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Neural regeneration across long gaps in mammalian peripheral nervesEarly morphological findings.

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NEURAL REGENERATION ACROSS LOXG
GAPS TN MAMMALIAN PERIT'HEBAL NERVES :
EARLY MORPHOLOGICAL FINDINGS
CHARLES R. NOBACK, J A K O B HUSBY, J. MARTIN GIRADO,
C. ANDREW L. BASSETT AND J A M E S B. CAMPBELL','
D e p a r t m m t s of Anatomy, Neurological Surgery, and Orthopedic Surgery, College
o f Physicians and Surgeons, Columbia University, N e w Pork
THIRTEEN FIGURES
INTRODUCTIOK
The regenerative potential of the peripheral iiervous system
has long been known. Huber ( '27)' Rarrihn y Cajal ( '28)'
Sanders ('42)) Young ('42)' MTeiss ('50) and the recent
review of Guth ( '56) provide a n extensive bacligrouiid in the
morpliology of neural regeneration arid evaluate attempts to
utilize growth dynamics to achieve peripheral nerve repair.
Irreducihle gaps have heen bridged by several techniques
with varying degrees of success. Cable grafts, tubulation, and
lengthening by stretching all leave sometliing to be desired.
Algirc et al. ('54) used Millipore filters to study the homograft i ~ a c t i o nin vico. The properties of Millipore demonstrated by their investigation suggested that the plastic might
he used to develop a more uniformly successful method for
hridging gaps in peripheral nerves. Preliminary reports
Supported by grants from Department of the Army (Surgeon Gelier:tl)
DA-49-007-MD-545; Playtex P a r k Research Institute; United Cerebral Palsy
Associations, Iric. ; and U.S.P.H.S. Grant B-749.
This research would not have been possible without the collaboration of the
research and development divisions of the following industries : (1) Milliporc
Filter Corporation, Watertown, Massachusetts, ( 2 ) United States Catheter and
Instrument Corporation, Glens Falls, New York (reinforcing nylon mesh tubes),
( 3 ) now Corning Corporation, Midland, Michigan, and ( 4 ) The Surgical Products
Division of Anierican Cy:rnamid Company, Danbury, Coiniecticrit (silicone-contcd
surgical silk).
633
634
C H A R L E S R. NOBACK A N D O T H E R S
from these laboratories (Campbell et al., '56 ; Campbell and
Bassett, '57; Noback et al., '57; Campbell e t al., '57) have
indicated that feline peripheral iierve o r spinal cord gaps
encased with Millipore regenerated in a reproducible iiiainier.
The purpose of this corrirriuiiication is to record the sequence
of rriorphologic changes that follow tlie creation of a sizeable
peripheral 11erve gap until functioii is restored.
Pore volume 80 %
S o l i d (matrix) volume 20%
Fig. 1 Seheiiiatie diagram of Milliporc, Filter niaterial. Pores arc 0.46
diamctrr in t h e H. A. forniulntioii.
p
in
M A T E R I A L A X D METHODS
11illipore filter material is ordinarily pi*oduced in shccts.
This cellulose acetate plastic resembles a honeycomb (fig. 1).
Tlic 11. A. formulation with 0.45 p pores and a thiclmess of
130 to 200 I.( w a s used in t h e experiments. Since Millipow
is brittle when dry aiid frialdc when wet, reinfonmncwt was
ii(wssai*yto rriake its surgical use practical. Therefore, tubes
were falwicatcd by irripregiiatiiig a loosely woveii, inonofilanieiit nyloii mesh with the plastic.
The principal data to be presented were derived from adult
cats sulmittecl to rescction of 1 em scgniciits of the postc~ioi.
tibia1 division of tlie sciatic iicrve. Oiic em of each ncrve end
was drawn into a tube 3 rrirri in diameter and 3 ern long wit11 a
singlc sling stitch spaillling tlic 1 ern gap (fig. 2 ) . Twcnty
iierves ~ v e r eprepared in this way and removed 2, 4, 6, 9, 12,
KEGENERATIOX O F PEHIPHERAL NERVES
635
17, 21, 28, 36 and 70 days after operation. A control group of
6 nerves w1-e treated similarly, except that no tube was ernployed. These animals were kept for 60 days. Smaller groups
were created to study the results with gaps as long a s 2.5 cm
and the results when no sling stitch was employed. These
iiei~vcswc1-c removed at time intervals from 20 to 82 clays.
