- Email: [email protected]
Current surgical techniques of peripheral nerve repair
Current Surgical Techniques of Peripheral Nerve Repair Kasra Rowshan, MD, Neil F. Jones, MD, and Ranjan Gupta, MD Transection of peripheral nerves results in Wallerian degeneration of the distal stump with varying degrees of degeneration in the proximal stump. After degeneration, the proximal neuron 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, epineurium, nerve repair, microsurgery, Schwann cell, Wallerian degeneration
T
ransection of a peripheral nerve results in significant and complex changes in the proximal and distal nerve segments. An understanding of subsequent cellular changes is essential to determine the proper timing and technique of nerve repair to produce optimal functional results. After transection, Wallerian degeneration will occur in the distal portion of the nerve. These histological changes are characterized by axonal degeneration of both myelinated and unmyelinated fibers, myelin degradation, and subsequent Schwann cell proliferation. There are also changes within the proximal segment of the damaged nerve to help prepare the axon for regeneration. The extent of the degeneration depends on the severity of injury. The proliferating Schwann cells in the distal nerve begin to organize themselves into columns, known as Bands of Bugner, which will support subsequent regeneration from the proximal stump of the severed nerve into the distal environment. After a period of axonal degeneration and Schwann cell proliferation, axons from the proximal stump will sprout in attempts to re-innervate the distal stump. Unless the neural injury is the result of crush injury where the nerve architecture is relatively preserved, spontaneous re-innervation of the distal segment by the proximal stump usually does not occur. When a nerve fiber is divided, surgical nerve repair is required. The primary aim of surgical intervention is to direct the regenerating proximal fibers into the environment of the degenerating distal stump. An effective repair is directly related
Peripheral Nerve Research Lab, Department of Orthopaedic Surgery, University of California, Irvine, Irvine, CA. Address reprint requests to: Ranjan Gupta, MD, Peripheral Nerve Research Lab, Department of Orthopaedic Surgery, University of California, Irvine, Medical Sciences I, Room B120, Irvine, CA 92697.
1048-6666/04/$-see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1053/j.oto.2004.06.006
to sensory, motor, and autonomic axons making the appropriate connections with their distal organs. Such results are dependent on and influenced by the severity and extent of injury, timing of repair, fascicular anatomy and re-alignment, surgical technique, patient age, and underlying patient issues and morbidity.
Peripheral Nerve Anatomy Proper understanding of both the timing and technique of nerve repair require a clear and complete understanding of peripheral nerve anatomy. The peripheral nerve is composed of motor, sensory, and sympathetic nerve fibers. Such fibers can be either myelinated or unmyelinated. The average diameter of myelinated fibers is 2 to 22 m1 and unmyelinated axons are 0.4 to 1.25 m.2 Surrounding the individual myelinated nerve fibers or the group of unmyelinated nerve fibers is the endoneurium, a collection of thin collagen strands that provide adequate nourishment and protect the individual axons. Multiple nerve fibers collect to form a group of fibers called a fascicle. Such fascicles are bound and encircled by the perineurium, a collection of a connective tissue sheath composed of perineurial cells. The perineurium is the major contributor to the nerve’s tensile integrity and strength and is also the blood–nerve barrier. Several fascicles may be arranged into a group fascicle surrounded by connective tissue, termed the internal or interfascicular epineurium. The connective tissue that surrounds the periphery of the entire nerve is called the external or extrafascicular epineurium. The primary function of this connective tissue structure is to nourish and protect the fascicles. Fascicular patterns are divided into the following 3 types: monofascicular, oligofascicular, and polyfascicular.3 Mono163
164
K. Rowshan, N.F. Jones, and R. Gupta
fascicular patterns consist of one large fascicle, whereas oligofascicular 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 monofascicular 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 injury. In surgical nerve repair, proper identification of fascicular arrangement is crucial to achieving a successful outcome. Peripheral nerves are extensively vascularized with separate yet interconnected microvascular systems in the epineurium, perineurium, and endoneurium.6,7 The vascular pattern of the peripheral nerve is characterized by longitudinally oriented groups of vessels, with a great number of communicating anastomoses.7 The vasculature is composed of an intrinsic vascular system consisting of vascular plexa in the epineurium, perineurium, and endoneurium and an extrinsic 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 vascular damage secondary to surgical manipulation need to be considered.5
General Principles in Surgical Repair The primary purpose of nerve repair is to correctly approximate the severed nerve segments in hopes of achieving functional re-innervation of the end organs. Four general principles for proper coaptation of divided nerves have been outlined.8 Initially, preparation of the stumps is accomplished surgically with either a number 11 scalpel blade, an ophthalmic knife, or a sterile razor blade against a wooden disposable tongue blade. After this, the surgeon should be able to identify and separate individual fascicles or group fascicles. Trimming the nerve ends removes dead or severely damaged tissue. Second, trial approximation of the proximal stump to the distal stump is attempted to gauge the amount of tension necessary, which is related to the length of the gap between the stumps. Third, coaptation or neurorrhaphy of the nerve stumps is performed, which describes the apposition of corresponding nerve ends with special attention to bringing fascicles into optimal contact. Direct coaptation can oppose stump-to-stump, fascicle-to-fascicle, or group fascicle-to-group fascicle in the corresponding ends (Fig. 1). An indirect coaptation can be performed by interposing a nerve graft. Lastly, maintenance of coaptation must be achieved with the use of nonabsorbable sutures, glue or a natural fibrin clot. Giddins et al showed that 9-0 monofilament nylon suture withstood the greatest distractive force, whereas 10-0 failed under
Figure 1 Schematic depiction of the different types of nerve repair after laceration.
