angiosome territories of the nerves of the upper limbs

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HAND/PERIPHERAL NERVE Angiosome Territories of the Nerves of the Upper Limbs Matthew K.-H. Hong, B.Med.Sc. Michael K.-Y. Hong, B.Med.Sc. G. Ian Taylor, M.D. Parkville, Victoria, Australia Background: The use of free vascularized nerve grafts requires intimate knowl- edge of the blood supply of peripheral nerves. The authors aimed to demon- strate radiographically the topography of the upper limb nerves with their blood supply, and to examine them as an application of the angiosome concept. An angiosome is a three-dimensional block of composite tissue supplied by a single source artery. Methods: This anatomical study involved the meticulous dissection of four fresh upper limb specimens injected intraarterially with a gelatin–lead oxide mixture. The nerves were tagged circumferentially with copper wire and radiographs were taken of the nerves with their arterial blood supply. The median, ulnar, radial, musculocutaneous, and axillary nerves were examined. Results: The authors showed that the nerves of the upper limb were supplied segmentally by source vessels, which reinforced the angiosome concept. The suitability of each nerve for harvest in free vascularized nerve transfer was assessed according to its pattern of blood supply. Conclusions: The authors’ work has a wide range of clinical applications and provides an anatomical basis for neurovascular and neurocutaneous flaps and free vascularized nerve grafting. (Plast. Reconstr. Surg. 118: 148, 2006.) T he blood supply of the peripheral nerves has been well studied over the centuries. Earlier works occurred when interest in the peripheral nervous system was dominated by processes of nerve degeneration and regenera- tion. Later, the overflow of complicated nerve injuries from the two world wars demanded a reappraisal of the blood supply in the context of nerve injury and repair. Significant advances were made in our understanding of the topog- raphy and morphology of the minute vasa ner- vorum by the work of Sir Sydney Sunderland. 1–3 He concluded that although the precise loca- tions of the vasa nervorum were mostly highly variable, any artery favorably placed to do so would send branches to the nerve. He added that these source arteries were reasonably con- stant, given that the gross neurovascular relation- ships of the upper limb are reasonably constant. The introduction of the “free vascularized nerve graft” by Taylor and Ham in 1976 4 prompted further study of the blood supply of peripheral nerves. This technique has been re- served for exceptional cases of nerve injury when (1) the recipient bed is heavily scarred as a result of ischemia or previous radiotherapy; (2) the defect is exceptionally large; and (3) the distant transfer of a thick nerve is desired. To aid in the description of donor nerves, Taylor developed a system that classified peripheral nerves accord- ing to their blood supply, with special reference to their suitability for microvascular free transfer (Fig. 1). 5,6 In 1987, Taylor and Palmer introduced the angiosome concept, whereby the body is consid- ered to consist of three-dimensional blocks of tissue supplied by particular source arteries. 7 From their study of the relationship of vessels to nerves, they noted that “the vessels hitchhiked with the nerves.” Their observation led to the expectation that peripheral nerves would also be supplied segmentally by source arteries. More recently, Taylor’s group reexamined the blood supply of each lower limb nerve and as- sessed the potential of each segment of each nerve for vascularized transfer. 8 They demon- strated the nerves with their blood supply radio- graphically and applied the angiosome concept to the nerves, providing the anatomical basis not From the Jack Brockhoff Reconstructive Plastic Surgery Re- search Unit, Department of Anatomy and Cell Biology, Uni- versity of Melbourne. Received for publication August 28, 2005; accepted Decem- ber 29, 2005. Copyright ©2006 by the American Society of Plastic Surgeons DOI: 10.1097/01.prs.0000221075.91038.08 www.PRSJournal.com 148

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Angiosome Territories of the Nerves of the Upper Limbs

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HAND/PERIPHERAL NERVE

Angiosome Territories of the Nerves of theUpper Limbs

Matthew K.-H. Hong,B.Med.Sc.

Michael K.-Y. Hong,B.Med.Sc.

G. Ian Taylor, M.D.

Parkville, Victoria, Australia

Background: The use of free vascularized nerve grafts requires intimate knowl-edge of the blood supply of peripheral nerves. The authors aimed to demon-strate radiographically the topography of the upper limb nerves with their bloodsupply, and to examine them as an application of the angiosome concept. Anangiosome is a three-dimensional block of composite tissue supplied by a singlesource artery.Methods: This anatomical study involved the meticulous dissection of four freshupper limb specimens injected intraarterially with a gelatin–lead oxide mixture.The nerves were tagged circumferentially with copper wire and radiographswere taken of the nerves with their arterial blood supply. The median, ulnar,radial, musculocutaneous, and axillary nerves were examined.Results: The authors showed that the nerves of the upper limb were suppliedsegmentally by source vessels, which reinforced the angiosome concept. Thesuitability of each nerve for harvest in free vascularized nerve transfer wasassessed according to its pattern of blood supply.Conclusions: The authors’ work has a wide range of clinical applications andprovides an anatomical basis for neurovascular and neurocutaneous flaps andfree vascularized nerve grafting. (Plast. Reconstr. Surg. 118: 148, 2006.)

