|Year : 2019 | Volume
| Issue : 2 | Page : 65-73
Limb salvage using microvascular reconstructions for secondary regional vascular insufficiency in the neuro ischemic diabetic foot; is it making impact?
Thalaivirithan Margabandu Balakrishnan1, Illayakumar Pramasivam2, Krishnakumar Thirunavukarasu1, Jaganmohan Janardhanan1, Sritharan Narayanan2
1 Department of Plastic and Faciomaxillary Surgery, Madras Medical College, Chennai, Tamil Nadu, India
2 Institute of Vascular Surgery, Madras Medical College, Chennai, Tamil Nadu, India
|Date of Web Publication||6-Jun-2019|
Dr. Thalaivirithan Margabandu Balakrishnan
Department of Plastic and Faciomaxillary Surgery, Madras Medical College, Chennai, Tamil Naduw
Source of Support: None, Conflict of Interest: None
Introduction: Secondary regional vascular insufficiency (RVI) is a pathophysiological state that occurs most commonly following the successfully involved perforosome-directed distal revascularization (IPDDR). This IPDDR renders bounding pulse in the vicinity of diabetic foot ulcer, which shows no signs of early granulation (the sign of healing potential) for variable time. This is the main cause for delaying the definitive reconstruction in the successfully revascularized diabetic foot. Aim: The aim of this study is to evaluate the effectiveness of microvascular and nonmicrovascular reconstructions (NMVRs) in the treatment of secondary RVI of the neuroischemic diabetic foot following successful IPDDR. Endpoints assessed in this study were as follows: (1) Time taken to render a stable and shoe able foot or foot residuum following successful revascularization of the neuroischemic diabetic foot. (2) Time interval between IPDDR and definitive reconstruction in both groups. (3) Rate of complications including recurrence of foot ulcers and failures of reconstruction in each group. Patients and Methods: From 2014 to 2017, 128 neuroischemic diabetic foot patients (a multicenter study) after successful IPDDR for their critical limb ischemia subsequently underwent various types of reconstructions. All had a variable period of secondary RVI following successful revascularization. A retrospective study was conducted by dividing them into two groups – MVR group with 69 patients and NMVR group with 59 patients. The interval between the IPDDR and definitive reconstructions in each group was called the “latent period.” All were followed up for an average period of 30 months. The standard postoperative care and offloading techniques were followed in both groups. Results: The average time taken for obtaining shoeable and stable foot or its residuum in the MVR group was 55.5 days and NMVR group was 76.5 days. By statistical analysis, the MVR group had lesser latency period (P = 0.042), lesser ulcer recurrences (P = 0.044), and lesser flap and reconstruction failures leading to amputation (P = 0.0345). Conclusion: The MVR by bringing tissue from above or at the level of hip area produces sound and early healing of secondary RVI with higher limb salvage rate following the successful revascularization of neuroischemic diabetic foot.
Keywords: Internal offloading, involved perforosome-directed distal revascularization, microvascular reconstruction of neuroischemic diabetic foot, neuroischemic diabetic foot, secondary regional vascular insufficiency
|How to cite this article:|
Balakrishnan TM, Pramasivam I, Thirunavukarasu K, Janardhanan J, Narayanan S. Limb salvage using microvascular reconstructions for secondary regional vascular insufficiency in the neuro ischemic diabetic foot; is it making impact?. Indian J Vasc Endovasc Surg 2019;6:65-73
|How to cite this URL:|
Balakrishnan TM, Pramasivam I, Thirunavukarasu K, Janardhanan J, Narayanan S. Limb salvage using microvascular reconstructions for secondary regional vascular insufficiency in the neuro ischemic diabetic foot; is it making impact?. Indian J Vasc Endovasc Surg [serial online] 2019 [cited 2020 Apr 7];6:65-73. Available from: http://www.indjvascsurg.org/text.asp?2019/6/2/65/259648
| Introduction|| |
The ongoing unabated epidemic of noncommunicable disease, the diabetes mellitus (DM) in the developing world, is causing the increasing social and economic burden. They are producing a colossal impact on devising health-care policies and allocation of health-related funds. Global prevalence of DM has risen to 8.8% in 2015, which corresponds to 415 million patients. The current data from the International Diabetes Federation says that 425 million people have diabetes in the world and 82 million people in the SEA Region; by 2045, this will rise to 151 million. There were over 72,946,400 cases of diabetes in India in 2017. The most important and burgeoning locoregional complication of DM – the diabetic foot ulcers are also on the rise., On an average for every 20 s, one diabetes-related lower-extremity amputation occurs in the world. Data emanating from developing countries , lucidly illustrate the rise of diabetes-related lower-extremity amputations. This scenario of rising diabetes-related morbidity is the same in the developed nations. In the last decade, several studies revealed that there was an increase in the prevalence of neuroischemic diabetic foot lesions.,, The preliminary data from our institutional epidemiological study also reported an increase in the prevalence of neuroischemic diabetic foot lesions from 11.8% in 2012 to 13.5% in 2016 in our population. Several studies ,,, also reported an increase in the prevalence of lower-extremity arterial disease in the diabetic population attributing to increased limb loss. Neuroischemic diabetic foot lesions always occur as a result of the combined effect of macroangiopathy and microangiopathy.,,,
