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«A Practical Approach to Nerve Grafting in the Upper Extremity David J. Slutsky, MD, FRCS(C) Private Practice, South Bay Hand Surgery Center, 3475 ...»

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Atlas Hand Clin 10 (2005) 73–92

A Practical Approach to Nerve Grafting in the Upper

Extremity

David J. Slutsky, MD, FRCS(C)

Private Practice, South Bay Hand Surgery Center, 3475 Torrance Boulevard, Suite F, Torrance, CA 90503, USA

In this era of tissue bioengineering an autogenous nerve graft may be considered the ultimate

biocompatible, resorbable nerve conduit, with a basil lamina, preformed guidance channels,

a reserve of viable Schwann cells, and nerve growth factors. In addition, it is capable of developing an intrinsic circulation. The nerve graft provides a regenerating axon with a means for passage to the distal nerve stump, while protecting it from the surrounding environment.

There is no foreign body reaction and no graft-versus-host response. An enterprising biotechnology company undoubtedly would have no difficulty marketing this product. The results obtained with nerve autografts constitute the gold standard by which nerve conduits are designed and measured. Despite this seemingly utopian picture, the donor site morbidity and the limitations of nerve grafting have led to a search for alternate methods. This search has been addressed eloquently by Strauch and Chui and their coauthors elsewhere in this issue. This article focuses on the ways in which the nerve responds to injury and how it regenerates, followed by some practical considerations for autologous nerve grafting.

Nerve response to injury Cell body The neuron consists of a central cell body, located within the central nervous system, and a peripheral axon. The axon represents a tremendously elongated process attached to the nerve cell body. Thousands of axons make up the substance of a peripheral nerve. The axon contains 90% of the axoplasmic volume. When a nerve is severed, one immediate consequence is loss of this vital fluid [1]. The normal retrograde transport of neurotrophic factors from the target organ ceases. The cell body undergoes chromatolysis, which includes mitochondrial swelling, migration of the nucleus to the periphery, and dispersal of Nissl substance. The more proximal the site of transection, the more intense the reaction, which peaks by 2 to 3 weeks. The cell body may die and is lost from the neuron pool. If it survives, however, the cell body shifts its resources toward replacing the axoplasm and rebuilding the axon.

Distal axon The distal axon cannot survive without its connection to the cell body and disintegrates (ie, wallerian degeneration). Endoneurial edema occurs within a few hours [2]. The microtubules and neurofilaments of the distal axon, which are responsible for axoplasmic transport, undergo proteolysis by a calcium-activated neutral protease [3]. At 72 hours, the Schwann cells can be seen digesting the myelin sheath and axonal subcomponents [4]. Endoneurial collagen E-mail address: d-slutsky@msn.com

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production from Schwann cells and fibroblasts increases, causing progressive shrinkage of the distal tubules [5]. The Schwann cells rapidly proliferate, forming columns (the bands of Bungner) that appear to stimulate the direction and magnitude of axonal growth.

¨

Proximal axon

After transection, there is demyelination of the distal stump. The axons degenerate to one or more proximal internodes. The distance varies with the severity of injury, ranging from a few millimeters with mild trauma to several centimeters with severe injury [6]. The endoneurial tube lies empty, consisting mostly of the Schwann cell basal lamina.

Axon regeneration

Nerve regeneration does not involve mitosis and multiplication of nerve cells. Instead the cell body restores nerve continuity by growing a new axon. Axon sprouting has been shown 24 hours after nerve transection. One axon sends out multiple unmyelinated axon sprouts from the tip of the remaining axon or collateral sprouts from a nearby proximal node of Ranvier. The distal sprout contains the growth cone; this sends out filopodia [7], which adhere to sticky glycoprotein molecules in the basil lamina of Schwann cells, such as laminin and fibronectin (neurite-promoting factors) [8]. The filopodia contain actin, which aids in pulling the growth cone distally [9]. The basil lamina of two abutting Schwann cells forms a potential endoneurial tube into which the regenerating axon grows. These axons deteriorate if a connection with a target organ is not reached. There are 50 advancing sprouts from one axon. Initially, there are many more nerve fibers crossing a nerve repair than in the parent nerve [10]. Although more than one axon may enter the same endoneurial tube, there is eventual resorption of the multiple sprouts, leaving one dominant axon.

