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Comparison between fascicular and whole sural nerve biopsy.

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Comparison between Fascicular
and Whole Sural Nerve Biopsy
Martin Pollock, FRACP," Hitoshi Nukada, MD,* Peter Taylor, MSc," Ivan Donaldson, M D , t
and Grant Carroll, M S c t
Sural nerve regeneration and sensation were evaluated in 16 subjects five or more years after fascicular or whole
nerve biopsy. Conduction studies demonstrated successful nerve regeneration in all subjects who had whole nerve
biopsy. Postbiopsy interrogation revealed no long-term pain or paresthesias but a high incidence of tactile-induced
dysesthesias. No significant difference was seen when areas of sural sensory loss were compared in fascicular and
whole nerve biopsy groups. We conclude that whole nerve biopsy should be recommended in preference to fascicular biopsy since it is simpler, has greater diagnostic potential, and allows for a more complete morphological
evaluation.
Pollock M, Nukada H, Taylor P, Donaldson I, Carroll G. Comparison between fascicular and wholc surd
nerve biopsy. Ann Neurol 13:65-68, 1983
Better understanding of the morphological changes
in peripheral neuropathy has brought forth increasing requests for nerve biopsy. This paper addresses
the question of the relative merits of fascicular versus
whole s u r d nerve biopsy.
An advantage of whole nerve biopsy is that
magnification is usually not required and the procedure is simpler and faster. Where multiple interfascicular bridges exist, a common occurrence in sural
nerve, whole nerve biopsy is also less painful. For the
morphologist, only this specimen provides the potential for a detailed and accurate analysis of whole
nerve morphometry and pathology. Where vasculitis
or amyloidosis is suspected, there is no alternative
to whole nerve biopsy [I].
T h e principal argument for fascicular biopsy in
contrast to whole nerve biopsy relates to residual
sensory deficit and long-term dysesthesias [91. With
less nerve removed, there should be less permanent
sensory loss and perhaps fewer sensory symptoms.
However, this concept is based on two postal questionnaire surveys [3, 91, and no long-term clinical
studies have been undertaken to determine accurately sensory loss and symptoms following fascicular
and whole nerve biopsy. Also, electrophysiological
studies have not been reported to indicate how effectively the s u r d nerve regenerates following nerve
biopsy. W e have therefore undertaken sensory examinations and nerve conduction studies in subjects
five or more years after they have undergone fascicular or whole sural nerve biopsy.
From the "Division of Neurology, Department of Medicine, University of Otago Medical School, Dunedin, and the tNeurology
Department, Christchurch Hospital, Christchurch, New Zealand.
Received Dec 17, 1981, and in revised form Apr 15, 1982. Accepted for publication Apr I S , 1982.
Methods
I n a long-term study, 16 subjects aged 1 5 to 68 years
(mean, 48 years) who had undergone fascicular (11 subjects) or whole ( 5 subjects) sural nerve biopsy were selected. Final evaluation was made at least five years after
biopsy. The subjects, 5 normal controls and 11 neurological controls (Table), had no sensory symptoms or signs in
the affected foot prior to biopsy and none outside the denervated sural nerve territory at final evaluation. T h e sural
nerve biopsy was taken at the ankle under local anesthesia
by an experienced operator in one institution. The incision
began 1 cm proximal to the lateral malleolus and extended
proximally for 6 to 8 cm. Proximal transection of the nerve
trunk with a new scalpel blade was done first t o render the
distal transection painless. In both fascicular and whole
nerve procedures, 3.5 to 5 cm of sural nerve was removed.
All subjects were confined to bed for a minimum of 24
hours after biopsy. On the day following the procedure the
wound was inspected and sural nerve sensory loss in the
foot confirmed. Nerve morphometry, including number of
fascicles and fascicular or whole nerve area, was undertaken
in all biopsied nerves by previously described methods 181.
Sensory examinations were performed in a silent closed
room with an ambient temperature of 22" to 23°C. The
skin temperature of the foot was maintained at 30" to 32°C.