The blood supply of the peripheral nerveshas been well studied over the centuries.Earlier works occurred when interest in the

peripheral nervous system was dominated byprocesses of nerve degeneration and regenera-tion. Later, the overflow of complicated nerveinjuries from the two world wars demanded areappraisal of the blood supply in the context ofnerve injury and repair. Significant advanceswere made in our understanding of the topog-raphy and morphology of the minute vasa ner-vorum by the work of Sir Sydney Sunderland.1–3

He concluded that although the precise loca-tions of the vasa nervorum were mostly highlyvariable, any artery favorably placed to do sowould send branches to the nerve. He addedthat these source arteries were reasonably con-stant, given that the gross neurovascular relation-ships of the upper limb are reasonably constant.

The introduction of the “free vascularizednerve graft” by Taylor and Ham in 19764

prompted further study of the blood supply ofperipheral nerves. This technique has been re-served for exceptional cases of nerve injury when(1) the recipient bed is heavily scarred as a resultof ischemia or previous radiotherapy; (2) thedefect is exceptionally large; and (3) the distanttransfer of a thick nerve is desired. To aid in thedescription of donor nerves, Taylor developed asystem that classified peripheral nerves accord-ing to their blood supply, with special referenceto their suitability for microvascular free transfer(Fig. 1).5,6

In 1987, Taylor and Palmer introduced theangiosome concept, whereby the body is consid-ered to consist of three-dimensional blocks oftissue supplied by particular source arteries.7From their study of the relationship of vessels tonerves, they noted that “the vessels hitchhikedwith the nerves.” Their observation led to theexpectation that peripheral nerves would also besupplied segmentally by source arteries.

More recently, Taylor’s group reexamined theblood supply of each lower limb nerve and as-sessed the potential of each segment of eachnerve for vascularized transfer.8 They demon-strated the nerves with their blood supply radio-graphically and applied the angiosome conceptto the nerves, providing the anatomical basis not

From the Jack Brockhoff Reconstructive Plastic Surgery Re-search Unit, Department of Anatomy and Cell Biology, Uni-versity of Melbourne.Received for publication August 28, 2005; accepted Decem-ber 29, 2005.Copyright ©2006 by the American Society of Plastic Surgeons

DOI: 10.1097/01.prs.0000221075.91038.08

www.PRSJournal.com148

only for vascularized nerve grafts from the re-gion but also virtually any composite tissue freeflap that might include a vascularized nerve. It isthe intention of this present study to perform asimilar assessment of the upper limb nerves.

MATERIALS AND METHODSFour upper limb specimens from three fresh

cadavers were used in this study. Although a seriesof 20 specimens would have been ideal, the num-ber of specimens studied was severely restricted bythe availability of fresh cadavers suitable for totalbody perfusion, the requirement for adequateperfusion, and the extensive work required to dis-sect each specimen fully. The first and secondauthors performed the dissections, and the seniorauthor assessed progress regularly. In each ca-daver, total body perfusion of the arterial systemwas performed with a gelatin–lead oxide mixturemade up according to the protocol described byRees and Taylor in 1986.9 The upper limbs weredisarticulated and the skin was carefully removed.The radial, axillary, musculocutaneous, median,and ulnar nerves were exposed with their sourcevessels and meticulously dissected to their termi-nal muscles or cutaneous branches. The nerves

were tagged circumferentially with fine electricalcopper wiring at 3-mm intervals along their entirelength. The wire allowed the outline of the nervesto be identified on radiographs and would allowsimultaneous demonstration of nerves andvessels.8 With minimal disruption to the tissuesaround the nerves, the bones were removed toenable radiography of the injected vessels andtagged nerves without bone shadows (Fig. 2). Themuscles were then removed and a dissecting mi-croscope used to meticulously dissect and exam-ine the fine vasa nervorum.

Photographs were taken through the micro-scope to document these tiny vessels along theentire length of each nerve. Radiographs weretaken at each stage of dissection for all specimens.Every radiograph was reviewed and, by consensusof all authors, those radiographs considered todemonstrate the extrinsic blood supply of indi-vidual nerves most representatively were digitallytraced to produce schematic diagrams of thenerves with their blood supply. Similarly, conclu-sions about the general nature of the topographyof the extrinsic blood supply of the upper limbnerves were drawn from observations made of theradiographs and photographs across the speci-

Fig. 1. Classification of peripheral nerves according to their suitability for microvascular free trans-fer, with type A being the best and type E being the worst. Type A indicates an unbranched nervesupplied segmentally by a vessel in parallel; type B is similar but the nerve has branches. Type C hasa long vessel coursing in the epineurium of an unbranched nerve. In types D and E, the nerve has afragmented blood supply or many branches. Reprinted with permission from Taylor, G. I. Free vas-cularized nerve transfer in the upper extremity. Hand Clin. 15: 673, 1999.

