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Recovery of sympathetic skin responses after digit-to-digit replantation and toe-to-digit transplantation in humans.

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Uglt-toNai-Shin Chu, MD
Sympathetic skin response was utilized to study recovery of sudomotor function in 8 patients who had digit-to-digit
replantation and 9 patients who had toe-to-digit transplantation. Sympathetic skin responses evoked by median nerve
stimulation or magnetic stimulation of the neck were recorded from the tip of the replanted digits or transplanted toes.
The contralateral normal fingers served as controls. The mean intervals between surgery and study were 33 and 37
months, respectively, for digit replantation and toe transplantation. In normal subjects, the sympathetic skin responses
recorded from the fingertip were abolished by local anesthesia or cooling of the finger, while those recorded from the
palm were not affected. Ischemia of the finger only transiently affected the digit sympathetic skin responses. These data
indicate that the digit responses were locally generated and mediated by unmyelinated fibers. After digit replantation,
the palm and digit sympathetic skin responses were not different between replanted and normal sides. After toe transplantation, palm sympathetic skin responses were normal, but digit ones had prolonged latency and reduced amplitude.
The present findings suggest that recovery of sympathetic sudomotor activity can be nearly complete in digit replantation
but less satisfactory in toe transplantation.
Chu N-S. Recovery of sympathetic skin responses after digit-to-digit replantation
and toe-to-digit transplantation in humans. Ann Neurol 1996;40:67-74
Recent advances in microsurgical techniques have
greatly improved the results of nerve repair in injured
hands and fingers [I]. An immediate digit-to-digit replantation is performed when there is a sharply cut
amputation whereas a delayed toe-to-digit transplantation is performed when there is a crushing or lacerating
multiple digit amputation [2]. In these two types of
nerve repair, anomalous innervation and crossover innervation are avoided. Therefore, digit replantation
and toe transplantation provide excellent models for
the study of nerve regeneration and functional recovery.
Recently, colleagues and I [3, 41 studied nerve regeneration following digit replantation and toe transplantation by conventional nerve conduction and somatosensotry evoked potentials, which evaluate the
function of large myelinated nerves. However, sensory
testing of transplanted toes revealed that the recovery
of small nerve fiber functions such as pinprick and
temperature sensations is as satisfactory as that of large
nerve fiber functions such as touch and vibration [ 3 ] .
These findings suggest that regeneration of unmyelin-
ated fibers may be as satisfactory as that of large myelinated fibers.
Current knowledge of unmyelinated nerve regeneration is still inadequate, particularly in humans. In animal studies, regeneration of unmyelinated fibers seems
as rapid and vigorous as that of large myelinated fibers
[5-81. O n the contrary, regeneration of unmyelinated
fibers in humans is controversial. The rate of regeneration has been variously reported to be slow or as rapid
as that of motor or sensory fibers [9-121. Onne observed a nearly complete recovery of the sudomotor
activity of the sweat glands following median or ulnar
nerve repair [13].
Inadequate study of unmyelinated nerve regeneration in humans is likely due to lack of suitable models
and suitable methods. This study has taken advantage
of the fact that the sympathetic skin response (SSR)
evoked by activation of sympathetic unniyeiinated efferents can be recorded from almost any skin surface
of the body [14, 151. A method of recording SSRs
from the tip of the replanted digits and transplanted
toes is described. This method allowed evaluation of
From the Department of Neurology, Chang Gung Medical College
and Memorial Hospital, Taipei, Taiwan.
Address correspondence to Dr Chu, Department of Neurology,
Chang Gung Memorial Hospital, 139 Tung-Hwa N Road, Taipei,
Received Dec 6, 1995, and in revised form Jan 31, 1396. Accepted
for publication Feb 1, 1996.