The nerves were fixed in 10% formalin. Longituclinal sectioris were made of all specimens and cross sections of the
proximal and distal ends of the more mature specimens. Hematoxyliri-cosin and plzospliotungstic acid-hematoxylin stains
were used to stain certain tissue elements. The Botliau protargol method and the Romaries ’ silver impregnation technique were used to dernonsti-ate axons. The Ahlion stain was
used to determine the presence of myelin.
Fig. 2 Diagram of nerve immediately after operation. Gap was created by
resecting one em or more of nerve. Proximal stump, gap, a n d distal stump are
enenscd by n tube of reinforced Millipore. A sling stitch bridges the gap whicli
fills with plasma.
OBSERVATIOh7S
Gross aizutonzy. Several hours after completion of the operation, the gap between the severed ends of the nerve was
filled with a yellowish-pink to light red clot in the living
animal. Outgrowth of tissue occurred from both stumps and
conformed to the internal surfaces of the tube. Gradually
it reduced the gap until anatomical continuity was restored
during the third week. P r i o r to the time when bridging was
complete, both advancing tips of outgrowing tissue were
marked by one to two mm transverse blood-colored bands.
Regeneration from the proximal segment mas more rapid
than from the distal segment. Union was established at a site
approximately two-thirds of the way donTn the 1 ern gap. The
636
C H A R L E S R . NOBACK A N D O T H E R S
young neural tissue bridges were translucent, but became progressively more opaque with tlie passage of time. I n the fixed
spcciniens, the diameter of the Inridge was approximately
of the original nerve. This discrepancy became less obvious
by the fifth week, and was not apparent at 70 days. I n a preliminary study there was evidence of the return of function iii
the older preparations. Stimulation of the iicrve proximal
to the gap in several cats produced gastrociiemius coiitractions between the tenth and eleventh weeks after ope1'a t'1011.
The control experiments demonstrated bulb-shaped nerve
ends firmly adherent to surrounding tissues. The sling stitch
uniting the nerve segments was encapsulated. When tlic Nillipore tube was displaced from its position shielding the gap,
the results resembled the control experiment. 111addition,
\\-lien tlie Millipore wall was perforated prior to the time
when the bridging was complete, tissue from the bed invaded
tlie gap through the rent. I n experiments when the sling
stitch was omitted, there were comparatively few anatomical
unions. Tl'sually, the stumps appeared a s neatly tapered cones.
Tissue I-cacti011to Millipore was minimal. F r o m the third
week on, the tubes were encased ivithin a diaphanous nicnibrarie which was continuous with the epincurium of the prosimal ancl distal stumps. Tlic nerves were not adlicrent to the
iiiside of the tube.
Microscopic anntom!y. Degenerative and regenerative
changes in the proximal and distal nerve stumps were essentially similar to those in the classic descriptions of R a m h
y Cajal ('28) and others. To spare repetition, findings in the
stumps will be referred to only wlien they are related to
phenonicna in the gap. Unless otherwise specified, the follo\ving microscopic findings were derived from animals with 1 ern
gaps.
On the second day after operation, the fibrin in tlie clot
which filled the Millipore tube had become aligned a s parallel
strands in the immediate vicinity of the tube walls ancl the
sling stitch (figs. 3, 4 and 5). A t either end of the gap, a
succession of arched fibrin strands curved between these two
areas of linear alignment. The convexity of the arches was
:x
REGENERATION OF PERIPHERAL NERVES
637
directed toward the stumps. The intervening areas were occupied by a fine reticular network of fibrin micelli with random orientation. Some blood cells were scattered throughout
the clot. I n the “necrotic zone” (fig. 3, A) of both stumps
(Ram6n y Cajal, ’28), angiogenesis was the predominant
feature.
Invasion of both ends of the clot-filled gap was first noted
on the fourth day after operation (fig. 3). A vanguard of
spindle-shaped cells and capillaries from the “necrotic zone ”
penetrated the clot along the sling stitch. At the same time,
cells were migrating along the most proximal and distal fibrin
strands toward the Millipore wall. However, these strands
2-4 Days
9-15 Days
17-21 Days
1
Fig. 3 Diagrams of longitudinal sections of the proximal stump (left), gap
and distal stump (right) of a peripheral nerve t o illustrate the general sequence
of events during regeneration. Stumps and gap are encased by the Millipore and
bridged by a central sling stitch. A = “necrotic” zone, B = “regenerating”
zone, C = flanking peripheral wave, D = advancing central tip, E = area of
junction. (See text f o r further description.)