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mens, again by general consensus. This includedclassification of the neuronal vascular supply ac-cording to the five categories devised by Taylor.5,6

Review of the radiographs before and after dis-section allowed us to apply the angiosome conceptto the upper limb nerves.

RESULTSPrevious work on the neurovascular relation-

ships in the skin10 showed the inductive effectnerves have on nearby blood vessels, and our in-vestigations confirmed this in the deep tissues.Two observations about the arterial supply of up-per limb nerves are worthy of mention.

First, an epineurial longitudinal arterial sys-tem accompanies each peripheral nerve and mayhave “choke zones” and true anastomoses betweenlong ascending and descending branches of Y-shaped arteriae nervorum. Furthermore, branch-

ing of this system matches the branching of thenerve. Sometimes, the arterial branches are re-current and opposite in direction to the nervebranching. Interestingly, these vascular branchpatterns often reflect the choke zones betweenconsecutive angiosomes (Figs. 3 through 5).

Second, nerves unaccompanied by prominentvessels receive important supply from muscles.Where a nerve is closely related to a muscle, it mayreceive small branches from the vessels within thatmuscle. This occurs even where large nutrient ar-teries exist nearby, with tiny vessels connecting thelongitudinal anastomotic system of the nerve andthe vasculature in the muscle. For example, de-spite the presence of a median artery, the vasanervorum of the median nerve appears to freelyshare arterial connections with the vascular net-work within the flexor digitorum superficialis mus-cle. These vessels from within a muscle are espe-

Fig. 2. Dissected specimen of the median and ulnar nerves with their blood supply (left). Radio-graphs were taken (center) with the nerves being delineated by circumferential copper wires (right).An arterial lead oxide injection has allowed the arteries to be demonstrated simultaneously.

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cially important when no major arteries are inclose accompaniment with a nerve. Of note is themusculocutaneous nerve, which may directly re-ceive a large artery from within the biceps muscle.In general, nerve branches to muscles are suppliedby vessels traveling retrogradely from within themuscles.

Median NerveThe median nerve is supplied consecutively by

the brachial, ulnar, and radial angiosomes, andthen the ulnar angiosome again. In the arm, themedian nerve has a type A pattern of blood supply.It is characterized by well-developed longitudinalarterial channels on its surface and receives

branches directly from the brachial artery or frombranches to nearby muscles such as the brachialis.In the cubital and proximal forearm regions, themedian nerve is type E. After the inferior ulnarcollateral artery nourishes it, the median nervebranches extensively and its blood supply is frag-mented with nutrient vessels from second- andthird-order arterial branches. Nerve branches tothe pronator teres and flexor carpi radialis aresupplied by twigs from the anastomotic system

Fig. 3. Fine radiograph and corresponding schematic diagramof the median nerve from the upper arm to the wrist demonstrat-ing the main features of the longitudinal arterial system of a pe-ripheral nerve. The system traverses the entire length of thenerve, and includes (1) choke anastomosis, (2) true anastomosisbetween adjacent nutrient vessels, (3) branch point of nerve, and(4) segmental supply of the median artery to the median nerve.

Fig. 4. Magnified view of the longitudinal arterial system of thesuperficial radial nerve showing a long recurrent branch. The ar-tery is colored by a lead oxide injection.

Fig. 5. The ulnar nerve with circumferential copper wires beforeradiography. A typical Y-shaped arteriae nervorum supplies thenerve from the adjacent superior ulnar collateral artery.

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between the inferior ulnar collateral and recur-rent ulnar arteries.

In the forearm, the median nerve is a type Cnerve, as it may have a well-developed medianartery on its surface feeding branches to the nervesegmentally. The nerve branches to the flexordigitorum superficialis and the median nerve inthe immediate vicinity are supplied by vessels fromthe proximal arterial pedicle of the muscle, whichmay give rise to the median artery. As the nerveprogresses down the forearm, the median arteryoccasionally sends branches to the overlying flexordigitorum superficialis muscle and forms an anas-tomotic network with the vasculature within thismuscle. The median nerve is supplied by longbranches directly from the radial artery as thenerve leaves the cover of the flexor digitorumsuperficialis. Notably, at the level of the proximalborder of the pronator quadratus, a large, prom-inent direct branch from the radial artery maysupply the nerve. A branch of this vessel may sup-ply the distal portion of the flexor pollicis longus.