tension, and 8-0 had a tendency to pull off the repaired nerve endings.9 However, 10-0 or 8-0 suture is often used based on the size of the nerve to be repaired. Surgical repair of peripheral nerves requires the use of an operating microscope, loupes, microsurgical instruments, bipolar cautery, nerve sectioning knife, and appropriate nylon sutures with 50- to 100-m needles.10 Nerve-wrapping materials are not recommended at the site of repair because they have been shown to increase neural edema and may impair blood supply.10 Traditionally, neurorrhaphy is performed without tension at the site of repair. It is the current practice of most hand surgeons to attempt nerve coaptation of major peripheral nerves with two 8-0 nylon sutures within the nerve epineurium. If the nerve cannot be approximated with these 2 sutures, then a nerve graft should be strongly considered. However, studies in primates have shown that direct repair under modest tension yields better results relative to a tension-free repair,11 but this remains controversial. Furthermore, primate studies have shown that a direct nerve repair under tension may perform better than a nerve graft.12 Currently, most hand surgeons agree that if a tension-free or minimal tension repair is not possible, then an interposition nerve graft should be used. Postoperative sensory re-education 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.
Epineurial Repair Epineurial repair is the traditional method of repair for severed peripheral nerves. Initially, the surgeon sections the nerve ends until all visible signs of the damage have been removed and a fascicular pattern can be seen.4 The goal of successful repair is to establish continuity of the nerve with proper rotational alignment and without tension. Rotational alignment of both stumps is performed either by aligning an external marker such as a vessel on the surface of the proximal and distal nerve or by matching the mirror images of the fascicular pattern in the proximal and distal nerve ends. Coaptation is achieved with nonabsorbable sutures of either 8-0 nylon for larger nerves or 10-0 nylon for smaller nerves. The first suture is passed through the epineurium proximally and distally and then tied so that the nerve ends just “kiss” each other, ensuring minimal tension at the repair
site. A second suture is then placed in the same manner. The remaining epineurium is closed by halving the distance on both the anterior and posterior aspects of the nerve. The number of sutures varies depending on the nerve thickness; a digital nerve may only require 2 or 3 sutures, whereas the median or ulnar nerve at the wrist or elbow may require 8 to 10 sutures. If the severed nerve cannot be approximated with two 8-0 nylon sutures, then the tension within the nerve is considered excessive and a nerve graft should be performed. Proper care must be taken to ensure that no fascicles protrude between the suture lines (Fig. 2).
