COMPARISON OF DIFFERENT MANAGEMENTS OF LARGESUPERFICIAL VEINS IN DISTALLY BASED FASCIOCUTANEOUSFLAPS WITH A VENO-NEURO-ADIPOFASCIAL PEDICLE:AN EXPERIMENTAL STUDY USING A RABBIT MODEL

SHI-MIN CHANG, M.D., Ph.D.,* YU-DONG GU, M.D., AND

JI-FENG LI, M.D.

The role of large superficial veins in the survival of a distallybased fasciocutaneous flap with a veno-neuro-adipofascialpedicle was studied in a rabbit model. A sural veno-neuro-fasciocutaneous flap model (6 · 2 cm) with a distally basedlesser saphenous veno-neuro-adipofascial pedicle (1.5 cm)was established. Fifteen rabbits were randomly divided intothree groups with 10 flaps in each group. In group I, the distallesser saphenous vein was left open (venous inflow re-mained) after the flap was raised. In group II, the lessersaphenous vein was ligated in the pedicle (no venous inflow).In group III, the venous pedicle was left open in the pedicle,and the proximal end was microsurgically anastomosed tothe recipient vein (outflow established). Intravenous pres-sure, flap survival, and histology were examined. The resultsshowed that the values of intravenous pressure in group I

were significantly higher than in group II (P < 0.001). Themean flap survival rate of group III (94.5%) was significantlyhigher (P < 0.001) than of groups I (22.7%) and II (55.5%).Histology showed that the lesser saphenous vein in group Iwas extremely dilated and filled with thrombosis. This ex-periment demonstrated that establishing a superficial venousoutflow channel by anastomosis at the proximal end, or in-terrupting the inflow channel by ligation at the distal pedicle,may significantly improve the survival rate of distally basedveno-neuro-fasciocutaneous flaps.

ª 2003 Wiley-Liss, Inc.

MICROSURGERY 23:555–560 2003

Since the first description of neurocutaneous flaps byMasquelet et al.1 and Bertelli and Khoury2 in 1992,various distally based flaps with a wide veno-neuro-adipofascial pedicle have been used in various recon-structions of the distal portion of the upper and lowerextremities. Distally based flaps are not synonymouswith reverse-flow island flaps, although both have thesame advantages, including 1) the ability to be trans-ferred from a proximal donor site to a distal recipient, 2)the avoidance of hand or foot dependence, and 3) a one-stage rapid procedure which requires no microsurgicaltechnique.3 However, reverse-flow island flaps are sup-plied by nonphysiologic retrograde arterial inflow andvenous outflow through the deep vascular bundles, e.g.,the radial artery and its venae comitantes. Distally based

flaps are supplied by a more physiologic circulationthrough distal collateral vessels, such as the ascendingbranch of a dominant perforator, the recurrent branchof a direct cutaneous vessel, or the chain-linked vascularplexuses of the integument.4,5 If designed properly, dis-tally based flaps may also have physiologic orthogradevenous drainage because 1) valves in the partner as-cending or recurrent venous branches are directed pri-marily to their distal original stems, and 2) valvelessvenous plexuses of the integument serving as oscillatingchannels allow venous flow in any direction underpressure.6 However, there are many reports of postop-erative complications such as prolonged edema, partialnecrosis, and congestive total necrosis of the flap.7�10

The cause of these complications remains unknown.Extensive clinical applications of distally based veno-neuro-fasciocutaneous flaps without thorough experi-mental studies might be one of the reasons for the fre-quent complications.11,12 Because the large superficialveins in the extremities are disposed longitudinally,many distally based flaps must incorporate these largesuperficial veins, e.g., the cephalic and basilic vein in theforearm,3,13 and the great and lesser saphenous vein inthe lower leg.7�10,14,15 These large superficial veins aredirect flow channels of the hand and foot, and they areprovided with valves to prevent the reflux of venous

Department of Hand Surgery, Huashan Hospital, Fudan University MedicalCollege, Shanghai, People’s Republic of China

Grant sponsor: China Postdoctoral Science Fundation; Grant number:2002031176.

*Correspondence to: Shi-Min Chang, M.D., Ph.D., Department of Hand Sur-gery, Huashan Hospital, Fudan University Medical College, Shanghai200040, People’s Republic of China. E-mail: shiminchang@yahoo.com.cn

Received 3 March 2003;5 Accepted 17 July 2003

Published online in Wiley InterScience (www.interscience.wiley.com). DOI:10.1002/micr.10211

ª 2003 Wiley-Liss, Inc.

blood from proximal to distal.6 In distally based flaps,the proximal outflow channel is dissected and ligated.Therefore, the role of large superficial veins in distallybased flaps needs to be evaluated. Can they help venousdrainage and flap survival? What is the fate of theselarge superficial veins in distally based flaps? In thisexperimental study, we compared the distally basedveno-neuro-adipofascial flap with different patterns ofsuperficial venous pedicles to determine if changes intheir inflow or outflow correlate with flap survival.