Beyond this, the blood supply becomes frag-mented again and the median nerve gains a typeE pattern. In the carpal tunnel, the median nervereceives no branches, but as it exits, it receives longretrograde vessels from the superficial palmararch. The common digital nerves and branches tothe muscles of the thenar eminence are accom-panied also by arterial branches from the super-ficial arch (Fig. 6).

The anterior interosseous nerve originatesfrom between the two heads of the pronator teresand dives deep to run anterior to the interosseousmembrane. It has a type A pattern overall as itreceives supply from the intimately related ante-rior interosseous artery.

Ulnar NerveThe ulnar nerve is supplied by the brachial

and the ulnar angiosomes. The deep branch in thehand appears to be supplied by the radial angio-some. In the arm, the ulnar nerve is type C as itcourses distally with the superior ulnar collateralartery on its surface. In the posterior compartmentof the arm, the ulnar nerve receives some vesselsfrom within the long head of the triceps muscle(seen in all specimens).

Around the elbow, the blood supply becomessomewhat fragmented, with a type E pattern. As itpasses behind the medial epicondyle, the ulnarnerve is nourished by the anastomotic systemformed by the superior ulnar collateral and pos-terior ulnar recurrent arteries. Arterial branches

from the ulnar artery destined for nearby musclescontribute to the fragmented blood supply of thenerve as they cross it. In the forearm, the ulnarnerve receives a type A supply as it accompaniesthe ulnar artery, receiving many characteristic Y-shaped arteriae nervorum.

In the hand, the ulnar nerve has a type E bloodsupply pattern again. At first, the nerve is met bylong “retrograde” branches from the superficialpalmar arch. From then on, the ulnar nerve andits branches receive a fragmented and complexblood supply, with contributions from both super-ficial and deep palmar arches (Fig. 6).

Radial NerveThe radial nerve is supplied by the brachial,

profunda brachii, and radial angiosomes. The pos-terior interosseous nerve begins in the radial an-giosome and is then supplied by the posteriorinterosseous artery and finally by the anterior in-terosseous artery.

Throughout most of its course, the radialnerve is characterized by early and prolific branch-ing. It first receives supply from the axillary arteryand then the brachial artery. The nerve wrapsaround the humerus posteriorly in the spiralgroove, intimately related to the profunda brachii.Here, the nerve is type B, and the extensivebranching of the nerve before and in the spiralgroove results in branches from the profundabrachii supplying several nerve trunks simulta-neously. Despite this branching, the radial collat-eral branch of the profunda brachii gains intimaterelation to the radial nerve and eventually appearsto be part of the longitudinal arterial system on thenerve, making the nerve segment type C as it de-scends to the elbow. The middle collateral branchof the profunda brachii artery accompanies thebranches to the medial head of the triceps andanconeus, and the lower lateral brachial cutane-ous nerve pierces the deep fascia in company withan arterial perforator.

Around the elbow, the radial nerve gains a typeE pattern as it branches extensively and receives afragmented blood supply. The nerve is accompa-nied and nourished by the radial collateral branchof the profunda brachii artery and the anastomosiswith the radial recurrent artery. The latter vesselfrom the radial artery runs along the nerve prox-imally, sending Y-shaped branches to it and thenerve branches to the brachioradialis, extensorcarpi radialis longus, and brachialis. The radialnerve continues to receive supply from the radialrecurrent artery as it divides into its terminal

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branches, the superficial radial and posterior in-terosseous nerves.

The posterior interosseous nerve is predomi-nantly a type E nerve. As it exits from between thetwo heads of supinator, the nerve showers into a

multitude of branches and gains a loose associa-tion with the posterior interosseous artery beforeslipping deep to the extensor pollicis longus. Anerve branch to the extensor indicis may continuewith the artery (one specimen).

Fig. 6. Diagram of the blood supply of the median and ulnar nerves (left) traced from the radiograph in Figure 2. The radial nerve (right)and its blood supply have been traced from similar radiographs. The arteries (center) are colored to demonstrate the angiosomes.

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Distally, the posterior interosseous nerve andits terminal branches are met by vessels from theanterior interosseous artery penetrating posteri-orly through the interosseous membrane. The an-terior interosseous artery turns dorsally to meetand accompany the terminal portion of the pos-terior interosseous nerve, which it now suppliesdirectly to give a type A pattern of blood supply.

In contrast, the superficial radial nerve is atype A nerve. It gains a close relationship with theradial artery early and receives many short, directvasa nervorum. As it begins to move away from theradial artery, the superficial radial nerve gains avascular pedicle that accompanies the nerve dis-tally into the hand for a considerable distance(Fig. 6).

