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Revascularization of a Specific Angiosome for Limb Salvage: Does the Target Artery Matter?
Revascularization of a Specific Angiosome for Limb Salvage: Does the Target Artery Matter? Richard F. Neville,1 Christopher E. Attinger,2 Erwin J. Bulan,2 Ivica Ducic,2 Michael Thomassen,2 and Anton N. Sidawy,3 Washington, D.C.
Ischemic wounds of the lower extremity can fail to heal despite successful revascularization. The foot can be divided into six anatomic regions (angiosomes) fed by distinct source arteries arising from the posterior tibial (three), anterior tibial (one), and peroneal (two) arteries. This study investigated whether bypass to the artery directly feeding the ischemic angiosome had an impact on wound healing and limb salvage. Retrospective analysis was performed for 52 nonhealing lower extremity wounds (48 patients) requiring tibial bypass over a 2-year period. Preoperative arteriograms were reviewed to determine arterial anatomy relative to each wound’s specific angiosome and bypass anatomy. Patients were divided into two groups; direct revascularization (DR, bypass to the artery directly feeding the ischemic angiosome) or indirect revascularization (IR, bypass unrelated to the ischemic angiosome). Wound outcome was analyzed with regard to the endpoints of complete healing, amputation, or death unrelated to the wound. Time to healing was also noted for healed wounds. Based on preoperative arteriography, 51% (n ¼ 27) of the wounds received DR to the ischemic angiosome, while 49% (n ¼ 25) underwent IR. There were no statistically significant differences in the comorbidities of the two groups. Revascularization was via tibial bypass using the saphenous vein (n ¼ 34, 65%) or polytetrafluoroethylene with a distal vein patch (n ¼ 18, 35%). Bypasses were performed to the anterior tibial (n ¼ 22, 42%), posterior tibial (n ¼ 17, 33%), or peroneal (n ¼ 13, 25%) arteries based on the surgeon’s judgment. One bypass failed in the perioperative period and was excluded from the analysis. The remaining bypasses were patent at the time of wound analysis. Due to a 17% mortality rate during follow-up, 43 wounds were available for endpoint analysis. This analysis demonstrated that 77% of wounds (n ¼ 33) progressed to complete healing and 23% of wounds (n ¼ 10) failed to heal with resultant amputation. In the DR group, there was 91% healing with a 9% amputation rate. In the IR group, there was 62% healing with a 38% amputation rate ( p ¼ 0.03). In those wounds that did heal, total time to healing was not significantly differentdDR 162.4 days versus IR 159.8 days ( p ¼ 0.95). Revascularization plays a crucial role in the treatment of ischemic lower extremity wounds. We believe that direct revascularization of the angiosome specific to the anatomy of the wound leads to a higher rate of healing and limb salvage. Although many factors must be considered in choosing the target artery for revascularization, consideration should be given to revascularization of the artery directly feeding the ischemic angiosome.
Presented at the Southern Association for Vascular Surgery meeting, Puerto Rico, January 18, 2007. 1
Department of Surgery, Division of Vascular Surgery, Georgetown University Hospital, Washington, D.C. 2
Department of Plastic Surgery, Georgetown University Hospital, Washington, D.C. 3 Department of Surgery, Georgetown University Hospital, and Surgery Service, VA Medical Center, Washington, D.C.
Correspondence to Richard F. Neville, MD, Division of Vascular Surgery, Georgetown University Hospital, 4PHC, 3800 Reservoir Road NW, Washington, D.C. 20007, E-mail: [email protected] Ann Vasc Surg 2009; 23: 367-373 DOI: 10.1016/j.avsg.2008.08.022 Ó Annals of Vascular Surgery Inc. Published online: January 29, 2009
INTRODUCTION Advances in distal lower extremity revascularization have revolutionized salvage of the ischemic limb. A committed effort to limb salvage requires an aggressive approach to revascularization that includes endovascular techniques, vein bypass, and prosthetic graft bypass with the consideration of adjuncts to improve graft performance such as autogenous venous tissue at the distal anastomoses or addition of a distal arteriovenous fistula.1-4 However, despite these advances, vascular bypass can 367
368 Neville et al.
fail to heal ischemic lower extremity wounds even if the patient underwent a successful revascularization procedure.5-17 Gooden et al.18 found that up to 25% of patients with heel ulcers ultimately underwent to a major lower extremity amputation despite a palpable pedal pulse. Part of the failure is due to inadequate treatment of the wound postoperatively.6 However, wounds may also fail to heal because of inadequate local revascularization due to inadequate vascular connections between the revascularized artery and the local ischemic area. We hypothesize that wound healing and limb salvage for ischemic wounds would be optimized by direct revascularization (DR) of the involved area of the foot. In 1987, Taylor and Palmer19,20 introduced the ‘‘angiosome’’ concept that divides the body into three-dimensional vascular territories supplied by specific source arteries and drained by specific veins. Taylor and Pan21 defined five distinct angiosomes of the lower leg as fed by the medial sural artery, the lateral sural artery, the posterior tibial artery, the peroneal artery, and the anterior tibial artery. The foot and ankle area has six distinct angiosomes arising from the posterior tibial artery (n ¼ 3), the anterior tibial artery (n ¼ 1), and the peroneal artery (n ¼ 2). The posterior tibial artery gives rise to a calcaneal branch that supplies the medial ankle and plantar heel, a medial planter branch that feeds the medial plantar instep, and a lateral plantar branch that supplies the lateral forefoot, plantar midfoot, and entire plantar forefoot (Fig. 1). The anterior tibial artery continues on to the dorsum of the foot as the dorsalis pedis (Fig. 2). The peroneal artery supplies the lateral ankle and plantar heel via the calcaneal branch and the anterior upper ankle via an anterior branch (Fig. 3). The literature states that bypassing to one distal artery is often sufficient to heal foot and ankle wounds. Choice of the target artery for bypass is determined by factors such as bypass length, availability of conduit, and quality of the recipient artery. We hypothesized that another consideration should be the arterial anatomy specific to the ischemic angiosome. For example, bypass to the dorsalis pedis artery for heel ulceration has led to 85% healing and limb salvage.5 However, there remains a 15% residual failure rate. It stands to reason that for the wound to heal, the new blood flow to the dorsalis pedis artery has to reach the heel in adequate amount to result in healing. If the arterial connections between the dorsal and plantar circulation are not adequate, the wound may not have as good a chance to heal. DR of either the posterior tibial or peroneal arteries, both of which have
Annals of Vascular Surgery
Fig. 1. Angiosomes of the foot arising from the posterior tibial artery (n ¼ 3): calcaneal branch, medial plantar branch, lateral plantar branch.
calcaneal branches directly supplying the plantar heel, may be more likely to heal a plantar heel wound than revascularization of the dorsalis pedis that relies on arterial-arterial connections through the pedal arch for the blood flow to reach the ischemic tissue.