638
CHARLES R. NOBACK AND OTHERS
seemed to pose no insuperable barrier to the passage of cells.
Invasion of the clot was relatively slow until the ninth postoperative day, when the waves of spindle-shaped cells and
capillaries had advanced one mm in the region of the sling
stitch. Relatively few Schwann cells had migrated from the
stumps at this time.
I n the proximal stump during the first 9 days, the tempo
of cellular and axonal activity increased in the “regenerating
zone ” (figs. 3, B and 11) (Ram6n y Cajal, ’28), just proximal
to the “necrotic zone.” This activity became quite apparent
by the ninth day when heavy peripheral bands of “Schwann
cell cords” and axons (fig. 3, C) advanced toward the clot,
flanking the “necrotic zone.’’ During the next three days
these bands of regenerating tissue grew sufficiently f a r to
enter the clot in the region of the Millipore tube wall. At 12
days, advanced cells had travelled about 2 mm into the clot
in the region of the sling stitch and had aligned themselves on
the parallel fibrin strands. However, in the sling stitch area
between the “necrotic zone” and the advancing tip (fig. 3, D),
there was cell packing with a gradually increasing disruption
of orderly alignment.
From the twelfth day on, cellular proliferation became
markedly accelerated. Heavy mitotic activity was no longer
restricted to the stump, but occurred in the bridge as well.
The wave of regenerating tissue from the proximal stump
swept forward along the internal surface of the Millipore tube,
traversing the remaining gap of 5 mm in about 7 days. During the entire bridging sequence, spindle-shaped cells and
capillaries (fig. 6 and 7 from area C in fig. 3) were in the
lead, followed closely by “Schwann cell cords” and then by
axons (figs. 8, 9, and 10). The capillaries had enlarged to
form arterioles and venules in the more mature regions of
the bridge at 28 days.
Regeneration upward from the distal stump began to be
evident on the fourth day. The cellular components followed
the same sequence as noted in the proximal stump. The advance of the cellular wave upward from the distal stump proceeded slowly on a broad front and met the down-growing
REGENERATION O F P E R I P H E R A L N ERV ES
639
vanguard cells at about 21 days (fig. 3, E). Interruption of
the linear orientation was evident at the junction where the
proximal outgrowth met the distal outgrowth. End-to-end
abutment was not established but rather, opposing lines of
cells interdigitated. This led to swirling and overlapping
which in turn caused regenerating axons from the proximal
stump to lose their linear orientation; each following the
trellis provided by its particular cord of Schwann cells (fig.
12 from area E in fig. 3). Between the 21st and 28th days,
the more peripheral cords of Schwann cells flanked this area
of disorganization. The axons entered the distal stump at
28 days by converging, and at this time, nearly all Schwann
cords of the stump contained at least one or more fibers.
Once in the stump, the fibers seemed to seek the pathways provided by the pre-existing Schwann cords or band fibers. During all phases of axonal regeneration, terminal budding and
collateral sprouting gave rise to increasing numbers of fibers
in the proximal stump and bridge. With the passage of time,
the size of the regenerated fibers increased. Beginning myelinization was noted in the bridge at 36 days.
Several obvious changes occurred in the maturing bridge
after fibers had spanned the gap. I n the bridge area, there
was less collagenous staining material than in the nerve
stumps. Even in the early period of collagen production there
was little resemblance to scar formation. On the other hand,
the amount of connective tissue fibers seemed to be sufficient
to lend tensile strength to the bridge.
The disorganized area where proximal and distal regenerative waves met, disappeared and finally presented a linear
pattern (fig.13). Compaction occurred as fibers and cells were
added, improving the general linearity in all areas except in
the immediate region of the sling stitch.
The control animals which survived 60 days with a sling
stitch uniting the unshielded stumps produced classic neuromata at their proximal and distal ends. There was extensive
invasion of the stumps by connective tissues and capillaries
from the operative bed. Some axons passed along the stitch
from the proximal neuroma to enter the distal stump.
640
CHARLES R. NOBACK A N D OTHERS
With the passage of time, a synovia-like membrane several
cells thick developed on both sides of the tube. There was no
evidence of acute or chronic foreign body response t o Millipore except in the areas where extraneous matter (lint, talc,
starch, etc.) had been accidently introduced with the tubes.
