of forearm and hand function
when 1 or 2 avulsed roots were reimplanted into the cord, while the others were intact
conformed with other reports in the literature [[9 ]]. Interestingly, however, no cocontractions were recorded. Of equal interest was
the disappearance of pain after cord reimplantation in these cases, but not in total
avulsions [[70 ]].
In Case 5, the biceps and anterior deltoid improved from Grade0 to Grade5; the lateral
and posterior deltoid, the supraspinatus, the subscapularis, pectoral and clavicular
heads of pectoralis major, latissimus dorsi, triceps improved from Grade 0 to Grade
4. The infraspinatus, pronator teres, extensor carpi ulnaris, extensor carpi radialis
longus and brevis, flexor carpi ulnaris, flexor carpi radialis, thumb and finger extensors,
flexor digitorum profundus and superficialis, flexor pollicis longus improved from
Grade 0 to Grade 3. The intrinsic muscles of the hand improved from Grade 0 to Grade
2. Cocontractions occurred between the lateral deltoid, biceps and finger extensors
on active shoulder abduction. Case 5 achieved a Narakas score of good, a Grade3 Gilbert
shoulder score, a Gilbert elbow score of good and a Raimondi score of 0 to a score
of 4. These findings were in accordance with those reported in the literature of restoration
of hand function in the paediatric age group [[10 ]]. Contrary to adult cases, cocontractions persisted, however.
Shortcomings of the technique
Sixth, there are still shortcomings of the technique. As mentioned before, direct
cord implantation is a kind of single donor to multiple recipient neurotization. Success
of that procedure depends upon choosing a donor with high axonal count (the spinal
cord), on increasing the number of grafts and on increasing the recipient-graft and
graft donor contact areas. Only through this could several muscles reach motor power
greater than Grade 3 without cocontractions. We managed to increase the recipient-graft
contact area by using closed loop grafting neurorrhaphy [[30 ]]. The graft donor contact area was increased by placing the grafts in an end(graft)-to-side(cord)
and side(graft)-to-side(cord) fashion for about 4 cms along the anterior cord close
to the midline sulcus in a subpial plane.
Increasing the number of grafts, however, is limited by the number of sensory nerves
that could be used as grafts. This incited scientists to develop synthetic nerve grafts.
Actually, a natural nerve graft should be considered as a complex of proportionate
amounts of Schwann cells, neurotrophic factors, cell adhesion molecules and neurite-outgrowth-promoting
factors (such as laminin), all four of which are essential to axonal regeneration
[[71 ]]. Simply applying high levels of neurotrophic factors alone to nerve roots directly
implanted into the ventral horn without adding proportionate amounts of cell adhesion
molecules and neurite-outgrowth promoting factors (laminin) might explain the poor
result obtained by other authors [[63 ],[72 ]]. The adequate exposure provided by our approach allows not only for placing many
side grafts along an extensive donor recipient area, but for associating them with
an expandable amount of synthetic grafts as well.
Limitations of this study
Seventh, we should point out the limitations of this study. We reported cocontractions
and Grade4 shoulder improvement in total avulsions; absence of cocontractions, Grade4-5
shoulder improvement and extension of improvement into the forearm in C5,6ruptures,
C7,8T1 avulsions. These are relatively good results in relatively poor situations.
We attributed this to enhanced side neurotization due the extensive contact areas
between the cord (high axonal load donor) and the grafts proximally and between the
grafts and brachial plexus trunks, divisions and cords distally. This should be weighed,
however, against other aspects: spontaneous recovery despite MRI appearance of avulsions,
fallacies in intraoperative determining of avulsions (wrong diagnosis, wrong level);
small sample size; no controls rule out superiority of this technique versus other
direct cord reimplantation techniques or other neurotization procedures; intra- and
interobserver variability in testing muscle power and cocontractions.
Nevertheless, direct cord implantation is now an established procedure. It is therefore
hoped, the single stage combined anterior (first) posterior (second) approach approach
might stimulate brachial plexus surgeons to go more for direct cord implantation,
whether they use side grafting, fibrin glue, end to end grafting or any other established
neurorrhaphy techniques.
Conclusion
Through providing proper exposure to the brachial plexus and to the cervical cord,
the single stage combined anterior (first) posterior (second) approach might stimulate
brachial plexus surgeons to go more for direct cord implantation. In this study, it
allowed for placing side grafts along an extensive donor recipient area by end-to-side
side-to-side grafting neurorrhaphy and thus improved results.
Consent
Written informed consent was obtained from the patients for publication of the accompanying
images.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
All authors were involved in the conception and design of the study. All authors read
and approved the final manuscript. SMA wrote the rough draft. Brachial plexus exploration
was carried out by SMA, ANM, RERE. Cervical laminectomy was carried out by SMA and
AMK. Extraction of the nerve grafts was performed by AME, AMSA
