Vol. 17A, No. 1 January 1992
Electrodiagnosis of Martin-Gruber connection
of severe ulnar nerve lesions at the elbow. Electromyogr Clin Neurophysiol 1987;27:13-8. 14. Srinivasan R, Rhodes J. The median-ulnar anastomosis (Martin-Gruber) in normal and congenitally abnormal fetuses. Arch Neurol 1981;38:418-9. syndrome, 15. Spinner M. The anterior interosseous-nerve with special attention to its variations. J Bone Joint Surg 1970;52A:84-94. 16. Iyer V, Fenichel GM. Normal median nerve proximal latency in carnal tunnel syndrome: a clue to coexisting
Martin-Gruber anastomosis. J Neurol Neurosurg Psychiatry 1976;39:449-52. 17. Murphey F, Kirklin JW, Finlayson AI. Anomalous innervation of the intrinsic muscles of the hand. Surg Gynecol Obstet 1946;83:15-23. 18. Uncini A, Lange DJ, Lovelace RE. Anomalous intrinsic hand muscle innervation in median and ulnar nerve lesions: an electrophysiological study. Ital J Neurol Sci 1988;9:497-503.
Sensory recovery after median nerve grafting Fourteen patients were evaluated prospectively after median nerve grafts. Twelve male and two female patients with a mean age of 41 years were included. Mean time since surgery was 4 years. Detailed sensory evaluations were completed. Statistical evaluation analyzed relationships between object identification, sensory tests, and graft length. According to the S-O to S-4 grading system, 11 patients were considered to be S-3+ or greater. Recovery of moving two-point discrimination of 2 to 3 mm. was achieved by 50% of the patients. Strong correlations were found between object identification and static two-point discrimination, moving two-point discrimination, and graft length. Cutaneous pressure threshold and vibration threshold correlated weakly with object identification. (J HANDSURC 1992;17A:59-68.3
Christine B. Novak, BScKin,
BScPT, St. Louis, MO., Louise Kelly, BSc, OT(C), Toronto, Ontario, Canada, and Susan E. Mackinnon, MD, FRCS(C), FACS,
St. Louis, MO.
0
ptimal hand function depends on the integration of sensory input. Injury to the median nerve often compromises hand sensibility, resulting in a sig-
From the Department of Occupational Therapy, University of Toronto, Toronto, Ontario, Canada. and the Division of Plastic Surgery, Department of Surgery, Washington University School of Medicine,
St. Louis. MO.
Presented at the annual meeting of the American Society for Reconstructive Microsurgery, Toronto. Ontario. September 1990. Received for publication April 12. 1991.
Nov. 8. 1990; accepted
in revised form
No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Reprint requests: Susan E. Mackinnon, MD, Washington University School of Medicine, Division of Plastic Surgery, Suite 17424. One Barnes Hospital Plaza. St. Louis. MO 631 IO. 3/l/30611
nificant functional deficit for the patient. Sensibility after median nerve injury has not been consistently documented in the literature, and therefore assessment of functional recovery is hampered by the lack of a standardized means of reporting. This study reports sensibility in the hands of patients after median nerve graft at the mid-distal forearm level.
Material and methods Clinical data. Fourteen patients were evaluated prospectively at least 2 years after median nerve graft at the mid-distal forearm level. This patient group included 12 men and 2 women with a mean age of 41 years (range, 27 to 78 years). The mean time since injury was 8 years (range, 2 to 36 years). (The median nerve injury sustained 36 years previously was an unrecognized childhood injury.) The mechanisms of injury included ten lacerations, one puncture/laceration, one crush injury, one tumor, and one electrical bum. The
THE JOURNAL
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60
The Journal of HAND SURGERY
Novak et al.
Fig. 1. Object identification used in the assessment
7
Patients
assessment. The 15 large objects (right) and the 16 small objects (lefr) of object identification.
M
6
1 0
O-.9
l-l.9
2-2.9 Vibration
3-3.9 Threshold
Fig. 2. Distribution of vibratory thresholds.
4-4.9 (microns
5-5.9
6-6.9
7-7.9
6-6.9
of motion)
The mean vibratory thresholds of the thumb, the index finger, and the long finger are shown. Six patients had mean vibratory thresholds between 3 and 3.9. The normal median nerve thresholds of 0.7 km of motion, as identified by the distributors of Vibratron II, was exceeded by all patients.
Vol. 17A, No. 1 January 1992
Sensory recovery after median nerve grafting
Patients
61
(n)
7
6
0 STRESS
2.83 .091 8.62
3.81 .213 9.29
4.31 1.86 29.6
4.60 2.81 36.6
6.18 18.6 84.9
6.66
Fig. 3. Distribution of cutaneous pressure thresholds as measured by Semmes-Weinstein (S-W) monofilaments with corresponding measures of force and stress is shown.5 The graph represents the smallest cutaneous patient
pressure threshold
of the thumb and the index and long fingers of each
mean time since surgery was 4 years (range, 2 to 6 years). Patients with multiple nerve and tendon injuries were included, but those whose bony and tendon injuries precluded object manipulation were excluded. Surgical procedure. In all patients treatment consisted of microsurgical fascicular grafting of the median nerve. The mean number of inter-positional grafts used was 4.5. The mean length of the nerve graft was 6 cm (range, 1 cm to 12 cm). (The 1 cm graft was performed in a delayed surgical procedure after a suicide attempt. Because of the retraction of the nerve ends, a repair was not possible except with maximum wrist flexion; therefore a 1 cm interpositional nerve graft was carried out.) In all cases, the median nerve injury was complete at the time of surgery and the entire median nerve was grafted, although distally the recurrent motor branch of the median nerve was identified and excluded from the graft. The carpal tunnel was released in all cases at the time of the nerve graft. The donor site was the sural nerve in 11 patients and the medial antebrachial cutaneous nerve in the remaining 3 patients. Sensory reeducation. All patients went through formal sensory reeducation sessions, as outlined by DelIon,’ with an experienced hand therapist (L. K.). Earlyphase sensory reeducation was introduced when vibra-
tion of a 30 cps tuning fork and moving touch were perceived in the hand. The progression of localization of moving and constant touch was continued to the distal pulp of each digit. Late-phase sensory reeducation was instituted when good localization of stimulus was perceived at the digit pulp. Emphasis in the later phase was on discriminatory tasks to improve two-point discrimination and object identification. Patients were educated with respect to nerve injury and regeneration and were reevaluated at follow-up clinics throughout the postoperative period. Sensory evaluation. The final evaluation was completed in one session in a quiet testing environment by a hand therapist (C. N.) experienced in the testing procedures, and the results were recorded on standardized data-collection forms. The sensory evaluation included heavy moving and constant touch,’ light moving and constant touch,’ qualitative and quantitative vibration thresholds, moving two-point discrimination (m2pd),’ static two-point discrimination (s2pd), and cutaneous pressure thresholds in the distribution of the median nerve (thumb, index, and long finger). The ulnar nerve distribution of the small finger was used as a control. Functional evaluation included small-object identification and large-object identification.