METHODS We retrospectively reviewed the charts of 56 consecutive patients with tissue loss due to ischemia who required lower extremity vascular reconstruction for wound closure. Patient demographics included diabetes mellitus, chronic renal failure defined as serum creatinine greater than or equal to 1.8, hypertension, and history of symptomatic coronary artery disease manifest as angina or coronary surgical revascularization. All wounds were treated according to the established protocol at the Georgetown University Limb Center. The protocol includes an assessment of the wound and the existing vascular status including examination of pulses and vascular laboratory studies to assess healing potential. Revascularization was considered if this
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Fig. 3. Angiosomes of the foot arising from the peroneal artery (n ¼ 2): calcaneal branch, anterior perforating branch.
Fig. 2. Angiosome of the foot arising from the anterior tibial artery (n ¼ 1): dorsalis pedis.
evaluation indicated a decreased ability for healing manifest as a lack of pedal pulses, ankle-brachial index (ABI) less than 0.3, monophasic segmental waveforms, transcutaneous oxygen tension (TcO2) less than 25 mm Hg absolute value, or TcO2 index less than 0.4.22 Arterial imaging with arteriography was performed for all limbs in need of revascularization. Wounds were debrided prior to revascularization if there was wet gangrene or necrotizing fasciitis present. Following revascularization, wounds were serially debrided and treated with appropriate topical wound care until showing signs of healing such as new granulation tissue. These debridements were done in the Limb Center on a weekly basis until a clean bed of granulation tissue was obtained and then on a biweekly basis until healing occurred or amputation was performed. Wound measurements were made during these follow-up visits. This protocol was similar in both experimental groups. Adjuncts to promote healing, such as hyperbaric oxygen, administration of topical growth factors, and cultured skin, were added to the
topical wound care regimen at the discretion of the treating physicians in the Limb Center. If the wound failed to respond despite maximum therapy, then the limb was considered nonsalvageable and amputation was advocated. Preoperative arteriograms were reviewed for each limb, and wounds were categorized by location according to the primary angiosome. This included the posterior tibial artery (calcaneal, medial plantar, lateral plantar), dorsalis pedis, and peroneal artery (calcaneal, anterior perforator).21 Angiograms and operative reports were reviewed in a blinded fashion to delineate preoperative arterial anatomy, type of bypass, and location of the distal anastomosis. We defined two study groups based on bypass anatomy: DR and indirect revascularization (IR). DR, which involved direct bypass to the artery supplying the source vessel of the angiosome where the ulcer was locateddbypass to the anterior tibial artery for a dorsal foot ulcer, bypass to the peroneal artery for a lateral ankle ulcer, and bypass to the posterior tibial artery for an ulcer at the medial plantar instep. An ulcer on the plantar heel was considered in the direct group if the bypass was to the peroneal or posterior tibial artery. IR involved bypass to an artery unrelated to the ischemic angiosome. Comprehensive documentation of the wound care delivered in
370 Neville et al.
the Limb Center was reviewed to assess rate of healing and final clinical results for each wound. The clinical outcome was then categorized as healed, failure to heal leading to major amputation (below-the-knee or above-the-knee amputation), or death clinically unrelated to the wound. Outcome in all cases, whether healed or amputated, as well as time to complete healing were compared between the two study groups. In addition, the incidence of risk factors was compared between the two groups. Such risk factors included diabetes, hypertension, chronic renal failure, and coronary artery disease.
RESULTS Sixty wounds were reviewed in 56 consecutive patients. Eight patients were lost to follow-up, leaving a study cohort of 52 wounds for analysis. In the total group, 87% of the patients were diabetic, 52% were diagnosed with chronic renal failure, and 36% admitted to actively using tobacco. There were no statistically significant differences in the comorbidities of the two bypass groups (Table I). All bypasses were performed to tibial arteries. The target artery was the anterior tibial in 22 (42%), the posterior tibial in 17 (33%), and the peroneal in 13 (25%). The distal bypass was performed with translocated saphenous vein in 34 cases (65%), and polytetrafluoroethylene (PTFE) with a distal vein patch in 18 cases (35%).4 There was one bypass that failed in the perioperative period. This bypass was to the peroneal artery using PTFE with distal vein patch. Approximately one third of the wounds were closed by topical wound care. Ten required delayed primary closure or a split-thickness skin graft (7 DR and 3 IR). Local flaps were required in 21 patients (12 DR and 9 IR). These flaps included ray, transmetatarsal, and Chopart’s amputations. Two free flaps were used to obtain final wound closure (1 DR and 1 IR). Thirty-three of the 52 wounds (63.5%) progressed to complete healing. Ten (19.2%) wounds failed to heal and the patients went on to major amputation. Death unrelated to the wound prior to complete healing or failure to heal occurred in 9 (17.3%) patients. Detailed analysis of the remaining 43 patients with a complete wound care course was performed. Arteriograms were available for review to delineate preoperative vascular anatomy. These were then compared with the type of bypass performed. Based on preoperative arteriograms and operative reports, 22 (51%) of the bypasses were performed directly to the artery supplying the source artery of the ulcerated angiosome, while 21
Annals of Vascular Surgery
(49%) underwent IR (Fig. 4). Bypass anatomy in the groups was similardDR (11 anterior tibial, 6 posterior tibial, 5 peroneal) and IR (8 anterior tibial, 8 posterior tibial, 6 peroneal). Type of bypass was also without significant differencesdDR (14 translocated vein grafts, 8 distal vein patch grafts23) and IR (16 translocated vein grafts, 5 distal vein patch grafts). Comparing the mean time to complete healing, there was no statistically significant difference between wounds that had DR versus those that underwent IR (DR 162.4 days versus IR 159.8 days, p ¼ 0.95). However, there was a statistically significant difference (Fisher’s exact test, p ¼ 0.03) in complete wound healing rate when comparing DR (90.9% wound healing) versus those that were indirectly revascularized (61.9% wound healing) (Fig. 5). Follow-up intervals for healing were similar in the two groups at 100-day intervals. Healing occurred by 100 days in 2 (10%) DR and 1 (8%) IR group, at 100 to 200 days in 13 (65%) DR and 9 (69%) IR groups, and at greater than 200 days in 5 (25%) DR and 3 (23%) IR groups. As an observation, the major amputation rate was four times greater in the IR group (one above-the-knee, seven belowthe-knee) compared with the group in which DR was supplied to the wound (two below-the-knee) (Table II).
