HAND/PERIPHERAL NERVE

Neural Perforasomes of the Upper Extremity

Steven M. Koehler, M.D.
Background: In the setting of the rapid advancement of integumentary vas-
Andrew P. Matson, M.D.
cular knowledge, the authors hypothesized that the extrinsic blood supply to
David S. Ruch, M.D.
the major peripheral nerves of the upper extremity could be categorized into
Suhail K. Mithani, M.D. discrete neural “perforasomes.”
Brooklyn, N.Y.; and Durham, N.C. Methods: Total limb perfusion of the arterial system was performed with gel-
atin–red lead oxide in cadaveric upper limbs. The perforating vessels to the
radial, median, and ulnar nerves were identified, confirmed with fluoroscopy,
and dissected. Distances to major anatomical landmarks of the upper extremity
were measured. Additional cadaveric limbs’ nerves were dissected and source
arteries were selectively cannulated and injected to assess specific contribution
to extrinsic nerve perfusion. The perfusion of each nerve was then calculated
among all specimens.
Downloaded from http://journals.lww.com/plasreconsurg by BhDMf5ePHKbH4TTImqenVFrctQzt46R2BPlXuzx8F0B8As8GPHXPQUAhrGNCA3QI on 12/09/2018

Results: The radial, median, and ulnar nerve perforators were mapped. The
corresponding neural perforasomes were mapped. The distal portions of the
superficial radial nerve and the posterior interosseous nerve demonstrated a
lack of staining. Similarly, at the carpal tunnel and at the proximal 25 percent
of the median nerve (corresponding to the pronator teres), the nerve lacked
vascular staining. At the Guyon canal and the flexor carpi ulnaris, the ulnar
nerve demonstrated a lack of vascular staining.
Conclusions: Peripheral nerves can be divided into neural perforasomes with
limited overlap. The extrinsic perfusion of peripheral nerves is highly segmen-
tal. Absent stains within the nerves correspond to common sites of compres-
sion: carpal tunnel and pronator teres for the median nerve, supinator for the
posterior interosseous nerve, and the Guyon canal and the flexor carpi ulnaris
for the ulnar nerve.  (Plast. Reconstr. Surg. 142: 1539, 2018.)

I
nitial breakthroughs in the understanding of
the blood supply to peripheral nerves are cred-
ited to Sir Sydney Sunderland, who demon-
strated that relationships between source arteries
and peripheral nerves are relatively consistent.1
Taylor and Ham then introduced the free vascu-
larized nerve graft in 1976 on the basis of these
source arteries.2 Taylor and Palmer proceeded
to develop a comprehensive three-dimensional
concept of the cutaneous vascular anatomy of the
body—the angiosome concept.3
The understanding of this concept, along
with the linkage of adjacent angiosomes, provides
the basis for microsurgical free tissue transfers.4–6
Taylor et al. also described a number of anatomi-
cal concepts based on their work, one of which
From the Department of Orthopaedic Surgery, SUNY Down-
state Medical Center; and the Division of Hand and Upper
Extremity, Department of Orthopaedic Surgery, Duke Uni-
versity.
Received for publication November 16, 2017; accepted May
16, 2018.
Copyright © 2018 by the American Society of Plastic Surgeons
DOI: 10.1097/PRS.0000000000004984
is that vessels “hitchhike” with nerves.7 Taylor’s
group then reexamined the source artery supply
of each peripheral nerve in the upper extremity
and assessed the potential of each segment of each
nerve for vascularized transfer.8 They demonstrated
the nerves’ source blood supply radiographically
and used the angiosome concept to provide an
anatomical rationalization for both vascularized
nerve grafts and composite free flaps contain-
ing vascularized nerves. To aid in the description
of donor nerves, Taylor then developed a system
that classifies peripheral nerves according to their
angiosomes, with special reference to their suitabil-
ity for microvascular free transfer.3,8,9
More recently, for the integumentary, Saint-
Cyr et al. put forth the “perforasome theory,”
which shifts the focus of vascular supply and
knowledge from source arteries to perforators
themselves.10 Inspired by this work, in the setting
of Taylor’s work, we hypothesized that the blood
Disclosure: The authors have no financial interest
to declare in relation to the content of this article.

