Nerve Reconstruction

Fig. 1.1

Preoperative brachial plexus chart

The British Medical Research Council grading scale is used by most physicians. This system has been further modified by Terzis [13] with intermediate grades of (+) and (−).

In cases of BP injuries, the presence of Horner’s sign is a strong indicator of avulsion of the C8 and T1 roots. Moreover, the absence of a Tinel’s sign in the supraclavicular area is a strong indicator of root avulsion and is a bad prognostic sign because it indicates lack of intraplexus donors for reconstruction. On the other hand, a positive Tinel’s sign is a strong indicator of roots connectivity with the spinal cord.

The initial electrodiagnostic evaluation of the upper extremity should include needle electromyography and nerve conduction studies. Axonal discontinuity results not only in predictable pathologic features but also in time-related electrical changes that parallel the pathophysiology of denervation. Wallerian degeneration results in the emergence of spontaneous electrical discharges for at least 3 weeks after the injury. Therefore, a needle electromyogram should be postponed for at least that long and preferably carried out at 6 weeks.

The lamina test is performed in cases of adult BP injuries. Tiny volleys of electrical stimulation are applied at the level of each foramen on each exiting root to determine whether the patient perceives the area of the dermatome innervated by this root. A positive response would be strong evidence against avulsion.

Depending on the mechanism of injury and the location of the nerve lesion, radiologic imaging may be necessary to confirm or support a diagnosis of a nerve injury. In cases of BP injuries, imaging studies (such as myelography, CT myelography, and magnetic resonance imaging) are used in order to detect abnormalities of the nerve roots (such as traumatic pseudomeningocele, deformity of nerve root sleeves, dural scar, and nerve root avulsion). A combination of myelography with computed tomography of the cervical spine is used to identify root avulsions (Fig. 1.2). In case of previous vascular injury and subsequent reconstruction, angiography should be employed to investigate the blood supply of the extremity and to identify any vascular compromise (Fig. 1.3).

Fig. 1.2

CT Myelography showing root avulsion. (a) Myelography of the Cervical spine in a patient with multiple root avulsions (arrows). (b) Example of CT myelography in a patient with severe right brachial plexus injury. Note avulsed root on the right (arrow)

Fig. 1.3

Angiography of upper extremity in cases of vascular injury. (a) Angiography of right upper extremity. Note interruption of (R) subclavian artery (arrow). Axillary artery receives flow from collateral vessels. (b) Normal angiography of left upper extremity

Treatment Options

Principles of Nerve Repair

The basic principles of nerve repair include a sequence of eight basic principles that represent the basis of the microsurgical management of the nerve injured patient [14]:

Preoperative assessment of motor and sensory function

Adequate debridement of the proximal and distal nerve stumps in order to allow nerve regeneration to proceed across the repair site

Utilization of microsurgical techniques

Tension-free repair

When a tension-free repair is not possible, use of other techniques for nerve repair; nerve grafts, end-to-side nerve repair or nerve transfers

Primary repair; when this is not possible, delay repair for approximately 3 weeks when the ‘zone of injury’ is clarified

Utilization of a nerve repair technique that allows early protected range of motion to permit nerve gliding

Occupational and physical therapy in order to maximize the clinical outcome

Timing of Nerve Repair

A primary nerve repair is defined as reconstruction shortly after the injury. Secondary repair is defined as occurring at a later period after injury. Several investigators have reported that nerve repair is better when performed within 6 weeks of injury and several studies have shown primary repair to be superior to secondary repair as long as the tissue bed is adequate [15, 16].

In general, nerve injuries associated with open wounds require early exploration except from gunshot wounds, which are more appropriate to be treated as closed or blunt trauma. In crush nerve lesions or injuries associated with significant soft tissue damage it can be difficult to estimate the extent of the zone of injury. In these cases, a delayed repair, after 3 weeks, is indicated, when the zone of injury becomes better demarcated and the extent of scar tissue can be easily defined.

In closed or blunt trauma, initial management is expectant with close observation. If complete recovery is not observed within 6 weeks, electrodiagnostic studies should be obtained for baseline evaluation. If at 12 weeks complete recovery has not occurred, repeat electrodiagnostic studies should take place. Presence of increase of motor units potentials in electromyography is an indicator that spontaneous reinnervation most likely will follow. Lack of signs of reinnervation (clinical or electrical) at 12 weeks post injury requires surgical exploration.

