tubular repair of the median or ulnar nerve in the human

TUBULAR REPAIR OF THE MEDIAN OR ULNAR NERVE IN
THE HUMAN FOREARM: A 5-YEAR FOLLOW-UP
!
!
G. LUNDBORG, B. ROSEN,
L. DAHLIN, J. HOLMBERG and I. ROSEN
From the Department of Hand Surgery, University Hospital MAS, Malmo,
. Sweden, and the Department of Clinical Neurophysiology,
Lund University, Sweden
The long-term outcome from silicone tube nerve repair was compared with the outcome from
routine microsurgical repair in a clinical randomized prospective study, comprising 30 patients with
median or ulnar nerve injuries in the distal forearm. Postoperatively, the patients underwent
neurophysiological and clinical assessments of sensory and motor function regularly over a 5-year
period. After 5 years there was no significant difference in outcome between the two techniques
except that cold intolerance was significantly less severe with the tubular technique. In the total
group there was ongoing improvement of functional sensibility throughout the 5 years after repair.
It is concluded that tubular repair of the median and ulnar nerves is at least as good as routine
microsurgical repair, and results in less cold intolerance.
Journal of Hand Surgery (British and European Volume, 2004) 29B: 2: 100–107
Keywords: nerve repair, outcome, tubes, silicone
We have used this technique for repair of human
median and ulnar nerves at the wrist and forearm level
(Lundborg et al., 1991, 1994). A clinical prospective
randomised study was initiated in 1991 with the aim of
comparing the outcome from tubular repair with
conventional microsurgical repair. At 3 months postoperatively the tubular technique showed a statistically
significant superior initial axonal outgrowth, but at 1year follow-up we could not find any differences
between the two techniques in terms of sensory and
motor recovery (Lundborg et al., 1997). Recently, we
showed that in seven cases treated with the silicone tube
there was, at reexploration due to local discomfort, a
new nerve structure between the severed nerve ends.
Furthermore, microscopic examination of the capsule
surrounding the silicone tube showed no, or only a
single patchy area of, inflammation (Dahlin et al., 2001).
We present the 5-year follow-up of the median or ulnar
nerve injured patients treated with tubular repair or
microsurgical repair and the time course of their
functional recovery over this period.
INTRODUCTION
There has been increasing interest in tubular repair of
peripheral nerves over the two last decades. Repair with
silicone tubes was first described 20 years ago as a useful
experimental tool for studying the biological mechanisms involved in nerve regeneration (Lundborg et al.,
1982b). This model has since been utilized in a number
of laboratories (Doolabh et al., 1996; Fields et al., 1989;
Lundborg, 2000) and it has been found that tissue fluid
accumulating in the tube contains several important
growth factors, such as NGF and CNTF, indicating
local synthesis of these factors in the damaged nerve
tissue (Danielsen et al., 1993; Danielsen and Varon,
1995; Longo et al., 1983a, b, 1984). The gap between the
two nerve ends inside such a tube is rapidly bridged by a
fibrin matrix which is invaded by macrophages, fibroblasts, Schwann cells, regenerating axons and capillaries
(Dahlin et al., 1995; Danielsen et al., 1993; Lundborg
et al., 1982b; Williams, 1987; Zhao et al., 1993). Within
weeks the nerve reconstructs itself within the tube
provided the gap does not exceed a critical length
(Lundborg et al., 1982a).
Over the years various tube models, such as vascular
structures, and different types of bio-resorbable tube
materials, e.g. collagen and polyglactic acid have been
used in experimental studies (Ansselin et al., 1997; Chiu
et al., 1988; Krarup et al., 2002; Molander et al., 1982;
Mosahebi et al., 2002; Rodriguez et al., 2000). The
effects of introducing varying types of gels, growth
factors and cells have also been analysed. However, only
silicone (Lundborg et al., 1991, 1994, 1997) and
polyglactic acid tubes (Weber et al., 2000) have been
used systematically in clinical practice to repair median
or ulnar nerves and digital nerves, respectively.