Sensation in the sural nerve territory was assessed for light
touch, pinprick including repetitive stimulation, warm
(53"C),cold (23"C),vibration (128 Hz), and position sense.
Address reprint requests to Dr Pollock, Department of Medicine,
LJniversity of Otago Medical School, PO Box 913, Dunedin, New
Zealand.
0364-5 134/83/010065-04$1.50 0 1982 by the American Neurological Association
65
Nerve Biopsy
Subject
No. of
FaS-
NO.,
Age (yr),
and Sex
Diagnosis
Fascicular biopsy
1. 35, F
MS
2 . 29,F
3. 56, M
4. 6 5 , F
5 . 59, M
6. 66, F
7 . 28, F
8 . 48, F
9.6 8 , F
10. 56, F
11. 54, F
SMA
C
MS
C
MS
MS
MS
MS
MS
MS
Whole nerve biopsy
12. 15, F
C
13. 6 4 , F
S
14. 55, M
C
15. 41, M
16. 5 2 , F
C
S
Side
cicles
R
1
L
L
L
L
L
L
K
R
L
L
4
4
4
L
R
R
L
R
8
8
3
2
2
4
3
3
4
7
8
8
Fascicular
Area
(mmz)
Duration
since
Biopsy
(yr)
0.242
0.357
0.2 14
0.548
0.402
0.255
0.218
0.468
0.279
0.231
0.43 1
5
5
5
5
5
5
6
7
8
8
+
0.564
0.859
0.963
0.948
0.928
5
5
5
0
8
5
6
Fascicular mean +- SD
Whole nerve mean t S D
Dysesthesia
0
-t
+
+
0
0
0
+
0
0
+
+
t
0
Pain
Summation
+
+
0
0
ND
+
+
+
+
0
0
+
+
+
+
+
Area of Sensory Loss
(cm')"
Pain
Touch
14
122
117
59
22
55
26
44
76
49
39
153
117
69
63
39
ND
ND
77
22
ND
105
22
68
66
99
96
63
68
44
38
80
85
74
43
114
135
45
33
59 t 33 78
62 k 31 77
Temperature
ND
104
87
79
*
5
44
91
82
169
45
34 7 3 ? 29
32 86 2 45
"No significant difference V, > 0.2 hy Student t test) herween areas of sensory loss for pain, touch, and temperature.
+ = present; 0 = absent; MS = multiple sclerosis; SMA = spinal muscular atrophy; C = control; S = stroke; ND = not done.
Sensory loss was always compared with the nonbiopsied
side, contrasting right with left and left wirh right responses. The area of sural sensory loss for each modality
was marked on the foot, copied onto transparent plastic
sheets, and measured with a digitizer. The biopsy incision
site and the denervated sural nerve area were rubbed and
palpated for evidence of hyperalgesia or formation of
neuroma.
Postbiopsy surd nerve conduction studies were undertaken using a Medelec eiectromyograph. Nerves were
stimulated antidromically using supramaximal stimulation
by means of a surface bipolar stimulator with the electrodes
placed proximal to the biopsy suture line 10 to I3 cm from
the active recording electrode. Recordings were made with
needle electrodes placed near the sural nerve distal to the
suture line, posterior to the lateral malleolus. Bipolar recording was used except where a long caudal incision
necessitated a unipolar technique. Sural nerve action potentials were recorded in the frequency range of 32 Hz to
3.2 kHz. After 128 responses had been averaged, the study
was repeated t o ensure reproducibility. T h e skin temperature of the foot was maintained at 32" t o 34°C.
