Current Surgical Techniques of Peripheral Repair Kasra Rowshan, MD, Neil F. Jones, MD, and Ranjan Gupta, MD

Transection of peripheral results in Wallerian degeneration of the distal stump with varying degrees of degeneration in the proximal stump. After degeneration, the proximal undergoes regenerative changes to make an appropriate connection with the degenerated distal segment. To improve recovery, surgical techniques have evolved to facilitate connection of the proximal to the distal stump. Current surgical strategies include epineurial and group fascicular repair under minimal tension at the repair site. We discuss the widely accepted surgical approaches to the repair of peripheral nerves and the issues to consider when selecting the appropriate surgical technique. Oper Tech Orthop 14:163-170 © 2004 Elsevier Inc. All rights reserved.

KEYWORDS peripheral nerve, , nerve repair, microsurgery, , Wallerian degeneration

ransection of a peripheral nerve results in significant and to sensory, motor, and autonomic making the appro- Tcomplex changes in the proximal and distal nerve seg- priate connections with their distal organs. Such results are ments. An understanding of subsequent cellular changes is dependent on and influenced by the severity and extent of essential to determine the proper timing and technique of injury, timing of repair, fascicular anatomy and re-alignment, nerve repair to produce optimal functional results. After tran- surgical technique, patient age, and underlying patient issues section, Wallerian degeneration will occur in the distal por- and morbidity. tion of the nerve. These histological changes are character- ized by axonal degeneration of both myelinated and Peripheral Nerve Anatomy unmyelinated fibers, degradation, and subsequent Schwann cell proliferation. There are also changes within the Proper understanding of both the timing and technique of proximal segment of the damaged nerve to help prepare the nerve repair require a clear and complete understanding of for regeneration. The extent of the degeneration de- peripheral nerve anatomy. The peripheral nerve is composed pends on the severity of injury. The proliferating Schwann of motor, sensory, and sympathetic nerve fibers. Such fibers cells in the distal nerve begin to organize themselves into can be either myelinated or unmyelinated. The average diam- columns, known as Bands of Bugner, which will support eter of myelinated fibers is 2 to 22 ␮m1 and unmyelinated subsequent regeneration from the proximal stump of the sev- axons are 0.4 to 1.25 ␮m.2 Surrounding the individual my- ered nerve into the distal environment. After a period of elinated nerve fibers or the group of unmyelinated nerve axonal degeneration and Schwann cell proliferation, axons fibers is the , a collection of thin collagen from the proximal stump will sprout in attempts to re-inner- strands that provide adequate nourishment and protect the vate the distal stump. Unless the neural injury is the result of individual axons. Multiple nerve fibers collect to form a crush injury where the nerve architecture is relatively pre- group of fibers called a fascicle. Such fascicles are bound and served, spontaneous re-innervation of the distal segment by encircled by the , a collection of a connective the proximal stump usually does not occur. When a nerve tissue sheath composed of perineurial cells. The perineurium fiber is divided, surgical nerve repair is required. is the major contributor to the nerve’s tensile integrity and The primary aim of surgical intervention is to direct the strength and is also the blood–nerve barrier. Several fascicles regenerating proximal fibers into the environment of the de- may be arranged into a group fascicle surrounded by connec- generating distal stump. An effective repair is directly related tive tissue, termed the internal or interfascicular epineurium. The that surrounds the periphery of the entire nerve is called the external or extrafascicular Peripheral Nerve Research Lab, Department of Orthopaedic Surgery, Uni- epineurium. The primary function of this connective tissue versity of California, Irvine, Irvine, CA. Address reprint requests to: Ranjan Gupta, MD, Peripheral Nerve Research structure is to nourish and protect the fascicles. Lab, Department of Orthopaedic Surgery, University of California, Ir- Fascicular patterns are divided into the following 3 types: vine, Medical Sciences I, Room B120, Irvine, CA 92697. monofascicular, oligofascicular, and polyfascicular.3 Mono-