PATIENTS AND METHODS
The study was approved by the Ethical Committee at
Lund University. Thirty patients with a fresh and
complete clean-cut transection of the median or ulnar
nerve at wrist or distal forearm level (less than 10 cm
from the wrist) were included after they had consented
to participate. Patients with nerve injuries at more than
one level or combined nerve injuries were excluded.
Communication problems due to language or severe
psychiatric problems were also an exclusion criteria. The
100
SILICONE TUBE NERVE REPAIR
101
patients were randomized to either tubular repair or
conventional microsurgical repair, and surgery was
performed in all cases within 48 hours. Randomization
was performed with sealed envelopes. All analyses of
data were carried out on an intent-to-treat basis, and
there were no deviations from random allocation. The
examiner was blinded during the first follow-up year. In
eight cases a secondary surgical procedure was carried
out at a later stage to remove the tube because of slight
local discomfort (Dahlin et al., 2001). For description of
the study group see Table 1.
Surgical procedure
The tubular repair technique has been described in
previous reports (Lundborg et al., 1994, 1997). A 2 to
3 cm length of silicone tube with a diameter that
exceeded the nerve diameter by about 30% was used.
The nerve ends were carefully pulled into the tube and
towards each other, avoiding any rotation of the nerve
ends. The ends were fixed to the wall of the silicone tube
under slight tension with two single monofilament
polyamid epineural 9-0 or 6-0 stitches in each segment
close to the cut ends. A gap of 3 to 5 mm was
intentionally left between the nerve ends and the space
was filled with saline. In the nerve suture group the
nerve ends were approximated and sutured with single
9-0 sutures (Ethilons) placed in the epineurium. Special
attention was paid to the motor branch which, if
possible, was sutured separately. The wrist was immobilized in a semiflexed position for 3 weeks and in a
neutral position for another 3 weeks. Antibiotics were
given when appropriate based on the nature of the
injury.
Sensory re-education
Sensory re-education, with a well-established and
routine programme was commenced when touch could
be perceived in the palm approximately 3 months after
repair (Dellon, 1981, 1997;Wynn-Parry and Salter,
1976).
Follow-up
The follow-up period was 5 years in 28 cases, with
clinical assessments at 3, 6, 12, 24, 36, 48 and 60 months.
In two cases the initial assessment was performed at 6
months, and two other cases dropped out after 24
months because of other severe injuries or disease (Table
1). Seventeen patients underwent a neurophysiological
examination, 14 with a needle technique and three with
surface electrodes.
Assessments
Clinical examination
The recovery was initially classified according to the
British Medical Research Council (MRC) modified by
MacKinnon and Dellon (MacKinnon and Dellon,
1988). In addition the ‘‘Model Instrument for Outcome
after Nerve Repair’’ was used to quantify and express
the outcome in a more comprehensive way (Rose! n and
Lundborg, 2000, 2001). This recently introduced diagnosis-specific outcome instrument has good reliability
and validity and is based on a selection of assessment
instruments that reflect the recovery of three key
domains of specific interest after nerve injury. The three
domains are: sensory including assessment with Semmes
Weinstein monofilaments (ASHT, 1992), s2PD (ASHT,
1992), STI-test i.e. shape–texture identification test
(Rose! n and Lundborg, 1998) and three selected tasks
of the Sollerman hand function test (ASHT, 1992);
motor including assessment with manual muscle testing
(Brandsma et al., 1995), grip strength (ASHT, 1992),
and; pain/discomfort including the patient’s subjective
assessments of cold intolerance and hyperaesthesia on a
graded scale (Table 2). With this model the raw data are
Table 1—Description of the study group and the follow-up
Study group
Patients (n)
Men/women (n)
Age (years): mean (range)
Dominant hand injured
Injured tendons
Injured vessels
Additional complicating injury (ligament injury)
30
26/4
33(12–72)
14
28
19
1
Follow-up
Blind assessment
n
3-month follow-up
6-month follow-up
12-month follow-up
24-month follow-up
36/48-month follow-up
60-month follow-upn
Tubular repair
Conventional repair
17
13/4
32(12–72)
9
15
10
1
13
13/0
33(15–64)
5
13
9
Median (n)
Ulnar (n)
Median (n)
Ulnar (n)
6
7
7
7
6
6
10
10
10
10
10
10
6
6
6
5
5
5
6
7
7
6
6
7
Fourteen of the patients completed the neurophysiological examination with both the needle and surface electrodes techniques. An additional
three patients were assessed only with surface electrodes.