www.PRSJournal.com 1539
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 Plastic and Reconstructive Surgery • December 2018
supply to the major peripheral nerves of the
upper extremity could also be categorized into
neural perforasomes, each with discrete areas of
neural perfusion.
MATERIALS AND METHODS
This study was deemed exempt by the
Duke University Institutional Review Board
(Pro00075741). Twelve upper limb specimens
from fresh cadavers were used in this study. All
limbs were procured recently deceased cadavers,
without cachexia, prior upper extremity trauma,
or known prior vascular disease.
Perforators
In six specimens, total limb perfusion of the
arterial system was performed with a gelatin–red
lead oxide mixture according to the protocol
described by Tang and colleagues.11 The radial,
median, and ulnar nerves were dissected under
loupe magnification to identify the perforating
vessels supplying the extrinsic blood supply of
the individual nerves (Fig. 1). To ensure that all
perforating vessels were identified, biplanar fluo-
roscopy was used to image each nerve’s vascular
supply after painting the nerve with 40 percent
lead white paint.
The distance of each perforator from major
landmarks to their entrance into the nerve was
Fig. 1. Representative images demonstrating gross and fine dissection of the ulnar nerve
after gelatin–red lead oxide injection to highlight the neural extrinsic blood supply.
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Copyright © 2018 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
measured (Fig. 1). For the radial nerve (includ-
ing the superficial radial nerve and the posterior
interosseous nerve), the distance from the lateral
epicondyle was used for all perforator measure-
ments. For the median nerve, forearm perforators
were measured from the distal radial lunate facet
and upper arm perforators were measured from
the medial epicondyle. The ulnar nerve perfora-
tors were measured from the pisiform in the fore-
arm and from the medial epicondyle in the upper
arm. The total length of the forearm and arm of
each cadaver was then measured for normaliza-
tion of perforator distance as a percentage of the
forearm or the upper arm. Average perforator dis-
tance was then calculated.
Perforasomes
The remaining six limbs were thawed to room
temperature; before dissection, the brachial artery
was identified and cannulated at the level of shoul-
der disarticulation. Embalming Sofner solution
(ESCO, East Lyme, Conn.) was injected into the
brachial artery to clear the arms of blood. Next,
the radial, median, and ulnar nerves were com-
pletely dissected with their extrinsic perforators.
Source arteries were selectively cannulated and
injected with different color inks (i.e., red, green,
black, and blue) to assess specific contribution
to extrinsic nerve perfusion. Injections occurred
 Volume 142, Number 6 • Upper Extremity Neural Perforasomes