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Patients
(n) S-3+
2-3
4-6
7-9
m
10-12
Mean s2pd
Static
Two-point
.
m
13-15
s-3
.
None
Best s2pd
Discrimination
(mm)
Fig. 4. Recovery of static two-point discrimination.
The graph represents mean s2pd of thumb, index finger, and long finger and best s2pd. According to a modification of Highet’s classification. a s2pd of < 6 mm is S-4, 7 to 15 mm is S-3 + , and greater than 15 mm is S-3.
Table I. Results of median nerve graft Sensory recovery (%) Reference
Gap grafed
No. cases
Bunnell and Boyes, 1939 Seddon, 1947 Brooks, 1955 Millesi et al., 1972, 1976 Walton and Finseth, 1977 Tallas et al., 1978 Young et al., 1980 Beazley et al., 1984
3-15 5-15 2 4-6
32 11 33 38 8 6 8 5
15-57 0.5-71
Novak et al., 1991
1-12
14
20-70
Age (Yr)
Adult 8-62 17-38
Follow-up (Yr) I-l.5 2-3 >5 5-11 1.5-2.5 1.5-2.5 1-5
s2
s2 +
s3
s3 +
10 21 3 13
18 0 0 0
45 69 60 12
0
37
38
18 0 34 63 33 25 0
s4 3 0 0 3 12 0
Average S2 2-10 21
Vibration thresholds were evaluated qualitatively with 30 cps and 256 cps tuning forks.‘,’ The prolonged ends of the tuning fork were applied longitudinally to the pulp of the subject’s digit. A comparison was then made between the stimulus perceived on that digit and that perceived on the ipsilateral digits as well as on the contralateral hand. This was recorded as increased (+ l), decreased (- l), or equal (0).
29
50
The quantification of the threshold of the quickly adapting fibers was measured with the Vibratron II instrument (Sensortek, Inc., Clifton, N.J.).3 This fixedfrequency (120 hertz) variable-amplitude instrument measured the vibration threshold on a relative scale from 1 to 20 units. The patient placed the pulp of one digit onto the vibrating portion of the instrument. The intensity was increased until a stimulus was perceived
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17A,
January
No.
1 Sensory
1992
and, through small incremental changes of intensity, the threshold amplitude was recorded. This procedure was repeated for each digit. Semmes-Weinstein monofilaments were used to evaluate cutaneous pressure thresholds.4. ’ M2pd and s2pd were evaluated with a Disk-Criminator testing device (The Disk-Criminator, Baltimore, Md . ) . 6.’ Global functional assessment was based on largeobject and small-object identification, pinch strength, grip strength, and subjective data. Object identification included objects not used previously in testing or sensory reeducation sessions and was completed with a glove on the hand, which allowed exposure of the lateral digits. The blindfolded subject was given an object and allowed a maximum of 30 seconds to identify it. This procedure was repeated for each of the 15 large objects and 16 small objects (Fig. 1) in random order. Lateral key pinch strength and grip strength were measured in kilograms with a standard pinch gauge and a Jamar dynamometer, respectively.’ Each subject was requested to rank pain, numbness, weakness, cold intolerance, and paresthesia from the most disturbing to the least disturbing, if applicable. Statistical analysis. Spearman rank correlation coefficients were used to investigate relationships between object identification and sensory tests and graft length.
recover?,
Table II. Classification Grade
after median nerve grafting
63
of sensory recovery
SZPD
MZPD
(mm)
(mm)
SO
-
-
Sl
-
-
s1+
-
-
s2
-
s2+
-
-
s3
>15
>I
s3+
7-15
4-7
s4
2-6
2-3
Recoveyv of sensibility No recovery of sensibility in the autonomous zone of the nerve Recovery of deep cutaneous pain sensibility in the autonomous zone of the nerve Recovery of superficial pain sensibility Recovery of supeficial pain and some touch sensibility As in S2, but with overresponse Recovery of pain and touch sensibility with disappearance of overresponse As in S3. but good localization of the stimulus and imnerfeet recovery of’ two-point discrimination Complete recovery
Results
SZPD = Static two-Point discrimination; MZPD = moving two-Point discrimination.
Subjective data. Cold intolerance was noted as a problem in 12 patients, and 4 patients ranked it as their primary complaint. Weakness was a primary complaint in four patients, numbness in three patients, and pain in two patients. None of those evaluated ranked paresthesia as a primary complaint. The dominant hand was involved in 8 of the 14 cases. Eight patients had injuries that were insured by the Worker’s Compensation Board, and one patient was compensated by insurance benefits. Twelve patients had returned to work at the time of evaluation, one patient had not returned to work, and one patient had retired for reasons unrelated to his injury. Touch sensibility. Accurate localization of moving touch was present in all digits in 12 of the 14 patients. Eight patients had accurate localization of constant touch to all median nerve innervated digits. Two patients lacked localization of heavy constant touch to the index and long finger. Four patients lacked localization of light constant touch to at least one digit. Two patients lacked localization of light moving touch to one digit. One patient lacked localization of heavy moving touch to three digits. Seven patients (50%) recovered percep-
tion of 256 cps vibratory stimulus at the fingertip before localization of light constant touch. The time required for the recovery of complete touch sensation ranged from 3 to 9 months. Vibration threshold. One patient qualitatively noted equal vibratory stimulus in all digits with the 256 cps tuning fork and the 30 cps tuning fork. Three patients noted either hyposensitivity or hypersensitivity in all median nerve-innervated digits with both the 256 cps tuning fork and the 30 cps tuning fork. The other 11 patients noted either hyposensitivity or hypersensitivity in at least one median nerve-innervated digit with both the 256 cps and the 30 cps tuning fork. The distribution of the vibratory thresholds of the first three digits is shown in Fig. 2. Cutaneous pressure thresholds. The smallest cutaneous pressure threshold from the first three digits was taken for each patient; these ranged from 2.83 to 5.18. The distribution of these cutaneous pressure thresholds is shown in Fig. 3. Two-point discrimination. The distribution of s2pd is shown in Fig. 4. The smallest measured s2pd was
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Novak et al.
Patients
(n)
4-7
2-3
10-12
8-9
m
Mean m2pd
Moving Two-point
13-15
None
Best m2pd Discrimination
(mm)
Fig. 5. Recovery of moving two-point discrimination
(m2pd). The mean m2pd of the thumb and the index and long fingers and the best m2pd are shown. Using the modification” of Highet’s classification, we have assigned an m2pd of 2 to 3 mm to S-4, 4 to 7 mm to S-3 + , and greater than 7 mm to S-3.
