FUNCTIONAL AND ELECTROPHYSIOLOGICAL OUTCOME AFTER AUTOGENOUS VEIN WRAPPING OF PRIMARY REPAIRED ULNAR NERVES AHMED F. SADEK, M.D.,1* EZZAT H. FOULY, M.D.,1 and MONA HAMDY, M.D.2
Purpose: This study aimed at assessing the functional and electrophysiological recovery after vein wrapping of primary repaired ulnar nerves Methods: From January 2010 till December 2012, 23 patients (diagnosed with distal ulnar nerve injury) were prospectively studied where they were divided into two groups; group one (11 patients) and group two (12 patients). The injury was sharp in all cases but for one. The first group was managed by primary epineurorraphy. The second group was managed by primary epineurorraphy and autogenous vein wrapping. Final outcome was based on sensory recovery, motor recovery, and the presence or absence of electrophysiological response Results: Clinically, only one case in each group exhibited negative Tinel’s sign. The second group achieved statistically significant superiority regarding motor recovery (P 5 0.018), sensory recovery (P 5 0.042) and electrophysiological recovery (P 5 0.044). Group one showed two good, two satisfactory, six moderate, and one bad results while the second group showed five good, six satisfactory, one bad and no moderate results (P 5 0.026). The first time to show clinical response in group one was the third month while in the second group it was at 1.5 month (P < 0.001). In addition, the first time to show electromyographic response in group one was at the sixth month while in group two it was at the third month Conclusions: Vein wrapping is a simple technique that could be used reliably to augment primary neurorrhaphy particularly in cases with associated vascular or tendon injuries to prevent scarring and enhance functional and elecC 2013 Wiley Periodicals, Inc. Microsurgery 34:361–366, 2014. trophysiological recovery. V
The
objective of repair after nerve injury is to restore normal sensitivity and motor function. Recovery from peripheral nerve injury may occur by one of three mechanisms namely; remyelination, collateral axonal sprouting, or regeneration from the proximal injury site.1 The control of postsurgical scar formation has been the goal of microsurgeons many decades.2–4 That is why interposition materials have been tested to prevent postoperative adhesions between nerves and surrounding tissues in various clinical settings.5 In recent years, autogenous vein wrapping has gained good reputation among microsurgeons.6 Masear et al.5 first described the technique of vein wrapping. This technique was first applied for the treatment of painful neuroma incontinuity by Gould.6 This could be attributed to the fact that veins meet all criteria required for ideal wrapping of nerves namely; constituting a biological barrier protecting the nerve from compression by surrounding scarring, inhibiting the formation of adherent scar to surrounding tissue, preserving the gliding function of a nerve during extremity motion and lastly resisting degradation.7 Vardakas et al., have explored a case of recurrent ulnar tunnel syndrome 1 Consultant Orthopaedic Surgeon, Orthopaedic Surgery Department, El Minia University Hospital, Minya, Egypt 2 Consultant Rheumatology and Rehabilitation, Rheumatology and Rehabilitation Department, El Minia University Hospital, Minya, Egypt *Correspondence to: Ahmed Fathy Sadek, MD, Consultant Orthopaedic Surgeon, Lecturer of Orthopaedic Surgery and Traumatology, Orthopaedic Surgery Department, El Minia University Hospital, Egypt. E-mail: [email protected] Received 2 July 2013; Revision accepted 25 October 2013; Accepted 30 October 2013 Published online 15 November 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22207
Ó 2013 Wiley Periodicals, Inc.
that was previously vein wrapped and found that the vein was intact around the ulnar nerve with no scarring encountered between the vein and nerve, which confirms the protective effect of autogenous vein wrapping against adhesions.8 Experimentally, very encouraging results were encountered that dictated the use of vein wrapping in preventing adhesions between repair sites of adjacent injured structures particularly when an extensive fibrosis is expected, such as combined injuries affecting nerves, tendons, and arteries.9 The aim of this study is to assess the functional and electrophysiologic recovery after vein wrapping of primary repaired ulnar nerves. PATIENTS AND METHODS
During the period from January 2010 till December 2012, 23 patients who were diagnosed with distal ulnar nerve injury were prospectively studied at the unit of hand and microsurgery of our institution where they were divided into two groups by random selection (group one having 11 patients and group two having 12 patients). The first group was managed uniformly by exploration and primary microsurgical epineurorraphy. On the other hand, the second group was managed by exploration and primary microsurgical epineurorraphy complemented with autogenous vein wrapping. All cases of both groups were managed within the first 48 hours following injury. Final outcome was defined on the basis of sensory recovery, motor recovery, and the presence or absence of electrophysiological response. This study was approved by El Minia Faculty of Medicine review board. A full informed
362
Sadek et al.