MATERIALS AND METHODS

Fifteen New Zealand White rabbits with bodyweights of 2.5�3.0 kg were used. The animals were caredfor according to the university’s experimentation guide.Anesthesia consisted of intravenous pentobarbital 20mg/kg, supplemented as necessary. Both hindlimbs wereshaved and prepped with betadine solution. A venoustourniquet was applied to the hindlimb to delineate thelocation and direction of the lesser saphenous vein.

Flap Model

The lesser saphenous sural veno-neuro-adipofascialpedicled fasciocutaneous flap in New Zealand Whiterabbits was investigated anatomically before experi-mental study. The lesser saphenous vein and suralnerve are located in the posteriolateral aspect in thehindlimb at the popliteal fossa, with the vein lyinganterior to the nerve. In about 3-kg rabbits, the vesselis approximately 1.0�1.2 mm in diameter. No apparentartery was found to accompany the lesser saphenousvein. Initially, this veno-neural bundle passes betweenthe two heads of the gastrocnemius muscle and beneathits fascia. After exiting the gastrocnemius fascia, theveno-neural bundle becomes more superficial. At themidleg, the lesser saphenous vein divides into twobranches. The anterior one is larger, running downobliquely and anteriorly to the lateral malleolus, ter-minating in the dorsum of the paw. The posterior oneis a little smaller, running down straight and posteri-orly to the lateral malleolus, terminating in the plantarof the paw. The sural nerve divides in the same way toaccompany the vein. It is about 10 cm in length fromthe knee joint to the malleolus level. In retrograde in-jection of China ink, we found 5�6 valves in the mainstem and its anterior branch. The strongest valve islocated in the anterior branch before it joins the stem,which can prevent reflux under 60�100 cm H2O ret-rograde pressure. Ten flaps were used for retrogradevenographic study. Ten milliliters of 76% angiografinwere injected through the catheter retrogradely into the

lesser saphenous vein by manual pressure in 1 min. Theflap was x-ray-monitored for 1 h. An oblique fascio-cutaneous flap measuring 6.0 · 2.0 cm along the mainstem and its anterior branch of the lesser saphenousvein was designed in the midportion of the leg. Theveno-neuro-adipofascial pedicle was 1.5 cm in width.The length-to-width ratio was 4:1 (Fig. 1).

Experimental Design

The hindlimbs of animals were randomly allocatedinto three groups of distally based flaps with differentmanagements of the lesser saphenous vein. In group I (n= 10), a skin incision was made, but the lesser saph-enous vein was left intact (venous inflow) in the distalveno-neuro-adipofascial base. In group II (n = 10), thelesser saphenous vein was microsurgically divided andligated at 1 cm distal to the veno-neuro-adipofascialbase. In group III (n = 10), the lesser saphenous veinwas left intact in the distal base, but in the proximal end(flap tip) it was microsurgically anastomosed (venous

Figure 1. Outline of distally based lesser saphenous sural veno-

neuro-fasciocutaneous island flap in rabbit.

556 Chang et al.

flow-through). After the completion of each procedure,thin plastic sheeting was placed under the flaps andsutured in place with skin closure to avoid graft survival.A bolus of antibiotic was injected intramuscularly im-mediately after the operation. Preoperatively and post-operatively, the animals were maintained with routinelaboratory housing and feeding, and no attempt wasmade to immobilize the extremities.

Intravenous Pressure Measurement

In groups I and II, after flaps were elevated and thelesser saphenous vein was differently manipulated in thedistal base, a 4F catheter with heparin connected toSMUP-C Biological Signals (factory of Shanghai Med-ical University) in the other tip was introduced into theproximal end of the lesser saphenous vein. The pneu-matic tourniquet was then removed to allow bloodperfusion to the flap. Intravenous pressure was recordedat intervals of 5, 15, 30, and 60 min after tourniquetrelease. For avoidance of venous trauma, no measure-ment was applied for group III.

Assessment of Flap Survival

All flaps were observed daily. As the flap area had10�25% shrinkage after the operation, the percentage ofthe survival skin area of the flap was used as a com-parison among groups. They were determined byplanimetry 10 days after surgery.

Histological Examination

After survival rate assessment, the flaps near thedistal pedicle were harvested for routine histologicalexamination using hematoxylin-eosin (H&E) stain, withspecial reference to changes in the lesser saphenousvein.

Statistical Analysis

All values are reported as mean ± standard devia-tion. Student’s t-test was used for comparison amonggroups. The critical level of statistical significance was P< 0.05.

RESULTS

All animals survived the operation. Postoperatively,two flaps developed infection in groups 1 and 2, re-spectively. These two flaps were excluded from the finalanalysis.