Copyright 0 1996 by the American Neurological Association
Table I . Clinical Data of 8 Patients with Digit-to-Digit Replantation and 9 Patients with Toe-to-Digit Transplantation
A. Digit replantation
B. Toe transplantation
Digit Replanted
or Transplanted
Time from
Injury to Surgery
Time from
Surgery to Study
5 hr
5 hr
35 mo
8 hr
8 hr
32 mo
36 mo
6 hr
39 mo
7 ht
5 hr
9 hr
35 mo
31 mo
32 mo
13 mo
32 mo
4 mo
4 mo
9 mo
60 mo
66 mo
31 mo
36 mo
R- I
L- I +R-I
13 mo
right; L
= left
the recovery of unmyelinated nerve function following
digital nerve repair in humans.
Materials and Methods
Clinical data on 8 patients who had digit-to-digit replantation and 9 patients who had toe-to-digit transplantation are
summarized in Table 1. Digit replantation was performed
within several hours (mean, 7 5 2 hours) and toe transplantation, in 7 days to 17 months (mean, 9 f 5 months)
after injury. The interval between surgery and study was 33
2 2 months for digit replantation and 37 2 17 months for
toe transplantation. These intervals were sufficiently long for
the final stage of regeneration to be reached [ 161. The majority of the patients who had toe transplantation sustained
hand injuries on the job and usually had multiple digits mutilated. The patients who had digit replantation sustained
injuries on the job or at home, and had a single digit amputated. The reconstructive surgery consisted of end-to-end
nerve suture, anasromosis of arteries and veins, and reattachment of tendons [2].
All patients had nerve conduction and somatosensory
evoked potential studies performed previously. None of them
had evidence of neuropathies or carpal tunnel syndrome. In
addition, none were taking sedative or cardiovascular drugs
that might affect autonomic function. Patients with central
nervous system (CNS) disorders were also excluded. Patients
were asked about symptoms thought to be related to autonomic function or function of unmyelinated fibers. All sub-
68 Annals of Neurology Vol 40
No 1
July 1996
jects gave informed consent to the procedures, which were
approved by the hospital ethics committee.
Two methods of sympathetic activation were adopted: O n e
was electrical stimulation of the contralateral median nerve
at the wrist [15, 171, and another was magnetic stimulation
of the neck, presumably activating the sympathetic trunks
within the spinal cnnal [18, 191. Electrical stimulation consisted of constant current square pulses 5 to 1 5 mA in intensity and 0.2 msec in duration, delivered through an electromyographic (EMG) machine (Viking IIe, Nicolet, Madison,
WI). Magstim model 200 (Novametrix, United Kingdom)
was used to deliver magnetic pulse stimuli through a circular
coil stimulator in a 90-mm-diameter plate. The center of the
stimulator was placed over the seventh cervical spinous process or the first thoracic spinous process. The stimulus pulse
was 1 msec in duration. The stimulus intensity was expressed
as the percentage of the maximal output, which was 1.5 T
at the center of the coil and 1
25 mm below the center.
Counterclockwise current flow in the coil (A surface) was
used. T h e stimulus intensity was around 70% of the maximal
output. Auditory stimuli from the magnetic coil were excluded by placing ear plugs into the ears during the stimulation.
Recordings of SSRs were conducted with the patient in a
comfortable sitting position in the room with the ambient
temperature maintained at 22°C by thermostat. Palm SSRs
were recorded from disk electrodes placed on the volar and
dorsal surfaces of the hand, respectively, as active and reference sites. Digit SSRs were recorded from two electrodes
placed on the pulp and dorsal surface of the tip of the replanted digit or transplanted toe. The ground electrode was
situated in the forearm. Responses were amplified with a
bandpass between 0.01 and 3,000 Hz, with an analysis time
of 10 seconds. The latency of the SSR was the onset time
of the first deflection from the baseline, and the amplitude
was measured from the first deflection to the following deflection (peak to peak). Usually five responses were obtained
to calculate the mean value. The contralateral palm and corresponding finger served as controls. Because of some individual variations in response amplitude, simultaneous recordings of palm and digit SSRs from both sides were always
obtained. The skin temperature of the hands and fingers was
maintained at 32 to 34°C.
After the procedure was explained, the subject was encouraged to relax but remain awake. For electrical stimulation of
the median nerve, the stimulation was given unexpectedly at
random intervals of longer than 1 minute to avoid habituation. For magnetic stimulation of the neck, the stimulation
was given usually at an interval of approximately 1 minute.