DISCUSSION Effective revascularization continues to be a major component in the treatment of ischemic lower extremity ulcers. Intuitively, providing direct blood flow to the specific area of an ischemic foot ulcer should be preferable to nonspecific revascularization with subsequent reliance on collateral vessels for healing. The concept of distinct vascular territories (i.e., angiosomes) of the foot and ankle provides an anatomic basis for analysis of this intuitive concept. This selective approach to revascularization of the ischemic foot and ankle relies on knowledge of the anatomy of these three-dimensional blocks of tissue supplied by ‘‘source’’ arteries. The posterior tibial artery supplies three vascular territories to the foot. After supplying the medial and medial-posterior ankle, the posterior tibial supplies blood flow to the medial and plantar heel via the calcaneal branch, to the plantar instep via the medial plantar artery, and to the lateral plantar midfoot and entire plantar forefoot via the lateral plantar artery. The distal peroneal supplies the lateral anterior upper ankle via the anterior perforating branch and the lateral and plantar heel via the calcaneal branch.
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Table I. Patient demographics Total
Direct*
Indirect*
Female Male
26 (46.4%) 30 (53.6%)
13 (48.1%) 14 (51.9%)
13 (44.8%) 16 (55.2%)
Diabetes Chronic renal failure Hypertension Coronary artery disease Active tobacco use
49 29 22 16 20
23 13 8 9 9
26 16 14 7 11
(87.5%) (51.8%) (39.3%) (28.6%) (35.7%)
(85.2%) (48.1%) (29.6%) (33.3%) (33.3%)
(89.7%) (55.2%) (48.3%) (24.1%) (37.9%)
*p ¼ NS.
Direct Revascularization
Revascularization of the ischemic angiosome
91%
9%
Indirect Revascularization 38%
62%
60 consecutive wounds
8 excluded, incomplete f/u
52 wounds 9 premature death
100 90 80 70 60 50 40 30 20 10 0 Direct (n=22)
43 wounds
22 directly revascularized
20 healed
2 failed
Complete healing
21 indirectly revascularized
13 healed
Indirect (n=21) Failed to heal
Fig. 5. Complete wound healing based on direct versus indirect revascularization for those 43 wounds with known outcome and follow-up. There was a statistically significant difference in complete healing rate with p ¼ 0.03 (Fisher’s exact test).
8 failed
Fig. 4. Patient cohort with follow-up based on type of revascularization.
The anterior tibial artery supplies the anterior ankle and then becomes the dorsalis pedis artery, supplying the dorsum of the foot. Our retrospective evaluation of revascularization based on the angiosome concept suggests that DR of the ischemic angiosome is more likely to result in successful healing and limb salvage than is IR. The corollary is that subsequent major amputation rate was also lower. This supports our initial hypothesis that it is preferable to provide direct antegrade blood flow to the anatomic area containing the wound than to rely on indirect flow via arterial-arterial connections of the vessels in the foot. An equally important aspect in the management of the ischemic wound is the quality of wound care. Many limbs successfully bypassed are lost due to overwhelming or uncontrollable infection. The attempt to prematurely close an infected wound will
lead to further tissue infection and necrosis. It has been shown that TcO2 around an ischemic wound raises slowly after vascular bypass and peaks at 24 weeks after revascularization.24 This indicates that maximal healing benefit from the renewed blood flow may not be fully realized for more than 1 week after revascularization. Aggressive early wound closure or definitive amputation may be disadvantageous. The wound should be carefully prepared and the soft tissue reconstruction delayed until all signs of inflammation and infection have resolved and the wound is showing initial signs of healing. In our practice, the time between revascularization and soft tissue reconstruction is often 24 weeks. The patient is often discharged after the revascularization and initial wound debridement with follow-up care delivered as an outpatient. The outpatient regimen consist of a wound care plan determined by the Limb Center physicians and carried out by visiting nurses with additional evaluation and treatment during frequent visits to the Limb Center. The status of the revascularization
372 Neville et al.
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Table II. Amputation rate for direct versus indirect revascularization
Complete healing Amputation Mortality
Total
Direct
Indirect
(N ¼ 43)
(n ¼ 22)
(n ¼ 21)
33 (63.5%) 10 (19.2%)
20 (90.9%)* 2 (9.1%)
13 (61.9%)* 8 (38.1%)
9 (17.3%)
3
6
*p ¼ 0.03.