Table 1.  Median Nerve Perforators Ulnar Nerve

The ulnar nerve had an average of 15 extrinsic
Average Raw Perforator
No. of Distance from Distance neural perforators (range, 12 to 15). There were
Perforators Radiolunate as % of seven in the forearm and eight in the upper arm
Perfusing (Distal Joint ± SD Forearm/ (Tables 3 and 4). The extrinsic perforators origi-
Artery to Proximal) (cm) Arm
nated from ulnar, proximal ulnar recurrent, infe-
Radial 1 0.4 ± 0.3 1.9 rior ulnar collateral, or superior ulnar collateral
Ulnar 2 1.3 ± 0.2 4.5
Radial 3 1.7 ± 0.6 7.3 source arteries: five from the ulnar artery, three
Ulnar 4 3.7 ± 1.1 12.9 from the proximal ulnar recurrent artery, two
Radial 5 5.9 ± 1.2 23.0 from the inferior ulnar collateral artery, and five
Radial 6 10.2 ± 1.8 42.0
Radial 7 13.3 ± 1.1 52.3 from the superior ulnar collateral artery (Fig. 2).
Radial 8 19.7 ± 1 72.8 At, and just distal to, the Osborne ligament, there
were no extrinsic neural perforators identified
within 4 cm. Likewise, there were no extrinsic
from distal to proximal. To control the direction neural perforators within the Guyon canal or
of ink flow, upstream arteries were cross-clamped proximal for 1.5 cm.
before injection with microvascular clamps. The
radial, median, and ulnar nerves were then sec- Radial Nerve
tioned and examined for colored ink staining to The radial nerve proper consistently had
assess neural perfusion. The distance of colored eight extrinsic neural perforators (range, seven
ink staining was measured from the above land- to eight), one in the proximal forearm from the
marks for each respective nerve and normalized radial recurrent artery and seven in the upper
to the overall length of each forearm and arm. arm (two from the radial recurrent artery dis-
The average percentage of perfusion of each tally and five from the profunda brachii artery)
nerve was then calculated among all specimens. (Table 5 and Fig. 2). The perforators providing
extrinsic blood supply to the superficial radial
and posterior interosseous nerves were likewise
RESULTS identified and measured. Four extrinsic neural
Upper Extremity Nerve Perforator Identification perforators supplied the superficial radial nerve,
Median Nerve one from the recurrent radial and three from the
The median nerve consistently demonstrated radial artery (Table 5 and Fig. 2). Three extrinsic
13 extrinsic neural perforators (range, 12 to 13), neural perforators supplied the posterior interos-
eight in the forearm and five in the upper arm seous nerve, one from the radial artery and two
(Tables 1 and 2). The neural perforators origi- from the posterior interosseous artery (Table 5
nated from radial, ulnar, or brachial source arter- and Fig. 2). There was no extrinsic neural perfo-
ies: two from the ulnar artery, seven from the rator to the radial artery identified at the level of
radial artery, and four from the brachial artery. the supinator.
The average locations of these perforators were
then mapped (Fig. 2). There were no extrinsic Upper Extremity Neural Perforasomes
neural perforators identified within or 0.5 cm Median Nerve
proximal to the carpal tunnel. Similarly, adjacent In the forearm, 60 percent of the median
to the region where the nerve passes between the nerve was extrinsically supplied by the radial
two heads of the pronator, there were no extrinsic artery neural perforators and 5 percent by bra-
neural perforators within 5 cm. chial artery neural perforators (Table 6 and
Fig. 3). There was no staining by the extrinsic
Table 2.  Median Nerve Perforators neural perforators identified originating from
Average Raw the ulnar artery. The distal 10 percent of the
No. of Distance median nerve, including the carpal tunnel, dem-
Perforators from Medial Perforator onstrated no dye within the nerve under dissec-
Perfusing (Distal to Epicondyle Distance as % of F tion. Proximally, 25 percent of the nerve in the
Artery Proximal) ± SD (cm) orearm/Arm
forearm demonstrated limited staining, which
Radial 9 1.9 ± 0.4 6.5 corresponded to the area adjacent to where the
Brachial 10 5.9 ± 1.1 21.0
Brachial 11 10.8 ± 0.7 40.3 nerve traverses between the two heads of the
Brachial 12 14.5 ± 0.6 53.8 pronator teres. The most proximal 5 percent of
Brachial 13 19.8 ± 0.9 75.4 the nerve was stained by brachial artery neural

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 Plastic and Reconstructive Surgery • December 2018

Fig. 2. Map of perforators supplying the extrinsic blood supply to the median, ulnar, and radial nerves. The major source vessels
are labeled.