The revascularization science strategies in the neuroischemic diabetic foot have advanced and successfully culled the widespread long-held misunderstanding–the “untreatable occlusive microangiopathy” which was popularly called “small vessel disease.” However, various studies ,,,,,,, have established nonocclusive functional microangiopathy as the cause of regional vascular insufficiency (RVI). There was a stride in the advancement of revascularization when the indirect revascularization technique was replaced by the involved perforosome-directed distal revascularization (IPDDR) when it was understood that the interconnecting vessels between three axial vessels of the leg were involved by the disease. Despite this, RVI ,, is a pathophysiological state that commonly occurs following the IPDDR which renders bounding pulse in the vicinity of diabetic foot ulcer that shows no immediate granulation – “the sign of healing potential” for variable period. This pathophysiological state is known as secondary RVI because it is seen after IPDDR. In a simple sense, RVI is the localized manifestation of microcirculatory failure. What characterize the RVI is the functional microangiopathy that is due to endothelial dysfunction contributing to following two pathologies: (a) failure of the proliferation of fibrocapillary network the organ of repair when exposed to normal oxygen gradient in the wound and (b) failure of capillaries to dilate in response to injury. Akbari and LoGerfo  had shown in their study that even in healthy participants endothelium-dependent and nonendothelium-dependent vasodilation of capillaries are low in the foot when compared to forearm. Therefore, this explains how feet are more vulnerable for RVI. This is the main cause for delaying the definitive reconstruction following the revascularization of neuroischemic diabetic foot. The literature on the postrevascularization management of diabetic foot ulcers are also scant.,,, Except for the author's previous study, there are only four other relevant studies ,,, dealing with the post-IPDDR diabetic foot ulcers management, but none of them taking into the account of secondary RVI specifically. This article examines the outcome of microvascular and nonmicrovascular reconstructions (NMVRs) of secondary RVI following successful IPDDR.
Aim of the study
The aim is to evaluate the effectiveness of microvascular and NMVRs in the treatment of secondary RVI of neuroischemic diabetic foot following successful IPDDR. Endpoints assessed in this study were:
- Time taken to render a stable and shoeable foot or foot residuum following successful revascularization of neuroischemic diabetic foot
- Time interval between IPDDR and definitive reconstruction in both groups
- Rate of complications including recurrence of foot ulcers and failures of reconstruction in each group.
| Patients and Methods|| |
As per the institutional protocol, author currently performs IPDDR  in all critically ischemic diabetic foot. From 2014 to 2017, 128 patients underwent various types of reconstructions after successful IPDDR for their critical neuroischemic diabetic foot. All had a variable period of secondary RVI following successful revascularization. Retrospective cohort study was conducted by dividing them into following two groups – MVR group with 69 cases (M:F ratio was 50:19) and NMVR group with 59 patients (M:F ratio was 46:13). The average age was 55 years in the MVR group and 52.5 years in the NMVR group. The interval between the IPDDR and definitive reconstructions in each case was called “latent period.” All were followed up for an average period of 30 months. The standard postoperative care and offloading techniques were followed in both groups. In the immediate postrevascularization, all patients had unmasking of functional microangiopathy, which was the basic pathophysiology of the secondary RVI. All these patients were managed with balanced debridement (method of saving all the potentially salvageable ischemic tissues which are prone for exposure desiccation, death process, and at the same time excising all the suppurated, sloughed out tissues) and active dressings for a variable period (called latent period) in the post-IPPDR phase before definitive reconstructions. In both groups, patients had full complement or part of quality intact pedal vessels.
- Those patients with manifestations of RVI such as peri-wound ischemia (as shown by transcutaneous measurements (TcPO2) <30 mm of Hg and no immediate granulation following successful IPDDR were included)
- Those patients who had stable cardiac status and general condition fit enough to undergo IPDDR and subsequent reconstructions
- Those who had full complement or part of quality intact pedal vessels as seen in digital substraction angiography.
- Those with the neuroischemic diabetic foot with a history of tobacco use in the form of smoking, chewing, and insufflation
- Those with neuroischemic diabetic foot with compromised cardiac pulmonary status and severe renal diseases (continuous dialysis-dependent patients with the estimated glomerular filtration rate (eGFR) receptor < 30 ml/min/1.73 m2)
- Those who had unsuccessful IPDDR attempts like loss of graft patencies or re-thrombosis of involved vessel or those who required late graft revisions
- Those who had severe bleeding diathesis and had complications of IPDDR
- Those who had uncontrolled sepsis despite successful IPDDR and subsequently underwent lower limb amputations even before any reconstructive procedures
- Those with primary RVI and had reconstructions
- Those with no peripheral run off with extensive tissue loss of the perforosomes and Rutherford (CLI) Grade 3 category 6 patients who were not the candidates for IPDDR.