BP injuries are worth specific consideration regarding the timing of exploration and reconstruction. Such injuries require extra care since BP injuries usually come with other associated injuries including fractures, vascular injuries and associated soft-tissue injury. Although exploration of the BP injury may need to be performed with a slight delay, the modern management of BP injuries is early aggressive microsurgical reconstruction [17].

Techniques of Nerve Repair

In general, nerve exploration and repair should be performed under high magnification of the operating microscope. Exploration always takes place proximal and distal to the lesion site until normal nerve to inspection and palpation is encountered. If the history and physical examination is suspicious of double level injury then the entire length of the nerve needs to be explored. The ideal scenario for nerve repair is end-to-end coaptation of the nerve stumps.

The procedure of repairing a nerve trunk can be divided into four steps. After the zone of injury is defined, the nerve endings are cut back to healthy fascicles. Then, the nerve ends are approximated keeping in mind the importance of considering the length of the gap and possible tension at the coaptation site. If additional nerve length is required, releasing constricting fascia, dividing adventitia attachments, dissecting any tethering bands, transposing nerves (e.g. ulnar at elbow) and flexing neighboring joints (e.g. wrist for median and ulnar lesions in Zone 5) will mobilize the nerve further. Tensionless repairs have demonstrated superior results. Exceeding 10 % of the resting length of the peripheral nerve has been shown to decrease blood flow to the nerve by 50 % [18]. Tension is assessed intra-operatively to determine the need for grafting. A good rule of thumb is that if nerve ends can be approximated with 8-0 sutures, then grafting is not required.

The next step is the correctly aligned coaptation of the nerve ends. Last step is the maintenance of nerve repair with microsutures (9-0 or 10-0 nylon) which are inserted into the epineurium. Placement of the sutures should avoid malrotation of the nerve ends.

Epineurial repair has been shown to have similar functional results to group fascicular repair in smaller, more distal nerves [19]. Group fascicular repair is preferred in larger nerves where motor and sensory fasicles can be accurately matched (most notably the ulnar nerve below the elbow). The cross-sectional appearance of the proximal and distal stumps should be carefully inspected under high magnification prior to proceeding with the nerve repair.

The accuracy of nerve apposition at the repair site influences the functional restoration. Presently, anatomic axon-to-axon reconnection and normal restoration of function after significant nerve injury remain an unobtainable goal. Electrophysiologically-aided motor- and sensory- fascicle differentiation has been an important tool that facilitates our ability to depict the intraneural composition of sensory and motor bundles prior to nerve coaptation [20]. In 1976, Williams and Terzis [21] introduced single fascicular recordings as an intraoperative diagnostic tool for the management of peripheral nerve lesions in continuity which was a new method of sophisticated intraoperative differentiation between motor and sensory components.

Several histochemical methods have been developed to permit differentiation of motor and sensory fibers. The enzyme carbonic anhydrase can differentiate between motor and sensory fascicles of peripheral nerves [22] (Fig. 1.4). The application of this staining method to human peripheral nerve was first described by Riley and Lang in 1984 [22] and later modified for widespread clinical use by Carson and Terzis in 1985 [23]. Although it can provide a convenient method for identifying predominantly sensory versus motor fascicles in cut ends of peripheral nerves, its use depends on the surgeon’s experience, available operating time and existence of an experienced laboratory in nerve histochemistry. Acetylcholinesterase histochemistry was also used in conjunction with peripheral nerve surgery, this enzyme in contrast to carbonic anhydrase, is present only in motor fibers [24].

Fig. 1.4

Example of Carbonic Anhydrase staining. (a) Cross section of a motor fascicle. Note lack of axonal staining with the carbonic anhydrase (arrows). (b) Cross section of a sensory fascicle. Note dark staining of the axons (arrows)

End-to-End-Repair

The surgeon should be familiar with the various techniques available and tailor them to the situation, taking into account which nerve is injured and the level of the injury in the upper extremity. The basic choices include epineurial repair, group fascicular repair, fascicular repair or a combination of those techniques. The goal is to achieve tension free coaptation and proper alignment.