1048-6666/04/$-see front matter © 2004 Elsevier Inc. All rights reserved. 163 doi:10.1053/j.oto.2004.06.006 164 K. Rowshan, N.F. Jones, and R. Gupta fascicular patterns consist of one large fascicle, whereas oli- gofascicular patterns consist of a few fascicles; polyfascicular patterns consist of many fascicles of varying sizes that can be arranged with or without groupings of fascicles. Nerves found in the upper arm are routinely polyfascicular.4 In its course from the upper arm to the fingertips, a peripheral nerve will undergo changes from polyfascicular pattern in the upper arm, oligofascicular in the elbow region, and monofas- cicular in the hand and fingers.5 For example, the ulnar nerve is polyfascicular as it exits the brachial plexus until just before the elbow, at which point it becomes oligofascicular. After the division into the motor branch at the wrist, the pattern is monofascicular. These patterns may help to determine which type of nerve repair is appropriate for a particular nerve in- jury. In surgical nerve repair, proper identification of fascic- ular arrangement is crucial to achieving a successful out- come. Peripheral nerves are extensively vascularized with sepa- rate yet interconnected microvascular systems in the epineurium, perineurium, and endoneurium.6,7 The vascular pattern of the peripheral nerve is characterized by longitudi- nally oriented groups of vessels, with a great number of com- municating anastomoses.7 The vasculature is composed of an intrinsic vascular system consisting of vascular plexa in the epineurium, perineurium, and endoneurium and an extrin- sic system derived from closely associated vessels running with the nerve. From a surgical perspective, the role of the intraneural microvascular system is vital in regards to the effects of chronic irritation, compression, mobilization, stretching, and transection. If considering a group fascicular or fascicular repair technique, the effects of intraneurial vas- cular damage secondary to surgical manipulation need to be considered.5 Figure 1 Schematic depiction of the different types of nerve repair General Principles after laceration. in Surgical Repair tension, and 8-0 had a tendency to pull off the repaired nerve The primary purpose of nerve repair is to correctly approximate endings.9 However, 10-0 or 8-0 suture is often used based on the severed nerve segments in hopes of achieving functional the size of the nerve to be repaired. re-innervation of the end organs. Four general principles for Surgical repair of peripheral nerves requires the use of an proper coaptation of divided nerves have been outlined.8 Ini- operating microscope, loupes, microsurgical instruments, bi- tially, preparation of the stumps is accomplished surgically with polar cautery, nerve sectioning knife, and appropriate nylon either a number 11 scalpel blade, an ophthalmic knife, or a sutures with 50- to 100-␮m needles.10 Nerve-wrapping ma- sterile razor blade against a wooden disposable tongue blade. terials are not recommended at the site of repair because they After this, the surgeon should be able to identify and separate have been shown to increase neural edema and may impair individual fascicles or group fascicles. Trimming the nerve ends blood supply.10 Traditionally, neurorrhaphy is performed removes dead or severely damaged tissue. Second, trial approx- without tension at the site of repair. It is the current practice imation of the proximal stump to the distal stump is attempted of most hand surgeons to attempt nerve coaptation of major to gauge the amount of tension necessary, which is related to the peripheral nerves with two 8-0 nylon sutures within the length of the gap between the stumps. Third, coaptation or nerve epineurium. If the nerve cannot be approximated with neurorrhaphy of the nerve stumps is performed, which de- these 2 sutures, then a nerve graft should be strongly consid- scribes the apposition of corresponding nerve ends with special ered. However, studies in primates have shown that direct attention to bringing fascicles into optimal contact. Direct coap- repair under modest tension yields better results relative to a tation can oppose stump-to-stump, fascicle-to-fascicle, or group tension-free repair,11 but this remains controversial. Further- fascicle-to-group fascicle in the corresponding ends (Fig. 1). An more, primate studies have shown that a direct nerve repair indirect coaptation can be performed by interposing a nerve under tension may perform better than a nerve graft.12 Cur- graft. Lastly, maintenance of coaptation must be achieved with rently, most hand surgeons agree that if a tension-free or the use of nonabsorbable sutures, glue or a natural fibrin clot. minimal tension repair is not possible, then an interposition Giddins et al showed that 9-0 monofilament nylon suture with- nerve graft should be used. Postoperative sensory re-educa- stood the greatest distractive force, whereas 10-0 failed under tion is critical to ensure maximal outcome.13 Surgical techniques of peripheral nerve repair 165

Figure 2 (A) Median nerve laceration at the wrist before repair. (B) Median nerve after .

Epineurial Repair site. A second suture is then placed in the same manner. The Epineurial repair is the traditional method of repair for sev- remaining epineurium is closed by halving the distance on ered peripheral nerves. Initially, the surgeon sections the both the anterior and posterior aspects of the nerve. The nerve ends until all visible signs of the damage have been number of sutures varies depending on the nerve thickness; a removed and a fascicular pattern can be seen.4 The goal of digital nerve may only require 2 or 3 sutures, whereas the successful repair is to establish continuity of the nerve with median or ulnar nerve at the wrist or elbow may require 8 to proper rotational alignment and without tension. Rotational 10 sutures. If the severed nerve cannot be approximated with alignment of both stumps is performed either by aligning an two 8-0 nylon sutures, then the tension within the nerve is external marker such as a vessel on the surface of the proxi- considered excessive and a nerve graft should be performed. mal and distal nerve or by matching the mirror images of the Proper care must be taken to ensure that no fascicles protrude fascicular pattern in the proximal and distal nerve ends. between the suture lines (Fig. 2). Coaptation is achieved with nonabsorbable sutures of ei- ther 8-0 nylon for larger nerves or 10-0 nylon for smaller Group Fascicular Repair nerves. The first suture is passed through the epineurium In theory, group fascicular repair is a more accurate tech- proximally and distally and then tied so that the nerve ends nique of nerve repair. Initially, the nerve ends are sharply just “kiss” each other, ensuring minimal tension at the repair divided and the anatomical cross-sectional appearance of 166 K. Rowshan, N.F. Jones, and R. Gupta