Musculocutaneous NerveThe musculocutaneous nerve runs entirely in

the brachial angiosome. It continues as the lateralantebrachial cutaneous nerve in the radial angio-some. The musculocutaneous nerve receives afragmented blood supply for its entire length andis therefore predominantly type E. Near its originin the brachial plexus, the musculocutaneousnerve receives branches from the axillary artery.From then on, in the absence of a close accom-panying axial artery, this nerve relies on direct vasanervorum from the vascular pedicles of the cora-cobrachialis, biceps, and brachialis. The longitu-dinal system also receives contributions by retro-grade vessels arising from the vasculature withinthe muscles and running back along the nervebranches. More distally, the musculocutaneousnerve gains a close relationship with the bicepsmuscle and is nourished by vessels that arise fromwithin the muscle. These vessels may be relativelylarge should the proximal blood supply to thenerve prove meager. The rest of the nerve is sus-tained by its intrinsic system reinforced at irreg-ular intervals by small vessels arising from net-works in the surrounding connective tissue.

The lateral antebrachial cutaneous nerve isthe continuation of the musculocutaneous nerve,and more proximally is a type D nerve. It becomesclosely related to the cephalic vein and receivesarterial supply from the small chain-linked systemsof the superficial fascia, which are in turn suppliedby the radial artery (Fig. 7).

Axillary NerveThe axillary nerve originates in the brachial

angiosome but rapidly gains its supply from theposterior circumflex humeral angiosome. The

nerve is accompanied through the quadrangularspace by the posterior circumflex humeral artery.The association between nerve and artery hereappears to be looser than other nerve–artery re-lationships. As such, instead of short direct arte-riae nervorum from the posterior circumflex hu-meral artery, the axillary nerve receives long directvessels. It also receives indirect vessels by means ofthe surrounding connective tissue. Nevertheless,the nerve and artery become more intimately re-lated as they approach the deltoid. The branchingof the nerve and its blood supply result in a typeE nerve.

Of note is the close accompaniment of a mus-culocutaneous skin perforator from the posteriorcircumflex humeral artery with the upper lateralbrachial cutaneous nerve. The nerve–artery rela-tionship occurs throughout from within the del-toid muscle to the skin (Fig. 7).

Cutaneous NervesThe neurovascular relationships in the integ-

ument has been the subject of previous work.10

The authors found that the arterial relationshipwith the cutaneous nerves was obvious in the re-gion of the shoulder and palm of the hand,whereas veins dominated the picture in the arm,forearm, and dorsum of the hand. Our work ex-tends this to emphasize that when cutaneousnerves pierce the deep fascia accompanied by adedicated perforating artery, this artery wouldcontribute to a separate longitudinal epineurialvessel observed on the nerve. When closely relatedto a vein, the nerve would be followed by a chain-linked system of arteries that would segmentallysend short branches to the cutaneous nerve. Thesystem of arteries usually shared many connec-tions with the vasa vasorum around the adjacentsuperficial vein, and often sent branches to thesurrounding skin and superficial fascia. In addi-tion to a close venous relationship, a prominentcompanion artery would at times accompany anerve.

Indeed, the upper and lower lateral brachialcutaneous nerves are accompanied by dedicatedarteries, and the relationship is formed early,some distance before piercing the deep fascia.The medial brachial and medial, lateral, and pos-terior antebrachial nerves were accompanied bylarge veins and their tributaries and received ar-terial supply segmentally from a less conspicuouschain-linked system.

As a cutaneous nerve passes through differentvascular territories of the skin, it comes to be sup-

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plied by the same source vessels. The angiosomesof the cutaneous nerves match the angiosomes ofthe skin.

DISCUSSIONWe have radiographically demonstrated the

upper limb nerves with their arterial blood supplyand shown that the arteries supplying each nerveare derived from the source vessels of consecutiveangiosomes as the nerve crosses them. The angio-somes of the upper limb define the various tissuesthat can be combined together or raised sepa-rately on the various source arteries. As certainthick nerves with a vasculature suitable for vascu-larized nerve grafting may be available in raresituations, our study included all major nerves of

the upper limb. We traced the nerves with theirvessels from the deep tissues to the skin and wereable to determine the patterns of blood supply tothe various nerve segments according to Taylor’sclassification system (Fig. 8). We aimed to explorethe general patterns of the extrinsic blood supply,rather than count and tally the individual arteriaenervorum. This work was completed by Sunder-land, who aptly stated: “a study of the number ofvessels alone can give no true conception of theblood supply of a nerve.”11

Several general observations were made in re-gard to the arterial blood supply of the upper limbnerves. When an axial artery accompanies them,the nerves tend to be supplied with direct arteriaenervorum. In the absence of such an axial artery,

Fig. 7. Diagrams of the blood supply of the musculocutaneous (left) and axillary (right) nerves.