102
THE JOURNAL OF HAND SURGERY VOL. 29B No. 2 APRIL
2004
Table 2—Results at 5-year follow-up after nerve repair using either the tubular or the conventional repair technique for median or ulnar nerves in the
human forearm
Sensory
Innervation (SWM)
Tactile gnosis (s2PD)
Tactile gnosis (STI-test)
Dexterity (Sollerman test; task 4,8,10)
Motor
Innervation (Manual muscle test: median nerve: palmar
abduction of thumb: ulnar nerve: ab-adduction little
finger and abduction index finger)
Grip/strength (Jamar dynamometer)
Pain/
discomfort
Cold intolerance (none/minor, moderate, disturbing or
hinders function)
Hyperaesthesia (none/minor, moderate, disturbing or
hinders function)
Total score
Tubular repair
Conventional repair
0.57 (0.47–0.66)
0.80 (0.60–0.93)
0 (0–0.17)
0.50 (0.33–0.67)
0.88 (0.75–1)
0.52 (0.37–0.66)
0.80 (0.60–0.93)
0 (0–0.33)
0.33 (0.08–0.50)
0.80 (0.58–1)
0.73 (0.71–0.91)
0.53 (0.53–0.90)
0.87 (0.76–0.94)
0.8 (0.53–1)
0.90 (0.85–0.98)
0.92 (0.75–1)
0.95 (0.89–1)
0.67 (0.33–0.83)
0.83 (0.67–1)n
0.50 (0.33–0.67)
1.0 (0.83–1)
0.83 (0.5–1)
2.2 (2.2–2.5)
2.1 (1.7–2.3)
The scoring is according to the ‘‘Model for Documentation of Outcome after Nerve Repair’’, with transformed raw data (Ros!en and Lundborg,
2000, 2001). Median and interquartile-range are noted from each separate test (score 0–1), each domain (sensory, motor, pain/discomfort) (score
0–1), and the total score which is the summary of the three domains (score 0–3).
n
Significant difference (P=0.01).
transformed to a 0 to 1 scale by dividing the obtained
result by the ‘‘normal result’’. The results are presented
for each assessment (score 0–1), the mean score for each
domain is calculated (score 0–1), and a total score is
calculated which is the summary of the three domains
(score 0–3) (Rose! n and Lundborg, 2000) (Table 2).
Based on this model data have already been published
that illustrate the typical outcome after a median or
ulnar nerve repair in adults (Rose! n and Lundborg,
2001).
Neurophysiological examination
Motor and sensory nerve conduction studies were
performed with surface and needle techniques using
Nicolet VikingTM equipment. The peripheral hand
temperature was monitored and not allowed to fall
below 301C.
*
*
*
Motor conduction was examined with the active
recording surface electrode over the abductor pollicis
brevis or abductor digiti minimi muscle and with
stimulation of the respective nerve at the wrist and
elbow.
A needle electrode was placed close to the nerve
proximal to the site of injury and used for near nerve
stimulation. The distal motor latency was determined
by recording from the target muscle with a concentric
EMG needle electrode. The EMG electrode was used
for determination of spontaneous denervation activity, MUP-recording and estimation of the amount of
maximal voluntary activity.
Sensory conduction was examined with surface
electrodes placed over the median and ulnar nerves
*
2 cm proximal to the wrist crease and stimulation of
thumb, index and long finger (median nerve lesions)
or the little finger (ulnar nerve lesions) with pairs of
ring electrodes.