All suture material used as sling stitch in the bridge caused
a foreign body response. Limited experience has indicated
that silicone-coated silk causes less reaction than uncoated silk.
DISCUSS103
The millipore tubulation technique of Campbell and Bassett (’57) employed in these experiments gives reproducible
bridging of large gaps in peripheral nerves. Aside from its
implications from the clinical standpoint, the method currently
offers many advantages for study of the pattern, tempo and
physiology of neural regeneration. The results of the microscopic examinations suggest strongly that the environment
within the Millipore tube has many features of tissue culture.
I n neural growth, orientation of cells has been found to
follow interfaces provided by viable or nonviable elements.
The directional growth of the neural elements was called
“tactile adhesion” (Ram6n y Cajal, ’10, ’ZS), “contact sensibility” and “haptotropism” (Dustin, ’lo), “stereotropism”
(Loeb, ’12 and Harrison, ’12) and “contact guidance” (T$7eiss,
’41, ’55). The concept of interface orientation explains many
of the phenomena observed in the experiments under discussion. Acting in concert, the Millipore tube and sling stitch
determine, in large measure, the orientation of the fibrin
strands and micelli of the plasma clot. The linearly oriented
fibrin strands provide the guiding interface for the regenerating elements that emerge from the nerve ends. The arches
of the fibrin running across the line of migration act as minor
barriers which are later obliterated by cell metabolism. It is
probable that the linearly oriented tissue on the internal surface of the Millipore tube serves as a guide to orient the
migration of succeeding cells and axons.
I n the gap three cell types with a specific morphologic
pattern are identified ; spindle-shaped cells, angioblastic cells
REGENERATION O F PERIPHERAL NERVES
641
and Schwann cells. The angioblastic cells are present in
association with capillary buds. The Schwann cells are identified by their tendency to be arranged in longitudinal cords,
several cells thick and separated by little or no collagen
(Holmes and Young, ’42). Many of the spindle-shaped cells
are seen in close association with the small amounts of collagenous and reticular fibers in the bridge and in the connective
tissue outside the tube. These cells are probably fibroblasts.
A controversy is current as to whether the Schwann cells
play a significant role in guiding regenerating axons across
a gap (Guth, ’56). Because the axons in the gaps in these
experiments are closely associated with “Schwann cell
cords, ” it is concluded that these cells may play a role in guiding axons. This concurs with the thesis of Holmes and Young
(’42) and Weddell ( ’42).
Of major importance is the capacity of the regenerating
axons to divide and branch in the gap. This phenomenon
makes it possible for many of the advanced axons to penetrate
the distal stump beyond the area of disruption. Early in
regeneration there are many disoriented Schwann cords.
Therefore, there are many disoriented axons. The disruption
is most evident in the areas where cells from the proximal
and distal stumps make contact. The mechanism by which the
areas of cellular disorientation are eliminated is not clear.
However, successful axonal bridging of the gap and cellular
compaction within the confines of the tube may direct the
reorientation process. Once the neural bridge has matured,
the pattern is so like the original nerve that the point of resection cannot be detected except in the area of the sling stitch.
In the region of the sling stitch the pattern of regeneration is
invariably tortuous during the maturing phase. There seems,
however, to be little question that the sling stitch serves a
critical function in the early phases of regeneration. It helps
orient the fibrin pattern of the clot and serves as an additional interface for cell migration. I n spite of attempts to find
and use relatively inert suture materials, disruption of an
organized cell pattern in the region of the stitch is still the
rule. I n the long term preparations, scarring persists around
642
CHARLES R. NOBACIC AND O T H E R S
tlie suture and is responsible for the major portion of collagen
in the bridge. Methods for fibrin network orientation, other
than incorporation of non-absorbable material, are being
investigated. At the present time, however, the use of a sling
stitch seems a necessary adjunct to the Millipore tubulation
technique of nerve repair in dealing with large gaps. The
few successes obtained in animals in which the stitch was
absent must be attributed to chance o r compressive-tensive
forces which may have oriented the fibrin strands in a direction favorable for linear regeneration.
The total function of the Millipore tube is still not completely clear. The pore diameter of 0.45 p is small enough
to prevent mesenchymal cells from the tissue bed entering the
gap. I n addition, it limits regenerating tissue elements to a
sharply demarcated tract. The tube favors the deposition of
a linearly oriented fibrin network on its internal surface. This,
then acts as a linear substrate for migrating cells. Theoretically, extracellular fluids passing through the pores may add to
the formation of the plasma clot and to the nutrition of cells
on the internal surface of the tube wall. The importance of
permeability is currently under investigation.