Static
Two-Doint
OL
0
Fig. 6. Relationship
Discrimination
(mm)
I
I
5 Moving
between crimination (s2pd). The mean were correlated with use of (r = 0.92, p < 0.0001) was
Two-point
10 Discrimination
15 (mm)
20
moving two-point discrimination (m2pd) and static two-point dism2pd and the mean s2pd of the thumb and the index and long fingers the Spearman rank correlation coefficient; a strong relationship identified between m2pd and s2pd.
Vol. 17A, No. 1 January 1992
Sensory recovery after median nerve grafting
65
Objects (n)
r
0
5
10
15
n
0.77
20
Moving Two-point Discrimination (mm) Fig. 7. Relationship between total number of objects (large and small) identified and mean m2pd of thumb and index and long fingers. With Spearman rank correlation coefficient, r = 0.77 (p -=I0.005).
noted in the thumb in six patients, in the index finger in two patients, and in the long finger in three patients. Three patients had no s2pd in either the thumb, the index finger, or the long finger. One patient had the same s2pd in all median nerve-innervated digits measured. A modification of Highet’s classification,’ which classifies sensory recovery based on s2pd, has been traditionally used to report sensibility results. Grade S-4 was recovered in 50% of the patients, grade S-3+ in 29%, and grade S-3 in the remaining 21%. Table I facilitates comparison with other reported results. The classification of sensory recovery was modified by Mackinnon and Dellon” to include m2pd (Table II). In our series of patients, 50% achieved a m2pd grade of S-4, 14% were Grade S-3 + , and the remaining 36% were grade S-3. The distribution of m2pd is shown in Fig. 5. The smallest m2pd was noted in the thumb in five patients, the index finger in one patient, and the long finger in two patients. Three patients had equal m2pd in both the thumb and the index finger, and two patients had equal m2pd in all median nerveinnervated digits. Two patients had no m2pd in the distribution of the median nerve (thumb, index finger, or long finger). A correlation coefficient of 0.92 (p < 0.0001) was found between m2pd and s2pd (Fig. 6).
Object identification. A strong relationship was found between total object identification (large and small) and mean m2pd (Fig. 7) and mean s2pd (Fig. 8). The relationship between number of small objects identified and mean m2pd was r = 0.73 (p < 0.003). When the relationship between smallest m2pd of the first three digits and number of small objects identified was examined, the correlation coefficient dropped to r = 0.55 (p < 0.042). The relationship of number of small objects identified and mean s2pd was r = 0.71 (p < 0.004). Assessment of correlational relationships between graft length and object identification revealed r = 0.66 (p < 0.020) with large objects and r = 0.74 (p < 0.006) with small objects. Weak correlational relationships were found between object identification and cutaneous pressure thresholds (r = 0.55, p < 0.038) and vibratory thresholds (r = 0.59, p < 0.025). Strength. With dominant hand involvement, the grip strength was less than that of the nondominant hand in six patients, and in two cases the dominant grip strength exceeded the nondominant hand by 2 kg. The mean percentage difference between dominant and nondominant grip strength was 60% with dominant hand involvement and 73% with nondominant hand involvement .
66
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Objects
(n)
2s
20
5 Static Two-point
10 Discrimination
16 (mm)
Fig. 8. Relationship between total number of objects (large and small) identified and mean s2pd
of thumb and index and long fingers. With Spearman rank correlation coefficient, r = 0.77 (p -=Z0.005).
Key pinch strength was diminished, as compared with that of the nondominant hand, in 12 patients and equal to that of the noninvolved hand in two cases. The mean percentage difference between dominant and nondominant key pinch was 57% with dominant hand involvement and 54% with nondominant hand involvement. Discussion Historically, poor functional results are to be expected after median nerve graft (Table I).” In previously reported results,“-‘* a grade S-3 or less was achieved by more than 60% of the patients. Therefore the majority of these patients still had limited discriminatory ability and a poor result based on s2pd. 0nne19 demonstrated that adult s2pd does not return to normal values after median nerve repair. Therefore if s2pd is used as the only outcome measure of sensory recovery, then the results will be less than acceptable, on the basis of normal values of 6 mm or less, without regard to the patient’s functional status. Studies by Wynn-Parry and SalterZOand Dellon et al.” demonstrated that good hand function can occur after median nerve repair despite abnormal s2pd. Walton and Finseth’* reported grade S-3 + or S-4 in 75% of their patients after median nerve graft. Our study supports these findings and reports good hand sensibility as measured by two-point dis-
crimination and object identification in persons who have had median nerve grafts. Several factors may have contributed to these favorable results. Consideration must be given to the advancement of microsurgical fascicular nerve grafting and its importance to the functional end result. The return of limited sensory components, however, does not ensure a good functional result, and initially there may be sensory confusion because of the misdirection of regenerating axons external to their original endoneurial tubes and resultant reinnervation of different sensory end organs. Sensory reeducation allows the patient to relearn and correctly interpret the sensory stimuli that are being discharged. The literature’s lo*23-25suggests that sensory reeducation is important in maximizing sensory recovery after nerve regeneration. Recent experimental studies have demonstrated cortical plasticity in adult primates26-29after nerve injury and repair and the production of projection neurons in normal adult avians,30 giving an experimental basis for these rehabilitation techniques. Sensory reeducation was included in the rehabilitation program of our patients, which may have contributed to the good functional results. Return to the work force is a good indication of overall recovery, and in this group of patients 86% went back to work. A retrospective review of the charts revealed a pattern
Vol. 17A. No. 1
January 1992
of recovery of touch sensation similar to that described by Dellon. ’ Perception of 30 cps vibratory stimulus was followed by localization of heavy moving touch, then heavy constant touch; localization of light moving touch recovered more slowly. After the initial return of touch perception, complete touch sensation was present within 3 to 9 months in those patients who regained all components of light and heavy touch perception. Despite the recovery of good function as measured by employment status, object identification, and grip strength, subjective recovery remains less than optimum. Subjective complaints range from painful, disabling cold intolerance to slight weakness and numbness. Previous studies”, ” have reported a relationship between cold intolerance and vascularity and sensory recovery, suggesting that cold intolerance decreases with the return of good sensibility. Glickman and Mackinnon3’ also noted cold intolerance as a consistent residual problem after digital replantation, citing this as a limiting factor in the recovery of good function. Our results suggested that cold intolerance remained a consistent subjective complaint despite the recovery of good two-point discrimination. This problem, which is often underestimated, is now being ,more widely recognized, offering the opportunity for further investigation. Correlational analysis revealed a strong relationship between two-point discrimination and object identification. As illustrated by Dellon and Kallman,‘4 m2pd is a good predictor of object identification. Our series illustrated a strong correlation between m2pd and s2pd, suggesting a relationship in the return of innervation density of the quickly and slowly adapting fibers. S2pd measures the innervation density of the slowly adapting fibers, which is important in maintaining grasp and static pressure on an object. Therefore persons with poor s2pd will be unable to maintain static grasp of an object and, with vision occluded, will drop the object. In this study, when allowed 30 seconds to identify each object, persons with poor s2pd had ample time to replace the object in the hand if it was dropped and thus identify it in the allotted time. We have not differentiated time as a factor in identification of the object; perhaps if recognition time had been recorded, correlational differences between s2pd and m2pd might have been identified. Our results also suggest a relationship between functional hand sensibility and nerve graft length. Those persons with shorter nerve grafts achieved a better functional result, which may be attributed to a shorter distance between the level of the injury and the sensory receptors. An m2pd of 2 to 3 mm in at least one digit was achieved by 50% of the patients in this series. With the
Sensory recovery after median nerve grafting
67
exception of one who had poor motor recovery, all of these patients achieved good object identification. Therefore in persons with good thumb opposition, perhaps only one digit with good two-point discrimination may be needed for good object identification. Improvements in microsurgical technique have allowed improvement in functional recovery after nerve repair, and sensory reeducation” in the postoperative period facilitates recovery of sensibility. Functional results after median nerve repair and graft continue to provide the impetus for improvement in surgical and rehabilitation techniques. We thank Mr. M. Katie, Department of Biostatistics and Research Design, Sunnybrook Health Science Centre, Toronto, Ontario, for his assistance Mrs. G. Burke for her assistance
with the data analysis and in this study.