Group Fascicular Repair In theory, group fascicular repair is a more accurate technique of nerve repair. Initially, the nerve ends are sharply 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 fascicular 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 under the microscope to determine corresponding groups of fascicles.4 Each group fascicule may be slightly separated by dissection between the group fascicles, or if matching group fascicles are easily visualized, no further dissection is necessary. Each group fascicle, usually 3 to 5 in the proximal nerve, is coapted to its corresponding group fascicle in the distal nerve with 2 to 4 9-0 nylon sutures placed through the internal epineurium or perineurium.8,14-16 If motor and sensory group fascicles are appropriately aligned, motor-to-motor and sensory-to-sensory, then this technique offers a significant advantage over an epineurial repair. This would reduce the chances of motor axons being directed down endoneurial tubes to sensory end organs or sensory axons being directed down endoneurial tubes to motor endplates.17 The potential benefit of this technique, however, must be
weighed against the potential increased fibrosis associated with greater dissection and more intraneural suture material. Technically, the external epineurium must be dissected with special care taken to preserve the adjacent perineurium, which carries the blood supply to the nerve. Individual group fascicles are identified under the operating microscope in the proximal and distal nerve ends (Fig. 3). Two sutures are placed through the perineurium or internal epineurium at 180° from one another for each group fascicle, but occasionally 3 or even 4 sutures may be necessary. Nylon suture (10-0) with a 70- or 50-m needle is preferred. Usually 3 to 5 group fascicles are copated in a median or ulnar nerve repair at the wrist or forearm level. Traditionally, after group fascicular repair, the epineurium is also sutured to provide additional support and alignment. Occasionally, a flap of 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 techniques. 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 repair of the sciatic nerve.17,24 Additionally, studies comparing epineurial to intrafascicular perineurial repairs have demonstrated no advantages for either of the surgical procedures.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 improved 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 produces a similar outcome when compared with a group fascicular repair. Perhaps the technical aspects of group fascicular repair prohibit the realization of the theoretical advantages of this technique. It is therefore recommended that both techniques be considered and employed in repairing a damaged nerve.27 The technique selected depends on the nature and location of injury, the timing of nerve repair, and the identification of the fascicular arrangement in the nerve. If an acute injury results in a sharp clean laceration, an epineurial repair can usually be performed because surface landmarks can be used to align nerve ends. Digital nerves are always repaired with an epineurial technique (Figs. 5 and 6). If a specific motor or sensory group fascicle can be identified by distal dissection of the distal nerve stump, then a group fascicular repair may be performed. The remainder of the repair can be completed with epineurial technique. Various techniques have been used to determine the specific function of each group fascicle. Visual matching of the “mirror images” of the group fascicular pattern in the proximal and distal nerve ends is the simplest method. However, in crushing and avulsion injuries, topographic matching may be difficult. Electrical stimulation can be used to identify sensory group fascicles by inducing sensation in the awake patient (Triepel and Koman, this issue). Although distal nerve degeneration begins within the first 48 hours of injury, stimulating the motor group fascicle in the distal nerve will produce contraction of the thenar or interosseous muscles. Stimulating the proximal motor fascicle should not induce
Figure 6 Repair of radial and ulnar digital nerves with epineurial repair technique.
any sensation. Alternatively, immunohistochemistry may help to differentiate between motor and sensory axons. Gu et al showed that blue-SAb staining for 30 minutes accurately identified sensory fascicles without later adverse effects on the growth and metabolism of neurons.28 Carbonic anhydrase staining of sensory fascicles and acteylcholinesterase staining of motor fascicles will allow differentiation of the motor and sensory group fascicles, but this technique is rarely used clinically.29 The location of the nerve injury in the extremity is of critical importance. Proximally, the fascicular pattern is commonly polyfascicular, mandating an epineurial repair. Distally, nerves are routinely mono- or oligofascicular. In such a pattern, it is appropriate to carry out a group fascicular repair with a minimum number of sutures. Individual fascicular repair is usually not recommended except when repairing small, near-terminal branches of digital nerves.
Evaluation of Functional Recovery after Nerve Repair The Medical Research Council developed a widely accepted grading system for nerve recovery after nerve repair (Table 1).30,31 Sensory recovery is graded on a scale from S0 –S4 and motor function from M0 –M5, based on physical examination. Semiobjective measurements of sensory nerve recovery include density testing with the use of static and moving
170 Table 1 Medical Research Council System for Grading Nerve Recovery Motor recovery M0 No contraction M1 Return of perceptible contraction in the proximal muscles M2 Return of perceptible contraction in the proximal and distal muscles M3 Return of function in proximal and distal muscles to such a degree that all important muscles are sufficiently powerful to act against gravity M4 All muscles act against strong resistance, and some independent movements are possible M5 Full recovery of all muscles Sensory recovery S0 No recovery S1 Recovery of deep cutaneous pain S1 ⴙ Recovery of superficial pain S2 Recovery of superficial pain and some touch S2 ⴙ As in S2, but with over response S3 Recovery of pain and touch sensibility with disappearance of over response S3 ⴙ As in S3, but localization of the stimulus is good, and there is imperfect recovery of 2-point discrimination S4 Complete recovery
2-point discrimination. It is important to realize that threshold testing with von Frey or Semmes–S4 Weinstein filaments should primarily be used for evaluating compression neuropathies.32
Conclusions To maximize re-innervation of the regenerating proximal stump to the degenerating distal stump after nerve axonotomy, surgical nerve repair is usually necessary. Epineurial repair has traditionally been used for most nerve injuries; however, recent studies have shown that a combination of epineurial and group fascicular repair may improve the outcome. Although good to excellent results may be expected for young patients under 20 years of age, functional re-innervation remains limited for adult patients, even with optimal microsurgical techniques. It is likely that in the future, surgical nerve repairs will be augmented with neurotrophic agents to improve the outcome and restore normal function after neural injury.