Table 3.  Ulnar Nerve Perforators Table 4.  Ulnar Nerve Perforators
No. of Average Raw Average Raw
Perforators Distance from Perforator No. of Distance Perforator
Perfusing (Distal to Pisiform Distance as % of Perforators from Medial Distance
Artery Proximal) ± SD (cm) Forearm/Arm Perfusing (Distal to Epicondyle as % of
Ulnar 1 1.5 ± 0.4 5.3 Artery Proximal) ± SD (cm) Forearm/Arm
Ulnar 2 3 ± 0.6 11.2 PURA 8 1.1 ± 0.5 4.5
Ulnar 3 5.6 ± 0.7 20.9 IUCA 9 1.8 ± 0.4 6.6
Ulnar 4 15.3 ± 1.2 57.9 IUCA 10 4.1 ± 0.6 16.0
Ulnar 5 17.1 ± 1 64.6 SUCA 11 7.3 ± 0.7 26.7
PURA 6 22.1 ± 2 83.2 SUCA 12 9.3 ± 0.8 33.2
PURA 7 25.2 ± 2.6 95.0 Brachial 13 11.1 ± 1 41.6
PURA, proximal ulnar recurrent artery. Brachial 14 14.6 ± 0.8 51.8
Brachial 15 18.8 ± 1.8 67.7
PURA, proximal ulnar recurrent artery; IUCA, inferior ulnar collat-
eral artery; SUCA, superior ulnar collateral artery.
perforators, and in the upper arm, 100 percent
of the nerve demonstrated dye staining from the
brachial artery neural perforators; thus, 105 per- the proximal flexor carpi ulnaris (20 percent).
cent of the nerve was stained by brachial artery There was no staining of the ulnar nerve by dye
extrinsic neural perforators (Fig. 3).
injection of the proximal ulnar recurrent artery.
Ulnar Nerve Selective cannulation and dye injection of the
In the forearm, 70 percent of the ulnar inferior ulnar collateral artery resulted in dye
nerve demonstrated dye staining from the ulnar staining of 2 percent of the nerve in the forearm
artery extrinsic neural perforators (Table 6 and and 3 percent of the nerve in the upper arm.
Fig. 3). This corresponded to 5 to 75 percent Selective cannulation and dye injection of the
of the length of the forearm, with limited to superior collateral artery extrinsic neural perfo-
no dye staining at the Guyon canal (5 percent) rators demonstrated staining of the remaining
and from distal to the Osborne ligament to 97 percent of the nerve.

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 Volume 142, Number 6 • Upper Extremity Neural Perforasomes

Table 5.  Radial Nerve Perforators

No. of
Perforators Average Raw ­ Perforator
(Distal to Distance from Lateral Distance as % of
Perfusing Artery Proximal) ­Epicondyle ± SD (cm) Forearm/Arm
Radial nerve (proper)
 Recurrent radial 1 1.5 ± 0.4 5.3
 Recurrent radial 2 3 ± 0.6 11.2
 Recurrent radial 3 5.6 ± 0.7 20.9
 Profunda 4 15.3 ± 1.2 57.9
 Profunda 5 17.1 ± 1 64.6
 Profunda 6 22.1 ± 2 83.2
 Profunda 7
 Profunda 8 25.2 ± 2.6 95.0
Superficial radial nerve
 Recurrent radial 1 6.8 ± 1 74.2
 Radial 2 11.6 ± 0.5 56.6
 Radial 3 18.2 ± 0.6 11.6
Posterior interosseous nerve
 Radial 1 4.5 ± 0.4 83.1
 PIA 2 6.6 ± 0.6 75.1
 PIA 3 11.8 ± 0.3 55.2
PIA, posterior interosseous artery.