REFERENCES 1. Dellon AL. Evaluation of sensibility and re-education of sensation in the hand. Baltimore: Williams & Wilkins, 1981. 2. Dellon AL. Clinical use of vibratory stimuli to evaluate peripheral nerve injury and compression neuropathy. Plast Reconstr Surg 1980;65:466-76. 3. Dellon AL. The vibrometer. Plast Reconstr Surg 1983;7 1:427-3 1. 4. Bell-Krotoski J, Tomancik E. The repeatability of testing with Semmes-Weinstein monofilaments. J HAND SURG 1987:12A:155-61. 5. Levin S. Pearsall G, Ruderman RJ. Von Frey’s method of measuring pressure sensibility in the hand: an engineering analysis of the Weinstein-Semmes pressure aesthiometer. J HAND SURG 1978;3:21 l-6. 6. Dellon AL, Mackinnon SE, Crosby PM. Reliability of two-point discrimination measurements. J HAND SURG 1987;12A:693-6. 7. Dellon AL. The moving two-point discrimination test: clinical evaluation of the quickly adapting fiber/receptor system. J HAND SURG 1978;3:474-8 I. 8. Mackinnon SE. Dellon AL. Two-point discrimination tester. J HAND SURG 1985;lOA:906-7. 9. Mathiowetz V, Weber K, Volland G, Kashman N. Reliability and validity of grip and pinch strength evaluations. J HAND SURG 1984;9A:222-6. 10. Mackinnon SE, Dellon AL. Surgery of the peripheral nerve. New York: Thime. 1988. 11. Bunnell S, Boyes JH. Nerve grafts. Am J Surg 1939;44:64-75. 12. Seddon HJ. The use of autogenous grafts for repair of large gaps in peripheral nerves. Br J Surg 1947:35:15167. 13. Brooks D. The place of nerve grafting in orthopedic surgery. J Bone Joint Surg 1955:37A:299-326, 14. Millesi H. Meissl G. Berger A. The interfascicular nerve grafting of the median and ulnar nerves. J Bone Joint Surg 1972:54A:727-50,
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15. Millesi H, Meissl G, Berger A. Further experience with interfascicular grafting of the median, ulnar and radial nerves. J Bone Joint Surg 1976;58A:209-18. 16. Tallas R, Staniforth P, Fisher TR. Neurophysiological studies of autogenous nerve grafts. J Neurol Neurosurg Psychiatry 1978;41:677-83. 17. Young VL, Wray CR, Weeks PM. The results of nerve grafting in the wrist and hand. Ann Plast Surg 1980;5:212-5. 18. Beazley RW, Milek MA, Reiss BH. Results of nerve grafting in severe soft tissue injuries. Clin Orthop 1984;188:208-12. 19. Onne L. Recovery of sensibility and sudomotor activity in the hand after nerve suture. Acta Chir Stand (Suppl) 1962;300:1-70. 20. Wynn-Parry CB, Salter M. Sensory re-education after median nerve lesions. Hand 1976;8:250-7. 21. Dellon AL, Curtis RM, Edgerton MT. Reeducation of sensation in the hand after nerve injury and repair. Plast Reconstr Surg 1974;53:297-305. 22. Walton R, Finseth F. Nerve grafting in the repair of complicated peripheral nerve trauma. J Trauma 1977;17:793-6. 23. Dellon AL, Jabaley ME. Reeducation of sensation in the hand following nerve suture. Clin Orthop 1982; 163:75-9. 24. Wynn-Parry CB. Peripheral nerve injuries: sensation. J Bone Joint Surg 1986:68B:15-9. 25. Brand PW. Rehabilitation of the hand with motor and sensory impairment. Orthop Clin North Am 1973; 4: 1135-9.
The Journal of HAND SURGERY
26. Merzenich MM. Alteration in cortical map following preferential digital stimulation in the adult monkey (Abstr). Neuroscience 1984;10:34. 27. Jenkins WM, Merzenich MM. Reorganization of neocortical representations after brain surgery. Brain Res 1987;71:249-66. 28. Wall JT, Kaas JH, Sur M, Nelson RJ, Fellernan DJ, Merzenich MM. Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans. J Neurosci 1986;6:218-33. 29. Wall JT, Kaas JH. Long-term cortical consequences of reinnervation errors after nerve regeneration in monkeys. Brain Res 1986;372:400-4. 30. Alvarez-Buylla A, Kim JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 1990;249 (4975): 1444-6. 31. Gelberman RH, Urbaniak JR, Bright DS, Levin LS. Digital sensibility following replantation. J HAND SURG 1978;3:313-9. 32. Koman LA, Nunley JA. Thermoregulatory control after upper extremity replantation. J HAND SURG 1986; 1 lA:548-52. 33. Glickman LT, Mackinnon SE. Sensory recovery following digital replantation. Microsurgery 1990; 11:236-42. 34. Dellon AL, Kallman CH. Evaluation of functional sensation in the hand. J HAND SURC 1983;8:865-70. 35. Imai H, Tajima T, Natsumi Y. Successful reeducation of functional sensibiIity after median nerve repair at the wrist. J HAND SURG 1991;16A:60-5.