The near nerve needle electrode was used for
recording sensory nerve responses evoked by finger
stimulation (20 mA, 0.3 ms duration, average of 50
stimulation responses).
Analysis of data
The Mann–Whitney U-test was used for comparison of
the two surgical technique groups. For investigation of
longitudinal recovery in the whole study group the
Wilcoxon signed rank test, using the regression coefficient for each individual between 3 and 24 months and
24 and 60 months, respectively.
RESULTS
Early clinical results
The early results, at 12 months follow up, of 18 of the 30
patients included in this study have already been
published (Lundborg et al., 1997). No difference
between the two techniques was demonstrated at this
time, except that cutaneous touch/pressure thresholds
were significantly better at the 3-month follow–up for
the tubular repair technique. These results were confirmed after analysis of the data for 28 of the 30 patients
(P=0.03).
SILICONE TUBE NERVE REPAIR
103
Outcome after five years
Results from the clinical tests and the neurophysiological examination are presented in Tables 2, 3, 4.
With exception for cold intolerance, there were no
statistical significant differences in clinical (Tables 2 and
3) or neurophysiological (Table 4) outcomes of the two
techniques after 5 years. Cold intolerance was significantly less prominent (P=0.01) after the tubular repair
technique (Fig 1, Table 2), but was equally frequent in
patients with median and ulnar nerve repairs.
documented reliability and validity. It is however a fairly
new test and could only be applied throughout the
whole follow-up period in 13 of the 30 patients. The
patients’ perceived problems from cold intolerance and
Development over time
We have previously reported significant clinical improvements over time for at least 4 years after the repair
using the ‘‘Model Instrument for Outcome after Nerve
Repair’’ (Rose! n and Lundborg, 2000). Clinical assessment of tactile gnosis in this study demonstrated an
ongoing improvement during the 5-year follow-up (3–24
months P=0.03; 24–60 months P=0.05 (Fig 3). The test
instrument chosen for assessment of tactile gnosis was
the STI-test (Rose! n and Lundborg, 1998) which has
Fig 1
Box plot illustrating the perceived problems from cold
intolerance at 5-year follow-up. Patients who underwent a
tubular repair had significantly (P=0.01) less troublesome
cold intolerance.Note: Each box encloses 50% of the data
with the median value displayed as a line. The top and bottom
of the box mark the upper and lower quartile. The lines
extending from the top and bottom of each box mark the 90th
and the 10th percentile. Any value outside this range, (outlier)
is displayed as an individual point.
Table 3—MRC-classification, (Mackinnon, Dellon, 1988) at 5-year follow-up
S0
S1
S1+
S2
S2+
S3
S3+
S4
Conventional
repair (n)
Tubular repair (n)
–
–
–
–
–
3
3
3
–
5
2
5
3
3
0
1
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 superficial pain and some touch sensibility
As in S2 but with overresponse
s2PD over 15 mm, m2PD over7 mm. Recovery of pain and
touch sensibility with disappearance of overresponse
s2PD 7 to 15 mm, m2PD 4 to 7 mm.As in S3 but good
localization of the stimulus and imperfect recovery of two-point
discrimination
s2PD 2 to 6 mm, m2PD 2 to 3 mm. Complete recovery
Table 4—Results of the neurophysiological examination at 5 years
Sensory function
n
Conduction velocity (m/s)
Needle
n
Median/ulnar
Surface
n
Median/ulnar
Motor function
n
Amplitude (mV)
+
Latency
(ms)
Amplitude+ (mV)
Tube
Suture
Tube
Suture
Tube
Suture
Tube
Suture
39(35–41)
10
4/6
38(6–40)
12
5/7
43(40–46)
4
2/2
40(0–43)
5
2/3
1.5(1–3)
10
4/6)
1.5(0.5–2.9)
12
5/7
1.9(1.2–2)
4
2/2
0.7(0–2)
5
2/3
5.2(4.5–6)
10
4/6)
4.5(3.6–5.4)
12
5/7
4.2(3.7–4.8)
4
2/2
4.1(3.7–4.4)
5
2/3
4.9(2.7–7)
12
5/7
5.9(4.4–6.6)
5
2/3
Comparison between silicon tube and conventional nerve repair showed no significant differences; median (interquartile range).
n
Recording from median nerve with needle (index finger) or surface (middle finger) recordings respectively, or the little finger (ulnar nerve). The
recordings from median and ulnar nerve injuries are combined.