Axons grow 1 to 2 mm/day [11]. The normal 16-day turnover rate of acetylcholine receptors is shortened in denervated muscle to about 4 days [12]. For practical purposes, the maximum length that a nerve can grow to restore motor function is approximately 35 cm. This fact in part accounts for the poor motor recovery when grafting nerve defects proximal to the elbow in adults. Sensory end organs remain viable because there is no end plate and retain the potential for reinnervation [13]. Nerve grafting a digital nerve defect may provide protective sensation even after many years.

Role of the Schwann cell





The importance of maintaining Schwann cell viability in the nerve graft is evident. After nerve transection, the Schwann cell removes the axonal and myelin debris in the severed nerve ends and the nerve graft. Schwann cells produce an immediate source of nerve growth factor, which helps to support the proximal stump [14,15]. The Schwann cell expresses nerve growth factor receptors, which aid in directing the advancing growth cone [16]. It also increases its production of other neurotrophic factors, including ciliary neurotrophic factor, brain-derived neurotrophic factor, and fibroblast growth factor, which promote axonal growth [17]. The laminin and fibronectin in the Schwann cell basil lamina act as a rail for the advanced axon sprouts to grow down. The Schwann cell produces a myelin sheath for the immature axon sprout. Cell biologists have attempted to mimic these functions by incorporating Schwann cells, laminin, fibronectin, and nerve growth factors into synthetically engineered nerve conduits.

Role of the nerve graft

The nerve graft acts to provide a source of empty endoneurial tubes through which the regenerating axons can be directed. Any tissue that contains a basil lamina, such as freeze-dried muscle or tendon, can be substituted [18], but only the autogenous nerve graft also provides a

A PRACTICAL APPROACH TO NERVE GRAFTING IN THE UPPER EXTREMITY

source of viable Schwann cells. To be effective, the graft must acquire a blood supply. If the nerve graft survives, the Schwann cells also survive [19].

Graft incorporation When separated from its blood supply, the graft undergoes wallerian degeneration. Schwann cells can survive 7 days, depending purely on diffusion [19a]. By 3 days after implantation, there is invasion of the nerve graft by endothelial buds from the surrounding tissue bed, with evidence of high nerve blood flows by 1 week [20,21]. This segmental vascular sprouting from extraneural vessels is not limited by the length of the graft [22,23]. The length of the graft is, within certain limits, of no significance to the end result, provided that there is a tension-free anastomosis [24].

The ingrowth of vessels from the ends of the graft (inosculation) does not seem to be of major importance, unless the recipient bed is poorly vascularized [23]. The late phase of nerve graft incorporation shows migration of Schwann cells from the proximal nerve end into the graft and from the graft into both host nerve ends [25].

Graft diameter

Small-diameter grafts spontaneously revascularize, but large-diameter grafts do so incompletely [26]. Thick grafts undergo central necrosis with subsequent endoneurial fibrosis. This fibrosis ultimately impedes the advancement of any ingrowing axon sprouts. Cable nerve grafts are similar to thick grafts. They consist of numerous nerve grafts that are sutured or glued together to match the caliber of the recipient nerve. Because a large percentage of the surface is in contact with another graft and not in contact with the recipient bed, the central portions may not revascularize. With large-diameter recipient nerves, it is preferable to use multiple smaller caliber grafts to bridge fascicular groups in the proximal and distal stumps to increase the surface area that is in contact with the recipient bed.

Nerve biomechanics

A normal nerve has longitudinal excursion, which subjects it to a certain amount of stress and strain in situ. Peripheral nerve is initially easily extensible. It rapidly becomes stiff with further elongation as a result of the stretching of the connective tissue within the nerve [27].

Chronically injured nerves become even stiffer [28]. Elasticity decreases by 50% in the delayed repair of nerves in which wallerian degeneration has occurred [29]. Experimentally, blood flow is reduced by 50% when the nerve is stretched 8% beyond its in vivo length. Complete ischemia occurs at 15% [30]. Suture pullout does not occur until a 17% increase in length; this suggests that ischemia and not disruption of the anastomosis is the limiting factor in acute nerve repairs [31]. This observation also is applicable to nerve grafting.