Figure 3 (A) Ulnar nerve laceration at the wrist before repair. (B) Dissection of 3 group fascicles. (C) Ulnar nerve after group fascic- ular repair. Surgical techniques of peripheral nerve repair 167

Figure 4 (A) Epineurial sleeve before nerve repair. (B) The back wall of the epineurial sleeve has been repaired and the group fascicles are partially repaired.

both the proximal and distal nerve stumps are examined weighed against the potential increased fibrosis associated under the microscope to determine corresponding groups of with greater dissection and more intraneural suture material. fascicles.4 Each group fascicule may be slightly separated by Technically, the external epineurium must be dissected dissection between the group fascicles, or if matching group with special care taken to preserve the adjacent perineurium, fascicles are easily visualized, no further dissection is neces- which carries the blood supply to the nerve. Individual group sary. Each group fascicle, usually 3 to 5 in the proximal fascicles are identified under the operating microscope in the nerve, is coapted to its corresponding group fascicle in the proximal and distal nerve ends (Fig. 3). Two sutures are distal nerve with 2 to 4 9-0 nylon sutures placed through the placed through the perineurium or internal epineurium at internal epineurium or perineurium.8,14-16 If motor and sen- 180° from one another for each group fascicle, but occasion- sory group fascicles are appropriately aligned, motor-to-mo- ally 3 or even 4 sutures may be necessary. Nylon suture tor and sensory-to-sensory, then this technique offers a sig- (10-0) with a 70- or 50-␮m needle is preferred. Usually 3 to nificant advantage over an epineurial repair. This would 5 group fascicles are copated in a median or ulnar nerve reduce the chances of motor axons being directed down en- repair at the wrist or forearm level. Traditionally, after group doneurial tubes to sensory end organs or sensory axons being fascicular repair, the epineurium is also sutured to provide directed down endoneurial tubes to motor endplates.17 The additional support and alignment. Occasionally, a flap of potential benefit of this technique, however, must be epineurium can be dissected off each of the proximal and 168 K. Rowshan, N.F. Jones, and R. Gupta

Figure 5 (A) Radial digital nerve laceration at the distal interphalangeal joint. (B) High-power view of the nerve ends. (C) High-power view of repaired digital nerve with epineurial technique. (D) Repaired radial digital nerve. Surgical techniques of peripheral nerve repair 169 distal ends, and this epineurial flap is sutured with 6-0 nylon to take the tension off the subsequent group fascicular repair (Fig. 4).18 However, studies in primates have shown that there is no difference in outcome whether the epineurium is resected or repaired in conjunction with group fascicular nerve repair.19,20