References 1. Sunderland S, Lavarack JO, Ray LJ: The calibre of nerve fibres in human cutaneous nerves. J Comp Neurol 91:87-101, 1949 2. Gasser HS: Properties of dorsal root unmedullated fibers on the two sides of the ganglion. J Gen Physiol 38:709-728, 1955 3. Mackinnon SE, Dellon AL (eds): Surgery of the Peripheral Nerve. New York, Thieme Medical, 1988 4. Wilgis E: Techniques of epineural and group fascicular repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 287-293 5. Lundborg G: Nerve Injury and Repair. Edinburgh, Churchill Livingstone, 1988
K. Rowshan, N.F. Jones, and R. Gupta 6. Bell MA, Weddell AG: A morphometric study of intrafascicular vessels of mammalian sciatic nerve. Muscle Nerve 7:524-534, 1984 7. Lundborg G: The intrinsic vascularization of human peripheral nerves: structural and functional aspects. J Hand Surg [Am] 4:34-41, 1979 8. Millesi H, Terzis JK: Nomenclature in peripheral nerve surgery. Committee report of the International Society of Reconstructive Microsurgery. Clin Plast Surg 11:3-8, 1984 9. Giddins GE, Wade PJ, Amis AA: Primary nerve repair: Strength of repair with different gauges of nylon suture material. J Hand Surg [Br] 14:301-302, 1989 10. Gorman PW, Dell PC: Instrumentation for nerve repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 275-85 11. Wood MB: Peroneal nerve repair. Surgical results. Clin Orthop 267: 206-210, 1991 12. Hentz VR, Rosen JM, Xiao SJ, et al: The nerve gap dilemma: A comparison of nerves repaired end to end under tension with nerve grafts in a primate model. J Hand Surg [Am] 18:417-425, 1993 13. Dellon A: Evaluation of sensibility in re-education of sensation of the hand. Baltimore, MD, Williams and Wilkins, 1981 14. Sunderland S: The adipose tissue of peripheral nerves. Brain 68:118, 1945 15. Sunderland S: Founder’s Lecture—American Society for Surgery of the Hand. J Hand Surg [Am] 4:201-211, 1979 16. Sunderland S: The intraneural topography of the radial, median and ulnar nerves. Brain 68:243, 1945 17. Brushart TM, Tarlov EC, Mesulam MM: Specificity of muscle reinnervation after epineurial and individual fascicular suture of the rat sciatic 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. J Neurosurg 54:513520, 1981 20. Tupper JW: Fascicular repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 295-303 21. Cabaud HE, Rodkey WG, McCarroll HR Jr, et al: Epineurial and perineurial fascicular nerve repairs: A critical comparison. J Hand Surg [Am] 1:131-137, 1976 22. Murray JA, Willins M, Mountain RE: A comparison of epineurial and perineurial sutures for the repair of a divided rat sciatic nerve. Clin Otolaryngol 19:95-97, 1994 23. Orgel MG: Epineurial versus perineurial repair of peripheral nerves. Clin Plast Surg 11:101-104, 1984 24. Brushart TM, Mesulam MM: Alteration in connections between muscle and anterior horn motoneurons after peripheral nerve repair. Science 208:603-605, 1980 25. Cabaud HE, Rodkey WG, McCarroll HR Jr: Peripheral nerve injuries: Studies in higher nonhuman primates. J Hand Surg [Am] 5:201-206, 1980 26. Tupper JW, Crick JC, Matteck LR: Fascicular nerve repairs. A comparative study of epineurial and fascicular (perineurial) techniques. Orthop Clin North Am 19:57-69, 1988 27. Matsuyama T, Mackay M, Midha R: Peripheral nerve repair and grafting techniques: A review. Neurol Med Chir (Tokyo) 40:187-199, 2000 28. Gu XS, Yan ZQ, Yan WX, et al: Rapid immunostaining of live nerve for identification of sensory and motor fasciculi. Chin Med J (Engl) 105: 949-952, 1992 29. Sanger JR, Riley DA, Matloub HS, et al: Effects of axotomy on the cholinesterase and carbonic anhydrase activities of axons in the proximal and distal stumps of rabbit sciatic nerves: A temporal study. Plast Reconstr Surg 87:726-740, 1991 30. Medical Research Council, Nerve Injuries Committee. Aids to Investigation of Peripheral Nerve Injuries. MRC War memorandum No. 7 His Majesty’s Stationery Office, 1943. London, Balliere Tindall, 1986. 31. Medical Research Council. Aids to the Examination of the Peripheral Nervous System. Memorandum No. 45. London, Her Majesty’s Stationary Office, 1976. 32. Lee SK, Wolfe SW: Peripheral nerve injury and repair. J Am Acad Orthop Surg 8:243-252, 2000
T
ransection of a peripheral nerve results in significant and complex changes in the proximal and distal nerve segments. An understanding of subsequent cellular changes is essential to determine the proper timing and technique of nerve repair to produce optimal functional results. After transection, Wallerian degeneration will occur in the distal portion of the nerve. These histological changes are characterized by axonal degeneration of both myelinated and unmyelinated fibers, myelin degradation, and subsequent Schwann cell proliferation. There are also changes within the proximal segment of the damaged nerve to help prepare the axon for regeneration. The extent of the degeneration depends on the severity of injury. The proliferating Schwann cells in the distal nerve begin to organize themselves into columns, known as Bands of Bugner, which will support subsequent regeneration from the proximal stump of the severed nerve into the distal environment. After a period of axonal degeneration and Schwann cell proliferation, axons from the proximal stump will sprout in attempts to re-innervate the distal stump. Unless the neural injury is the result of crush injury where the nerve architecture is relatively preserved, spontaneous re-innervation of the distal segment by the proximal stump usually does not occur. When a nerve fiber is divided, surgical nerve repair is required. The primary aim of surgical intervention is to direct the regenerating proximal fibers into the environment of the degenerating distal stump. An effective repair is directly related