Electrodiagnosis of Martin-Gruber connection
of severe ulnar nerve lesions at the elbow. Electromyogr Clin Neurophysiol 1987;27:13-8. 14. Srinivasan R, Rhodes J. The median-ulnar anastomosis (Martin-Gruber) in normal and congenitally abnormal fetuses. Arch Neurol 1981;38:418-9. syndrome, 15. Spinner M. The anterior interosseous-nerve with special attention to its variations. J Bone Joint Surg 1970;52A:84-94. 16. Iyer V, Fenichel GM. Normal median nerve proximal latency in carnal tunnel syndrome: a clue to coexisting
Martin-Gruber anastomosis. J Neurol Neurosurg Psychiatry 1976;39:449-52. 17. Murphey F, Kirklin JW, Finlayson AI. Anomalous innervation of the intrinsic muscles of the hand. Surg Gynecol Obstet 1946;83:15-23. 18. Uncini A, Lange DJ, Lovelace RE. Anomalous intrinsic hand muscle innervation in median and ulnar nerve lesions: an electrophysiological study. Ital J Neurol Sci 1988;9:497-503.
Sensory recovery after median nerve grafting Fourteen patients were evaluated prospectively after median nerve grafts. Twelve male and two female patients with a mean age of 41 years were included. Mean time since surgery was 4 years. Detailed sensory evaluations were completed. Statistical evaluation analyzed relationships between object identification, sensory tests, and graft length. According to the S-O to S-4 grading system, 11 patients were considered to be S-3+ or greater. Recovery of moving two-point discrimination of 2 to 3 mm. was achieved by 50% of the patients. Strong correlations were found between object identification and static two-point discrimination, moving two-point discrimination, and graft length. Cutaneous pressure threshold and vibration threshold correlated weakly with object identification. (J HANDSURC 1992;17A:59-68.3
Christine B. Novak, BScKin,
BScPT, St. Louis, MO., Louise Kelly, BSc, OT(C), Toronto, Ontario, Canada, and Susan E. Mackinnon, MD, FRCS(C), FACS,
St. Louis, MO.
0
ptimal hand function depends on the integration of sensory input. Injury to the median nerve often compromises hand sensibility, resulting in a sig-
From the Department of Occupational Therapy, University of Toronto, Toronto, Ontario, Canada. and the Division of Plastic Surgery, Department of Surgery, Washington University School of Medicine,
St. Louis. MO.
Presented at the annual meeting of the American Society for Reconstructive Microsurgery, Toronto. Ontario. September 1990. Received for publication April 12. 1991.
Nov. 8. 1990; accepted
in revised form
No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Reprint requests: Susan E. Mackinnon, MD, Washington University School of Medicine, Division of Plastic Surgery, Suite 17424. One Barnes Hospital Plaza. St. Louis. MO 631 IO. 3/l/30611
nificant functional deficit for the patient. Sensibility after median nerve injury has not been consistently documented in the literature, and therefore assessment of functional recovery is hampered by the lack of a standardized means of reporting. This study reports sensibility in the hands of patients after median nerve graft at the mid-distal forearm level.
Material and methods Clinical data. Fourteen patients were evaluated prospectively at least 2 years after median nerve graft at the mid-distal forearm level. This patient group included 12 men and 2 women with a mean age of 41 years (range, 27 to 78 years). The mean time since injury was 8 years (range, 2 to 36 years). (The median nerve injury sustained 36 years previously was an unrecognized childhood injury.) The mechanisms of injury included ten lacerations, one puncture/laceration, one crush injury, one tumor, and one electrical bum. The
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Fig. 1. Object identification used in the assessment
7
Patients
assessment. The 15 large objects (right) and the 16 small objects (lefr) of object identification.
M
6
1 0
O-.9
l-l.9
2-2.9 Vibration
3-3.9 Threshold
Fig. 2. Distribution of vibratory thresholds.
4-4.9 (microns
5-5.9
6-6.9
7-7.9
6-6.9
of motion)
The mean vibratory thresholds of the thumb, the index finger, and the long finger are shown. Six patients had mean vibratory thresholds between 3 and 3.9. The normal median nerve thresholds of 0.7 km of motion, as identified by the distributors of Vibratron II, was exceeded by all patients.
Vol. 17A, No. 1 January 1992
Sensory recovery after median nerve grafting
Patients
61
(n)
7
6
0 STRESS
2.83 .091 8.62
3.81 .213 9.29
4.31 1.86 29.6
4.60 2.81 36.6
6.18 18.6 84.9
6.66
Fig. 3. Distribution of cutaneous pressure thresholds as measured by Semmes-Weinstein (S-W) monofilaments with corresponding measures of force and stress is shown.5 The graph represents the smallest cutaneous patient
pressure threshold
of the thumb and the index and long fingers of each
mean time since surgery was 4 years (range, 2 to 6 years). Patients with multiple nerve and tendon injuries were included, but those whose bony and tendon injuries precluded object manipulation were excluded. Surgical procedure. In all patients treatment consisted of microsurgical fascicular grafting of the median nerve. The mean number of inter-positional grafts used was 4.5. The mean length of the nerve graft was 6 cm (range, 1 cm to 12 cm). (The 1 cm graft was performed in a delayed surgical procedure after a suicide attempt. Because of the retraction of the nerve ends, a repair was not possible except with maximum wrist flexion; therefore a 1 cm interpositional nerve graft was carried out.) In all cases, the median nerve injury was complete at the time of surgery and the entire median nerve was grafted, although distally the recurrent motor branch of the median nerve was identified and excluded from the graft. The carpal tunnel was released in all cases at the time of the nerve graft. The donor site was the sural nerve in 11 patients and the medial antebrachial cutaneous nerve in the remaining 3 patients. Sensory reeducation. All patients went through formal sensory reeducation sessions, as outlined by DelIon,’ with an experienced hand therapist (L. K.). Earlyphase sensory reeducation was introduced when vibra-
tion of a 30 cps tuning fork and moving touch were perceived in the hand. The progression of localization of moving and constant touch was continued to the distal pulp of each digit. Late-phase sensory reeducation was instituted when good localization of stimulus was perceived at the digit pulp. Emphasis in the later phase was on discriminatory tasks to improve two-point discrimination and object identification. Patients were educated with respect to nerve injury and regeneration and were reevaluated at follow-up clinics throughout the postoperative period. Sensory evaluation. The final evaluation was completed in one session in a quiet testing environment by a hand therapist (C. N.) experienced in the testing procedures, and the results were recorded on standardized data-collection forms. The sensory evaluation included heavy moving and constant touch,’ light moving and constant touch,’ qualitative and quantitative vibration thresholds, moving two-point discrimination (m2pd),’ static two-point discrimination (s2pd), and cutaneous pressure thresholds in the distribution of the median nerve (thumb, index, and long finger). The ulnar nerve distribution of the small finger was used as a control. Functional evaluation included small-object identification and large-object identification.