In the epineurial repair, coaptation is achieved by single epineurial stitches in the epineurium along the circumference of the nerve. A perfect superficial alignment can be achieved using epineurial vessels as landmarks, but the internal orientation of fascicular bundles and individual fascicles may not be correct. This method is indicated when one or only few fascicles are injured and is appropriate for distal nerve repairs (digital nerves).

In group fascicular repair, fascicular groups are coapted with single sutures in the perineurium or perifascicular connective tissue which surrounds groups of fascicles. Prior to coaptation, the fascicular groups need to be identified and matched together. In large nerves with multiple fascicles, nerve regeneration can be enhanced by use of this technique.

In fascicular repair, coaptation of individual fascicles is achieved by 10-0 or 11-0 microsutures in the internal epineurium surrounding individual fascicles. This type of repair is not feasible unless it can be performed with minimal tension.

End-to-Side Nerve Repair (Fig. 1.5)

Fig. 1.5

Example of end-to-side nerve repair. Example of an end-to-side neurorrhaphy in an obstetrical brachial plexus case. An epineurial and perineurial window has been made on the phrenic nerve. An interposition nerve graft (arrow) is coapted by end-to-side repair at the site of the window. The nerve graft is targeted to neurotize the musculocutaneous nerve (not shown). Because an end-to-side coaptation was used there is no downgrading of the function of the ipsilateral diaphragm

The idea of end-to-side nerve repair was popularized by Viterbo et al. in 1992 [25] after its introduction a century ago [26]. This technique allows for additional muscle reinnervation with minimal detriment to donor-nerve function [25]. Using this technique a neurorrhaphy is created between the proximal end of an injured nerve and the side of an uninjured donor nerve by simple microsurgical attachment at the site of a window (epineurial and/or perineurial window).

The efficacy of end-to-side neurorrhaphy has been established in several rat models. Noah et al. [27] suggested that more axons went through the coaptation site when a perineurial window or partial neurectomy was created in the donor-nerve prior to coaptation vs leaving the perineurium or epineurium intact. Okajima et al. [28] studied the early regenerative response after end-to-side neurorrhaphy and were able to identify increased nodal sprouting proximal to the perineurial window and/or partial neurectomy groups vs the intact epineurium group.

In clinical practice, Terzis [29] used end-to-side neurorrhaphy extensively in order to minimize morbidity from the various extraplexus donors. Thus, only the number of donor fibers needed are taken, such as in partial phrenic or partial hypoglossal transfers, which are used in combination with an end-to-side coaptation via an interposition nerve graft especially in cases of facial paralysis and obstetrical BP reconstruction.

Nerve Grafting (Fig. 1.6)

Fig. 1.6

Example of a case treated with interposition nerve grafting. A 19 year old boy was involved in an accident in which he sustained a glass laceration of the volar aspect of his right dominant wrist. He presented 18 months later to our Center with complete anesthesia of the thumb, index and radial side of the middle finger and had no thumb opposition (a, b). On exploration, a large median nerve neuroma was present (c, d). The neuroma was excised and the defect was reconstructed with five interposition sural nerve grafts (e). Eight months later, he also had opponensplasty which involved transfer of the sublimis tendon from the ring finger to the thumb to augment opposition. Upon follow-up the patient showed adequate pinch (f) and strong thumb opposition (g). Sensory return to the radial side of his hand has been satisfactory, enabling him to return to his previous work

When tension-free repair is not possible, a suitable alternative must be pursued. The surgical technique employed in these alternatives is similar, whether it be a nerve graft or nerve transfer.

Nerve grafting has long been considered the ‘gold standard’ for repair of irreducible nerve gaps. The choice of autogenous graft is dependent on several factors: the size of the nerve gap, location of proposed nerve repair, and associated donor-site morbidity.

Before grafting, the proximal and distal nerve stumps must be prepared to normal tissue outside of the zone of injury. In cases of polyfascicular nerve stumps, interfascicular dissection is preferred in order to prepare corresponding fascicular groups. The intraneural topography of both nerve stumps is obtained by means of intraoperative electrodiagnostic studies and carbonic anhydrase histochemistry.

Then, the defect size is measured and the nerve grafts are harvested. The nerve grafts are then tailored so that they bridge corresponding fascicular groups. The proximal end of each graft is coapted to the proximal fascicular group and its distal end to the corresponding distal bundles.