Peripheral Nerve Research Lab, Department of Orthopaedic Surgery, University of California, Irvine, Irvine, CA. Address reprint requests to: Ranjan Gupta, MD, Peripheral Nerve Research Lab, Department of Orthopaedic Surgery, University of California, Irvine, Medical Sciences I, Room B120, Irvine, CA 92697.
1048-6666/04/$-see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1053/j.oto.2004.06.006
to sensory, motor, and autonomic axons making the appropriate connections with their distal organs. Such results are dependent on and influenced by the severity and extent of injury, timing of repair, fascicular anatomy and re-alignment, surgical technique, patient age, and underlying patient issues and morbidity.
Peripheral Nerve Anatomy Proper understanding of both the timing and technique of nerve repair require a clear and complete understanding of peripheral nerve anatomy. The peripheral nerve is composed of motor, sensory, and sympathetic nerve fibers. Such fibers can be either myelinated or unmyelinated. The average diameter of myelinated fibers is 2 to 22 m1 and unmyelinated axons are 0.4 to 1.25 m.2 Surrounding the individual myelinated nerve fibers or the group of unmyelinated nerve fibers is the endoneurium, a collection of thin collagen strands that provide adequate nourishment and protect the individual axons. Multiple nerve fibers collect to form a group of fibers called a fascicle. Such fascicles are bound and encircled by the perineurium, a collection of a connective tissue sheath composed of perineurial cells. The perineurium is the major contributor to the nerve’s tensile integrity and strength and is also the blood–nerve barrier. Several fascicles may be arranged into a group fascicle surrounded by connective tissue, termed the internal or interfascicular epineurium. The connective tissue that surrounds the periphery of the entire nerve is called the external or extrafascicular epineurium. The primary function of this connective tissue structure is to nourish and protect the fascicles. Fascicular patterns are divided into the following 3 types: monofascicular, oligofascicular, and polyfascicular.3 Mono163
164
K. Rowshan, N.F. Jones, and R. Gupta
fascicular patterns consist of one large fascicle, whereas oligofascicular 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 monofascicular 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 injury. In surgical nerve repair, proper identification of fascicular arrangement is crucial to achieving a successful outcome. Peripheral nerves are extensively vascularized with separate yet interconnected microvascular systems in the epineurium, perineurium, and endoneurium.6,7 The vascular pattern of the peripheral nerve is characterized by longitudinally oriented groups of vessels, with a great number of communicating anastomoses.7 The vasculature is composed of an intrinsic vascular system consisting of vascular plexa in the epineurium, perineurium, and endoneurium and an extrinsic 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 vascular damage secondary to surgical manipulation need to be considered.5
General Principles in Surgical Repair The primary purpose of nerve repair is to correctly approximate the severed nerve segments in hopes of achieving functional re-innervation of the end organs. Four general principles for proper coaptation of divided nerves have been outlined.8 Initially, preparation of the stumps is accomplished surgically with either a number 11 scalpel blade, an ophthalmic knife, or a sterile razor blade against a wooden disposable tongue blade. After this, the surgeon should be able to identify and separate individual fascicles or group fascicles. Trimming the nerve ends removes dead or severely damaged tissue. Second, trial approximation of the proximal stump to the distal stump is attempted to gauge the amount of tension necessary, which is related to the length of the gap between the stumps. Third, coaptation or neurorrhaphy of the nerve stumps is performed, which describes the apposition of corresponding nerve ends with special attention to bringing fascicles into optimal contact. Direct coaptation can oppose stump-to-stump, fascicle-to-fascicle, or group fascicle-to-group fascicle in the corresponding ends (Fig. 1). An indirect coaptation can be performed by interposing a nerve graft. Lastly, maintenance of coaptation must be achieved with the use of nonabsorbable sutures, glue or a natural fibrin clot. Giddins et al showed that 9-0 monofilament nylon suture withstood the greatest distractive force, whereas 10-0 failed under
Figure 1 Schematic depiction of the different types of nerve repair after laceration.