Electric Stirn.
Magnetic Stirn.
( median n. )
J500 "V
1 set
Fig I . Representative recordings of palm and digit sympathetic
skin responses (SSRs) in a normal subject, evoked by electrical
stimulation of the median nerve and by magnetic stimulation
of the neck. The amplitudes of palm and digit SSRs from
magnetic stimulation were larger than those from electrical
Ischemic digit
Control Study of Digit Sympathetic Skin Responses
To ensure that the recorded digit SSR was generated locally
( L-11 )
A. Electric stirn.
at the tip of the digit, the following three conditions were
induced and studied in 5 normal subjects: (1) ischemia of
the finger produced by tightening a rubber band around the
base of the finger until the whole finger became numb, which
usually took about 20 to 30 minutes; (2) anesthesia of the
finger by local infiltration of 2% lidocaine solution at the
proximal end of the finger; and ( 3 ) cooling or warming of
the finger by dipping the finger into cold or warm water.
After the finger was dried quickly with a towel and the electrodes were reapplied, recording of SSRs was resumed. The
skin temperature of the finger was continuously monitored
by a polygraphic machine with a Biolab Computerized Physiological System (Autogenic Systems, Wood Dale, IL). Recording electrodes were attached to the side of the finger
between the distal and proximal interphalangeal joints.
The effects of the three conditions were usually studied
on the index finger. O n several occasions, SSRs were also
recorded from the neighboring finger, usually the middle
finger, during these procedures to ensure that the latter was
not affected.
Data Analysis
Because there might be large individual variations in SSR
amplitude, the amplitude measurement also included an amplitude ratio, which was obtained by dividing the SSR amplitude from the replanted digit or transplanted toe by the SSR
amplitude from the contralateral corresponding normal finger. Student's paired t test was used for statistical analysis.
Normal digit
( R-I1 )
0 rnin
1 rnin
6.Magnetic stirn.
o rnin
1 sec
Fig 2. Effect ofjnger ischemia on digit sympathetic skin
vesponse (SSR). Recordings were obtained from index Jingers
on both sides. Ischemia bad only a minimal transient effect
on digit SSRs.
Normal Palm and Digit Sympathetic Skin Responses
Figure 1 shows the normal palm and digit SSRs evoked
by electrical stimulation of the median nerve or by
magnetic stimulation of the neck. Both palm a n d digit
Chu: Sympathetic Skin Response after Digital Nerve Repair
Anesthetized digit
Normal digit
( R-It )
A. Electric stirn.
30 rnin
1 2 m V
v d i : l :
B. Anesthesia
B. Magnetic stirn.
10 min
A. Temperature
( L-ll )
Fzg 3. Effect offinger anesthesza on digit sympathetic skzn
response (SSR). Recordings of SSR were obtained from zndex
fingers bzlaterally. Dzgit SSRs were abolished by local anesthesia for approximately 30 minutes
SSRs were prominent and usually triphasic with an initial negative deflection. The palm and digit SSRs from
magnetic stimulation had a larger amplitude and a
smaller variation in amplitude and configuration than
did those from median nerve stimulation. The latency
of magnetically evoked SSRs was slightly shorter than
that from median nerve stimulation. The latency difference was approximately 100 to 200 msec. The amplitude of the palm SSR was larger than, usually twice,
that of the digit SSR. In 2 patients, the digit SSR was
equal to or slightly larger than the palm SSR. The latency difference between palm and digit SSRs was approximately 100 msec. These findings are in accordance with those of Matsunaga and coworkers [ 191.
Effects of Ischemiu, Anesthesiu, und Temperature
Ischemia had only a transient minimal effect on digit
SSRs evoked by median nerve stimulation or by magnetic stimulation (Fig 2). Digit SSRs were elicited by
magnetic stimulation immediately after relief of ischemia and by median nerve stimulation within 1 minute. Digit SSRs from magnetic stimulation showed full
recovery in 1 minute after relief of ischemia, while
those from median nerve stimulation showed recovery
within 15 minutes. Such an effect was not observed in
the digit SSRs recorded from the neighboring fingers.