62
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Novak et al.
Patients
(n) S-3+
2-3
4-6
7-9
m
10-12
Mean s2pd
Static
Two-point
.
m
13-15
s-3
.
None
Best s2pd
Discrimination
(mm)
Fig. 4. Recovery of static two-point discrimination.
The graph represents mean s2pd of thumb, index finger, and long finger and best s2pd. According to a modification of Highet’s classification. a s2pd of < 6 mm is S-4, 7 to 15 mm is S-3 + , and greater than 15 mm is S-3.
Table I. Results of median nerve graft Sensory recovery (%) Reference
Gap grafed
No. cases
Bunnell and Boyes, 1939 Seddon, 1947 Brooks, 1955 Millesi et al., 1972, 1976 Walton and Finseth, 1977 Tallas et al., 1978 Young et al., 1980 Beazley et al., 1984
3-15 5-15 2 4-6
32 11 33 38 8 6 8 5
15-57 0.5-71
Novak et al., 1991
1-12
14
20-70
Age (Yr)
Adult 8-62 17-38
Follow-up (Yr) I-l.5 2-3 >5 5-11 1.5-2.5 1.5-2.5 1-5
s2
s2 +
s3
s3 +
10 21 3 13
18 0 0 0
45 69 60 12
0
37
38
18 0 34 63 33 25 0
s4 3 0 0 3 12 0
Average S2 2-10 21
Vibration thresholds were evaluated qualitatively with 30 cps and 256 cps tuning forks.‘,’ The prolonged ends of the tuning fork were applied longitudinally to the pulp of the subject’s digit. A comparison was then made between the stimulus perceived on that digit and that perceived on the ipsilateral digits as well as on the contralateral hand. This was recorded as increased (+ l), decreased (- l), or equal (0).
29
50
The quantification of the threshold of the quickly adapting fibers was measured with the Vibratron II instrument (Sensortek, Inc., Clifton, N.J.).3 This fixedfrequency (120 hertz) variable-amplitude instrument measured the vibration threshold on a relative scale from 1 to 20 units. The patient placed the pulp of one digit onto the vibrating portion of the instrument. The intensity was increased until a stimulus was perceived
Vol.
17A,
January
No.
1 Sensory
1992
and, through small incremental changes of intensity, the threshold amplitude was recorded. This procedure was repeated for each digit. Semmes-Weinstein monofilaments were used to evaluate cutaneous pressure thresholds.4. ’ M2pd and s2pd were evaluated with a Disk-Criminator testing device (The Disk-Criminator, Baltimore, Md . ) . 6.’ Global functional assessment was based on largeobject and small-object identification, pinch strength, grip strength, and subjective data. Object identification included objects not used previously in testing or sensory reeducation sessions and was completed with a glove on the hand, which allowed exposure of the lateral digits. The blindfolded subject was given an object and allowed a maximum of 30 seconds to identify it. This procedure was repeated for each of the 15 large objects and 16 small objects (Fig. 1) in random order. Lateral key pinch strength and grip strength were measured in kilograms with a standard pinch gauge and a Jamar dynamometer, respectively.’ Each subject was requested to rank pain, numbness, weakness, cold intolerance, and paresthesia from the most disturbing to the least disturbing, if applicable. Statistical analysis. Spearman rank correlation coefficients were used to investigate relationships between object identification and sensory tests and graft length.
recover?,
Table II. Classification Grade
after median nerve grafting
63
of sensory recovery
SZPD
MZPD
(mm)
(mm)
SO
-
-
Sl
-
-
s1+
-
-
s2
-
s2+
-
-
s3
>15
>I
s3+
7-15
4-7
s4
2-6
2-3
Recoveyv of sensibility No recovery of sensibility in the autonomous zone of the nerve Recovery of deep cutaneous pain sensibility in the autonomous zone of the nerve Recovery of superficial pain sensibility Recovery of supeficial pain and some touch sensibility As in S2, but with overresponse Recovery of pain and touch sensibility with disappearance of overresponse As in S3. but good localization of the stimulus and imnerfeet recovery of’ two-point discrimination Complete recovery
Results
SZPD = Static two-Point discrimination; MZPD = moving two-Point discrimination.
Subjective data. Cold intolerance was noted as a problem in 12 patients, and 4 patients ranked it as their primary complaint. Weakness was a primary complaint in four patients, numbness in three patients, and pain in two patients. None of those evaluated ranked paresthesia as a primary complaint. The dominant hand was involved in 8 of the 14 cases. Eight patients had injuries that were insured by the Worker’s Compensation Board, and one patient was compensated by insurance benefits. Twelve patients had returned to work at the time of evaluation, one patient had not returned to work, and one patient had retired for reasons unrelated to his injury. Touch sensibility. Accurate localization of moving touch was present in all digits in 12 of the 14 patients. Eight patients had accurate localization of constant touch to all median nerve innervated digits. Two patients lacked localization of heavy constant touch to the index and long finger. Four patients lacked localization of light constant touch to at least one digit. Two patients lacked localization of light moving touch to one digit. One patient lacked localization of heavy moving touch to three digits. Seven patients (50%) recovered percep-
tion of 256 cps vibratory stimulus at the fingertip before localization of light constant touch. The time required for the recovery of complete touch sensation ranged from 3 to 9 months. Vibration threshold. One patient qualitatively noted equal vibratory stimulus in all digits with the 256 cps tuning fork and the 30 cps tuning fork. Three patients noted either hyposensitivity or hypersensitivity in all median nerve-innervated digits with both the 256 cps tuning fork and the 30 cps tuning fork. The other 11 patients noted either hyposensitivity or hypersensitivity in at least one median nerve-innervated digit with both the 256 cps and the 30 cps tuning fork. The distribution of the vibratory thresholds of the first three digits is shown in Fig. 2. Cutaneous pressure thresholds. The smallest cutaneous pressure threshold from the first three digits was taken for each patient; these ranged from 2.83 to 5.18. The distribution of these cutaneous pressure thresholds is shown in Fig. 3. Two-point discrimination. The distribution of s2pd is shown in Fig. 4. The smallest measured s2pd was
64
The Journal of HAND SURGERY
Novak et al.
Patients
(n)
4-7
2-3
10-12
8-9
m
Mean m2pd
Moving Two-point
13-15
None
Best m2pd Discrimination
(mm)
Fig. 5. Recovery of moving two-point discrimination
(m2pd). The mean m2pd of the thumb and the index and long fingers and the best m2pd are shown. Using the modification” of Highet’s classification, we have assigned an m2pd of 2 to 3 mm to S-4, 4 to 7 mm to S-3 + , and greater than 7 mm to S-3.