tension, and 8-0 had a tendency to pull off the repaired nerve endings.9 However, 10-0 or 8-0 suture is often used based on the size of the nerve to be repaired. Surgical repair of peripheral nerves requires the use of an operating microscope, loupes, microsurgical instruments, bipolar cautery, nerve sectioning knife, and appropriate nylon sutures with 50- to 100-m needles.10 Nerve-wrapping materials are not recommended at the site of repair because they have been shown to increase neural edema and may impair blood supply.10 Traditionally, neurorrhaphy is performed without tension at the site of repair. It is the current practice of most hand surgeons to attempt nerve coaptation of major peripheral nerves with two 8-0 nylon sutures within the nerve epineurium. If the nerve cannot be approximated with these 2 sutures, then a nerve graft should be strongly considered. However, studies in primates have shown that direct repair under modest tension yields better results relative to a tension-free repair,11 but this remains controversial. Furthermore, primate studies have shown that a direct nerve repair under tension may perform better than a nerve graft.12 Currently, most hand surgeons agree that if a tension-free or minimal tension repair is not possible, then an interposition nerve graft should be used. Postoperative sensory re-education 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.
Epineurial Repair Epineurial repair is the traditional method of repair for severed peripheral nerves. Initially, the surgeon sections the nerve ends until all visible signs of the damage have been removed and a fascicular pattern can be seen.4 The goal of successful repair is to establish continuity of the nerve with proper rotational alignment and without tension. Rotational alignment of both stumps is performed either by aligning an external marker such as a vessel on the surface of the proximal and distal nerve or by matching the mirror images of the fascicular pattern in the proximal and distal nerve ends. Coaptation is achieved with nonabsorbable sutures of either 8-0 nylon for larger nerves or 10-0 nylon for smaller nerves. The first suture is passed through the epineurium proximally and distally and then tied so that the nerve ends just “kiss” each other, ensuring minimal tension at the repair
site. A second suture is then placed in the same manner. The remaining epineurium is closed by halving the distance on both the anterior and posterior aspects of the nerve. The number of sutures varies depending on the nerve thickness; a digital nerve may only require 2 or 3 sutures, whereas the median or ulnar nerve at the wrist or elbow may require 8 to 10 sutures. If the severed nerve cannot be approximated with two 8-0 nylon sutures, then the tension within the nerve is considered excessive and a nerve graft should be performed. Proper care must be taken to ensure that no fascicles protrude between the suture lines (Fig. 2).
Group Fascicular Repair In theory, group fascicular repair is a more accurate technique of nerve repair. Initially, the nerve ends are sharply 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 fascicular 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 under the microscope to determine corresponding groups of fascicles.4 Each group fascicule may be slightly separated by dissection between the group fascicles, or if matching group fascicles are easily visualized, no further dissection is necessary. Each group fascicle, usually 3 to 5 in the proximal nerve, is coapted to its corresponding group fascicle in the distal nerve with 2 to 4 9-0 nylon sutures placed through the internal epineurium or perineurium.8,14-16 If motor and sensory group fascicles are appropriately aligned, motor-to-motor and sensory-to-sensory, then this technique offers a significant advantage over an epineurial repair. This would reduce the chances of motor axons being directed down endoneurial tubes to sensory end organs or sensory axons being directed down endoneurial tubes to motor endplates.17 The potential benefit of this technique, however, must be
weighed against the potential increased fibrosis associated with greater dissection and more intraneural suture material. Technically, the external epineurium must be dissected with special care taken to preserve the adjacent perineurium, which carries the blood supply to the nerve. Individual group fascicles are identified under the operating microscope in the proximal and distal nerve ends (Fig. 3). Two sutures are placed through the perineurium or internal epineurium at 180° from one another for each group fascicle, but occasionally 3 or even 4 sutures may be necessary. Nylon suture (10-0) with a 70- or 50-m needle is preferred. Usually 3 to 5 group fascicles are copated in a median or ulnar nerve repair at the wrist or forearm level. Traditionally, after group fascicular repair, the epineurium is also sutured to provide additional support and alignment. Occasionally, a flap of 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 techniques. 