Local anesthesia abolished digit SSRs from either
stimulation for almost 30 minutes (Fig 3). Full recov-
70 Annals of Neurology Vol 40
No 1 July 1996
Fig 4. (A) Effect o f temperature changes on palm and digit
sympathetic skin responses (SSRs). Cooling of the finger abolished digit SSRs while palm SSRs were not affected.
(B) Efect o f local anesthesia on neighboringJinger. Digit
SSRs were abolished in the anesthetized index finger, but
intact in tbe neighboring middle finger.
ery was usually not observed until 2 hours later. As in
ischemia, recovery was earlier for digit SSRs evoked by
magnetic stimulation. The effect of anesthesia was not
seen in the digit SSRs recorded from the neighboring
fingers (Fig 4 B ) .
Local cooling also abolished digit SSRs from either
stimulation (see Fig 4A).However, local warming had
no effect on digit SSRs, or only minimally increased
Tabte 2. Symptoms in 8 Replanted Digits and 9
Transplanted Toes
Hypersensitivity to
Hyposensitivity to
Decreased skin temperature
Diminished sweating
Increased sweating
Spontaneous pain
Keplanted Digit
Transplanted Toe
A. Electric stirn.
*\2&& -
11 mv
1Y C
Fig 5. Representative recordings of palm and digit sympathetic
skin responses (SSRs) j?om 2 patients with digit replantation
and toe transplantation, respectively. In toe transplantation,
digit SSRs showed a prolonged latency and reduced amplitude.
the amplitude of the digit SSR. As in ischemia and
anesthesia, digit SSRs recorded from the neighboring
fingers were not affected.
All three conditions had no effect on the palm SSRs
(see Fig 4A).
Sweating and Other Symptoms
Table 2 summarizes the data on sweating and other
symptoms thought to be related to the function of unmyelinated fibers or autonomic function. Some of
these symptoms are controversial with regard to the
pathophysiology observed in nerve regeneration [ 12,
20, 211. None of the patients had diminished sweating.
One patient after digit replantation and 2 patients after
toe transplantation had increased sweating during hot
weather. Hypersensitivity to cold or warm was more
common than hyposensitivity, but these symptoms
were mild. Slightly diminished skin temperature during
winter was fairly common. Spontaneous pain and hyperesthesia were rare and also mild.
Sympathetic Skin Responses in Replanted Digits
Representative recordings of palm and digit SSRs
evoked by median nerve stimulation or magnetic stimulation are shown in Figure 5. A summary of these
SSRs is presented in Table 3. Digit SSRs from replanted digits were elicited in all patients. The mean
latencies and amplitudes of palm and digit SSRs were
not different between normal and replanted sides. The
mean amplitude ratios were 1.0, indicating equal amplitudes between two sides for palm and digit SSRs.
Sympathetic Skin Responses in Transplanted Toes
Palm and digit SSRs from the transplanted side are
shown in Figure 5 and summarized in Table 3. In palm
SSRs, the latency and amplitude were not different between normal and transplanted sides, although the
mean latency tended to be longer and the mean amplitude smaller on the transplanted side.
Digit SSRs from the transplanted side were also elicited in all patients. However, the mean latency and
amplitude of the digit SSRs from the transplanted side
were significantly prolonged and reduced, respectively,
when compared to normal side. The mean amplitude
ratio was 0.5 for both digit SSRs evoked either by median nerve stimulation or by magnetic stimulation of
the neck. These mean amplitude ratios were statistically
significant, indicating a significant amplitude reduction
of the digit SSRs recorded from transplanted toes.
The present study demonstrated that the finger pulp
is a suitable site for recording SSRs. The digit SSRs
were prominent and easily evoked by median nerve
stimulation or by magnetic stimulation of the sympathetic trunk. In addition, the finger pulp has abundant
sweat glands, which have been studied previously in
the recovery of sudomotor activity following nerve repair [lo, 11, 131. The present study further demonstrated that the digit SSRs were not a volume-conducted potential from the palm, and exhibited the
same responses to ischemia, anesthesia, and temperature changes as did the sympathetic units in the skin
nerves in intraneural micrographic recordings [22-241.