consent was obtained from each patient participating in this study. The first group included 11 patients (11 nerves) of them eight males and three females with a mean age of (26.4 6 14.4 years). The injury level was in the distal 1/3 of the forearm in all patients. The offending agent was sharp object in all cases. The second group included 12 patients (12 nerves) of them seven males and five females with a mean age of (24.8 6 8.8 years). The injury level was in the distal 1/3 of the forearm in all patients. The offending injury was sharp object in all cases except for a single case that was injured in motor vehicle accident (Table 1). There were associated tendinuous or vascular injuries in nine out of 11 patients in the first group while in the second group, 11 out of 12 cases exhibited associated injuries. There was no nerve defect that could dictate the use of nerve graft in any case of this study. Surgical Technique for Vein Wrapping
Under general anesthesia the contralateral lower extremity was used for harvesting the great saphenous vein. This was the choice of the authors so that two team approach could be applied, which was time and effort effective. A longitudinal incision was made along the
course of the great saphenous vein starting anterior to the medial malleolus and extending proximally. The required length of the vein was determined according to the condition of the underlying bed and the diameter of the nerve. The remaining vein was ligated both proximally and distally. With the help of skin hooks the graft was held straight and incised longitudinally, using a pair of sharp scissors. On the other hand, the injured nerve was managed, simultaneously by another team, by microscopic epineurial repair using monofilament interrupted nylon suture (Ethilon 8/0). The splitted vein was then wrapped in a helical configuration around the site of repair. The vein-tovein junctures were sutured carefully with 6/0 nonabsorbable monofilament. The vein was routinely tagged to the underlying bed both proximally and distally by 6/0 nonabsorbable monofilament. The assessment of first time to show clinical response was done by applying the Tinel’s sign and its progression beyond the suture line. Sensory recovery was estimated according to the British Medical Research Council (MRC) for classification of sensory recovery (S0–S4), which was modified by MacKinnon and Dellon to include classic static two-point discrimination.10 Muscle strength was assessed with manual muscle strength testing according to the MRC muscle power grading (grades 0–5), which was modified by Brandsma et al.11 Index
Table 1. Data of Patients of Both Groups
Group (1)
Mean 6 SD Group (2)
Mean 6 SD
Case (n)
Age (years)
1 2 3 4 5 6 7 8 9 10 11
17 44 17 31 15 14 40 15 24 56 17 26.4 614.4 20 37 30 35 22 24 21 26 24 6 35 17 24.8 6 8.8
1 2 3 4 5 6 7 8 9 10 11 12
Sex
Associated injuries
M F M M M M F M M M F
FCU cut PL, FCR, FCU and FDS FCU cut PL, FDS FCU FCU cut PL, FCR, FCU and FDS FCU
M M F M M M M F F F M F
Cut Ulnar artery, FCU Cut Ulnar artery, FCU Cut Ulnar artery, FCU Cut Ulnar artery, FCU,PL Cut FCU None Cut Ulnar artery, FCU Cut PL,FCR Cut PL,FCR Cut PL,FCR, FDS Cut Ulnar artery, FCU Cut PL,FCR
Ulnar artery
Mechanism of injury
Follow-up (months)
Length of the graft (cm)
Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp
12 14 13 21 13 15 14 13 21 18 20 15.8 6 3.5 24 15 12 18 15 12 6 15 18 12 12 18 14.8 6 4.5
12 10 12 10 14 10 15 12 9 10 11 10 11.25
Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury MVA Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury
M, male; F, female; PL, palmaris longus; FCU, flexor carpi ulnaris; FCR, flexor carpi radialis; FDS, flexor digitorum profundus; MVA, motor vehicle accident.
Microsurgery DOI 10.1002/micr
Outcome After Vein Wrapping of Ulnar Nerves
finger abduction (first dorsal interosseous), little finger adduction (volar interosseous), and little finger abduction (abductor digiti minimi) were examined. The first time to perform (EDS) was at the end of the 6th week and then routinely every six weeks. Electrodiagnostic studies (EDS) were performed to all patients using Nihon Kohden MEB-9400K NeuropackS1 equipment, by the same examiner in the same room temperature between 21 and 34 C. Motor and sensory distal latencies, amplitudes of compound muscle action potential, and motor and sensory nerve conduction velocities were measured using standard methodologies.12 Abductor digiti minimi was used as primary recording site, if wasted or gave no response, first dorsal interosseous was used alternatively.13 Both ulnar and median nerves were stimulated above wrist, below and above elbow. The examination of the median nerve was mainly performed to exclude the presence of the Martin–Gruber Connection (MGC), which is the well-known connection that occurs at the various levels of the forearm between the median nerve or its anterior interosseous branch and the ulnar nerve.14 This was done by stimulating the median nerve just above and below the elbow using low voltage followed by high voltage and recording the compound muscle action potential (CMAP) in the abductor digiti minimi muscle. Regarding sensory nerve conduction study for ulnar nerve; little finger was used for recording. Concentric needle electromyography was done for the same muscles used for motor conduction.15 Assessment of electrophysiologic recovery was based on motor and sensory conduction velocity and was graded (Table 2).16 The final status of functional motor and sensory recovery was classified as good, satisfactory, moderate, and bad according to the rules confined in (Table 3). The final grading was set according to the least grade of the aforementioned three parameters.16 The expected factors to affect outcome; age, associated injuries, and technique of repair were analyzed. Statistical Analysis
Data processing was performed using SPSS for Windows software (version 20). Average values were presented as mean value 6 standard deviation. Independent Table 2. Grading of Electrophysiological Recovery E0
No MCV nor SCV
E1 E2 E3 E4
No or minimal SCV and MCV < 25 m/s SCV < 25 m/s and MCV 5 25–37 m/s SCV 5 25–37 m/s and MCV > 37 m/s Normal SCV And MCV,
E, electrophysiological response; MCV, motor conduction velocity; SCV, sensory conduction velocity.
363
Table 3. Grading for the Final Outcome Grade Good Satisfactory Moderate Bad
Motor
Sensory
Electromyographic
M5 OR M4 M3 M2 M1 OR M0
S4 OR S31 S3 S2 OR S21 S1 OR S0
E4 OR E3 E2 E1 M0
M, motor; S, sensory; E, electromyography.