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 repair of the sciatic nerve.17,24 Additionally, studies comparing epineurial to intrafascicular perineurial repairs have demonstrated no advantages for either of the surgical procedures.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 improved 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 produces a similar outcome when compared with a group fascicular repair. Perhaps the technical aspects of group fascicular repair prohibit the realization of the theoretical advantages of this technique. It is therefore recommended that both techniques be considered and employed in repairing a damaged nerve.27 The technique selected depends on the nature and location of injury, the timing of nerve repair, and the identification of the fascicular arrangement in the nerve. If an acute injury results in a sharp clean laceration, an epineurial repair can usually be performed because surface landmarks can be used to align nerve ends. Digital nerves are always repaired with an epineurial technique (Figs. 5 and 6). If a specific motor or sensory group fascicle can be identified by distal dissection of the distal nerve stump, then a group fascicular repair may be performed. The remainder of the repair can be completed with epineurial technique. Various techniques have been used to determine the specific function of each group fascicle. Visual matching of the “mirror images” of the group fascicular pattern in the proximal and distal nerve ends is the simplest method. However, in crushing and avulsion injuries, topographic matching may be difficult. Electrical stimulation can be used to identify sensory group fascicles by inducing sensation in the awake patient (Triepel and Koman, this issue). Although distal nerve degeneration begins within the first 48 hours of injury, stimulating the motor group fascicle in the distal nerve will produce contraction of the thenar or interosseous muscles. Stimulating the proximal motor fascicle should not induce
Figure 6 Repair of radial and ulnar digital nerves with epineurial repair technique.
any sensation. Alternatively, immunohistochemistry may help to differentiate between motor and sensory axons. Gu et al showed that blue-SAb staining for 30 minutes accurately identified sensory fascicles without later adverse effects on the growth and metabolism of neurons.28 Carbonic anhydrase staining of sensory fascicles and acteylcholinesterase staining of motor fascicles will allow differentiation of the motor and sensory group fascicles, but this technique is rarely used clinically.29 The location of the nerve injury in the extremity is of critical importance. Proximally, the fascicular pattern is commonly polyfascicular, mandating an epineurial repair. Distally, nerves are routinely mono- or oligofascicular. In such a pattern, it is appropriate to carry out a group fascicular repair with a minimum number of sutures. Individual fascicular repair is usually not recommended except when repairing small, near-terminal branches of digital nerves.
Evaluation of Functional Recovery after Nerve Repair The Medical Research Council developed a widely accepted grading system for nerve recovery after nerve repair (Table 1).30,31 Sensory recovery is graded on a scale from S0 –S4 and motor function from M0 –M5, based on physical examination. Semiobjective measurements of sensory nerve recovery include density testing with the use of static and moving
170 Table 1 Medical Research Council System for Grading Nerve Recovery Motor recovery M0 No contraction M1 Return of perceptible contraction in the proximal muscles M2 Return of perceptible contraction in the proximal and distal muscles M3 Return of function in proximal and distal muscles to such a degree that all important muscles are sufficiently powerful to act against gravity M4 All muscles act against strong resistance, and some independent movements are possible M5 Full recovery of all muscles Sensory recovery S0 No recovery S1 Recovery of deep cutaneous pain S1 ⴙ Recovery of superficial pain S2 Recovery of superficial pain and some touch S2 ⴙ As in S2, but with over response S3 Recovery of pain and touch sensibility with disappearance of over response S3 ⴙ As in S3, but localization of the stimulus is good, and there is imperfect recovery of 2-point discrimination S4 Complete recovery
2-point discrimination. It is important to realize that threshold testing with von Frey or Semmes–S4 Weinstein filaments should primarily be used for evaluating compression neuropathies.32
Conclusions To maximize re-innervation of the regenerating proximal stump to the degenerating distal stump after nerve axonotomy, surgical nerve repair is usually necessary. Epineurial repair has traditionally been used for most nerve injuries; however, recent studies have shown that a combination of epineurial and group fascicular repair may improve the outcome. Although good to excellent results may be expected for young patients under 20 years of age, functional re-innervation remains limited for adult patients, even with optimal microsurgical techniques. It is likely that in the future, surgical nerve repairs will be augmented with neurotrophic agents to improve the outcome and restore normal function after neural injury.