Selection of the graft donors is limited by the availability of donor nerves and the functional and aesthetic deficits created by their harvest. According to Sunderland and Roy [30] the ideal donor-nerve should possess the following characteristics:

the sensory deficit should occur in a non-critical area of the body

the donor-nerve should possess long, unbranched segments

the donor-nerve should easily be accessible and reliably located

the donor-nerve should be of overall diameter and possess large fascicles with little interfascicular connective tissue and few interfascicular connections

The commonly used donor-nerves available for grafting are typically the sural nerve, the saphenous nerve, the medial brachial cutaneous nerve and the lateral antebrachial cutaneous nerve.

Vascularized Nerve Grafts (Fig. 1.7)

Fig. 1.7

Example of a case with Vascularized Nerve Grafts. This is a 23 year old male who was involved in a boating accident in which the propeller of a motor boat ran over his left arm. He was taken emergently to a local hospital where he was noted to have severe neurovascular injuries as well as tissue loss of the left forearm. He received elsewhere emergency revascularization of his left extremity with the use of saphenous vein grafts. He also had multiple levels of nerve injuries of the left ulnar and median nerve. Preoperative view of the patient (a, b). Three months later, he underwent reconstruction of his left median nerve which was transected at four levels (c above). The sensory part of the superficial and deep peroneal nerves based on their common vascular supply was harvested and used to reconstruct the motor portion of the median nerve (3 × 15 cm, one deep and two superficial peroneal nerve grafts). Nonvascularized sural nerve grafts were used to reconstruct the sensory portion of the median nerve (2 cables × 15 cm proximally and 8 cables × 5.5 cm distally: c below). Close-up of the proximal coaptation: vascularized nerve grafts on the left, nonvascularized sural nerve grafts on the right (d). Seven months after the injury he underwent reconstruction of the left ulnar nerve utilizing vascularized saphenous nerve graft (1 cable × 30 cm) for the motor portion of the ulnar nerve and sural nerve graft for the sensory component of the ulnar nerve (e). Four years postoperatively, we can see very good results. Powerful finger flexion, thumb opposition, and intrinsic function (f–i). He can easily pick up a can of soda (j) and has never had any morbidity in the donor extremity (k) (Requested permission from: Terzis and Kostopoulos [67])

The first vascularized nerve graft in the upper extremity was a pedicled nerve graft in 1945 by St. Clair Strange for reconstruction of large nerve defect: the ulnar nerve was transferred in two stages to reconstruct the median nerve [31]. Taylor et al. [32] used the superficial radial nerve as a vascularized nerve graft, to repair a large defect of a median nerve.

In 1984, Breidenbach and Terzis [33] defined the blood supply of peripheral nerves that could be used for microvascular transfer and introduced a classification of the blood supply of nerves based on the number of dominant vascular pedicles.

The clinical indication for a vascularized nerve graft is a scarred recipient bed that will not support a nonvascularized nerve graft. In cases of long gaps, vascularized nerve grafts can be placed in association with nonvascularized nerve grafts to cover the cross-sectional area of the injured nerve. The obvious advantage of this technique is the ability to provide immediate intraneural perfusion in a poorly vascularized bed and to reconstruct large nerve defects.

The use of vascularized nerve grafts is particularly important in BP surgery. In cases of avulsion of the C8 and T1 roots, the ulnar nerve should be used as a vascularized nerve graft for ipsilateral plexus reconstruction or as a cross-chest nerve graft from the contralateral C7 root for neurotization of the denervated upper extremity [34] (Fig. 1.8).

Fig. 1.8

Example of a cross chest vascularized ulnar nerve graft. Cross chest vascularized ulnar nerve graft prior to tunneling. The proximal ulnar will be coapted to the anterior division of the right C7 root. The distal ulnar nerve will be coapted to the median nerve of the left paralyzed extremity. Arrow points to the metal “passer” that will be used to transfer the nerve across the chest

Breidenbach and Terzis [35] first reported that the ulnar nerve can be transferred in its total length on the superior ulnar collateral vascular pedicle (Fig. 1.9). Terzis subsequently reported a series of 151 vascularized ulnar nerve grafts for posttraumatic BP palsy patients [34]. According to this study, pedicled or free vascularized ulnar nerve grafts achieved superior results compared to those obtained with conventional nerve grafts.