sample t-test and chi square test were used to evaluate the results. The results were considered statistically significant if the P-value was less than 0.05. RESULTS
The average period of follow-up in the first group was 15.8 6 3.5 months (minimum 12 and maximum 21 months) while in the second group was 14.8 6 4.5 months (minimum 6 and maximum 24 months). The results of the first group of direct primary repair and the second group of vein wrapping are summarized in (Table 4). Regarding the grading, the first group showed two good, two satisfactory, six moderate, and one bad results (Table 3). On the other hand the second group showed better results in the form of five good, six satisfactory, one bad and no moderate results. These results showed statistically significant difference between both groups (P 5 0.026). By applying the Tinel’s sign, it was noted that the progression of this sign beyond the suture line was consistent in all cases of group one except in one case. On the other hand, in the second group only one case exhibited negative sign. In the first group, the first time to show clinical response was the third month, which was exhibited in four cases of this group with a mean time of 5 6 1.5 months. In addition, the first time to show electromyographic response was at the sixth month with a mean time of 6.5 6 1.7 months. On the other hand the first time to show clinical response in the second group was at 1.5 month, which was a common finding in eight cases of this group with a mean time of 1.8 6 0.5 months. In addition, the first time to show electromyographic response was at the third month with a mean time of 7.1 6 2.8 months. These results showed statistically significant difference between both groups regarding the first time to show clinical response (P < 0.001). On the other hand, there was no statistically significant difference between both groups regarding the first time of appearance of electromyographic response (P 5 0.784). No single case in this series exhibited positive (MGC). If we considered that both good and satisfactory results constitute successful results, so the second group achieved 92% successful results in comparison to 36% successful results in the first group. Microsurgery DOI 10.1002/micr
364
Sadek et al. Table 4. Functional and Electrophysiological Results of Both Groups
Group (1)
Case (n)
1st time to show clinical response (months)
1st time to show electric response (months)
6 6 3 6 6 6 6 3 6 3 3 5 6 1.5 2 3 2 1.5 1.5 1.5
6 6 6 6 6 6 12 6 6 6 6 6.5 6 1.7 12 12 6 6 3 6
1.5 1.5 1.5 1.5 1.5 1.8 6 0.5
6 6 6 6 6 7.1 6 2.8
1 2 3 4 5 6 7 8 9 10 11 Mean 6 SD Group (2)
1 2 3 4 5 6 7 8 9 10 11 12
Mean 6 SD
M
S
EMG
Grading
M2 M2 M2 M4 M3 M3 M1 M2 M4 M2 M2
S2 S2 S31 S31 S31 S31 S2 S31 S31 S21 S3
E2 E2 E3 E4 E3 E3 E2 E3 E4 E2 E2
Moderate Moderate Moderate Good Satisfactory Satisfactory Bad Moderate Good Moderate Moderate
M4 M3 M3 M4 M5 M4 M0 M5 M5 M5 M4 M5
S3 S3 S3 S31 S3 S3 S0 S4 S31 S4 S3 S31
E3 E3 E4 E4 E4 E3 E0 E4 E3 E4 E3 E4
Satisfactory Satisfactory Satisfactory Good Satisfactory Satisfactory Bad Good Good Good Satisfactory Good
M, motor; S, sensory; EMG, electromyography. 1st time to show clinical response: P < 0.001, 1st time to show electrophysiological response: P 5 0.784, motor recovery: P 5 0.018, sensory recovery, P 5 0.042; electrophysiological recovery: P 5 0.044, grading: P 5 0.026.
Regarding relation of age, associated vascular, tendinuous, or other soft tissue injuries there were no statistically significant differences between both groups. DISCUSSION
Surgical repair of ulnar nerve lesions do relatively poor as compared, for instance, to the radial and median nerves.17 In 1991, Birch and Raji had conducted a detailed and comprehensive study on 108 median and ulnar nerve injuries that were managed by either primary, delayed repair, or grafting. They concluded that primary repair is the best with achieving a few excellent results particularly in young age patients.18 The same authors concluded some of the factors jeopardizing the final results of primary repair provided that the technique utilized was proper with adhesions being the predominant factor. This emphasizes the positive role of vein wrapping to guard against adhesions. In our study, the authors preferred to harvest the great saphenous vein from the contralateral lower limb as the donor vein so that two team approaches could be applied, which was time and effort effective. Some authors believe that vein wrapping can be used to prevent adhesions between repair sites of adjacent injured structures.9 Our study confirms the role of vein Microsurgery DOI 10.1002/micr
wrapping in preventing adhesions in cases of simultaneous injured structures whereas 11 out of 12 cases of the second group had associated tendon or vascular injuries, which were believed to be limiting factor to ideal nerve recovery.19 Clinically, vein wrapping was applied to augment reconstruction of recurrent laryngeal nerve after extirpation of thyroid carcinoma to facilitate nerve regeneration, protect the nerve coaptation site mechanically, and prevent neuroma formation.20 According to that study, vein wrapping technique could be favored over conventional reconstruction techniques for nerve injuries. On experimental level, Dos Santos et al. confirmed these findings.21 In our study, the second group achieved 92% successful results in comparison to 36% successful results in the first group (i.e., better than reported in most series of the functioning hand after ulnar nerve injuries 19–84%.16). EDS for peripheral nerve injuries can provide precise information about localization and severity of the lesion in addition to determination of pathophysiology as these abnormalities may be clinically uncertain, silent, or unsuspected particularly when patient is noncooperative or in pain. They also provide information about prognosis, allowing one to reliably estimate the timing and extent of recovery.1
Outcome After Vein Wrapping of Ulnar Nerves
The first time to perform (EDS) was at the end of the 6th week and then routinely every six weeks. This could be explained by the fact that expected rate of nerve regeneration is 1 mm/day, knowing that the average distance between site of lesion and recording muscle is 4 cm, so the shortest expected time to see signs of reinnervation is 40 days (which almost equals 6 weeks). On 12th week follow-up, more evidence of reinnervation could be seen in positive cases depending on time lag between injury and surgical interference.22 It is commonly accepted, that nerve recovery in younger patients is superior to that in older patients.18 However, regarding relation of age to the outcome in our results there was no statistically significant differences between both groups. In a previous study, the long-term outcome from silicone tube nerve repair was compared to the outcome after routine microsurgical repair in a clinical randomized prospective study, including 30 patients with median or ulnar nerve injuries in the distal forearm. Postoperatively, no significant difference in outcome between the two techniques was exhibited except that cold intolerance was significantly less severe with the tubular technique.23 The authors believed that the silicone tube constitutes a “biological chamber” in which nerve regeneration can take place undisturbed. This belief is coincident with the belief of other authors about the role of biodegradable nerve guides for the repair of peripheral nerve gaps, which showed superior results in comparison to classic nerve grafts.24 In our study, we believe that vein wrapping around the site of repair constitute a biological barrier not chamber that serves to prevent adhesions and neuroma formation. Henry et al. conducted an experimental study to determine whether isolation of the nerve repair site using photochemical tissue bonding in combination with human amniotic membrane can improve both functional and histologic recovery. They found that nerves treated with amnion wraps demonstrated a statistically significant improvement than nerves repaired without wrapping on both functional and histologic parameters.25 Okui et al. concluded that honeycomb film may offer a suitable reinforcing material for adhesion-free neurorrhaphy.26 These two previous studies provide significant evidence that biological or biodegradable barriers could improve the healing environment for injured nerves which copes with our results. Using vein wrapping in nerve reconstruction can accelerate the rate of nerve healing.27 This is explained by the elaboration of trophic factors from the endothelial and smooth muscle cells of the vein graft with very high collagen content that allows a suitable environment for axon regeneration. At histological level, using vein graft wraps leads to thinner epineurium, more regenerated axons and fewer inflammatory cells.28 These observations and findings add to the advantages of vein wrapping.