is also assessed during these outpatient visits. Examination of appropriate pulses and Doppler signals are performed on each visit with formal Duplex graft surveillance at standard intervals: 3, 6, and 12 months. When the wound is deemed ready for closure, the patient returns to the hospital for final debridement and appropriate wound closure. This may take the form of primary closure after additional debridement, skin grafting, or local muscular flaps rotated into the wound. It is difficult to determine the functional quality of the arterial-arterial connections of the foot and ankle. Listening for antegrade and retrograde flow in the tibial arteries can be helpful, providing that the inflow is of sufficient volume to be evaluated by Doppler. Doppler signals in the dorsalis pedis can be evaluated with compression of the posterior tibial with reversal of the situation as well. The arteriogram does not always show these connections, especially in the setting of compromised arterial inflow. Certainly IR leads to wound healing. Therefore, if these connections exist and are adequate, then IR can be successful. This reflects the clinical experience that good rates of healing and limb salvage are reported with successful bypass regardless of consideration of angiosome anatomy. Berceli, Carsten and others have shown that limb loss can certainly occur despite a patent bypass graft.5,7 Berceli et al.5 report an 86% healing rate of heel lesions after dorsalis pedis bypass despite the lack of an intact pedal arch, which would be an IR according to the angiosome concept. However, these authors recognize the problematic nature of this situation and agree that healing is dependent on restoration of adequate local blood flow to the wound. In our series, 62% of the wounds were documented to have IR healed. We observed that if the arterial-arterial connections in the foot are clearly absent on arteriography and there is no arterial blush over the angiosome containing the ischemic ulcer, then the chances of healing may become more problematic. Our retrospective data suggest that, when the
vascular surgeon has a choice of target arteries for revascularization, preference should be given to the artery directly feeding the affected angiosome. However, if the only artery available does not provide direct flow to the affected angiosome, revascularization remains indicated even if arterial-arterial connections are not obviously present. In this setting, limb salvage may not be as high as that in which the DR is possible.
CONCLUSION Revascularization plays a crucial role in the treatment of ischemic lower extremity wounds. Based on our retrospective evaluation, we believe that DR of the angiosome specific to the anatomy of the nonhealing wound leads to a higher rate of healing and limb salvage. The quality of subsequent wound care is also a critical component in promoting healing and avoiding further tissue loss. Although many factors are involved in the choice of target artery for revascularization, consideration should be given to revascularization of the artery directly feeding the ischemic angiosome as an additional consideration in planning lower extremity revascularization. REFERENCES 1. Neville RF, Attinger C, Sidawy AN. Prosthetic bypass with a distal vein patch for limb salvage. Am J Surg 1997;174: 173. 2. Pappas PJ, Hobson RW, Meyers MG, Jamil Z, et al. Patency of infrainguinal polytetrafluoroethylene bypass grafts with distal interposition vein cuffs. Cardiovasc Surg 1998;6:19. 3. Kansal N, Pappas PJ, Gwertzman GA, Silva MB, Jr, et al. Patency and limb salvage for polytetrafluoroethylene bypasses with vein interposition cuffs. Ann Vasc Surg 1999;13:386. 4. Neville RF, Tempesta B, Sidawy AN. Tibial bypass for limb salvage using polytetrafluoroethylene and a distal vein patch. J Vasc Surg 2001;33:266. 5. Berceli SA, Chan AK, Pomposelli FB, et al. Efficacy of dorsal pedal artery bypass in limb salvage for ischemic heel ulcers. J Vasc Surg 1999;30:499.
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6. Treiman GS, Oderich GS, Ashrafi A, Schneider PA. Management of ischemic heel ulceration and gangrene: An evaluation of factors associated with successful healing. J Vasc Surg 2000;31:1110. 7. Carsten CG, III, Taylor SM, Langan EM, III, Crane MM. Factors associated with limb loss despite a patent infrainguinal bypass graft. Am Surg 1998;64:33. 8. Edwards JM, Taylor LM, Porter JM. Limb salvage in endstage renal disease (ESRD), comparison of modern results in patients with and without ESRD. Arch Surg 1998;123: 1164. 9. Chang BB, Paty PK, Shah DM, Kaufman JL, Leather RP. Results of infrainguinal bypass for limb salvage in patients with end-stage renal disease. Surgery 1990;108:742. 10. Karp NS, Kasabian AK, Siebert JW, et al. Microvascular freeflap salvage of the diabetic foot: A 5 year experience. Plast Reconstr Surg 1994;84:834. 11. Andros G, Harris RW, Dulawa LB, et al. The need for arteriography in diabetic patients with gangrene and palpable foot pulses. Arch Surg 1984;119:1260. 12. Johnson BL, Glickman MH, Bandyk DF, Esses GE. Failure of foot salvage in patients with end-stage renal disease after surgical revascularization. J Vasc Surg 1995;22:280. 13. Elliot BM, Robison JG, Brothers TE, Cross MA. Limitations of peroneal artery bypass grafting for limb salvage. J Vasc Surg 1993;18:881. 14. Bergamini TM, George SM, Massey HT, et al. Pedal or peroneal bypass: Which is better when both are patent? J Vasc Surg 1994;20:347.
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15. Seeger JM, Pretus HA, Carlton LC, et al. Potential predictors of outcome in patients with tissue loss who undergo infrainguinal vein bypass grafting. J Vasc Surg 1999;30:427. 16. Darling RC, III, Chang BB, Paty PS, et al. Choice of peroneal or dorsalis pedis artery bypass for limb salvage. Am J Surg 1995;170:109. 17. Abou-Zamzam AM, Moneta GL, Lee RW, et al. Peroneal bypass is equivalent to inframalleolar bypass for ischemic pedal gangrene. Arch Surg 1996;131:894. 18. Gooden MA, Gentile AT, Mills JL, et al. Free tissue transfer to extend the limits of limb salvage for lower extremity tissue loss. Am J Surg 1997;174:644. 19. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: Experimental study and clinical applications. Br J Plast Surg 1987;40:113. 20. Taylor GI, Palmer JH. Angiosome theory. Br J Plast Surg 1992;45:327. 21. Taylor GI, Pan WR. Angiosomes of the leg: Anatomic study and clinical implications. Plast Reconstr Surg 1998;102:599. 22. Hauser CJ, Shoemaker WC. Use of transcutaneous PO2 regional perfusion index to quantify tissue perfusion in peripheral vascular disease. Ann Surg 1983;197:337. 23. Neville RF, Tempesta B, Sidawy AN. Tibial bypass for limb salvage using polytetrafluoroethylene with a distal vein patch. J Vasc Surg 2001;33:266. 24. Caselli A, Latini V, Lapenna A, et al. Transcutaneous oxygen tension monitoring after successful revascularization in diabetic patients with ischemic foot ulcers. Diab Med 2005;22: 460.