Retrograde Venographic Results

Retrograde flow of contrast under manual pressurewas observed during monitoring (Fig. 2A). Aftermanual pressure withdrawal, no retrograde flow wasobserved. One hour later, the1 radiopaque were stillaccumulated at the proximal end of the lessersaphenous vein; some retrogradely entered the flap(Fig. 2B).

Hemodynamic Results

In group I, after the pneumatic tourniquet wasremoved, the lesser saphenous vein was gradually di-lated with the continuous blood filling from its distalend. The tightness of the venous wall became strongerand stronger with time (Fig. 3). The flaps became

Figure 2. A: Retrograde venography showed that reverse flow oc-

curred under pressure in lesser saphenous vein. B: After pressure

withdrawal, no retrograde flow was observed.4 Radiopaque were

accumulated at proximal end, and some retrogradely entered flap.

Large Superficial Veins in Distally Based Flaps 557

congested and developed cyanosis. The values of in-travenous pressure in group I at each time intervalwere significantly higher (P < 0.001) than in group II(Table 1).

Survival Rate of the Flap

In group I2 (distally based flap with intact inflowlarge vein), after release of the pneumatic, all flapsshowed immediate venous congestion with cyanoticbleeding from the flap skin margins in combinationwith progressive swelling of the flap. The lesser saph-enous vein was overdilated and full of blood, whichmade it clearly visible from the skin surface. In fourflaps, cyanosis and venous congestion resolved to someextent over 2�3 days, and only the partial flap nearthe distal base showed survival. The remaining fiveflaps were found to be completely necrosed in 3�5days. The average flap survival rate of group I was22.7 ± 24.9%. In group II (distally based flap withinterrupted inflow large vein), mild to moderate cya-nosis was observed in nine flaps. The lesser saphenousvein could be seen from the skin surface as it was fullof blood, but its diameter was normal. All flaps in thisgroup had partial to subtotal survival. The necrosedarea was located in the distal part of the flap. Themean survival rate of group II was 55.5 ± 9.4%. Ingroup III (distally based flap with flow-through largevein), all flaps showed normal blood circulation with ahealthy pink color. No cyanosis and venous congestionor edema was observed. Five flaps showed completesurvival, and five had distal tip necrosis. Averagesurvival was 94.5 ± 7.1% in this group. Statisticalanalysis revealed a significant difference between allgroups (Table 2).

Histological Findings

On histological examination, all flaps in group Ishowed extreme venous congestion. Thrombosis filledthe dilated venous cavity completely (Fig. 4). In groupII, as the lesser saphenous vein was ligated both proxi-mally and distally, venous thrombosis was smaller thanin group I. In group III, the lesser saphenous veins werecompetent, and no thrombosis was found.

DISCUSSION

Since the 1980s, the reverse-flow island flap anddistally based flaps have been commonly used forwound coverage and soft-tissue reconstruction for thedistal extremities. These are good flaps for the hand andwrist in the upper limb and the foot and ankle in thelower limb. However, distally based flaps are not syn-onymous with reverse-flow flaps. The circulatory char-acteristics of reverse-flow island flaps (e.g., radialforearm flap pedicled on the radial artery and its venaecomitantes), especially regarding the deep venous systemand retrograde venous drainage, were extensively in-vestigated both anatomically and physiologically.16�23

However, the superficial venous system, especially thelarge superficial vein and venous drainage in simpledistally based flaps (e.g., the distally based lesser saph-enous sural veno-neuro-fasciocutaneous flap), has re-ceived little attention.24�26

In normal extremities, venous outflow may be eitherthrough the superficial veins in the subcutaneous adi-pose tissue or through the deep venae comitantes. Bothof these vessels are provided with valves to direct venousreturn proximally. The superficial and deep venoussystems are connected with each other by perforating

Figure 3. Elevation of distally based veno-neuro-fasciocutaneous

island flap. Note that lesser saphenous vein (group I) was extremely

dilated due to continuous filling from its distal connection.

Figure 4. Histological view of distal pedicle in group I flap, showing

necrosis due to venous congestion. Note vein overfilled with throm-

bosis (H&E, x40).