+
Recording from the abductor pollicis brevis muscle (median nerve) or the abductor digiti minimi muscle.The recordings from median and ulnar
nerve injuries are combined.
104
hyperaesthesia did not decrease significantly during the
follow-up time.
The neurophysiological examinations in the total
group showed an ongoing recovery over the 5-year
period. The improvement of motor (distal motor
latency) and sensory (conduction velocity and amplitude) functions was significant during the first 24
months (P=0.0001). During the following 36 months
the improvement in motor function (distal motor
latency) was statistically significant (P=0.008), but
sensory function did not improve significantly over this
period (Fig 2).
THE JOURNAL OF HAND SURGERY VOL. 29B No. 2 APRIL
2004
DISCUSSION
Our results show that the clinical and neurophysiological results of conventional microsurgical repair of
median and ulnar nerves at the wrist and forearm level
are not significant different from those of tubular repair,
in which a short gap is intentionally left between the
nerve ends. As the study was designed as a prospective
randomized trial with very strict inclusion criteria, the
number of patients recruited is limited, which might
have influenced our results and caused a Type II
statistical error. One clinical study which also used
Fig 2 The results from neurophysiological examination (needle) during the 5 years. The calculations were based on the regression coefficient for
each individual recovery between 3 and 24 months as well as 60 months. A P value o0.05 was considered significant. The number of
patients completing the neurophysiological examination decreased with time (3 months: n=27; 6 months: n=24; 12 months: n=23; 24
months: n=21; 36 months: n=13; 48 months: n=16; 60 months: n=14). See note to Fig 1 for explanatory of data presentation.
SILICONE TUBE NERVE REPAIR
105
Fig 3 The longitudinal recovery of tactile gnosis (STI-test, raw data score 0–6) in 13 patients was calculated based on the regression coefficients
for each individual between 3 and 24 and 24 and 60 months. A P-value o0.05 was considered significant. See note to Fig 1 for explanatory
of data presentation.
silicone tubes, for reconstruction of human major nerves
demonstrated varying results when longer distances
were left between the nerve ends (Braga-Silva, 1999).
Our results are not surprising in view of those of a large
number of experimental studies (see Doolabh et al.,
1996; Fields et al., 1989 for review), which indicate that
encasing the repair site in a silicone tube results in
accumulation of growth factors, formation of a longitudinally oriented fibrin matrix containing macrophages, migration of Schwann cells, rapid ingrowth of
axons and neovascularization of the newly formed nerve
trunk. The concept is also valid in humans (Dahlin et al.,
2001; Lundborg, 1999; Lundborg et al., 1994) and the
silicone tube constitutes a ‘‘biological chamber’’ in
which chemical and cellular events associated with nerve
regeneration can take place undisturbed. The advancement and growth direction of regenerating axons is
regulated by delicate molecular mechanisms which
influence the migration of Schwann cells and the
motility and advancement of growth cones at the tip
of advancing sprouts (Fu and Gordon, 1997). The
surgeon, no matter how sophisticated his/her surgical
technique, can only adapt the outer sheaths of the nerve:
the epineurium or perineurium. In this respect the
tubular repair concept represents a biological approach
to the biological battlefield taking place between the
severed nerve ends.
Silicone is a biologically inert material which has
been used in hand surgery for arthroplasty and twostage tendon grafting procedures. We used silicone tubes
with an inner diameter which exceeded the nerve
diameter by about 30% to allow for swelling of the
nerve ends. The tubes were removed because of slight
local problems in eight of our cases and we found that
they were surrounded by a smooth membrane which
showed no microscopic or macroscopic signs of
inflammation (Dahlin et al., 2001). Furthermore, there
were no signs of compression of the nerve trunk as has
been claimed to occur when small silicone tubes or
membranes have been used in humans (Merle et al.,
1989).