Table 6.  Upper Extremity Nerve Perforasomes The proximal 5 percent of the posterior interos-
seous nerve demonstrated limited dye staining
Area of Perfusion
of Forearm/ Total Amount at the radial tunnel. There was no staining of the
Perfusing Artery Arm (%) of Perfusion (%) posterior interosseous nerve by selective cannula-
Median nerve tion and dye injection of the radial artery. Distally,
 Radial 10–70 (forearm) 60 35 percent of the posterior interosseous nerve
 Brachial −5–100 (arm) 105 demonstrated limited dye staining.
Ulnar nerve
 Ulnar 5–75 (forearm) 70
 IUCA −2–3 (arm) 5
 SUCA 3–100 (arm 97 DISCUSSION
Radial nerve Since Ian McGregor and Ian Jackson first
 Recurrent 97–100 (forearm) 3
 Profunda 0–100 (arm) 100 focused the world’s attention on cutaneous free
Posterior tissue transfer, there have been significant gains
interosseous nerve in the knowledge and science of vascular anat-
 PIA 5–65 60
Superficial radial nerve omy.12 This has critically increased the capacity for
 Radial 35–97 62 successful reconstruction of the integumentary.
IUCA, inferior ulnar collateral artery; SUCA, superior ulnar collat- However, despite advances in reconstructive sur-
eral artery; PIA, posterior interosseous artery.
gery, consistent, predictable success in peripheral
nerve injuries remains elusive.13
Radial Nerve It has been shown that an important compo-
The radial nerve proper was 100 percent nent of successful nerve recovery is the presence
stained by selective cannulation and dye injection of adequate blood flow.14,15 Much of this research
of the extrinsic neural perforators arising from stems from the early work on nerve grafts. It is
the profunda brachii artery in the upper arm. In established that nerve recovery requires an appro-
the forearm, the proximal 3 percent of the proper priate blood supply and that functional results are
nerve was stained by injection of the recurrent poor when nerve grafts are placed in a scarred
radial artery. At the origin of the superficial radial bed.16 When avascular grafts are placed in a recip-
nerve, dye injection of the radial artery stained 62 ient bed, they are revascularized by two means:
percent of the superficial radial nerve (Table 6 inosculation and centripetal revascularization.
and Fig. 3). The distal 38 percent of the superfi- Centripetal revascularization is the dominant
cial radial nerve demonstrated limited dye stain- means of revascularization, which emphasizes the
ing. Selective cannulation and dye injection of the importance of a well-vascularized recipient bed.17–
posterior interosseous artery resulted in staining 19
Vascularized nerve grafts were developed to
of 60 percent of the posterior interosseous nerve. provide a solution to scarred, poorly vascularized

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 Plastic and Reconstructive Surgery • December 2018

Fig. 3. Map of the perforasomes of the median, ulnar, and radial nerves. Yellow areas of the nerves had absent or limited staining.
Well-perfused areas are colored with their respective source vessel and amount of perfusion labeled.

recipient beds and central necrosis, which would
occur in large trunk grafts.20
Vascularized nerve grafting is based on the
source blood supply of the intrinsic nerve vas-
culature. Taylor and Ham reported on the first
successful free vascularized nerve graft in 1976.2
Lundborg described the intrinsic vasculariza-
tion of peripheral nerves by injecting nerves with
India ink and identifying large, longitudinal ves-
sels that segmentally supplied vasculature to fas-
cicles.21 However, vascularized nerve grafting has
proved to be difficult: it requires the availability
of a suitable autograft nerve. Also, the outcomes
have been found inferior to alternatives to nerve
grafting, such as free functional muscle transfer.22
Notably, there has been a decrease in studies
examining nerve vascularization. We hypothesize
that this is because many surgeons and investi-
gators feel that adequate knowledge has been
obtained. However, the poor performance of
vascularized nerve grafts suggests that although
nerves may be able to “survive” on a single longitu-
dinal source artery, it is insufficient for full recov-
ery and optimal function. In addition, despite our
knowledge, even recovery after decompression of
compressive neuropathy is not optimal. Lundborg
postulated that compression applied to nerves will
compress the intrinsic vasculature. He and others
demonstrated that compression to nerves results
in the closure of the endoneurial capillaries and
ischemia.23 This “vascular factor” was discussed
by Sunderland, who suggested a mechanism for
the development of epineural scar on the basis of
ischemia in compressive peripheral neuropathy.24
This study pursues a more detailed and com-
prehensive understanding of segmental extrinsic
peripheral nerve vascularity in the upper extrem-
ity. Our findings demonstrate that peripheral
nerves can be divided into “neural perforasomes,”
or vascular territories. Each neural perforasome
carries a discrete perfusion pattern. The extrinsic
perfusion of peripheral nerves is highly segmental,
with areas of diminished perfusion that notably
correspond to the sites of compression of periph-
eral nerves (Fig. 3): carpal tunnel and pronator
teres for the median nerve, supinator/radial tun-
nel for the posterior interosseous nerve, and the
Guyon canal and the cubital tunnel for the ulnar
nerve. Our data corroborate earlier investigations
that suggest chronic compression neuropathies
may be related to nerve ischemia.25–27 Building on
the foundation established by Lundborg that the
intrinsic vasculature of nerves is compromised in
compressive states, this study suggests the sites of