Ischemic wounds of the lower extremity can fail to heal despite successful revascularization. The foot can be divided into six anatomic regions (angiosomes) fed by distinct source arteries arising from the posterior tibial (three), anterior tibial (one), and peroneal (two) arteries. This study investigated whether bypass to the artery directly feeding the ischemic angiosome had an impact on wound healing and limb salvage. Retrospective analysis was performed for 52 nonhealing lower extremity wounds (48 patients) requiring tibial bypass over a 2-year period. Preoperative arteriograms were reviewed to determine arterial anatomy relative to each wound’s specific angiosome and bypass anatomy. Patients were divided into two groups; direct revascularization (DR, bypass to the artery directly feeding the ischemic angiosome) or indirect revascularization (IR, bypass unrelated to the ischemic angiosome). Wound outcome was analyzed with regard to the endpoints of complete healing, amputation, or death unrelated to the wound. Time to healing was also noted for healed wounds. Based on preoperative arteriography, 51% (n ¼ 27) of the wounds received DR to the ischemic angiosome, while 49% (n ¼ 25) underwent IR. There were no statistically significant differences in the comorbidities of the two groups. Revascularization was via tibial bypass using the saphenous vein (n ¼ 34, 65%) or polytetrafluoroethylene with a distal vein patch (n ¼ 18, 35%). Bypasses were performed to the anterior tibial (n ¼ 22, 42%), posterior tibial (n ¼ 17, 33%), or peroneal (n ¼ 13, 25%) arteries based on the surgeon’s judgment. One bypass failed in the perioperative period and was excluded from the analysis. The remaining bypasses were patent at the time of wound analysis. Due to a 17% mortality rate during follow-up, 43 wounds were available for endpoint analysis. This analysis demonstrated that 77% of wounds (n ¼ 33) progressed to complete healing and 23% of wounds (n ¼ 10) failed to heal with resultant amputation. In the DR group, there was 91% healing with a 9% amputation rate. In the IR group, there was 62% healing with a 38% amputation rate ( p ¼ 0.03). In those wounds that did heal, total time to healing was not significantly differentdDR 162.4 days versus IR 159.8 days ( p ¼ 0.95). Revascularization plays a crucial role in the treatment of ischemic lower extremity wounds. We believe that direct revascularization of the angiosome specific to the anatomy of the wound leads to a higher rate of healing and limb salvage. Although many factors must be considered in choosing the target artery for revascularization, consideration should be given to revascularization of the artery directly feeding the ischemic angiosome.
Presented at the Southern Association for Vascular Surgery meeting, Puerto Rico, January 18, 2007. 1
Department of Surgery, Division of Vascular Surgery, Georgetown University Hospital, Washington, D.C. 2
Department of Plastic Surgery, Georgetown University Hospital, Washington, D.C. 3 Department of Surgery, Georgetown University Hospital, and Surgery Service, VA Medical Center, Washington, D.C.
Correspondence to Richard F. Neville, MD, Division of Vascular Surgery, Georgetown University Hospital, 4PHC, 3800 Reservoir Road NW, Washington, D.C. 20007, E-mail: [email protected] Ann Vasc Surg 2009; 23: 367-373 DOI: 10.1016/j.avsg.2008.08.022 Ó Annals of Vascular Surgery Inc. Published online: January 29, 2009
INTRODUCTION Advances in distal lower extremity revascularization have revolutionized salvage of the ischemic limb. A committed effort to limb salvage requires an aggressive approach to revascularization that includes endovascular techniques, vein bypass, and prosthetic graft bypass with the consideration of adjuncts to improve graft performance such as autogenous venous tissue at the distal anastomoses or addition of a distal arteriovenous fistula.1-4 However, despite these advances, vascular bypass can 367
368 Neville et al.
fail to heal ischemic lower extremity wounds even if the patient underwent a successful revascularization procedure.5-17 Gooden et al.18 found that up to 25% of patients with heel ulcers ultimately underwent to a major lower extremity amputation despite a palpable pedal pulse. Part of the failure is due to inadequate treatment of the wound postoperatively.6 However, wounds may also fail to heal because of inadequate local revascularization due to inadequate vascular connections between the revascularized artery and the local ischemic area. We hypothesize that wound healing and limb salvage for ischemic wounds would be optimized by direct revascularization (DR) of the involved area of the foot. In 1987, Taylor and Palmer19,20 introduced the ‘‘angiosome’’ concept that divides the body into three-dimensional vascular territories supplied by specific source arteries and drained by specific veins. Taylor and Pan21 defined five distinct angiosomes of the lower leg as fed by the medial sural artery, the lateral sural artery, the posterior tibial artery, the peroneal artery, and the anterior tibial artery. The foot and ankle area has six distinct angiosomes arising from the posterior tibial artery (n ¼ 3), the anterior tibial artery (n ¼ 1), and the peroneal artery (n ¼ 2). The posterior tibial artery gives rise to a calcaneal branch that supplies the medial ankle and plantar heel, a medial planter branch that feeds the medial plantar instep, and a lateral plantar branch that supplies the lateral forefoot, plantar midfoot, and entire plantar forefoot (Fig. 1). The anterior tibial artery continues on to the dorsum of the foot as the dorsalis pedis (Fig. 2). The peroneal artery supplies the lateral ankle and plantar heel via the calcaneal branch and the anterior upper ankle via an anterior branch (Fig. 3). The literature states that bypassing to one distal artery is often sufficient to heal foot and ankle wounds. Choice of the target artery for bypass is determined by factors such as bypass length, availability of conduit, and quality of the recipient artery. We hypothesized that another consideration should be the arterial anatomy specific to the ischemic angiosome. For example, bypass to the dorsalis pedis artery for heel ulceration has led to 85% healing and limb salvage.5 However, there remains a 15% residual failure rate. It stands to reason that for the wound to heal, the new blood flow to the dorsalis pedis artery has to reach the heel in adequate amount to result in healing. If the arterial connections between the dorsal and plantar circulation are not adequate, the wound may not have as good a chance to heal. DR of either the posterior tibial or peroneal arteries, both of which have
Annals of Vascular Surgery
Fig. 1. Angiosomes of the foot arising from the posterior tibial artery (n ¼ 3): calcaneal branch, medial plantar branch, lateral plantar branch.
calcaneal branches directly supplying the plantar heel, may be more likely to heal a plantar heel wound than revascularization of the dorsalis pedis that relies on arterial-arterial connections through the pedal arch for the blood flow to reach the ischemic tissue.