There are points of similarity between the tubulation technique reported by Matson et al. ('48) and the method herein
described. Several dissimilar features deserve emphasis since
the current report may aid in interpreting the earlier work
and provides a method which has greater clinical potential. A
viable autogenous vein wall is more difficult to obtain than a
Millipore tube and is relatively more impermeable to tissue
fluids. The use of multiple tantalum or nylon filaments in the
work of Matson and his co-workers gave rise to extensive
scarring which may have reduced the caliber of axons in the
bridge. The current sequential study of neural regeneration
suggests that the multiple filaments may have initially functioned to orient the fibrin clot and provide a linear pattern for
cell migration. However, their size and nature as foreign
bodies augur poorly f o r the return of a normal nenrohistologic pattern in the bridge.
REGENERATION O F PERIPHERAL NERVES
643
SUMMARY
1. These experiments record the sequence of events during
regeneration across a Millipore-protected gap in peripheral
nerves.
2. One to 2.5 em gaps in the posterior tibia1 division of the
sciatic nerve in adult cats were studied at intervals up to 82
days when function had returned.
3. Each gap became filled with a plasma clot having a characteristic pattern. Cells from both stumps migrated into the
gap following the linear orientation provided by the Millipore
tube, sling stitch and plasma clot.
4. From both stumps, spindle-shaped cells and angioblastic
cells were first to invade the clot and were followed by (‘cords
of Schwann cells. ” Regenerating axons of the proximal stump
followed the “Schwann cell cords” and finally entered the
distal stump during the fourth week.
5. Subsequently, axons thickened, and myelinated. In previously disoriented areas, axons became linearly arranged.
LITERATURE CITED
ALGIRE,G . H., J. WEAVERAND R. PREHN 1954 Growth of cells in vivo
diffusion chambers. I. Survival of homografts in immunized mice.
J. Nat. Cancer Inst., 15: 493-507.
CAMPBELL,
J. B., C. A. L. BASSETT,J. M. GIRADO,R. J. SEYMOUR
AND J. ROSSI
1956 Application of monomolecular filter tubes in bridging gaps in
peripheral nerves and for prevention of neuroma formation. J.
Neurosurg., 13: 635-637.
CAMPBELL,
J. B., AND C. A. L. BASSETT 1957 The surgical application of mo11omolecular filters (Millipore) to bridge gaps in peripheral nerves and
t o prevent neuroma formation. Surg. Forum, 7: 570-574.
CAMPBELL,
J. B., C. A. L. BASSETT,J. HUSBYAND C. R. NOBACK 1957 Regeneration of adult mammalian spinal cord. Science, 126: 929.
DUSTIN,A. 1910 Le rBle des tropismes et de l’odogenese d a m la rhgh6ration
du syst4me nerveux. Arch. de Biol., 25: 269-388.
GUTH, L. 1956 Regeneration in the mammalian peripheral nervous system.
Physiol. Rev., 3 6 : 441-478.
HARRISON,
R. 1912 The cultivation of tissues in extraneous media as a method
of morphogenetic study. Anat. Ree., 6: 181-193.
HOLMES,W.,AND J. Z. YOUNG 1942 Nerve regeneration after immediate and
delayed suture. J. Anat., 77: 63-96.
644
CHARLES R. NOBACK AND OTHERS
HUBER,G. C. 1927 Experimental observations on peripheral nerve repair. Med.
Dept. U. S. Army, 11: 1091-1283, P a r t I.
LOEB,L. 1912 Growth of tissue in culture media and its significance for the
analysis of growth phenomena. Anat. Rec., 6: 109-120.
MATSON,D. A., E. ALEXANDER
AND P. WEISS 1948 Experiments on the bridging
of gaps in severed peripheral nerves of monkeys. 3. Neurosurg., 5 :
230-248.
NOBACK,
C. R., J. M. GIRADO,C. A. L. BASSETTAND J. B. CANPBELL 1957 Regeneration of nerve fibers across large gaps. Anat. Rec., 127: 437-438.
RAN~N
Y CAJAL, 5. 1910 Algunas observaciones favorables 8. la hip6tesis
neuratrbpica. Trab. del Lab. de Invest. Biol., 8: 207. (Cited by Ram6n
y Cajal, S., 1928.)