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nerves receive blood supply from either a smallerartery skirting the surface or a fragmented bloodsupply from second- and third-order arterialbranches. Around the elbow and proximal part ofthe forearm there is a tendency for the bloodsupply to fragment as nerves and arteries branchextensively to the numerous forearm muscles.

Previous work has demonstrated the variouspatterns of venous drainage of the peripheralnerves (Fig. 9).12 Perhaps of note is the strikingconsistency with which the arterial patterns aremirrored in the patterns of venous drainage tothese nerves. It is often said that the venous drain-age of nerves parallels the arterial supply.

In type A segments of nerves, the venae nervo-rum tend to drain to the periarterial venous plex-uses, whereas in type C segments there is drainage tovenae comitantes or a vein accompanying the arteryon the surface of the nerve. For example, in the arm,the superior ulnar collateral artery runs on the ulnarnerve together with the corresponding vein. In theforearm, the ulnar nerve is supplied directly by theulnar artery, and its venous drainage is to the peri-arterial venous plexus.

Around the elbow, the situation appears dif-ferent. Although on the arterial side the tendency

is for fragmentation, the venous drainage appearsto be directly to nearby veins. Cutaneous nervesare generally followed by a chain-linked system ofarteries, and their venous drainage is to aperivenous plexus around the usual accompany-ing vein.

Intrinsic Blood SupplySir Sydney Sunderland noted that the nature

of the intraneural vascular pattern appeared toprovide a blood supply “in excess of that requiredfor the exclusive needs of the supporting connec-tive tissue of peripheral nerves.”3 This would ex-plain the resilience of the neural blood supply togross interference. Indeed, Lundborg describedat a microscopic level the way vessels would openor close in response to vascular challenges andhow flow in individual vessels could rapidly changedirection.13

More recent investigations have focused onthe interaction between the intrinsic blood supplyand the extrinsic system. Breidenbach’s groupdemonstrated that a long length of nerve canmaintain its flow based only on its intrinsic bloodsupply.14 They also showed that even with reliance

Fig. 8. Simplified diagram illustrating blood supply to the upper limb nerves. The nerve segmentsare classified as types A to E according to their suitability for vascularized transfer. From left to right:ulnar, median, radial, musculocutaneous, and axillary nerves. Some branches have been omitted forclarity.

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on a single extrinsic vessel, a significant length ofnerve could be maintained. This would suggestthat a long free vascularized nerve segment wouldhave its intrinsic arterial system sufficiently sup-plied by its pedicle.

Another interesting point raised by the studywas the significant blood flow achieved by vesselsof the nerve branches. This appears to correspondwith our observation of the significant number ofvessels from the muscles supplying the nervebranches and traveling retrogradely back towardthe main nerve.

Studies by Best and colleagues have high-lighted the importance of inosculation as themechanism for the revascularization of small-di-ameter nerve grafts15 and the rapidity with whichthis occurs.16 Although it took 7 days for revascu-larization of a nerve graft from surrounding tis-sues, ingrowth of epineurial vessels from the prox-imal stump was observed after 2 days. Thesefindings suggest that small-diameter nerve graftsspontaneously revascularize and microvasculartechniques are unnecessary. However, the studiesexamined relatively short segments of nerve, andit is unclear whether the early inosculation aloneis sufficient to allow adequate perfusion of the

middle segments of longer nerve grafts. In addi-tion, the thicker peroneal nerve in the ewe in onestudy failed to vascularize well, suggesting a rolefor free vascularized nerve grafting.15 This high-lights well the fact that rather than to replaceconventional techniques, the free vascularizednerve graft was introduced for specific indications:where the nerve gap is large, the recipient bed isheavily scarred, or when the transfer or a thicknerve is desired. More studies comparing vascu-larized and nonvascularized nerve grafts are re-quired in a setting where there is considerablechallenge to the reestablishment of an adequateblood supply.

Free Vascularized Nerve GraftingThe free vascularized nerve graft was devel-

oped not to replace conventional nerve graftingtechniques but to provide an alternative operationand a potential solution to the problem of graftsurvival in exceptional circumstances. These in-clude situations where (1) the nerve gap is verylarge (e.g., a 20-cm defect in the median nerve ofthe forearm); (2) transfer of a thick nerve is de-sired, such as a median or ulnar nerve, which may

Fig. 9. Schematic diagram of venous drainage of (A) ulnar; (B) median; (C) radial; (D) sciatic; and (E)cutaneous nerves. Arrows designate the level of the elbow and knee. Compare this with the arterialsupply of the upper limb nerves in Figure 8. The lateral antebrachial cutaneous nerve, the contin-uation of the musculocutaneous nerve, is best compared with the cutaneous nerve. Reprinted withpermission from Del Pinal, F., and Taylor, G. I. The venous drainage of nerves: Anatomical study andclinical implications. Br. J. Plast. Surg. 43: 511, 1990.