METHODS We retrospectively reviewed the charts of 56 consecutive patients with tissue loss due to ischemia who required lower extremity vascular reconstruction for wound closure. Patient demographics included diabetes mellitus, chronic renal failure defined as serum creatinine greater than or equal to 1.8, hypertension, and history of symptomatic coronary artery disease manifest as angina or coronary surgical revascularization. All wounds were treated according to the established protocol at the Georgetown University Limb Center. The protocol includes an assessment of the wound and the existing vascular status including examination of pulses and vascular laboratory studies to assess healing potential. Revascularization was considered if this
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Fig. 3. Angiosomes of the foot arising from the peroneal artery (n ¼ 2): calcaneal branch, anterior perforating branch.
Fig. 2. Angiosome of the foot arising from the anterior tibial artery (n ¼ 1): dorsalis pedis.
evaluation indicated a decreased ability for healing manifest as a lack of pedal pulses, ankle-brachial index (ABI) less than 0.3, monophasic segmental waveforms, transcutaneous oxygen tension (TcO2) less than 25 mm Hg absolute value, or TcO2 index less than 0.4.22 Arterial imaging with arteriography was performed for all limbs in need of revascularization. Wounds were debrided prior to revascularization if there was wet gangrene or necrotizing fasciitis present. Following revascularization, wounds were serially debrided and treated with appropriate topical wound care until showing signs of healing such as new granulation tissue. These debridements were done in the Limb Center on a weekly basis until a clean bed of granulation tissue was obtained and then on a biweekly basis until healing occurred or amputation was performed. Wound measurements were made during these follow-up visits. This protocol was similar in both experimental groups. Adjuncts to promote healing, such as hyperbaric oxygen, administration of topical growth factors, and cultured skin, were added to the
topical wound care regimen at the discretion of the treating physicians in the Limb Center. If the wound failed to respond despite maximum therapy, then the limb was considered nonsalvageable and amputation was advocated. Preoperative arteriograms were reviewed for each limb, and wounds were categorized by location according to the primary angiosome. This included the posterior tibial artery (calcaneal, medial plantar, lateral plantar), dorsalis pedis, and peroneal artery (calcaneal, anterior perforator).21 Angiograms and operative reports were reviewed in a blinded fashion to delineate preoperative arterial anatomy, type of bypass, and location of the distal anastomosis. We defined two study groups based on bypass anatomy: DR and indirect revascularization (IR). DR, which involved direct bypass to the artery supplying the source vessel of the angiosome where the ulcer was locateddbypass to the anterior tibial artery for a dorsal foot ulcer, bypass to the peroneal artery for a lateral ankle ulcer, and bypass to the posterior tibial artery for an ulcer at the medial plantar instep. An ulcer on the plantar heel was considered in the direct group if the bypass was to the peroneal or posterior tibial artery. IR involved bypass to an artery unrelated to the ischemic angiosome. Comprehensive documentation of the wound care delivered in
370 Neville et al.
the Limb Center was reviewed to assess rate of healing and final clinical results for each wound. The clinical outcome was then categorized as healed, failure to heal leading to major amputation (below-the-knee or above-the-knee amputation), or death clinically unrelated to the wound. Outcome in all cases, whether healed or amputated, as well as time to complete healing were compared between the two study groups. In addition, the incidence of risk factors was compared between the two groups. Such risk factors included diabetes, hypertension, chronic renal failure, and coronary artery disease.
RESULTS Sixty wounds were reviewed in 56 consecutive patients. Eight patients were lost to follow-up, leaving a study cohort of 52 wounds for analysis. In the total group, 87% of the patients were diabetic, 52% were diagnosed with chronic renal failure, and 36% admitted to actively using tobacco. There were no statistically significant differences in the comorbidities of the two bypass groups (Table I). All bypasses were performed to tibial arteries. The target artery was the anterior tibial in 22 (42%), the posterior tibial in 17 (33%), and the peroneal in 13 (25%). The distal bypass was performed with translocated saphenous vein in 34 cases (65%), and polytetrafluoroethylene (PTFE) with a distal vein patch in 18 cases (35%).4 There was one bypass that failed in the perioperative period. This bypass was to the peroneal artery using PTFE with distal vein patch. Approximately one third of the wounds were closed by topical wound care. Ten required delayed primary closure or a split-thickness skin graft (7 DR and 3 IR). Local flaps were required in 21 patients (12 DR and 9 IR). These flaps included ray, transmetatarsal, and Chopart’s amputations. Two free flaps were used to obtain final wound closure (1 DR and 1 IR). Thirty-three of the 52 wounds (63.5%) progressed to complete healing. Ten (19.2%) wounds failed to heal and the patients went on to major amputation. Death unrelated to the wound prior to complete healing or failure to heal occurred in 9 (17.3%) patients. Detailed analysis of the remaining 43 patients with a complete wound care course was performed. Arteriograms were available for review to delineate preoperative vascular anatomy. These were then compared with the type of bypass performed. Based on preoperative arteriograms and operative reports, 22 (51%) of the bypasses were performed directly to the artery supplying the source artery of the ulcerated angiosome, while 21
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(49%) underwent IR (Fig. 4). Bypass anatomy in the groups was similardDR (11 anterior tibial, 6 posterior tibial, 5 peroneal) and IR (8 anterior tibial, 8 posterior tibial, 6 peroneal). Type of bypass was also without significant differencesdDR (14 translocated vein grafts, 8 distal vein patch grafts23) and IR (16 translocated vein grafts, 5 distal vein patch grafts). Comparing the mean time to complete healing, there was no statistically significant difference between wounds that had DR versus those that underwent IR (DR 162.4 days versus IR 159.8 days, p ¼ 0.95). However, there was a statistically significant difference (Fisher’s exact test, p ¼ 0.03) in complete wound healing rate when comparing DR (90.9% wound healing) versus those that were indirectly revascularized (61.9% wound healing) (Fig. 5). Follow-up intervals for healing were similar in the two groups at 100-day intervals. Healing occurred by 100 days in 2 (10%) DR and 1 (8%) IR group, at 100 to 200 days in 13 (65%) DR and 9 (69%) IR groups, and at greater than 200 days in 5 (25%) DR and 3 (23%) IR groups. As an observation, the major amputation rate was four times greater in the IR group (one above-the-knee, seven belowthe-knee) compared with the group in which DR was supplied to the wound (two below-the-knee) (Table II).