Nerve is a viscoelastic tissue in that when low loading in tension is applied over time, the nerve elongates, without a deterioration in nerve conduction velocities. Stress relaxation results in recovery of blood flow within 30 minutes at 8% elongation [29]. Intriguing experimental work has been done with gradual nerve elongation to overcome nerve gaps using tissue expansion [32] and external fixation [33], but this cannot be considered an accepted standard of treatment as yet.

A normal nerve can compensate for the change in length with limb flexion and extension because it is surrounded by gliding tissue that permits longitudinal movement. The change in length is distributed over the entire nerve so that the elongation of each nerve segment is small.

A nerve graft becomes welded to its recipient bed by the adhesions through which it becomes vascularized. As a consequence, the nerve graft is exquisitely sensitive to tension because it has no longitudinal excursion. The harvested length of the graft must be long enough to span the nerve gap without tension while the adjacent joints are extended; this is also the position of temporary immobilization. If the limb or digit is immobilized with joint flexion, the graft becomes fixed in this position. When the limb is mobilized at 8 days, the proximal and distal stumps are subject to tension even though the graft initially was long enough. Early attempts at lengthening the graft lead to disruption of the anastomosis.

76 SLUTSKY

Grafting versus primary repair

A tension-free repair is the goal for any nerve anastomosis. When there is a clean transection of the nerve and the gap is caused by elastic retraction, an acute primary repair is indicated. When treatment of a nerve laceration is delayed, fibrosis of the nerve ends prevents approximation, and nerve grafting is indicated even though there is no loss of nerve tissue. As a general rule, primary nerve repair yields superior results to nerve grafting, provided that there is no tension across the anastomotic site [34]. Grafting can obtain similar results to primary repair under ideal conditions [35]. If a nerve is repaired under tension, however, the results are superior with an interpositional graft [36]. Axon sprouts are able to cross two tension-free anastomotic sites more easily than crossing one anastomosis that is under tension [37].

Nerve grafting is indicated to bridge a defect when greater than 10% elongation of the nerve would be necessary to bridge the gap [29]. This is a better indication for grafting than the nerve gap per se, although 4 cm is often used as the critical defect for grafting in the limb [38]. Defects less than this may be overcome by nerve rerouting and transposition in some instances.

Nerve gap

There is a difference between the nerve gap and a nerve defect. A nerve gap refers to the distance between the nerve ends, whereas a nerve defect refers to the actual amount of nerve tissue that is lost. With simple nerve retraction after division, the fascicular arrangement is similar. As the defect between the proximal and distal stumps increases, there is a greater fascicular mismatch between the stumps, which leads to poorer outcomes. Gaps greater than 5 cm have been reported to affect the result adversely [39].

Considerations for donor nerve grafts

Many conditions must be met for a nerve to be considered as a potential graft. First, the relationship between the surface area and the diameter of the graft must be optimal to allow rapid revascularization. The donor site defect from sacrifice of any given nerve must be acceptable for the patient. The harvested nerve must be long enough to ensure a tension-free anastomosis with the adjacent joints in full extension. Finally, the cross-sectional area and number of fascicles should match those of the recipient nerve at the level of injury as closely as possible. For these reasons, most of the available grafts are cutaneous nerves.

Most donor grafts are imperfect matches of the recipient nerve. The fascicular arrangement of the nerve graft is dissimilar to the nerve being repaired in size, number, and fascicular topography. The branching pattern of the grafts usually changes from an oligofascicular pattern proximally to a polyfascicular pattern distally, which typically corresponds to the branching pattern of the recipient nerve. There may be some loss of axon sprouts owing to growth down peripheral branches that leave the nerve graft. Some authors have recommended inserting the grafts in a retrograde manner for this reason, but others belief this is not warranted [24]. The choice of nerve graft is dictated by the length of the nerve gap, the cross-sectional area of the recipient nerve, the available expendable donor nerves for that particular nerve injury, and the surgeon’s preference.

Donor nerve grafts



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