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become available in an amputation stump5 or insome cases of brachial plexus injury17; and (3) therecipient bed is poor (e.g., a bony vascular bed, inareas of previous radiotherapy, or where there isextensive scarring).

In the search for donor sites, several systemshave been devised to classify the pattern of bloodsupply to peripheral nerves with regard to theirsuitability for free vascularized grafting. Most ap-pear to have been developed around only thosenerves seen as “potential” donors, as the assump-tion has been that the donor site is always com-pletely normal. In exceptional circumstances, do-nor nerves may become available withoutmorbidity. For example, an upper limb amputa-tion stump may yield the ulnar and median nervesof the arm as donors.5 To account for these situ-ations, each major nerve segment of the upperlimb must be assessed for its potential in vascu-larized nerve grafting.

Taylor’s system allows all peripheral nerves tobe classified and studied, some as potential donorsin special circumstances. Under this system, typeA and C patterns of blood supply indicate the mostideal donor nerves. Type A represents a nervesupplied segmentally by a long unbranching ar-tery, whereas type C is similar except the arterycourses on the surface of the nerve instead of inparallel. Type B is similar to type A, but the nervedivides early, and is suitable if the graft can bereversed.

Our study examined all the nerves of the up-per limb. According to our findings, we identifiedthe following nerves as suitable for microsurgicaltransfer, being of type A or C: (1) the ulnar nervein the upper arm and in the forearm; (2) themedian nerve in the upper arm and in the fore-arm; (3) the segment of anterior interosseousnerve distal to the flexor pollicis longus branch;(4) the upper lateral brachial nerve; (5) the lowerlateral brachial nerve; (6) the superficial radialnerve; (7) the terminal branch of posterior in-terosseous nerve; and (8) a branch to the extensorindicis following the posterior interosseous artery(when present).

In normal clinical situations, nerves 1 and 2cannot be used because of their functional im-portance. Harvest of nerve 3 results in lost func-tion of pronator quadratus, which may be accept-able. This leaves nerves 4 through 8 as donornerves for vascularized nerve transfer, and poten-tially nerve 3 in normal situations. It is notable thatmost of these are sensory or cutaneous nerves. Ourresults confirm the anatomical basis for the su-

perficial radial and ulnar nerves as vascularizednerve grafts.

The following donor sites have been identifiedpreviously for grafting: the superficial radial nervebased on the radial artery, the ulnar nerve basedon the superior ulnar collateral artery, the mediannerve based on the brachial artery,5 the sural nervebased on the superficial sural artery, the anteriortibial nerve based on the anterior tibial artery, thesuperficial peroneal nerve based on the peronealartery, the saphenous nerve based on the saphe-nous artery, the anterior interosseous nerve basedon the anterior interosseous artery, and the lateralbranch of the posterior interosseous nerve withthe posterior interosseous artery.18–20

The suitability of donor sites for free vascular-ized nerve grafts varies enormously with the de-mands of each clinical situation. For example,whereas the terminal portion of the posterior in-terosseous nerve lacks the length to bridge longnerve gaps, its length is adequate in most cases ofsingle digital nerve grafting. It may be possible toharvest this nerve segment with the distal portionof the anterior interosseous artery for simulta-neous reconstruction of both digital artery andnerve, which may occur in avulsion injuries of thethumb and fingers.19 In the event of a scarred orbony vascular bed, it is conceivable that some do-nor sites currently used in conventional free nervegrafts can yield a vascularized nerve graft (e.g., theanterior interosseous nerve transferred as a vas-cularized nerve graft with the anterior interosse-ous artery as the pedicle).

In clinical practice, the free vascularized nervegraft has led to good functional outcomes. Thesecases include large defects of the median nerverepaired with the free vascularized superficial ra-dial nerve, with follow-up as long as 23 years show-ing very good functional results.5 The free vascu-larized ulnar nerve based on the superior ulnarcollateral artery has also found a place in brachialplexus reconstruction.17 However, the techniqueof free vascularized nerve grafting is still reservedfor exceptional cases where conventional tech-niques are deemed insufficient.

Neurovascular FlapsKnowledge of the blood supply of the upper

limb nerves demonstrates the basis for many flapsalready in use. Mathes and Nahai present a myriadof musculocutaneous and fasciocutaneous flapsthat can be modified to make them sensate orfunctional.21 For example, the deltoid flap basedon the posterior deltoid subcutaneous artery can

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be a sensory flap based on the upper lateral bra-chial cutaneous nerve. The lateral arm flap has thelower lateral brachial cutaneous nerve in companywith the cutaneous perforator of the profundabrachii artery. In another example, the radial fore-arm flap, based on the radial artery, may includethe medial or lateral antebrachial nerves for sen-sation. In addition, the superficial radial nervemay be harvested as a vascularized nerve graft.21

Our observation that the nerves and skin are in thesame angiosomes supports the notion that nervesincorporated in these flaps are vascularized ontransfer. If a skin flap is based distally on a per-forating artery, and its longitudinal axis incorpo-rates one of the upper or lower lateral brachialnerves or the superficial radial nerve, it is likely tohave a superior blood supply. The detailed de-scription of the blood supply to the peripheralnerves of the upper limb suggests that there ispotential for refinements to be made to existingtechniques for local or free transfer of compositetissue.