DISCUSSION Effective revascularization continues to be a major component in the treatment of ischemic lower extremity ulcers. Intuitively, providing direct blood flow to the specific area of an ischemic foot ulcer should be preferable to nonspecific revascularization with subsequent reliance on collateral vessels for healing. The concept of distinct vascular territories (i.e., angiosomes) of the foot and ankle provides an anatomic basis for analysis of this intuitive concept. This selective approach to revascularization of the ischemic foot and ankle relies on knowledge of the anatomy of these three-dimensional blocks of tissue supplied by ‘‘source’’ arteries. The posterior tibial artery supplies three vascular territories to the foot. After supplying the medial and medial-posterior ankle, the posterior tibial supplies blood flow to the medial and plantar heel via the calcaneal branch, to the plantar instep via the medial plantar artery, and to the lateral plantar midfoot and entire plantar forefoot via the lateral plantar artery. The distal peroneal supplies the lateral anterior upper ankle via the anterior perforating branch and the lateral and plantar heel via the calcaneal branch.
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Table I. Patient demographics Total
Direct*
Indirect*
Female Male
26 (46.4%) 30 (53.6%)
13 (48.1%) 14 (51.9%)
13 (44.8%) 16 (55.2%)
Diabetes Chronic renal failure Hypertension Coronary artery disease Active tobacco use
49 29 22 16 20
23 13 8 9 9
26 16 14 7 11
(87.5%) (51.8%) (39.3%) (28.6%) (35.7%)
(85.2%) (48.1%) (29.6%) (33.3%) (33.3%)
(89.7%) (55.2%) (48.3%) (24.1%) (37.9%)
*p ¼ NS.
Direct Revascularization
Revascularization of the ischemic angiosome
91%
9%
Indirect Revascularization 38%
62%
60 consecutive wounds
8 excluded, incomplete f/u
52 wounds 9 premature death
100 90 80 70 60 50 40 30 20 10 0 Direct (n=22)
43 wounds
22 directly revascularized
20 healed
2 failed
Complete healing
21 indirectly revascularized
13 healed
Indirect (n=21) Failed to heal
Fig. 5. Complete wound healing based on direct versus indirect revascularization for those 43 wounds with known outcome and follow-up. There was a statistically significant difference in complete healing rate with p ¼ 0.03 (Fisher’s exact test).
8 failed
Fig. 4. Patient cohort with follow-up based on type of revascularization.
The anterior tibial artery supplies the anterior ankle and then becomes the dorsalis pedis artery, supplying the dorsum of the foot. Our retrospective evaluation of revascularization based on the angiosome concept suggests that DR of the ischemic angiosome is more likely to result in successful healing and limb salvage than is IR. The corollary is that subsequent major amputation rate was also lower. This supports our initial hypothesis that it is preferable to provide direct antegrade blood flow to the anatomic area containing the wound than to rely on indirect flow via arterial-arterial connections of the vessels in the foot. An equally important aspect in the management of the ischemic wound is the quality of wound care. Many limbs successfully bypassed are lost due to overwhelming or uncontrollable infection. The attempt to prematurely close an infected wound will
lead to further tissue infection and necrosis. It has been shown that TcO2 around an ischemic wound raises slowly after vascular bypass and peaks at 24 weeks after revascularization.24 This indicates that maximal healing benefit from the renewed blood flow may not be fully realized for more than 1 week after revascularization. Aggressive early wound closure or definitive amputation may be disadvantageous. The wound should be carefully prepared and the soft tissue reconstruction delayed until all signs of inflammation and infection have resolved and the wound is showing initial signs of healing. In our practice, the time between revascularization and soft tissue reconstruction is often 24 weeks. The patient is often discharged after the revascularization and initial wound debridement with follow-up care delivered as an outpatient. The outpatient regimen consist of a wound care plan determined by the Limb Center physicians and carried out by visiting nurses with additional evaluation and treatment during frequent visits to the Limb Center. The status of the revascularization
372 Neville et al.
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Table II. Amputation rate for direct versus indirect revascularization
Complete healing Amputation Mortality
Total
Direct
Indirect
(N ¼ 43)
(n ¼ 22)
(n ¼ 21)
33 (63.5%) 10 (19.2%)
20 (90.9%)* 2 (9.1%)
13 (61.9%)* 8 (38.1%)
9 (17.3%)
3
6
*p ¼ 0.03.