In this study, the replanted digits showed a nearly
complete recovery of sympathetic sudomotor function,
whether centrally mediated or by direct activation of
the nerves. The present data are in agreement with the
findings by Onne [13] on the sudomotor activity of
the finger pulp in 28 cases of median or ulnar nerve
repair with a mean follow-up of 4 to 5 years. The
majority of the patients had sweating indexes within
normal limits, although they seemed to have a tendency for hypohidrosis [ 131. There was no case of anhidrosis [13]. The present and Onne’s findings suggest
that recovery of sudomotor activity following nerve repair is satisfactory in general. Whether such conclusion
can be extended to the function of other unmyelinated
nerves such as nociceptive afferents remains to be investigated.
The recovery of sudomotor function of the transplanted toes was still satisfactory but not as satisfactory
as that of the replanted digits. The digit SSRs were
elicited in all patients, but had prolonged latency and
reduced amplitude. The less satisfactory recovery after
toe transplantation was not clear, but probably due to
more severe and extensive tissue damage, delay in nerve
repair, retrograde degeneration of the median nerve,
mismatch between recipient and donor nerves, and
mismatch of receptor density between the recipient
finger and transplanted toe [3, 4, 12, 25, 261.
Studies on the regeneration of unmyelinated nerves
in humans are relatively few. Onne’s study [ 131 on the
recovery of sudomotor activity, by counting the number of active sweat glands in the fingertip, showed a
Chu: Sympathetic Skin Response after Digital Nerve Repair 71
Table 3. Sympathetic Skin Responses Evoked by Median Nerve Stimulation and Magnetic Stimuhtion of the Neck in 8 Patients
with Digit Replantation and 9 Patients with Toe Transplantationa
Digit Replantation
A. Electrical stimulation
B. Magnetic stimulation
1.5 i 0.1
1.5 -C 0.1
Toe Transplantation
1.7 -C 1.0
1.6 -C 0.9
1.0 -C 0.5
1.4 t 0.1
1.5 -C 0.1
2.4 i 1.4
2.0 i- 2.0
0.9 -C 0.4
1.7 i 0.2
1.6 +- 0.1
0.8 -C 0.5
0.9 i 1.0
1.0 i 0.4
1.5 i 0.2
1.7 +- 0.2"
0.9 -C 0.8
0.3 -C
0.5 i 0.3'
1.3 i 0.1
1.4 i 0.2
2.9 -C 1.2
2.9 -C 1.3
1.0 i 0.2
1.3 i 0.0
1.4 i 0.1
3.8 -C 3.5
3.3 i 3.4
0.9 2 0.2
1.4 -C 0.1
1.5 ? 0.1
0.8 i 0.4
0.8 i 0.4
1.0 i 0.5
1.4 t 0.1
1.6 -+ 0 . l b
1.6 ? 1.5
0.8 ? 0.9"
0.5 -C 0.3'
'Values are means ? standard deviations
hp < 0.05 compared to normal side.
' p < 0.01 compared to normal side.
satisfactory recovery. Using cutaneous piloerection as a
marker, Gutrnann and colleagues [9] found a regenerating rate of 1.2 mm/day for sympathetic unmyelinated fibers, a value close to the rates of 1 to 3 mm/
day for motor or sensory nerve fibers [12]. After digit
replantation, the calculated regeneration rates for touch
and pain were 0.47 mm/day and 0.44 mm/day, respectively [I 11. Other studies on nerve regeneration showed
that pain is usually the first sensation to return [16,
26, 271. These data suggest that regeneration rates for
myelinated and unmyelinated nerves are probably similar.