Static
Two-Doint
OL
0
Fig. 6. Relationship
Discrimination
(mm)
I
I
5 Moving
between crimination (s2pd). The mean were correlated with use of (r = 0.92, p < 0.0001) was
Two-point
10 Discrimination
15 (mm)
20
moving two-point discrimination (m2pd) and static two-point dism2pd and the mean s2pd of the thumb and the index and long fingers the Spearman rank correlation coefficient; a strong relationship identified between m2pd and s2pd.
Vol. 17A, No. 1 January 1992
Sensory recovery after median nerve grafting
65
Objects (n)
r
0
5
10
15
n
0.77
20
Moving Two-point Discrimination (mm) Fig. 7. Relationship between total number of objects (large and small) identified and mean m2pd of thumb and index and long fingers. With Spearman rank correlation coefficient, r = 0.77 (p -=I0.005).
noted in the thumb in six patients, in the index finger in two patients, and in the long finger in three patients. Three patients had no s2pd in either the thumb, the index finger, or the long finger. One patient had the same s2pd in all median nerve-innervated digits measured. A modification of Highet’s classification,’ which classifies sensory recovery based on s2pd, has been traditionally used to report sensibility results. Grade S-4 was recovered in 50% of the patients, grade S-3+ in 29%, and grade S-3 in the remaining 21%. Table I facilitates comparison with other reported results. The classification of sensory recovery was modified by Mackinnon and Dellon” to include m2pd (Table II). In our series of patients, 50% achieved a m2pd grade of S-4, 14% were Grade S-3 + , and the remaining 36% were grade S-3. The distribution of m2pd is shown in Fig. 5. The smallest m2pd was noted in the thumb in five patients, the index finger in one patient, and the long finger in two patients. Three patients had equal m2pd in both the thumb and the index finger, and two patients had equal m2pd in all median nerveinnervated digits. Two patients had no m2pd in the distribution of the median nerve (thumb, index finger, or long finger). A correlation coefficient of 0.92 (p < 0.0001) was found between m2pd and s2pd (Fig. 6).
Object identification. A strong relationship was found between total object identification (large and small) and mean m2pd (Fig. 7) and mean s2pd (Fig. 8). The relationship between number of small objects identified and mean m2pd was r = 0.73 (p < 0.003). When the relationship between smallest m2pd of the first three digits and number of small objects identified was examined, the correlation coefficient dropped to r = 0.55 (p < 0.042). The relationship of number of small objects identified and mean s2pd was r = 0.71 (p < 0.004). Assessment of correlational relationships between graft length and object identification revealed r = 0.66 (p < 0.020) with large objects and r = 0.74 (p < 0.006) with small objects. Weak correlational relationships were found between object identification and cutaneous pressure thresholds (r = 0.55, p < 0.038) and vibratory thresholds (r = 0.59, p < 0.025). Strength. With dominant hand involvement, the grip strength was less than that of the nondominant hand in six patients, and in two cases the dominant grip strength exceeded the nondominant hand by 2 kg. The mean percentage difference between dominant and nondominant grip strength was 60% with dominant hand involvement and 73% with nondominant hand involvement .
66
The Jourlralof HAND SURGERY
Novak et al.
Objects
(n)
2s
20
5 Static Two-point
10 Discrimination
16 (mm)
Fig. 8. Relationship between total number of objects (large and small) identified and mean s2pd
of thumb and index and long fingers. With Spearman rank correlation coefficient, r = 0.77 (p -=Z0.005).
Key pinch strength was diminished, as compared with that of the nondominant hand, in 12 patients and equal to that of the noninvolved hand in two cases. The mean percentage difference between dominant and nondominant key pinch was 57% with dominant hand involvement and 54% with nondominant hand involvement. Discussion Historically, poor functional results are to be expected after median nerve graft (Table I).” In previously reported results,“-‘* a grade S-3 or less was achieved by more than 60% of the patients. Therefore the majority of these patients still had limited discriminatory ability and a poor result based on s2pd. 0nne19 demonstrated that adult s2pd does not return to normal values after median nerve repair. Therefore if s2pd is used as the only outcome measure of sensory recovery, then the results will be less than acceptable, on the basis of normal values of 6 mm or less, without regard to the patient’s functional status. Studies by Wynn-Parry and SalterZOand Dellon et al.” demonstrated that good hand function can occur after median nerve repair despite abnormal s2pd. Walton and Finseth’* reported grade S-3 + or S-4 in 75% of their patients after median nerve graft. Our study supports these findings and reports good hand sensibility as measured by two-point dis-
crimination and object identification in persons who have had median nerve grafts. Several factors may have contributed to these favorable results. Consideration must be given to the advancement of microsurgical fascicular nerve grafting and its importance to the functional end result. The return of limited sensory components, however, does not ensure a good functional result, and initially there may be sensory confusion because of the misdirection of regenerating axons external to their original endoneurial tubes and resultant reinnervation of different sensory end organs. Sensory reeducation allows the patient to relearn and correctly interpret the sensory stimuli that are being discharged. The literature’s lo*23-25suggests that sensory reeducation is important in maximizing sensory recovery after nerve regeneration. Recent experimental studies have demonstrated cortical plasticity in adult primates26-29after nerve injury and repair and the production of projection neurons in normal adult avians,30 giving an experimental basis for these rehabilitation techniques. Sensory reeducation was included in the rehabilitation program of our patients, which may have contributed to the good functional results. Return to the work force is a good indication of overall recovery, and in this group of patients 86% went back to work. A retrospective review of the charts revealed a pattern
Vol. 17A. No. 1
January 1992
of recovery of touch sensation similar to that described by Dellon. ’ Perception of 30 cps vibratory stimulus was followed by localization of heavy moving touch, then heavy constant touch; localization of light moving touch recovered more slowly. After the initial return of touch perception, complete touch sensation was present within 3 to 9 months in those patients who regained all components of light and heavy touch perception. Despite the recovery of good function as measured by employment status, object identification, and grip strength, subjective recovery remains less than optimum. Subjective complaints range from painful, disabling cold intolerance to slight weakness and numbness. Previous studies”, ” have reported a relationship between cold intolerance and vascularity and sensory recovery, suggesting that cold intolerance decreases with the return of good sensibility. Glickman and Mackinnon3’ also noted cold intolerance as a consistent residual problem after digital replantation, citing this as a limiting factor in the recovery of good function. Our results suggested that cold intolerance remained a consistent subjective complaint despite the recovery of good two-point discrimination. This problem, which is often underestimated, is now being ,more widely recognized, offering the opportunity for further investigation. Correlational analysis revealed a strong relationship between two-point discrimination and object identification. As illustrated by Dellon and Kallman,‘4 m2pd is a good predictor of object identification. Our series illustrated a strong correlation between m2pd and s2pd, suggesting a relationship in the return of innervation density of the quickly and slowly adapting fibers. S2pd measures the innervation density of the slowly adapting fibers, which is important in maintaining grasp and static pressure on an object. Therefore persons with poor s2pd will be unable to maintain static grasp of an object and, with vision occluded, will drop the object. In this study, when allowed 30 seconds to identify each object, persons with poor s2pd had ample time to replace the object in the hand if it was dropped and thus identify it in the allotted time. We have not differentiated time as a factor in identification of the object; perhaps if recognition time had been recorded, correlational differences between s2pd and m2pd might have been identified. Our results also suggest a relationship between functional hand sensibility and nerve graft length. Those persons with shorter nerve grafts achieved a better functional result, which may be attributed to a shorter distance between the level of the injury and the sensory receptors. An m2pd of 2 to 3 mm in at least one digit was achieved by 50% of the patients in this series. With the
Sensory recovery after median nerve grafting
67
exception of one who had poor motor recovery, all of these patients achieved good object identification. Therefore in persons with good thumb opposition, perhaps only one digit with good two-point discrimination may be needed for good object identification. Improvements in microsurgical technique have allowed improvement in functional recovery after nerve repair, and sensory reeducation” in the postoperative period facilitates recovery of sensibility. Functional results after median nerve repair and graft continue to provide the impetus for improvement in surgical and rehabilitation techniques. We thank Mr. M. Katie, Department of Biostatistics and Research Design, Sunnybrook Health Science Centre, Toronto, Ontario, for his assistance Mrs. G. Burke for her assistance
with the data analysis and in this study.