A puzzling finding in our study was that the patients
with silicone tubes suffered significantly less cold
intolerance. Cold intolerance is a common problem
after hand injuries (Craigen et al., 1999) and can be one
of the most disabling persisting symptoms after injury
(Collins et al., 1996; Irwin et al., 1997; Rose! n, 1996). The
pathogenesis of cold intolerance is still not well understood (Campbell and Kay, 1998) but may be attributable to a hyperirritability of nerve fibres normally
involved in temperature perception. Alternatively it may
be due to disorientation of such fibres or other nerve
components resulting in a distorted central nervous
response to stimuli which normally induce a physiological response. It might also be partially or entirely due
to impaired vasoregulation in response to odd stimuli
caused by the imperfect nerve representation. Whatever
the cause, tubular repair may offer a physiological
environment at the repair site which has a positive
influence on fibre orientation as well as maturation of
nerve fibres during and after the regeneration process.
Hyperaesthesia, another disturbing symptom for the
patient, also did not improve over time and occurred
irrespective of repair technique.
An interesting observation in the neurophysiologic
examinations was the constant ongoing improvement of
sensory and motor function over the whole 5-year
period. This is in line with a previous longitudinal study
with a 4-year follow-up, which included a limited
number of the patients in this study, which demonstrated significant improvement in clinical motor function for up to 4 years after nerve repair (Rose! n and
Lundborg, 2001). This finding could be interpreted as
demonstrating ongoing maturation of sensory and
motor axons. The sensory function, as assessed by the
clinical tests, showed an ongoing functional recovery
over the 5-years follow-up. Such an improvement may
reflect the importance of central nervous factors, such as
a continuous relearning based on cortical re-organizational processes which continues long after the reestablishment of peripheral connections. A large amount of
axonal misdirection occurs during re-innervation of the
106
hand, resulting in a functional re-organization of the
hand representation in somatosensory brain cortex
(Wall et al., 1986). Adaptation to this new cortical hand
map requires a sensory re-learning process, in many
ways analogous to acquisition of a second language
(Lundborg and Rosen, 2001). Such a re-learning may go
on for a long time and can be influenced by a number of
factors such as functional use of the hand, environmental factors and also the specific cognitive capacities
of the patient (Rose! n et al., 1994).
In conclusion, we used tubular repair with silicone
tubes in this clinical setting as an alternative to
conventional repair. Occasionally the tubes required
removal due to slight local discomfort. Ideally, a tube
used for nerve repair should be biodegradable and
should not cause any local discomfort or any inflammatory reaction during its degradation. However, there
may be a risk that the resorptive process itself may
induce a closed tissue response. Moreover, silicone is a
very inert material which induces no, or only a minor,
inflammatory response (Dahlin et al., 2001). Silicone
tubes have been widely used in animal experiments and
at the start of the study there were no appropriate
alternatives (Dahlin and Lundborg, 2001). At present
there is, in our view, no convincing evidence to
encourage the use of silicone tubes instead of primary
suture for the repair of fresh clean-cut nerve injuries, but
our findings may favour tube repair in the future when
appropriate bioresorbable materials are available.
Acknowledgements
Supported by grants from the Swedish Research Council, Swedish Brain
Foundation, Faculty of Medicine, Lund University.
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Received: 7 March 2003
Accepted after revision: 22 September 2003
.
Goran
Lundborg, Department of Hand Surgery, University Hospital MAS, SE-205 02
. Sweden. Tel.: +46-40-331721; fax: +46-40-928855;
Malmo,
E-mail: [email protected]
r 2004 The British Society for Surgery of the Hand. Published by Elsevier Ltd. All rights
reserved.
doi:10.1016/j.jhsb.2003.09.018 available online at http://www.sciencedirect.com