365
CONCLUSION
To our knowledge, there was no single clinical study that was performed to demonstrate the effect of vein wrapping as a complementary procedure to primary nerve repair. This study emphasizes the role of vein wrapping as a simple technique in complementing nerve repair in the different clinical settings particularly in cases with associated vascular or tendon injuries to prevent scarring, neuroma formation, and enhance recovery both on clinical and electrophysiological levels.
REFERENCES 1. Quann D, Bird SJ. Nerve conduction studies and electromyography in the evaluation of peripheral nerve injuries. Univ Pa Orthop J 1999;12:45–51. 2. Ducker TB, Hayes GJ. Experimental improvements in the use of Silastic cuff for peripheral nerve repair. J Neurosurg 1968;28: 582–587. 3. MacKay MA, Fischgrund JS, Herkowitz HN, Kurz LT, Hecht B, Schwartz M. The effect of interposition membrane on the outcome of lumbar laminectomy and discectomy. Spine 1995;20:1793–1796. 4. Dumanian GA, McClinton MA, Brushart TM. The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar. J Hand Surg 1999;24:30–36. 5. Masear JR, Tullos JR, Mary ET, Meyer RD. Venous wrapping of nerves to prevent scar-ring. J Hand Surg 1990;15:817–818. 6. Gould JS. Treatment of the painful injured nerve in-continuity. In: Gelberman RH, editor. Operative Nerve Repair and Reconstruction. Philadelphia: JB Lippincott; 1991. pp 1541–1549. 7. Xu J, Varitimidis SE, Fisher KJ, Tomaino MM, Sotereanos DG. The effect of wrapping scarred nerves with autogenous vein graft to treat recurrent chronic nerve compression. J Hand Surg 2000;25: 93–103. 8. Vardakas DG, Varitimidis SE, Sotereanos DG. Findings of exploration of a vein-wrapped ulnar nerve: Report of a case. J Hand Surg 2001;26:60–63. 9. Tuncali D, Cigsar B, Talim B, Barutcu AY, Aslan G. Insulation of simultaneous arterial and nerve repairs in the rat: The effectiveness of the autologous vein graft. Neuroanatomy 2004;3:51–53. 10. Mackinnon SE, Dellon AL. Surgery of the Peripheral Nerve. New York: Thieme Medical Publishers, 1988. 11. Brandsma JW, Schreuders TA, Birke JA, Piefer A, Oostendorp R. Manual muscle strength testing: Intraobserver and interobserver reliabilities for the intrinsic muscles of the hand. J Hand Ther 1995;8: 185–190. 12. Preston DC, Shapeiro BE. Routine upper extremity and facial nerve conduction techniques. In: Preston DC, Shapeiro BE, editor. Electromyography and Neuromuscular Disorders, Clinical-Electrophysiologic Correlations, 2nd ed. Philadelphia, PA: Butterworth-Heineman; 2007. pp 117–143. 13. Kincaid JC, Phillips LH, Daube JR. The evaluation of suspected ulnar neuropathy at the elbow: Normal conduction study values. Arch Neurol 1986;43:44. 14. Hodzic R, Piric N, Hodzic M, Kojic B. Electrophysiological evaluation of the incidence of Martin-Gruber Anastomosis in healthy bosnian population. Maced J Med Sci 2011;4:376–379. 15. Kothari MJ, Preston DC, Logigian EL. Lumbrical and interossei recordings localize ulnar neuropathy at the wrist. Muscle Nerve 1996;19:170–174. 16. Roganovic Z. Missile-caused ulnar nerve injuries: Outcomes of 128 repairs. Neurosurgery 2004;55:1–14. 17. Post R, De Boer KS, Malessy MJA. Outcome following nerve repair of high isolated clean sharp injuries of the ulnar nerve. PLoS ONE 2012 7:e47928. doi:10.1371/journal.pone.0047928.
Microsurgery DOI 10.1002/micr
366
Sadek et al.
18. Birch R, Raji ARM. Repair of median and ulnar nerves. Primary suture is best. J Bone Jt Surg Br 1991;73:154–157. 19. Rosenfield J, Paksima B. Peripheral nerve injuries and repair in the upper extremity. Hosp Jt Dis 2001/2002;60:155–161. 20. Yoo MY, Lee IJ, Lim H, Kim JH, Park MC. Vein wrapping technique for nerve reconstruction in patients with thyroid cancer invading the recurrent laryngeal nerve. Arch Plast Surg 2012;39:71–75. 21. Santos EB, Fernandes M, Santos JBG, Leite VM, Valente GS, Faloppa F. Study of tibial nerve regeneration in wistar rats in primary neurorrhaphy with and without gap, wrapped in vein segments. Acta Ortop Bras 2012;20: 165–169. 22. Campbell WW. Evaluation and management of peripheral nerve injury. Clin Neurophysiol 2008;119:1951–1965. 23. Lundborg G, Rosen B, Dahlin L, Holmberg J, Rosen I. Tubular repair of the median or ulnar nerve in the human forearm: A 5-year follow-up. J Hand Surg 2004;29B:100–107.
Microsurgery DOI 10.1002/micr
24. Meek MF, Coert JH, Robinson PH. Poor results after nerve grafting in the upper extremity: Quo vadis? Microsurgery 2005;25:396–402. 25. Henry FP, Goyal NA, David WS, Wes D, Bujold KE, Randolph MA, Winograd JM, Kochevar IE, Redmond RW. Improving electrophysiologic and histologic outcomes by photochemically sealing amnion to the peripheral nerve repair site. Surgery 2009;145:313–321. 26. Okui N, Yamamoto M, Fukuhira Y, Kaneko H, Hirata H. A new nerve coaptation technique using a biodegradable honeycombpatterned film. Microsurgery 2012;32:466–474. 27. Siemionow M, Uygur S, Ozturk C, Siemionow K. Techniques and materials for enhancement of peripheral nerve regeneration: A literature review. Microsurgery 2013;33:318–328. 28. Acar M, Karacalar A, Ayyildiz M, Unal B, Canan S, Agar E, Kaplan S. The effect of autogenous vein grafts on nerve repair with size discrepancy in rats: An electrophysiological and stereological analysis. Brain Res 2008;1198:171–181.