Epineurial Versus Group Fascicular Repair There have been multiple basic science experimental21-23 and clinical studies23 comparing the various surgical repair tech- niques. No significant data or evidence indicates that any one technique is better. However, experimental studies in rats have shown that there is an improved specificity of muscle re-innervation after fascicular repair relative to epineurial re- pair of the sciatic nerve.17,24 Additionally, studies comparing epineurial to intrafascicular perineurial repairs have demon- strated no advantages for either of the surgical proce- dures.21,25 There have been no randomized clinical trials to date to compare epineurial and group fascicular repair in humans. In theory, group fascicular repair should produce a better clinical outcome. However, the potential benefits of im- proved fascicular matching may not be realized secondary to the increased surgical manipulation, leading to fibrosis and the possibility of fascicular mismatch.26 Although epineurial alignment is less precise, it may allow for a neurotrophic effect to influence the direction of axonal sprouting and growth. This may explain why an epineurial repair usually Figure 6 Repair of radial and ulnar digital nerves with epineurial produces a similar outcome when compared with a group repair technique. fascicular repair. Perhaps the technical aspects of group fas- cicular repair prohibit the realization of the theoretical ad- vantages of this technique. any sensation. Alternatively, immunohistochemistry may It is therefore recommended that both techniques be help to differentiate between motor and sensory axons. Gu et considered and employed in repairing a damaged nerve.27 al showed that blue-SAb staining for 30 minutes accurately The technique selected depends on the nature and loca- identified sensory fascicles without later adverse effects on 28 tion of injury, the timing of nerve repair, and the identifi- the growth and metabolism of . Carbonic anhy- cation of the fascicular arrangement in the nerve. If an drase staining of sensory fascicles and acteylcholinesterase acute injury results in a sharp clean laceration, an epineur- staining of motor fascicles will allow differentiation of the ial repair can usually be performed because surface land- motor and sensory group fascicles, but this technique is 29 marks can be used to align nerve ends. Digital nerves are rarely used clinically. always repaired with an epineurial technique (Figs. 5 and The location of the in the extremity is of 6). If a specific motor or sensory group fascicle can be critical importance. Proximally, the fascicular pattern is com- identified by distal dissection of the distal nerve stump, monly polyfascicular, mandating an epineurial repair. Dis- then a group fascicular repair may be performed. The re- tally, nerves are routinely mono- or oligofascicular. In such a mainder of the repair can be completed with epineurial pattern, it is appropriate to carry out a group fascicular repair technique. with a minimum number of sutures. Individual fascicular Various techniques have been used to determine the spe- repair is usually not recommended except when repairing cific function of each group fascicle. Visual matching of the small, near-terminal branches of digital nerves. “mirror images” of the group fascicular pattern in the proxi- mal and distal nerve ends is the simplest method. However, Evaluation of Functional in crushing and avulsion injuries, topographic matching may Recovery after Nerve Repair be difficult. Electrical stimulation can be used to identify sensory group fascicles by inducing sensation in the awake The Medical Research Council developed a widely accepted patient (Triepel and Koman, this issue). Although distal grading system for nerve recovery after nerve repair (Table nerve degeneration begins within the first 48 hours of injury, 1).30,31 Sensory recovery is graded on a scale from S0–S4 and stimulating the motor group fascicle in the distal nerve will motor function from M0–M5, based on physical examina- produce contraction of the thenar or interosseous muscles. tion. Semiobjective measurements of recovery Stimulating the proximal motor fascicle should not induce include density testing with the use of static and moving 170 K. Rowshan, N.F. Jones, and R. Gupta

Table 1 Medical Research Council System for Grading Nerve 6. Bell MA, Weddell AG: A morphometric study of intrafascicular vessels Recovery of mammalian sciatic nerve. Muscle Nerve 7:524-534, 1984 7. Lundborg G: The intrinsic vascularization of human peripheral nerves: Motor recovery structural and functional aspects. J Hand Surg [Am] 4:34-41, 1979 M0 No contraction 8. Millesi H, Terzis JK: Nomenclature in peripheral nerve surgery. Com- M1 Return of perceptible contraction in the proximal mittee report of the International Society of Reconstructive Microsur- muscles gery. Clin Plast Surg 11:3-8, 1984 M2 Return of perceptible contraction in the proximal and 9. Giddins GE, Wade PJ, Amis AA: Primary nerve repair: Strength of distal muscles repair with different gauges of nylon suture material. J Hand Surg [Br] M3 Return of function in proximal and distal muscles to 14:301-302, 1989 10. Gorman PW, Dell PC: Instrumentation for nerve repair, in Gelberman such a degree that all important muscles are RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, sufficiently powerful to act against gravity Lippincott, 1991, pp 275-85 M4 All muscles act against strong resistance, and some 11. Wood MB: Peroneal nerve repair. Surgical results. Clin Orthop 267: independent movements are possible 206-210, 1991 M5 Full recovery of all muscles 12. Hentz VR, Rosen JM, Xiao SJ, et al: The nerve gap dilemma: A compar- Sensory recovery ison of nerves repaired end to end under tension with nerve grafts in a S0 No recovery primate model. J Hand Surg [Am] 18:417-425, 1993 S1 Recovery of deep cutaneous pain 13. Dellon A: Evaluation of sensibility in re-education of sensation of the hand. Baltimore, MD, Williams and Wilkins, 1981 S1 ؉ Recovery of superficial pain 14. Sunderland S: The adipose tissue of peripheral nerves. 68:118, S2 Recovery of superficial pain and some touch 1945 ؉ S2 As in S2, but with over response 15. Sunderland S: Founder’s Lecture—American Society for Surgery of the S3 Recovery of pain and touch sensibility with Hand. J Hand Surg [Am] 4:201-211, 1979 disappearance of over response 16. Sunderland S: The intraneural topography of the radial, median and S3 ؉ As in S3, but localization of the stimulus is good, ulnar nerves. Brain 68:243, 1945 and there is imperfect recovery of 2-point 17. Brushart TM, Tarlov EC, Mesulam MM: Specificity of muscle reinner- discrimination vation after epineurial and individual fascicular suture of the rat sciatic S4 Complete recovery nerve. J Hand Surg [Am] 8:248-253, 1983 18. Jabaley ME: Technical aspects of peripheral nerve repair. J Hand Surg [Br] 9:14-19, 1984 19. Kline DG, Hudson AR, Bratton BR: Experimental study of fascicular nerve repair with and without epineurial closure. 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