The reasons for satisfactory recoveiy of sympathetic
unmyelinated fibers remain unclear. Hallin and Torebjork [28, 231 demonstrated that afferent and sympathetic C-units can be distinguished in cutaneous
nerves. Afferent C-units are activated from defined receptive areas in the skin, whereas reflex responses in
sympathetic C-units can be elicited by various maneuvers that increase the attention [24, 28, 291. Hence,
stimuli applied anywhere on the body surface may induce sympathetic activity, and there are no specific receptive fields [24, 28, 291. Therefore, the outflow of
sympathetic impulses results in activation of large skin
areas of the body. The lack of specific receptive fields
in the skin for sympathetic efferents may account for
an earlier and probably more satisfactory reconection
with the end organs. O n the other hand, the recovery
of large myelinated fibers, which subserve discriminatory function and need more precise reconnection with
cutaneous receptors [ 2 5 ] , probably requires not only
72 Annals of Neurology Vol 40
No 1 July 1996
satisfactory peripheral regeneration but also certain
central reorganization [30-321. The latter contention
is in accordance with our previous and Onne's findings
that two-point discrimination has the worst recovery
following nerve repair [3, 131.
The pathophysiology of sympathetic nerve conduction abnormalities after toe transplantation is also not
clear. In animal studies [35, 361, nerve section with or
without suture results in a reduction of axon diameter,
particularly in the largest myelinated fibers, in the
proximal stump, even 300 days after injury. There is
a reduction in external fiber diameter and a lesser reduction in rnyelin sheath thickness [36]. Most nerves
recover normal conduction velocities by 200 days and
remain normal thereafter [36]. More recent studies in
cat showed that following permanent axotomy, axonal
atrophy is the prominent pathological feature of myelinated fibers of the proximal stump, which leads sequentially to myelin wrinkling, nodal lengthening, internodal dernyelination, and segmental remyelination
[37, 381. Fiber loss is minimal [38]. Whether unmyelinated nerves after transection without suture for
many months will develop permanent axonal atrophy
is not known.
In the present study, a decrease in sympathetic nerve
action potential amplitude might be indicative of a decrease in the number of nerve fibers, a reduction of
receptor density in the transplanted toe, or a combination of these conditions. An increase in the latency is
more difficult to interpret. Microneurographic study
showed that responses of human C-fibers to repeated
intradermal electrical stimulation are characterized by
an increase in latency or blocking of impulses [39].
Therefore, latency increase and blocking of impulse
conduction may conceivably occur in unmyelinated
nerve fibers that have less satisfactory regeneration, as
with toe transplantation.
Animal studies showed that central stumps of unmyelinated s o n s that have been interrupted by crushing
or cutting a nerve trunk have a strong regenerating
capacity. When the rat cervical sympathetic trunk was
crushed, numerous regenerating unmyelinated fibers
were obvious by 10 days, and the total number of unmyelinated fibers was even higher than normal by 57
to 104 days [7].Their conduction velocity is at first
half-normal, but reaches normal values by 30 to 40
days [6]. Following a crush of rabbit abdominal vagus
nerves, which are almost entirely unmyelinated, function eventually returns after a delay, which is probably
due to the lack of specific guiding channels in unmyelinated nerves [5, 401. After transection and repair of
the rabbit great auricular nerve, receptive properties of
C-fiber units approach the normal range within 5
months after transection [S]. Following crush lesions
of the rat peripheral nerves, initially the number of
unmyelinated axon sprouts is equal to the number of
myelinated fibers in the proximal nerve, but later the
number of unmyelinated axons is 18 to 60% higher
than normal [41]. During sciatic nerve regeneration
navigated by collagen grafts, both myelinated and unmyelinated fibers are equally prominent and eventually
form a functional connection between proximal and
distal stumps [42].These experimental findings suggest
that unmyelinated fibers are capable of making satisfactory peripheral reconnection.
In conclusion, the present study demonstrated that
SSRs recorded from the fingertip can be used to evaluate objectively the functional recovery of sympathetic
unmyelinated efferent fibers following digit reconstruction. The recovery of sudomotor activity was nearly
complete after digit replantation and also satisfactory
after toe transplantation. O u r present and previous
findings suggest that regeneration of unmyelinated fibers is at least as satisfactory as the regeneration of
myelinated fibers.
The author is deeply grateful to the staff, particularly D r F. C. Wei
of the Department of Plastic and Reconstructive Surgery for referral
of the patients. Appreciation is also extended to H. C. Chen for
technical assistance and to H . C. Chang for manuscript preparation.
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toe, recovery, response, digit, skin, replantation, sympathetic, human, transplantation
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