Purpose: This study aimed at assessing the functional and electrophysiological recovery after vein wrapping of primary repaired ulnar nerves Methods: From January 2010 till December 2012, 23 patients (diagnosed with distal ulnar nerve injury) were prospectively studied where they were divided into two groups; group one (11 patients) and group two (12 patients). The injury was sharp in all cases but for one. The first group was managed by primary epineurorraphy. The second group was managed by primary epineurorraphy and autogenous vein wrapping. Final outcome was based on sensory recovery, motor recovery, and the presence or absence of electrophysiological response Results: Clinically, only one case in each group exhibited negative Tinel’s sign. The second group achieved statistically significant superiority regarding motor recovery (P 5 0.018), sensory recovery (P 5 0.042) and electrophysiological recovery (P 5 0.044). Group one showed two good, two satisfactory, six moderate, and one bad results while the second group showed five good, six satisfactory, one bad and no moderate results (P 5 0.026). The first time to show clinical response in group one was the third month while in the second group it was at 1.5 month (P < 0.001). In addition, the first time to show electromyographic response in group one was at the sixth month while in group two it was at the third month Conclusions: Vein wrapping is a simple technique that could be used reliably to augment primary neurorrhaphy particularly in cases with associated vascular or tendon injuries to prevent scarring and enhance functional and elecC 2013 Wiley Periodicals, Inc. Microsurgery 34:361–366, 2014. trophysiological recovery. V
The
objective of repair after nerve injury is to restore normal sensitivity and motor function. Recovery from peripheral nerve injury may occur by one of three mechanisms namely; remyelination, collateral axonal sprouting, or regeneration from the proximal injury site.1 The control of postsurgical scar formation has been the goal of microsurgeons many decades.2–4 That is why interposition materials have been tested to prevent postoperative adhesions between nerves and surrounding tissues in various clinical settings.5 In recent years, autogenous vein wrapping has gained good reputation among microsurgeons.6 Masear et al.5 first described the technique of vein wrapping. This technique was first applied for the treatment of painful neuroma incontinuity by Gould.6 This could be attributed to the fact that veins meet all criteria required for ideal wrapping of nerves namely; constituting a biological barrier protecting the nerve from compression by surrounding scarring, inhibiting the formation of adherent scar to surrounding tissue, preserving the gliding function of a nerve during extremity motion and lastly resisting degradation.7 Vardakas et al., have explored a case of recurrent ulnar tunnel syndrome 1 Consultant Orthopaedic Surgeon, Orthopaedic Surgery Department, El Minia University Hospital, Minya, Egypt 2 Consultant Rheumatology and Rehabilitation, Rheumatology and Rehabilitation Department, El Minia University Hospital, Minya, Egypt *Correspondence to: Ahmed Fathy Sadek, MD, Consultant Orthopaedic Surgeon, Lecturer of Orthopaedic Surgery and Traumatology, Orthopaedic Surgery Department, El Minia University Hospital, Egypt. E-mail: [email protected] Received 2 July 2013; Revision accepted 25 October 2013; Accepted 30 October 2013 Published online 15 November 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22207
Ó 2013 Wiley Periodicals, Inc.
that was previously vein wrapped and found that the vein was intact around the ulnar nerve with no scarring encountered between the vein and nerve, which confirms the protective effect of autogenous vein wrapping against adhesions.8 Experimentally, very encouraging results were encountered that dictated the use of vein wrapping in preventing adhesions between repair sites of adjacent injured structures particularly when an extensive fibrosis is expected, such as combined injuries affecting nerves, tendons, and arteries.9 The aim of this study is to assess the functional and electrophysiologic recovery after vein wrapping of primary repaired ulnar nerves. PATIENTS AND METHODS
During the period from January 2010 till December 2012, 23 patients who were diagnosed with distal ulnar nerve injury were prospectively studied at the unit of hand and microsurgery of our institution where they were divided into two groups by random selection (group one having 11 patients and group two having 12 patients). The first group was managed uniformly by exploration and primary microsurgical epineurorraphy. On the other hand, the second group was managed by exploration and primary microsurgical epineurorraphy complemented with autogenous vein wrapping. All cases of both groups were managed within the first 48 hours following injury. Final outcome was defined on the basis of sensory recovery, motor recovery, and the presence or absence of electrophysiological response. This study was approved by El Minia Faculty of Medicine review board. A full informed
362
Sadek et al.