Results
Cliniml Findings
Immediately following nerve biopsy, 3 of the 16
subjects experienced an aching pain along the lateral
66 Annals of Neurology Vol 1 3 No 1 January 1983
aspect of the heel and foot, frequently aggravated by
dorsiflexion. In each subject the pain resolved within
one month. Early postbiopsy paresthesias (numbness,
pricking, or burning), experienced by 12 subjects, resolved within one to three months. Tactile-induced
d ysesthesias were the only long-term sensory symptoms after sural nerve biopsy. They were experienced by 11 subjects as an unpleasant tingling,
numbness, or raw sensation when the denervated
sural nerve area was touched or rubbed. Tactile
dysesthesias remitted in 3 subjects after three to five
years but persisted at final evaluation in 8 subjects,
representing 60% of the whole nerve biopsy group
and 45% of the fascicular biopsy group (see the
Table). Because of troublesome long-term dysesthesias, 2 subjects thought that nerve biopsies should
not be performed; one subject (No. 11) had had fascicular and one (subject 14) had had whole nerve
biopsy. With repetitive pinprick, lOOC/r of the subjects who had whole nerve biopsy and 60% of those
who had fascicular nerve biopsy experienced diffuse
tingling, sharp pain, or a stinging sensation, which increased in intensity (i.e., summated) and spread beyond sural nerve territory (see the Table).
Sensory impairment within the affected sural nerve
territory was present in all subjects five years after
F i g 2. Antidrornic suval vieroe action potential recarded after
whole nerve biops.y. Note thut the potential i i uni$,i-nr and hui
no late conzponenri. (Aniplitude .scale = 2.5 pV. Euih time
h a r e calibration point = 0.1 m.rec. i
F i g 1 . Maximum awa of hypoulgesia in 16 sub,jectsfve or
move years after .sui,al neroe biop.sy. The shaded area indicate.i
the i q i o n of greater .sensory impairment.
biopsy (Table; Fig 1). However, no significant difference was found between whole nerve and fascicular biopsy patients in the areas of pain, touch, or loss
of temperature sensation (see the Table). No
significant correlation was found in a regression analysis of area of sural sensory loss for light touch or
pain against fascicular area removed.
Efertrophysiologicaf Fzndings
Sural nerve sensory action potentials were recorded
from the biopsied side in all 5 subjects who had had
whole sural nerve biopsies (Fig 2) and in 10 of the 11
subjects who had had fascicular nerve biopsies. An
equivocal response only was obtained in Subject 4 ,
who had gross leg edema. No significant difference
was found between whole nerve and fascicular nerve
biopsy subjects with respect to amplitude of sural
nerve action potentials ( p = 0.3) o r conduction
velocity ( p > 0.05). Contralateral sural nerve
amplitudes and conduction velocities were normal in
all subjects (i.e., > I 0 p V and >40 misec, respectively).
Discussion
This study has shown that the area of sensory loss five
or more years after sural nerve biopsy is not
significantly different whether patients had fascicular
or whole nerve biopsies. In addition, no significant
correlation was found between the area of sural sensory loss and the fascicular area removed at nerve
biopsy. N o r was there a significant difference in the
amplitude of action potentials from biopsied sural
nerve when patients who had whole nerve biopsies
were compared with those who had fascicular biop-
sies. Two factors may at least partly account for these
surprising findings. First, cutting interfascicular
branches during the 3 to 5 cm fascicular dissection
may cause more extensive damage to sural nerve than
wouid be anticipated from the number of fascicles
removed. Second, the blood supply to intact fascicles
might be compromised by damage to the vasa nervorum.
No subject evaluated five or more years after sural
nerve biopsy had pain, paresthesia, analgesia, or
anesthesia in the affected foot. Previous detailed information on the sensory symptoms after sural nerve
biopsy had been restricted to three-month and
twelve-month reviews by mail 13, 91. Of the 97 patients who answered a questionnaire at twelve
months, 30% had intermittent mild persisting
symptoms and 10% were troubled by substantial
pain or paresthesias [91. Fascicular or whole nerve
biopsy made no difference as to whether the patients
thought nerve biopsies should or should not be done
[9]. In the present study, dysesthesia was the only
important symptom five or more years after nerve
biopsy. It was slightly more common following whole
nerve than fascicular biopsy. Most subjects had adjusted to this problem and carefully avoided precipitants.