is also assessed during these outpatient visits. Examination of appropriate pulses and Doppler signals are performed on each visit with formal Duplex graft surveillance at standard intervals: 3, 6, and 12 months. When the wound is deemed ready for closure, the patient returns to the hospital for final debridement and appropriate wound closure. This may take the form of primary closure after additional debridement, skin grafting, or local muscular flaps rotated into the wound. It is difficult to determine the functional quality of the arterial-arterial connections of the foot and ankle. Listening for antegrade and retrograde flow in the tibial arteries can be helpful, providing that the inflow is of sufficient volume to be evaluated by Doppler. Doppler signals in the dorsalis pedis can be evaluated with compression of the posterior tibial with reversal of the situation as well. The arteriogram does not always show these connections, especially in the setting of compromised arterial inflow. Certainly IR leads to wound healing. Therefore, if these connections exist and are adequate, then IR can be successful. This reflects the clinical experience that good rates of healing and limb salvage are reported with successful bypass regardless of consideration of angiosome anatomy. Berceli, Carsten and others have shown that limb loss can certainly occur despite a patent bypass graft.5,7 Berceli et al.5 report an 86% healing rate of heel lesions after dorsalis pedis bypass despite the lack of an intact pedal arch, which would be an IR according to the angiosome concept. However, these authors recognize the problematic nature of this situation and agree that healing is dependent on restoration of adequate local blood flow to the wound. In our series, 62% of the wounds were documented to have IR healed. We observed that if the arterial-arterial connections in the foot are clearly absent on arteriography and there is no arterial blush over the angiosome containing the ischemic ulcer, then the chances of healing may become more problematic. Our retrospective data suggest that, when the
vascular surgeon has a choice of target arteries for revascularization, preference should be given to the artery directly feeding the affected angiosome. However, if the only artery available does not provide direct flow to the affected angiosome, revascularization remains indicated even if arterial-arterial connections are not obviously present. In this setting, limb salvage may not be as high as that in which the DR is possible.
CONCLUSION Revascularization plays a crucial role in the treatment of ischemic lower extremity wounds. Based on our retrospective evaluation, we believe that DR of the angiosome specific to the anatomy of the nonhealing wound leads to a higher rate of healing and limb salvage. The quality of subsequent wound care is also a critical component in promoting healing and avoiding further tissue loss. Although many factors are involved in the choice of target artery for revascularization, consideration should be given to revascularization of the artery directly feeding the ischemic angiosome as an additional consideration in planning lower extremity revascularization. REFERENCES 1. Neville RF, Attinger C, Sidawy AN. Prosthetic bypass with a distal vein patch for limb salvage. Am J Surg 1997;174: 173. 2. Pappas PJ, Hobson RW, Meyers MG, Jamil Z, et al. Patency of infrainguinal polytetrafluoroethylene bypass grafts with distal interposition vein cuffs. Cardiovasc Surg 1998;6:19. 3. Kansal N, Pappas PJ, Gwertzman GA, Silva MB, Jr, et al. Patency and limb salvage for polytetrafluoroethylene bypasses with vein interposition cuffs. Ann Vasc Surg 1999;13:386. 4. Neville RF, Tempesta B, Sidawy AN. Tibial bypass for limb salvage using polytetrafluoroethylene and a distal vein patch. J Vasc Surg 2001;33:266. 5. Berceli SA, Chan AK, Pomposelli FB, et al. Efficacy of dorsal pedal artery bypass in limb salvage for ischemic heel ulcers. J Vasc Surg 1999;30:499.
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6. Treiman GS, Oderich GS, Ashrafi A, Schneider PA. Management of ischemic heel ulceration and gangrene: An evaluation of factors associated with successful healing. J Vasc Surg 2000;31:1110. 7. Carsten CG, III, Taylor SM, Langan EM, III, Crane MM. Factors associated with limb loss despite a patent infrainguinal bypass graft. Am Surg 1998;64:33. 8. Edwards JM, Taylor LM, Porter JM. Limb salvage in endstage renal disease (ESRD), comparison of modern results in patients with and without ESRD. Arch Surg 1998;123: 1164. 9. Chang BB, Paty PK, Shah DM, Kaufman JL, Leather RP. Results of infrainguinal bypass for limb salvage in patients with end-stage renal disease. Surgery 1990;108:742. 10. Karp NS, Kasabian AK, Siebert JW, et al. Microvascular freeflap salvage of the diabetic foot: A 5 year experience. Plast Reconstr Surg 1994;84:834. 11. Andros G, Harris RW, Dulawa LB, et al. The need for arteriography in diabetic patients with gangrene and palpable foot pulses. Arch Surg 1984;119:1260. 12. Johnson BL, Glickman MH, Bandyk DF, Esses GE. Failure of foot salvage in patients with end-stage renal disease after surgical revascularization. J Vasc Surg 1995;22:280. 13. Elliot BM, Robison JG, Brothers TE, Cross MA. Limitations of peroneal artery bypass grafting for limb salvage. J Vasc Surg 1993;18:881. 14. Bergamini TM, George SM, Massey HT, et al. Pedal or peroneal bypass: Which is better when both are patent? J Vasc Surg 1994;20:347.
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15. Seeger JM, Pretus HA, Carlton LC, et al. Potential predictors of outcome in patients with tissue loss who undergo infrainguinal vein bypass grafting. J Vasc Surg 1999;30:427. 16. Darling RC, III, Chang BB, Paty PS, et al. Choice of peroneal or dorsalis pedis artery bypass for limb salvage. Am J Surg 1995;170:109. 17. Abou-Zamzam AM, Moneta GL, Lee RW, et al. Peroneal bypass is equivalent to inframalleolar bypass for ischemic pedal gangrene. Arch Surg 1996;131:894. 18. Gooden MA, Gentile AT, Mills JL, et al. Free tissue transfer to extend the limits of limb salvage for lower extremity tissue loss. Am J Surg 1997;174:644. 19. Taylor GI, Palmer JH. The vascular territories (angiosomes) of the body: Experimental study and clinical applications. Br J Plast Surg 1987;40:113. 20. Taylor GI, Palmer JH. Angiosome theory. Br J Plast Surg 1992;45:327. 21. Taylor GI, Pan WR. Angiosomes of the leg: Anatomic study and clinical implications. Plast Reconstr Surg 1998;102:599. 22. Hauser CJ, Shoemaker WC. Use of transcutaneous PO2 regional perfusion index to quantify tissue perfusion in peripheral vascular disease. Ann Surg 1983;197:337. 23. Neville RF, Tempesta B, Sidawy AN. Tibial bypass for limb salvage using polytetrafluoroethylene with a distal vein patch. J Vasc Surg 2001;33:266. 24. Caselli A, Latini V, Lapenna A, et al. Transcutaneous oxygen tension monitoring after successful revascularization in diabetic patients with ischemic foot ulcers. Diab Med 2005;22: 460.