consent was obtained from each patient participating in this study. The first group included 11 patients (11 nerves) of them eight males and three females with a mean age of (26.4 6 14.4 years). The injury level was in the distal 1/3 of the forearm in all patients. The offending agent was sharp object in all cases. The second group included 12 patients (12 nerves) of them seven males and five females with a mean age of (24.8 6 8.8 years). The injury level was in the distal 1/3 of the forearm in all patients. The offending injury was sharp object in all cases except for a single case that was injured in motor vehicle accident (Table 1). There were associated tendinuous or vascular injuries in nine out of 11 patients in the first group while in the second group, 11 out of 12 cases exhibited associated injuries. There was no nerve defect that could dictate the use of nerve graft in any case of this study. Surgical Technique for Vein Wrapping
Under general anesthesia the contralateral lower extremity was used for harvesting the great saphenous vein. This was the choice of the authors so that two team approach could be applied, which was time and effort effective. A longitudinal incision was made along the
course of the great saphenous vein starting anterior to the medial malleolus and extending proximally. The required length of the vein was determined according to the condition of the underlying bed and the diameter of the nerve. The remaining vein was ligated both proximally and distally. With the help of skin hooks the graft was held straight and incised longitudinally, using a pair of sharp scissors. On the other hand, the injured nerve was managed, simultaneously by another team, by microscopic epineurial repair using monofilament interrupted nylon suture (Ethilon 8/0). The splitted vein was then wrapped in a helical configuration around the site of repair. The vein-tovein junctures were sutured carefully with 6/0 nonabsorbable monofilament. The vein was routinely tagged to the underlying bed both proximally and distally by 6/0 nonabsorbable monofilament. The assessment of first time to show clinical response was done by applying the Tinel’s sign and its progression beyond the suture line. Sensory recovery was estimated according to the British Medical Research Council (MRC) for classification of sensory recovery (S0–S4), which was modified by MacKinnon and Dellon to include classic static two-point discrimination.10 Muscle strength was assessed with manual muscle strength testing according to the MRC muscle power grading (grades 0–5), which was modified by Brandsma et al.11 Index
Table 1. Data of Patients of Both Groups
Group (1)
Mean 6 SD Group (2)
Mean 6 SD
Case (n)
Age (years)
1 2 3 4 5 6 7 8 9 10 11
17 44 17 31 15 14 40 15 24 56 17 26.4 614.4 20 37 30 35 22 24 21 26 24 6 35 17 24.8 6 8.8
1 2 3 4 5 6 7 8 9 10 11 12
Sex
Associated injuries
M F M M M M F M M M F
FCU cut PL, FCR, FCU and FDS FCU cut PL, FDS FCU FCU cut PL, FCR, FCU and FDS FCU
M M F M M M M F F F M F
Cut Ulnar artery, FCU Cut Ulnar artery, FCU Cut Ulnar artery, FCU Cut Ulnar artery, FCU,PL Cut FCU None Cut Ulnar artery, FCU Cut PL,FCR Cut PL,FCR Cut PL,FCR, FDS Cut Ulnar artery, FCU Cut PL,FCR
Ulnar artery
Mechanism of injury
Follow-up (months)
Length of the graft (cm)
Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp Sharp
12 14 13 21 13 15 14 13 21 18 20 15.8 6 3.5 24 15 12 18 15 12 6 15 18 12 12 18 14.8 6 4.5
12 10 12 10 14 10 15 12 9 10 11 10 11.25
Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury MVA Sharp injury Sharp injury Sharp injury Sharp injury Sharp injury
M, male; F, female; PL, palmaris longus; FCU, flexor carpi ulnaris; FCR, flexor carpi radialis; FDS, flexor digitorum profundus; MVA, motor vehicle accident.
Microsurgery DOI 10.1002/micr
Outcome After Vein Wrapping of Ulnar Nerves
finger abduction (first dorsal interosseous), little finger adduction (volar interosseous), and little finger abduction (abductor digiti minimi) were examined. The first time to perform (EDS) was at the end of the 6th week and then routinely every six weeks. Electrodiagnostic studies (EDS) were performed to all patients using Nihon Kohden MEB-9400K NeuropackS1 equipment, by the same examiner in the same room temperature between 21 and 34 C. Motor and sensory distal latencies, amplitudes of compound muscle action potential, and motor and sensory nerve conduction velocities were measured using standard methodologies.12 Abductor digiti minimi was used as primary recording site, if wasted or gave no response, first dorsal interosseous was used alternatively.13 Both ulnar and median nerves were stimulated above wrist, below and above elbow. The examination of the median nerve was mainly performed to exclude the presence of the Martin–Gruber Connection (MGC), which is the well-known connection that occurs at the various levels of the forearm between the median nerve or its anterior interosseous branch and the ulnar nerve.14 This was done by stimulating the median nerve just above and below the elbow using low voltage followed by high voltage and recording the compound muscle action potential (CMAP) in the abductor digiti minimi muscle. Regarding sensory nerve conduction study for ulnar nerve; little finger was used for recording. Concentric needle electromyography was done for the same muscles used for motor conduction.15 Assessment of electrophysiologic recovery was based on motor and sensory conduction velocity and was graded (Table 2).16 The final status of functional motor and sensory recovery was classified as good, satisfactory, moderate, and bad according to the rules confined in (Table 3). The final grading was set according to the least grade of the aforementioned three parameters.16 The expected factors to affect outcome; age, associated injuries, and technique of repair were analyzed. Statistical Analysis
Data processing was performed using SPSS for Windows software (version 20). Average values were presented as mean value 6 standard deviation. Independent Table 2. Grading of Electrophysiological Recovery E0
No MCV nor SCV
E1 E2 E3 E4
No or minimal SCV and MCV < 25 m/s SCV < 25 m/s and MCV 5 25–37 m/s SCV 5 25–37 m/s and MCV > 37 m/s Normal SCV And MCV,
E, electrophysiological response; MCV, motor conduction velocity; SCV, sensory conduction velocity.
363
Table 3. Grading for the Final Outcome Grade Good Satisfactory Moderate Bad
Motor
Sensory
Electromyographic
M5 OR M4 M3 M2 M1 OR M0
S4 OR S31 S3 S2 OR S21 S1 OR S0
E4 OR E3 E2 E1 M0
M, motor; S, sensory; E, electromyography.