All who had undergone whole nerve biopsy and
more than 509f who had had fascicular biopsy exhibited further evidence of hyperpathia [ S j in that repetitive pinprick in the affected sural nerve territory
led to temporal summation and radiation. These
phenomena have been previously observed following
sural nerve biopsy 13, 91. Skin biopsies from hyperpathic areas show a reduction of all neurocutaneous
elements [ b ] , suggesting that this phenomenon results from ineffective innervation of peripheral rcceptors.
In view of the high incidence of postbiopsy sympPollock et al: Fascicular and Whole Nerve Biopsy
67
toms and sensory loss, is peripheral nerve biopsy
clinically justified? We believe it is, provided patients
are carefully selected and a detailed morphometric
and light ultrastructural evaluation of nerve IS possible. Quantitative histological study of nerve is a more
sensitive method than electrophysiological study in
detecting mild or early neuropathy [2], and nerve
biopsy will in most cases settle the issue of whether
or not neuropathy is present. Nerve biopsy may also
establish the diagnosis of inherited neuropathy when
it is the only abnormality in affected kin [ 4 ] .In syndromes that may show clinical overlap and similar
neurophysiological findings, e.g., the hereditary sensory neuropathies types I and 11, nerve biopsy may be
required to settle the issue when inheritance is in
doubt [ 7 ] . Nerve biopsy is also required when a
suspected neuropathy has a distinctive histological
picture, e.g., vasculitis, amyloidosis, sarcoidosis,
leprosy, tomaculous neuropathy, or inflammatorydemyelinating polyradiculoneuropathy, and in lipidoses such as Tangier disease, metachromatic leukodystrophy, and Krabbe’s disease.
The results of this study suggest that most patients
and controls can be reassured that it is unlikely they
will experience long-term pain o r paresthesias as a result of sural nerve biopsy. Those with little or no sensory loss need to be warned of the permanent sensory impairment that follows nerve biopsy and of the
high incidence of tactile-induced dysesthesias. It is of
clinical importance that a comparison of whole nerve
and fascicular biopsy results showed no significant
difference in sensory loss and only a small difference
68 Annals of Neurology
Vol 1 3 No 1 January 1981
in long-term sensory symptoms. We therefore conclude that whole nerve rather than fascicular biopsy
should usually be recommended since it is simpler,
has greater diagnostic potential, and allows for a
more complete morphological evaluation.
This study was aided by grants from the Medical Research Council
of N e w Zealand and the New Zealand Neurological Foundation.
References
1. Asbury AK, Johnson PC: Technique of sural nerve biopsy. I n
Benningtoii JL (ed): Pathology of Peripheral Nerve. Philadelphia, Saunders, 1978, pp 268-271
2. Behse F, Buchthal F: Sensory action potentials and biopsy of
the sural nerve in neuropathy. Brain 101:473-493, 1978
3. Dyck PJ, Lofgren EP- Nerve biopsy. Choice of nerve, method,
symptoms and usefulness. Med Clin North Am 52:885-893,
1968
4. Dyck PJ, Oviarr KF, Lamberr EH: Intensive evaluation of referred unclassified neuropathies yields improved diagnosis.
Ann Neurol 10:222-226, 1981
5. Foerster 0: Die Lcirungsbahnen des Schmerzgefuhls und die
chirurgische Behandlung der Schmerzzustande. Vienna, Urban
& Schwarzenberg, I 927
6. Lourie H , King RB: Sensory and neurohistological correlates of
cutaneous hypcrpathia. Arch Neurol 14:3 13-320, 1966
7
I . Nukada H, Pollock M. Haas LF: The clinical spectrum and
morphology of type I1 hereditary sensory neuropathy. Brain (in
press)
8. Pollock M, Calcler C, Allpress S: Peripheral nerve abnormality
in multiple sclerosis. Ann Neurol 2:41-48, 197’
9. Stevens JC, Lofgren EP, Dyck PJ: Biopsy of peripheral nerves.
In Dyck PJ, Thomas PK, Lamberr EH (eds): Peripheral Neuropathy. Philadelphia, Saunders, 19’3, vol 1, pp 410-423
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