RAM6N Y CAJAL,S. 1928 Degeneration and Regeneration of the Nervous System.
Oxford, London. Vol. 1, pp. 1-396.
SANDERS,
F. K. 1942 The repair of large gaps in the peripheral nerves. Brain,
65: 281-337.
WEDDELL,
G. 1942 Axonal regeneration in cutaneous nerve plexuses. J. Anat.,
77: 49-62.
WEISS, P. 1941 Nerve patterns: The mechanics of nerve growth. Growth
(SUppl.), 5 : 163-203.
1950 An introduction to genetic neurology. I n : Genetic Seurology.
Univ. Chicago Press, Chicago, pp. 1-39.
1955 Nervous system. I n : Analysis of Development, Eds. B. Willier,
P. Weiss and V. Hamburger. W. B. Saunders, pp. 346-401.
POUNG,
J. Z. 1942 The functional repair of nervous tissue. Physiol. Rev., 22:
3 18-3 74.
PLATE 1
EXPLANATION OF FIGURES
4
Proximal stump and part of the gap filled with plasma enclosed within the
reinforced Millipore tube. The fibrin of the clot is aligned as a succession
of arched strands curving between the Millipore tube and the sling stitch.
Note on the right the nylon monofilaments reinforcing the Millipore tube.
Longitudinal section. Phosphotungstic acid-hematoxylin technique. Fourth
post-operative day. X 13.
5
The fibrin strands in the vicinity of the Millipore are aligned parallel to the
tube wall. Longitudinal section of Area C in figure 3. Phosphotungstic acidhematoxylin technique. Ninth post-operative day. X 140.
6
Spindle-shaped cells from the proximal stump penetrate the clot, paralleling
the longitudinally oriented fibrin strands seen in figure 5, just proximal t o
Area C in figure 3. Longitudinal section. Bodian stain. Twelfth post-operative
day. X 300.
7
Spindle-shaped cells, angioblasts and capillaries. This section is just proximal
to that of figure 6. Longitudinal seetion. Bodian stain. Twelfth post-operative day. X 300.
R E G E N E R A T I O N O F P E R I P H E R A L K’ERVES
C. R . NOBACK
A N D OTIIERR
645
EXPLASATIOS GI" FIGURES
Figures 8, 9, 10, 11 (13odi:cii st:ciii. T \ ~ e l f t lpost-operative
i
day. X 300)
8
Spiiidle-sli;ipetl cc~llsant1 c:rrly cords of Sc1iw:iiiii cells associated xitli early
rcgeiicr:ctiiig fibers. Loiigitiitliiial section f r o m area betwecii C :riitl 13 iii
fig~irc3, just prosiiiial t o figure 7.
9
Sl'iiidlc-sli:ipetl cclls :riitl cortls of Sc1i~r:iiiii c~,lls. Regeiitratiiig nerve fibrrs
folloir tlie orieiitatioii of the cortls. 1Joiigitudiii:il sectioii f r o m saiiic area
:is figiu.c 8, 11ut just proxiiiial to it.
10
Se\rly rc,geiier:itiiig iierve filwrs followiiig the oriciitetl pattcrii of the cortls
of Scli~r:iiiiicells aiitl spiiidlc-sliapc,(Ilcclls whose geiieology is difficult t o define.
IJoiigitutliiial sectioii just distal to Area B
iii
figure 3 .
11 1,ongitudiiinl seetioii of regeii(,r:itiieg area of proxini:rl steiiiip. (Area I3 ill
fig. 3 . )
1 % Jcuictioii :ircn wlicrc tlir ccllular outgrowths of tlic proxiilia1 sttinip iiitcr-
tligitxte with those of the distal stump. Disorieiitatioii is visible. 1migitudiii:iI
section. Bodiaii stain. Tweiityeiglitli post-operative d:~y. x 230.
13
Rcgeiieratcd iierve in the gap :it 70 days. Kote orieiited p r a l l e l fibc~swit11
iio eviileiice of scnrriiig. Although iiot visible in this figure, i11:iny fibers arc
iiiyeliiiatcd. Loiigitutliiial section. Rodian st:iiii. x 250.
646
RE(~CSEILAT1ON OF PERIPHERAL SEIWES
0 . R. S 0 l S A C K A S D OTHPRS
PLATE 2
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