REFERENCES 1. Dellon AL. Evaluation of sensibility and re-education of sensation in the hand. Baltimore: Williams & Wilkins, 1981. 2. Dellon AL. Clinical use of vibratory stimuli to evaluate peripheral nerve injury and compression neuropathy. Plast Reconstr Surg 1980;65:466-76. 3. Dellon AL. The vibrometer. Plast Reconstr Surg 1983;7 1:427-3 1. 4. Bell-Krotoski J, Tomancik E. The repeatability of testing with Semmes-Weinstein monofilaments. J HAND SURG 1987:12A:155-61. 5. Levin S. Pearsall G, Ruderman RJ. Von Frey’s method of measuring pressure sensibility in the hand: an engineering analysis of the Weinstein-Semmes pressure aesthiometer. J HAND SURG 1978;3:21 l-6. 6. Dellon AL, Mackinnon SE, Crosby PM. Reliability of two-point discrimination measurements. J HAND SURG 1987;12A:693-6. 7. Dellon AL. The moving two-point discrimination test: clinical evaluation of the quickly adapting fiber/receptor system. J HAND SURG 1978;3:474-8 I. 8. Mackinnon SE. Dellon AL. Two-point discrimination tester. J HAND SURG 1985;lOA:906-7. 9. Mathiowetz V, Weber K, Volland G, Kashman N. Reliability and validity of grip and pinch strength evaluations. J HAND SURG 1984;9A:222-6. 10. Mackinnon SE, Dellon AL. Surgery of the peripheral nerve. New York: Thime. 1988. 11. Bunnell S, Boyes JH. Nerve grafts. Am J Surg 1939;44:64-75. 12. Seddon HJ. The use of autogenous grafts for repair of large gaps in peripheral nerves. Br J Surg 1947:35:15167. 13. Brooks D. The place of nerve grafting in orthopedic surgery. J Bone Joint Surg 1955:37A:299-326, 14. Millesi H. Meissl G. Berger A. The interfascicular nerve grafting of the median and ulnar nerves. J Bone Joint Surg 1972:54A:727-50,
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15. Millesi H, Meissl G, Berger A. Further experience with interfascicular grafting of the median, ulnar and radial nerves. J Bone Joint Surg 1976;58A:209-18. 16. Tallas R, Staniforth P, Fisher TR. Neurophysiological studies of autogenous nerve grafts. J Neurol Neurosurg Psychiatry 1978;41:677-83. 17. Young VL, Wray CR, Weeks PM. The results of nerve grafting in the wrist and hand. Ann Plast Surg 1980;5:212-5. 18. Beazley RW, Milek MA, Reiss BH. Results of nerve grafting in severe soft tissue injuries. Clin Orthop 1984;188:208-12. 19. Onne L. Recovery of sensibility and sudomotor activity in the hand after nerve suture. Acta Chir Stand (Suppl) 1962;300:1-70. 20. Wynn-Parry CB, Salter M. Sensory re-education after median nerve lesions. Hand 1976;8:250-7. 21. Dellon AL, Curtis RM, Edgerton MT. Reeducation of sensation in the hand after nerve injury and repair. Plast Reconstr Surg 1974;53:297-305. 22. Walton R, Finseth F. Nerve grafting in the repair of complicated peripheral nerve trauma. J Trauma 1977;17:793-6. 23. Dellon AL, Jabaley ME. Reeducation of sensation in the hand following nerve suture. Clin Orthop 1982; 163:75-9. 24. Wynn-Parry CB. Peripheral nerve injuries: sensation. J Bone Joint Surg 1986:68B:15-9. 25. Brand PW. Rehabilitation of the hand with motor and sensory impairment. Orthop Clin North Am 1973; 4: 1135-9.
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26. Merzenich MM. Alteration in cortical map following preferential digital stimulation in the adult monkey (Abstr). Neuroscience 1984;10:34. 27. Jenkins WM, Merzenich MM. Reorganization of neocortical representations after brain surgery. Brain Res 1987;71:249-66. 28. Wall JT, Kaas JH, Sur M, Nelson RJ, Fellernan DJ, Merzenich MM. Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans. J Neurosci 1986;6:218-33. 29. Wall JT, Kaas JH. Long-term cortical consequences of reinnervation errors after nerve regeneration in monkeys. Brain Res 1986;372:400-4. 30. Alvarez-Buylla A, Kim JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 1990;249 (4975): 1444-6. 31. Gelberman RH, Urbaniak JR, Bright DS, Levin LS. Digital sensibility following replantation. J HAND SURG 1978;3:313-9. 32. Koman LA, Nunley JA. Thermoregulatory control after upper extremity replantation. J HAND SURG 1986; 1 lA:548-52. 33. Glickman LT, Mackinnon SE. Sensory recovery following digital replantation. Microsurgery 1990; 11:236-42. 34. Dellon AL, Kallman CH. Evaluation of functional sensation in the hand. J HAND SURC 1983;8:865-70. 35. Imai H, Tajima T, Natsumi Y. Successful reeducation of functional sensibiIity after median nerve repair at the wrist. J HAND SURG 1991;16A:60-5.