Fig. 1.9

Example of ulnar nerve harvested as a VNG next to the arm. Exploration of the right vascularized ulnar nerve graft prior to microvascular transfer. The entire length of the nerve receives its blood supply from the superior ulnar collateral vascular pedicle. Terzis’ method for the use of the free vascularized ulnar nerve for ipsilateral intraplexus reconstruction. The epineurium is transected longitudinally without compromising the longitudinal epineurial blood supply and the fascicles are transected transversely. The blood supply is maintained through the folded epineurium

Technique

Using this technique, the ulnar nerve with its supplying vascular pedicle is transferred as a pedicle or free vascularized nerve to bridge several nerve defects. The vascular pedicle is anastomosed to an artery and a vein of the recipient site and subsequently the nerve coaptations take place. The vascularized ulnar nerve graft is folded into segments maintaining their vascular connections according to the technique proposed by Terzis and Kostopoulos [34] (Fig. 1.10). In this situation, the longitudinal blood supply of the epineurium of the ulnar nerve is preserved while the intraneural contents are transected to address the bridging nerve defects, thus maintaining excellent blood supply throughout the vascularized ulnar nerve graft. In more distal lesions, vascularized fascia can be used to improve the blood supply of the underlying bed by enveloping the nerve reconstruction (Fig. 1.11).

Fig. 1.10

Terzis’ technique of using the vascularized ulnar nerve for ipsilateral BP reconstruction. Terzis’ technique of folding the vascularized ulnar nerve graft into segments while maintaining its blood supply by preserving the integrity of epineurial vessels

Fig. 1.11

Example of a vascularized fascia to improve the blood supply of nerve grafting in an unfavorable recipient bed. (a, b) Patient with right carpal tunnel syndrome and pain secondary to severe crush injury of the right distal forearm and hand. Note lack of opposition of the right thumb (a). Upon exploration a large neuroma in continuity of the median nerve was apparent (b). Extensive microneurolysis under high magnification of the operating microscope took place along with the transfer of a vascularized posterior calf fascia to envelop the nerve at the wrist. (c) The vascularized posterior calf fascia has been outlined in the non-dominant lower extremity. (d) The vascularized fascia flap after harvesting. (e) The vascularized fascia on the right wrist prior to microvascular anastomoses. (f, g) On the last follow-up, note excellent pinch and opposition. In addition, the patient is pain free and has returned full time to his job as a jeweler

Ulnar Nerve

Cases of global plexopathy with avulsion of the lower roots and rupture of the upper roots provide the best indication for using the ipsilateral ulnar as a vascularized graft for BP reconstruction. The ulnar nerve can be harvested on the superior ulnar collateral vascular pedicle. The superior ulnar collateral artery is sufficient to maintain the blood supply for the total length of the ulnar nerve (Fig. 1.9).

If used for ipsilateral BP reconstruction, the nerve is transected in the appropriate segments to bridge the nerve defects always preserving the epineurial blood supply (Fig. 1.10).

If used for neurotization of the median nerve from the contralateral C7 (cC7) root then the nerve is harvested as a free vascularized cross-chest graft (Fig. 1.8) and the superior ulnar collateral vascular pedicle is anastomosed to the transverse cervical vessels of the unaffected side prior to nerve coaptations of the proximal ulnar end with the anterior division of the cC7. Subsequently, the distal part of the ulnar nerve is coapted to the median nerve on the affected side.

Sural Nerve

Vascularized sural nerve graft for extremity nerve reconstruction should be used as a free vascularized nerve graft based on the sural artery, if available, or with an arterialized saphenous vein that is transferred in conjunction with the sural nerve (Fig. 1.12).

Fig. 1.12

Use of ipsilateral sural as a vascularized nerve graft for lower extremity nerve repair reconstruction. (a–f) A 41 year old male, who suffered a propeller injury and sustained a laceration at his right popliteal fossa. He presented to our Center with a right foot drop (a). Intraoperative view of the severed peroneal nerve stumps and the created five centimeter defect (b). Intraoperative view of the common peroneal nerve reconstruction using a combination of vascularized and nonvascularized sural nerve grafts (c, d). Patient at his last follow-up demonstrates excellent dorsiflexion of his right foot and is walking without a splint (e, f)

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