Neurocutaneous FlapsSince the introduction of neurocutaneous

flaps,22,23 there has been much interest in theiranatomical basis, with many reports of flaps basedon the dorsal branch of the ulnar nerve and thesaphenous and sural nerves. It is well known thatarteries always accompany nerves and that the sur-rounding chain-linked arterial networks in thesubcutaneous tissue are oriented in the directionof nerves.10 Given the strength of the longitudinalarterial systems in and around a nerve, it is notsurprising that small- to medium-sized flaps canalmost be supported by these blood vessels alone.The flap relies on the chain-linked arterial systemsthat follow in the same direction as the nerve. Thereliability of the neural blood supply inherentlyallows the design of distally based neurocutaneousflaps. Gurunluoglu et al. have demonstrated theimportance of neural vessels in these flaps in rats.24

It is worth reemphasizing that the course ofthe nerve should provide the longitudinal axis ofa robust skin flap10 and that neurocutaneous flapsare a direct application of the concept. Nervesprovide a link between adjacent vascular territo-ries of arterial perforators by means of their con-tinuous longitudinal systems. The effectiveness ofthese connections led Sir Sydney Sunderland tostate that “The anastomoses, on and within thenerve, between nutrient arteries derived from dif-ferent and widely separated major arteries formthe basis for the development of collateral circu-

lations when the major arterial channel to a limbhas been interrupted.”25

Functional Muscle TransferFree vascularized muscle transfers taken with

their nerve branches to restore function have be-come increasingly popular. Our finding that ves-sels from within a muscle and the muscle’s vascularpedicle all supply its nerve branches illustrates thatthe particular nerve segment is already vascular-ized on transfer in this case.

Various free composite grafts that include vas-cularized nerves have also been described. Forexample, the radial nerve has been taken togetherwith the brachioradialis to provide a functionalmuscle in a free composite graft.5

Vascularized Nerve and Composite TissueAllotransplantation

The use of nerve autografts will always be lim-ited by the availability of suitable donor sites. Theprospect of allografting in reconstructive surgeryhas become more promising with recent advancesin immunosuppression therapy.26 When consid-ering nerve allotransplantation, both the nerveregeneration process and rejection response toallogeneic tissue must be considered. Mackinnonhas pioneered the technique of nerve allografting,with encouraging results.27

Vascularized nerve allografts offer several the-oretical advantages: (1) to allow en bloc recon-struction of nerve plexi; (2) to enhance nerveregeneration rate; and (3) to permit the use oflarger “trunk” grafts without the problem of cen-tral necrosis.28 Should they find their place in re-constructive surgery, our work has direct applica-tion to the selection of suitable donor sites.

Composite tissue allografts have also madetheir way into clinical practice,26 with the first hu-man hand transplant occurring in 1998.29 Virtuallyany combination of tissues, matched to the needsof the recipient, may be harvested. The angiosomeconcept finds its place here, as it allows the re-constructive surgeon to understand what tissues orparts of tissues, including nerves, can be taken incombination with others based on one or moresource vessels. Such an understanding of bloodsupply is important for the clinical success of theseflaps.

CONCLUSIONSOur work has radiographically depicted the

blood supply of the upper limb nerves and shownthem to have angiosome territories that match

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those of the surrounding composite tissues. Fur-thermore, we have classified each nerve segmentaccording to its suitability for vascularized nervetransfer, confirming the anatomical basis for do-nor sites already in use and showing other siteswhose availability depends on the prevailing clin-ical circumstances. This work has important clin-ical applications in the reconstruction of nerves ofthe upper limb.

G. Ian Taylor, M.D.Jack Brockhoff Reconstructive Plastic Surgery Research

UnitDepartment of Anatomy and Cell Biology

University of MelbourneParkville, Victoria 3010, Australia

[email protected]

ACKNOWLEDGMENTSThis work was supported in part by The Jack Brock-

hoff Foundation and The Colonial Foundation. Theauthors thank the staff of the Jack Brockhoff Reconstruc-tive Plastic Surgery Research Unit and in particular Dr.Hiroo Suami and Dr. Wei-Ren Pan for their invaluablesupport of this study. They are also indebted to the De-partment of Anatomy and Cell Biology of the Universityof Melbourne for their assistance.

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