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 Volume 142, Number 6 • Upper Extremity Neural Perforasomes

common compression neuropathies are poten-
tially predisposed to significant ischemia based
on their lack of extrinsic vascularization. Further
study is warranted to investigate this correlation.
Recently, Taylor published his group’s findings
relating to the angiosome territories of the upper
extremity nerves and classified the ulnar, median,
and radial nerves.8 Using our neural perfusion
data, we have reclassified each of the nerves to
reflect a more physiologic state of extrinsic vascu-
larization (Fig. 4). In Taylor’s classification, type A
is the best and type E is the worst for microvascular
free transfer. Type A is an unbranched nerve that
is supplied segmentally by a parallel vessel. Type B
is similar to A, but the nerve has branches. Type
C has a long vessel that courses the epineurium of
an unbranched nerve. In types D and E, the nerve
has a fragmented blood supply or many branches.
We have found that in the upper arm, each nerve
was a type A. This trend continued in the forearm,
with the most variability existing about the elbow.
Limitations of this study are inherent in all
cadaver studies. Cadaveric specimens, through
the storage and preparation processes, may lose
some of their in vivo characteristics, thus render-
ing absolute measurements less accurate. Another
limitation may be difficulty in accounting for ana-
tomical variation. Lastly, the injection pressure
may have influenced what did or did not stain.
Our red lead oxide injections were performed
to stain the perforators of the skin. At this pres-
sure, we believe it sufficient to stain the nerves.
For the ink-based injections, it is certainly pos-
sible that our injection pressure was insufficient.
However, the consistency with which areas did not
stain challenge this notion. Also, the hands were
consistently stained, demonstrating adequate per-
fusion pressure. Moreover, our findings validate
prior anatomical studies.8,28
Unlike the integumentary system, few studies
have attempted to examine and quantitate the
contribution of the extrinsic vascular supply to
peripheral nerves.8,28 In part, this is likely attrib-
utable to the disappointing evidence regarding
vascularized nerve grafts, and the relative rarity
of occasions on which to perform a vascularized
nerve graft.29 However, our findings supersede the
topic of vascularized nerve grafting; rather, they
add to the knowledge of the correlation between
hypoperfusion and compression neuropathies,
first proffered by Sunderland and Lundborg.
We offer a theory for why particular portions of

Fig. 4. Simplified diagram illustrating the Taylor classification of the

ulnar, median, and radial nerves modified based on the neural perfora-
somes. The nerves are classified as types A to E according to their suit-
ability for vascularized transfer.

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Copyright © 2018 American Society of Plastic Surgeons. Unauthorized reproduction of this article is prohibited.
 Plastic and Reconstructive Surgery • December 2018
upper extremity nerves more commonly develop
compression neuropathy: these watershed sites lie
12. McGregor IA, Jackson IT. The groin flap. Br J Plast Surg.
between neural perforasomes and are thus vul-
nerable to hypoperfusion and at risk for ischemia.
Steven M. Koehler, M.D.
Department of Orthopaedic Surgery
SUNY Downstate Medical Center
450 Clarkson Avenue, MSC 30
Brooklyn, N.Y. 11203
steven.koehler@downstate.edu
ACKNOWLEDGMENTS
This research was supported by the American Foun-
dation for Surgery of the Hand and the Piedmont Ortho-
paedic Foundation.
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