558 Chang et al.

and communicating veins through the deep fascia.6 Interms of venous drainage of the flaps, the valves areorthograde in proximally based flaps, and proximallybased flaps have smooth drainage pathways. On theother hand, valves become retrograde in distally basedflaps, and that is a disadvantage for venous drainage. Atthe proximal end of distally based flaps, all vessels,whether arterial or venous, are dissected and ligated.Therefore, all venous outflow must theoretically bethrough the avalvular oscillating veins until they ulti-mately reach a perforator or communicator found in thedistal base of the flap; outflow then continues to thedeep system before orthograde return is reestablished.27

Large superficial veins of the extremities may havefour functions in distally based veno-neuro-fasciocuta-neous flaps. First, large superficial veins are direct re-turn channels of venous blood from the hand or foot. Ifthe large superficial veins were left in continuity to thedistal limb after flap elevation, they would conduct ve-nous blood from the hand or foot to the flap to causecongestion, increasing drainage load, and jeopardizingflap viability. In such circumstances, large superficialveins have a negative role in venous drainage for distallybased flaps.24,25 This was demonstrated by results of thecurrent experimental study. Venous pressures in group Iof continuous inflow 15 min later were above the normalarterial capillary pressure of humans (30 cm H2O).However, if the large superficial veins distal to the donorsite are already damaged, e.g., by the initial injury(which is common in clinical situation), this negativeeffect does not exist anymore, e.g., group II in our study.Second, large superficial veins are provided with strongvenous valves to prevent reflux from proximal to distal.Timmons17 proposed three criteria for immediate ve-nous retrograde flow through previously competentvalves, i.e., 1) higher venous pressure must be present

proximally in flow to the valve, 2) venous filling must bepresent proximal and distal to the valve, and 3) the ve-nous valve must be denervated. Unlike reverse-flow is-land flaps, the simple distally based veno-neuro-fasciocutaneous flap has no high arterial blood per-fusion. Therefore, higher venous pressure accumulationin the distal part of the flap cannot be achieved, and noreverse flow in the large superficial vein would occur,even if the valve were relatively regurgitant due to ex-treme venous wall distention (Fig. 2). Third, the vasavasorum of large superficial veins, located 10 mmaround the stem according to the anatomic study byNakajima et al. in the forearm and lower leg,28,29 willnot only nutrify the vessel wall, but also play an assist-ant role in feeding and draining the skin, as shown bythe radiographic perfusion study of Imanishi et al.26

Fourth, the venous blood in large superficial veins re-turned from the hand or foot still has approximately70% oxygen, which is sufficient to nourish a venous flap,provided an outflow channel is established (flow-through venous flap).30

Therefore, the final effect of large superficial veins indistally based veno-neuro-fasciocutaneous flaps is in-fluenced by many positive and negative factors. Fromthe current study, the most dangerous effect of the largesuperficial vein is continuous venous ingress to the flapwithout egress. Establishing an outflow channel of ve-nous blood by microsurgical anastomosis (group III) ina distally based flap is significantly superior to inter-rupting the inflow channel (group II), and both aresignificantly better than leaving it in continuity (groupI). However, finding a suitable vein clinically in the di-stal recipient site may be difficult, and applying amicrosurgical technique makes the flap lose its simpleand rapid advantage. In the clinic, a simple and effectivemethod to test the role of the large superficial vein is to

Table 1. Data of Intravenous Pressure Measurement

Intravenous pressure (mean ± SD) cmH2Oa

Groups 5 min 15 min 30 min 60 min

Group I (n = 10) 18.0 ± 3.5 37.6 ± 4.8 35.7 ± 5.4 31.9 ± 4.2Group II (n = 10) 9.1 ± 1.4 15.5 ± 2.3 19.9 ± 3.1 22.1 ± 3.1

aValues of intravenous pressure between groups I and II at each time interval were significantly different (Student’s t-test P < 0.001).

Table 2. Summary of Data From Flap Survival Study�

Groups Complete necrosis Partial survival Complete survival Mean survival rate (%) (mean ± SD)

Group I (n = 9) 5 4 22.7 ± 24.9Group II (n = 9) 9 55.5 ± 9.4*Group III (n = 10) 5 5 94.5 ± 7.1**

�Flap survival rate was significantly different among three groups by Student’s t-test.*P < 0.01.**P < 0.001.

Large Superficial Veins in Distally Based Flaps 559

release the pneumatic tourniquet after flap elevation. Byobserving flap color and palpating venous wall tight-ness, one can easily determine whether there is a nega-tive effect of the large superficial vein or not.31

Fortunately, most initial injuries to the hand or foot(especially the dorsum) also disrupt the large superficialveins, and venous congestion due to intact large super-ficial vein inflow is not common in practice. For ex-ample, we25 raised 34 distally based radial forearm veno-neuro-fasciocutaneous and adipofascial flaps for handreconstruction with preservation of the radial artery:only 5 cases showed a negative role of the superficialveins. These veins were all carefully ligated at 1�2 cmdistal to the adipofasical base, and the flaps survivedcompletely. Dissection and ligation should be closelyrestricted without disturbing the perivenous plexuses.

In conclusion, it is necessary in distally based flaps todistinguish whether large superficial veins conduct ve-nous blood from the distal limb to the flap to causecongestion and swelling. Establishing an outflow chan-nel by venous anastomosis at the proximal end, or in-terrupting the inflow channel by venous ligation at thedistal pedicle, may improve the survival rate of distallybased veno-neuro-fasciocutaneous flaps.

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