sample t-test and chi square test were used to evaluate the results. The results were considered statistically significant if the P-value was less than 0.05. RESULTS
The average period of follow-up in the first group was 15.8 6 3.5 months (minimum 12 and maximum 21 months) while in the second group was 14.8 6 4.5 months (minimum 6 and maximum 24 months). The results of the first group of direct primary repair and the second group of vein wrapping are summarized in (Table 4). Regarding the grading, the first group showed two good, two satisfactory, six moderate, and one bad results (Table 3). On the other hand the second group showed better results in the form of five good, six satisfactory, one bad and no moderate results. These results showed statistically significant difference between both groups (P 5 0.026). By applying the Tinel’s sign, it was noted that the progression of this sign beyond the suture line was consistent in all cases of group one except in one case. On the other hand, in the second group only one case exhibited negative sign. In the first group, the first time to show clinical response was the third month, which was exhibited in four cases of this group with a mean time of 5 6 1.5 months. In addition, the first time to show electromyographic response was at the sixth month with a mean time of 6.5 6 1.7 months. On the other hand the first time to show clinical response in the second group was at 1.5 month, which was a common finding in eight cases of this group with a mean time of 1.8 6 0.5 months. In addition, the first time to show electromyographic response was at the third month with a mean time of 7.1 6 2.8 months. These results showed statistically significant difference between both groups regarding the first time to show clinical response (P < 0.001). On the other hand, there was no statistically significant difference between both groups regarding the first time of appearance of electromyographic response (P 5 0.784). No single case in this series exhibited positive (MGC). If we considered that both good and satisfactory results constitute successful results, so the second group achieved 92% successful results in comparison to 36% successful results in the first group. Microsurgery DOI 10.1002/micr
364
Sadek et al. Table 4. Functional and Electrophysiological Results of Both Groups
Group (1)
Case (n)
1st time to show clinical response (months)
1st time to show electric response (months)
6 6 3 6 6 6 6 3 6 3 3 5 6 1.5 2 3 2 1.5 1.5 1.5
6 6 6 6 6 6 12 6 6 6 6 6.5 6 1.7 12 12 6 6 3 6
1.5 1.5 1.5 1.5 1.5 1.8 6 0.5
6 6 6 6 6 7.1 6 2.8
1 2 3 4 5 6 7 8 9 10 11 Mean 6 SD Group (2)
1 2 3 4 5 6 7 8 9 10 11 12
Mean 6 SD
M
S
EMG
Grading
M2 M2 M2 M4 M3 M3 M1 M2 M4 M2 M2
S2 S2 S31 S31 S31 S31 S2 S31 S31 S21 S3
E2 E2 E3 E4 E3 E3 E2 E3 E4 E2 E2
Moderate Moderate Moderate Good Satisfactory Satisfactory Bad Moderate Good Moderate Moderate
M4 M3 M3 M4 M5 M4 M0 M5 M5 M5 M4 M5
S3 S3 S3 S31 S3 S3 S0 S4 S31 S4 S3 S31
E3 E3 E4 E4 E4 E3 E0 E4 E3 E4 E3 E4
Satisfactory Satisfactory Satisfactory Good Satisfactory Satisfactory Bad Good Good Good Satisfactory Good
M, motor; S, sensory; EMG, electromyography. 1st time to show clinical response: P < 0.001, 1st time to show electrophysiological response: P 5 0.784, motor recovery: P 5 0.018, sensory recovery, P 5 0.042; electrophysiological recovery: P 5 0.044, grading: P 5 0.026.
Regarding relation of age, associated vascular, tendinuous, or other soft tissue injuries there were no statistically significant differences between both groups. DISCUSSION
Surgical repair of ulnar nerve lesions do relatively poor as compared, for instance, to the radial and median nerves.17 In 1991, Birch and Raji had conducted a detailed and comprehensive study on 108 median and ulnar nerve injuries that were managed by either primary, delayed repair, or grafting. They concluded that primary repair is the best with achieving a few excellent results particularly in young age patients.18 The same authors concluded some of the factors jeopardizing the final results of primary repair provided that the technique utilized was proper with adhesions being the predominant factor. This emphasizes the positive role of vein wrapping to guard against adhesions. In our study, the authors preferred to harvest the great saphenous vein from the contralateral lower limb as the donor vein so that two team approaches could be applied, which was time and effort effective. Some authors believe that vein wrapping can be used to prevent adhesions between repair sites of adjacent injured structures.9 Our study confirms the role of vein Microsurgery DOI 10.1002/micr
wrapping in preventing adhesions in cases of simultaneous injured structures whereas 11 out of 12 cases of the second group had associated tendon or vascular injuries, which were believed to be limiting factor to ideal nerve recovery.19 Clinically, vein wrapping was applied to augment reconstruction of recurrent laryngeal nerve after extirpation of thyroid carcinoma to facilitate nerve regeneration, protect the nerve coaptation site mechanically, and prevent neuroma formation.20 According to that study, vein wrapping technique could be favored over conventional reconstruction techniques for nerve injuries. On experimental level, Dos Santos et al. confirmed these findings.21 In our study, the second group achieved 92% successful results in comparison to 36% successful results in the first group (i.e., better than reported in most series of the functioning hand after ulnar nerve injuries 19–84%.16). EDS for peripheral nerve injuries can provide precise information about localization and severity of the lesion in addition to determination of pathophysiology as these abnormalities may be clinically uncertain, silent, or unsuspected particularly when patient is noncooperative or in pain. They also provide information about prognosis, allowing one to reliably estimate the timing and extent of recovery.1
Outcome After Vein Wrapping of Ulnar Nerves
The first time to perform (EDS) was at the end of the 6th week and then routinely every six weeks. This could be explained by the fact that expected rate of nerve regeneration is 1 mm/day, knowing that the average distance between site of lesion and recording muscle is 4 cm, so the shortest expected time to see signs of reinnervation is 40 days (which almost equals 6 weeks). On 12th week follow-up, more evidence of reinnervation could be seen in positive cases depending on time lag between injury and surgical interference.22 It is commonly accepted, that nerve recovery in younger patients is superior to that in older patients.18 However, regarding relation of age to the outcome in our results there was no statistically significant differences between both groups. In a previous study, the long-term outcome from silicone tube nerve repair was compared to the outcome after routine microsurgical repair in a clinical randomized prospective study, including 30 patients with median or ulnar nerve injuries in the distal forearm. Postoperatively, no significant difference in outcome between the two techniques was exhibited except that cold intolerance was significantly less severe with the tubular technique.23 The authors believed that the silicone tube constitutes a “biological chamber” in which nerve regeneration can take place undisturbed. This belief is coincident with the belief of other authors about the role of biodegradable nerve guides for the repair of peripheral nerve gaps, which showed superior results in comparison to classic nerve grafts.24 In our study, we believe that vein wrapping around the site of repair constitute a biological barrier not chamber that serves to prevent adhesions and neuroma formation. Henry et al. conducted an experimental study to determine whether isolation of the nerve repair site using photochemical tissue bonding in combination with human amniotic membrane can improve both functional and histologic recovery. They found that nerves treated with amnion wraps demonstrated a statistically significant improvement than nerves repaired without wrapping on both functional and histologic parameters.25 Okui et al. concluded that honeycomb film may offer a suitable reinforcing material for adhesion-free neurorrhaphy.26 These two previous studies provide significant evidence that biological or biodegradable barriers could improve the healing environment for injured nerves which copes with our results. Using vein wrapping in nerve reconstruction can accelerate the rate of nerve healing.27 This is explained by the elaboration of trophic factors from the endothelial and smooth muscle cells of the vein graft with very high collagen content that allows a suitable environment for axon regeneration. At histological level, using vein graft wraps leads to thinner epineurium, more regenerated axons and fewer inflammatory cells.28 These observations and findings add to the advantages of vein wrapping.