References 1. Sunderland S, Lavarack JO, Ray LJ: The calibre of nerve fibres in human cutaneous nerves. J Comp Neurol 91:87-101, 1949 2. Gasser HS: Properties of dorsal root unmedullated fibers on the two sides of the ganglion. J Gen Physiol 38:709-728, 1955 3. Mackinnon SE, Dellon AL (eds): Surgery of the Peripheral Nerve. New York, Thieme Medical, 1988 4. Wilgis E: Techniques of epineural and group fascicular repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 287-293 5. Lundborg G: Nerve Injury and Repair. Edinburgh, Churchill Livingstone, 1988
K. Rowshan, N.F. Jones, and R. Gupta 6. Bell MA, Weddell AG: A morphometric study of intrafascicular vessels of mammalian sciatic nerve. Muscle Nerve 7:524-534, 1984 7. Lundborg G: The intrinsic vascularization of human peripheral nerves: structural and functional aspects. J Hand Surg [Am] 4:34-41, 1979 8. Millesi H, Terzis JK: Nomenclature in peripheral nerve surgery. Committee report of the International Society of Reconstructive Microsurgery. Clin Plast Surg 11:3-8, 1984 9. Giddins GE, Wade PJ, Amis AA: Primary nerve repair: Strength of repair with different gauges of nylon suture material. J Hand Surg [Br] 14:301-302, 1989 10. Gorman PW, Dell PC: Instrumentation for nerve repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 275-85 11. Wood MB: Peroneal nerve repair. Surgical results. Clin Orthop 267: 206-210, 1991 12. Hentz VR, Rosen JM, Xiao SJ, et al: The nerve gap dilemma: A comparison of nerves repaired end to end under tension with nerve grafts in a primate model. J Hand Surg [Am] 18:417-425, 1993 13. Dellon A: Evaluation of sensibility in re-education of sensation of the hand. Baltimore, MD, Williams and Wilkins, 1981 14. Sunderland S: The adipose tissue of peripheral nerves. Brain 68:118, 1945 15. Sunderland S: Founder’s Lecture—American Society for Surgery of the Hand. J Hand Surg [Am] 4:201-211, 1979 16. Sunderland S: The intraneural topography of the radial, median and ulnar nerves. Brain 68:243, 1945 17. Brushart TM, Tarlov EC, Mesulam MM: Specificity of muscle reinnervation after epineurial and individual fascicular suture of the rat sciatic 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. J Neurosurg 54:513520, 1981 20. Tupper JW: Fascicular repair, in Gelberman RH (ed): Operative Nerve Repair and Reconstruction. Philadelphia, PA, Lippincott, 1991, pp 295-303 21. Cabaud HE, Rodkey WG, McCarroll HR Jr, et al: Epineurial and perineurial fascicular nerve repairs: A critical comparison. J Hand Surg [Am] 1:131-137, 1976 22. Murray JA, Willins M, Mountain RE: A comparison of epineurial and perineurial sutures for the repair of a divided rat sciatic nerve. Clin Otolaryngol 19:95-97, 1994 23. Orgel MG: Epineurial versus perineurial repair of peripheral nerves. Clin Plast Surg 11:101-104, 1984 24. Brushart TM, Mesulam MM: Alteration in connections between muscle and anterior horn motoneurons after peripheral nerve repair. Science 208:603-605, 1980 25. Cabaud HE, Rodkey WG, McCarroll HR Jr: Peripheral nerve injuries: Studies in higher nonhuman primates. J Hand Surg [Am] 5:201-206, 1980 26. Tupper JW, Crick JC, Matteck LR: Fascicular nerve repairs. A comparative study of epineurial and fascicular (perineurial) techniques. Orthop Clin North Am 19:57-69, 1988 27. Matsuyama T, Mackay M, Midha R: Peripheral nerve repair and grafting techniques: A review. Neurol Med Chir (Tokyo) 40:187-199, 2000 28. Gu XS, Yan ZQ, Yan WX, et al: Rapid immunostaining of live nerve for identification of sensory and motor fasciculi. Chin Med J (Engl) 105: 949-952, 1992 29. Sanger JR, Riley DA, Matloub HS, et al: Effects of axotomy on the cholinesterase and carbonic anhydrase activities of axons in the proximal and distal stumps of rabbit sciatic nerves: A temporal study. Plast Reconstr Surg 87:726-740, 1991 30. Medical Research Council, Nerve Injuries Committee. Aids to Investigation of Peripheral Nerve Injuries. MRC War memorandum No. 7 His Majesty’s Stationery Office, 1943. London, Balliere Tindall, 1986. 31. Medical Research Council. Aids to the Examination of the Peripheral Nervous System. Memorandum No. 45. London, Her Majesty’s Stationary Office, 1976. 32. Lee SK, Wolfe SW: Peripheral nerve injury and repair. J Am Acad Orthop Surg 8:243-252, 2000