365
CONCLUSION
To our knowledge, there was no single clinical study that was performed to demonstrate the effect of vein wrapping as a complementary procedure to primary nerve repair. This study emphasizes the role of vein wrapping as a simple technique in complementing nerve repair in the different clinical settings particularly in cases with associated vascular or tendon injuries to prevent scarring, neuroma formation, and enhance recovery both on clinical and electrophysiological levels.
REFERENCES 1. Quann D, Bird SJ. Nerve conduction studies and electromyography in the evaluation of peripheral nerve injuries. Univ Pa Orthop J 1999;12:45–51. 2. Ducker TB, Hayes GJ. Experimental improvements in the use of Silastic cuff for peripheral nerve repair. J Neurosurg 1968;28: 582–587. 3. MacKay MA, Fischgrund JS, Herkowitz HN, Kurz LT, Hecht B, Schwartz M. The effect of interposition membrane on the outcome of lumbar laminectomy and discectomy. Spine 1995;20:1793–1796. 4. Dumanian GA, McClinton MA, Brushart TM. The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar. J Hand Surg 1999;24:30–36. 5. Masear JR, Tullos JR, Mary ET, Meyer RD. Venous wrapping of nerves to prevent scar-ring. J Hand Surg 1990;15:817–818. 6. Gould JS. Treatment of the painful injured nerve in-continuity. In: Gelberman RH, editor. Operative Nerve Repair and Reconstruction. Philadelphia: JB Lippincott; 1991. pp 1541–1549. 7. Xu J, Varitimidis SE, Fisher KJ, Tomaino MM, Sotereanos DG. The effect of wrapping scarred nerves with autogenous vein graft to treat recurrent chronic nerve compression. J Hand Surg 2000;25: 93–103. 8. Vardakas DG, Varitimidis SE, Sotereanos DG. Findings of exploration of a vein-wrapped ulnar nerve: Report of a case. J Hand Surg 2001;26:60–63. 9. Tuncali D, Cigsar B, Talim B, Barutcu AY, Aslan G. Insulation of simultaneous arterial and nerve repairs in the rat: The effectiveness of the autologous vein graft. Neuroanatomy 2004;3:51–53. 10. Mackinnon SE, Dellon AL. Surgery of the Peripheral Nerve. New York: Thieme Medical Publishers, 1988. 11. Brandsma JW, Schreuders TA, Birke JA, Piefer A, Oostendorp R. Manual muscle strength testing: Intraobserver and interobserver reliabilities for the intrinsic muscles of the hand. J Hand Ther 1995;8: 185–190. 12. Preston DC, Shapeiro BE. Routine upper extremity and facial nerve conduction techniques. In: Preston DC, Shapeiro BE, editor. Electromyography and Neuromuscular Disorders, Clinical-Electrophysiologic Correlations, 2nd ed. Philadelphia, PA: Butterworth-Heineman; 2007. pp 117–143. 13. Kincaid JC, Phillips LH, Daube JR. The evaluation of suspected ulnar neuropathy at the elbow: Normal conduction study values. Arch Neurol 1986;43:44. 14. Hodzic R, Piric N, Hodzic M, Kojic B. Electrophysiological evaluation of the incidence of Martin-Gruber Anastomosis in healthy bosnian population. Maced J Med Sci 2011;4:376–379. 15. Kothari MJ, Preston DC, Logigian EL. Lumbrical and interossei recordings localize ulnar neuropathy at the wrist. Muscle Nerve 1996;19:170–174. 16. Roganovic Z. Missile-caused ulnar nerve injuries: Outcomes of 128 repairs. Neurosurgery 2004;55:1–14. 17. Post R, De Boer KS, Malessy MJA. Outcome following nerve repair of high isolated clean sharp injuries of the ulnar nerve. PLoS ONE 2012 7:e47928. doi:10.1371/journal.pone.0047928.
Microsurgery DOI 10.1002/micr
366
Sadek et al.
18. Birch R, Raji ARM. Repair of median and ulnar nerves. Primary suture is best. J Bone Jt Surg Br 1991;73:154–157. 19. Rosenfield J, Paksima B. Peripheral nerve injuries and repair in the upper extremity. Hosp Jt Dis 2001/2002;60:155–161. 20. Yoo MY, Lee IJ, Lim H, Kim JH, Park MC. Vein wrapping technique for nerve reconstruction in patients with thyroid cancer invading the recurrent laryngeal nerve. Arch Plast Surg 2012;39:71–75. 21. Santos EB, Fernandes M, Santos JBG, Leite VM, Valente GS, Faloppa F. Study of tibial nerve regeneration in wistar rats in primary neurorrhaphy with and without gap, wrapped in vein segments. Acta Ortop Bras 2012;20: 165–169. 22. Campbell WW. Evaluation and management of peripheral nerve injury. Clin Neurophysiol 2008;119:1951–1965. 23. Lundborg G, Rosen B, Dahlin L, Holmberg J, Rosen I. Tubular repair of the median or ulnar nerve in the human forearm: A 5-year follow-up. J Hand Surg 2004;29B:100–107.
Microsurgery DOI 10.1002/micr
24. Meek MF, Coert JH, Robinson PH. Poor results after nerve grafting in the upper extremity: Quo vadis? Microsurgery 2005;25:396–402. 25. Henry FP, Goyal NA, David WS, Wes D, Bujold KE, Randolph MA, Winograd JM, Kochevar IE, Redmond RW. Improving electrophysiologic and histologic outcomes by photochemically sealing amnion to the peripheral nerve repair site. Surgery 2009;145:313–321. 26. Okui N, Yamamoto M, Fukuhira Y, Kaneko H, Hirata H. A new nerve coaptation technique using a biodegradable honeycombpatterned film. Microsurgery 2012;32:466–474. 27. Siemionow M, Uygur S, Ozturk C, Siemionow K. Techniques and materials for enhancement of peripheral nerve regeneration: A literature review. Microsurgery 2013;33:318–328. 28. Acar M, Karacalar A, Ayyildiz M, Unal B, Canan S, Agar E, Kaplan S. The effect of autogenous vein grafts on nerve repair with size discrepancy in rats: An electrophysiological and stereological analysis. Brain Res 2008;1198:171–181.