Case illustration for microvascular reconstruction group
A 26-year-old female patient [Figure 1] presented with critical limb ischemia and calcaneal eschar with no subeschar loculation. The multispecialty-integrated team evaluated her. Angiogram revealed severe tibial disease with several stenoses in the popliteal artery with good peripheral runoff. She had Monckeberg's sclerosis of pedal vessels [Figure 2]. She had undergone angioplasty with stenting down to the level of posterior tibial with straight-line flow established down to calcaneal artery perforosomes. Following this IPDDR, she had bounding pulse in the posterior tibial in the vicinity of eschar, which prompted the vascular surgeon for immediate debridement of eschar with primary closure. However, within 24 h, there was severe devitalization along suture line despite no collection or tension underneath. The sutures were removed immediately [Figure 3]. Secondary RVI was diagnosed, and balanced debridements with topical negative dressing were done. In 9 weeks, the patient had good granulation with the healing of secondary RVI [Figure 4]. At the end of 9 weeks on clinical examination, she was found to be having tibialis anterior recruitment with calcaneal gait. The contralateral foot was flat but stable with Charcot's degeneration of tarsometatarsal joint in the consolidation phase. Pre- and post-angioplasty angiogram revealed good profunda femoris artery with good quality vessels. Therefore, with tibialis anterior oblique tenotomy at the musculocutaneous junction, a good plantar flexion was obtained with a range of mobility of 30°. Then, the free anterolateral thigh flap was used for reconstructing the calcaneal raw area. The lateral descending branch of the lateral circumflex femoral artery was anastomosed in the end-to-side fashion to posterior tibial artery [Figure 5]. Single venae comitantes was anastomosed to the great saphenous vein [Figure 5]. Donor site was primarily closed [Figure 6]. Until 6 weeks of postoperative period [Figure 6], she was ambulated on walker with global offloading of the operated foot with protective customized sole-containing footwear with silicone gel socks for the contralateral weight-bearing foot. She was followed up for 26 months, flap settled well, and there was no recurrence [Figure 7]. She was treated in the postoperative period by standard Type 1 footwear with silicone gel socks as locoregional offloading technique and assumed bipedal walking after 2 months postoperative.
|Figure 1: Eschar over calcaneal region in the patient with limb-threatening ischemia|
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|Figure 2: (a) Arterial angiogram showing multiple stenoses from popliteal level to tibial vessels. (b) Digital X-ray showing the Monckeberg's sclerosis of pedal vessels|
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|Figure 3: Secondary regional vascular insufficiency manifested immediately after the excision and suturing of the wound following the involved perforosome-directed distal revascularization|
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|Figure 4: Wound status after balanced debridement and negative topical pressure dressing|
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|Figure 5: Primarily thinned anterolateral thigh flap and microvascular anastomosis done to a posterior tibial artery in end-to-side fashion and in end-to-end fashion to great saphenous vein. Tibialis anterior oblique tenotomy was also performed simultaneously as an adjuvant internal offloading procedure to treat the calcaneal gait|
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|Figure 6: Immediate postoperative photographs of reconstructed and donor site|
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Case illustration for nonmicrovascular reconstruction group
A 54-year-old female presented with limb-threatening ischemia with dry gangrene of the first, second, and third toes [Figure 8]. Angiogram revealed multiple stenoses in the anterior tibial, posterior tibial, and dorsalis pedis artery segment that was treated by distal bypass to the posterior tibial artery. Post-IPDDR patient had secondary RVI treated by active dressing following the amputation of the first and the second toes. On the 4th week, encouraging granulation appeared on the debrided plantar aspect, but the 3rd metatarsophalangeal joint was devitalized. She was found to be having tendo-achilles contracted with more forefoot pressure. Percutaneous tendo-achilles lengthening was done as a first clean procedure. Third toe filleted flap was harvested after excising the skeleton down to the neck of the 3rd metatarsal bone for the distal coverage. Rest of the area were covered by split-thickness skin graft [Figure 9]. Subsequently, she was put on locoregional offloading on silicone gel socks and standard footwear. She attained bipedal walking after 10 weeks. She was followed for 24 months, and there was a transfer lesion on the plantar aspect of luxating 1st metatarsal bone at 20 weeks postoperative that was treated by tenotomy of peroneus longus insertion and local flap. There was no recurrence thereafter.
|Figure 8: Gangrenous patch on the sole with extension to toes and web spaces|
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|Figure 9: Postoperative photograph showing filleted toe flap and split-thickness skin grafting|
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| Results|| |
In the MVR group, 50 patients had a full complement of intact quality pedal vessels (72%) and remaining (28%) had part of it (atleast two pedal vascular arches were intact). In NMVR group, 43 patients had a full complement of intact quality pedal vessels (73%) and remaining (27%) had part of it. Statistically insignificant variables between these groups are sex ratio (M:F ratio in MVR 50:19 and NMVR 46:13 - for male gender P = 0.608), average body mass index (average BMI in the MVR group 25.5 and NMVR group 26 P = 0.03) and average age (55 years in MVR and 52.5 years in NMVR – P = 0.532). On the life table analysis, the average time taken for obtaining shoeable and stable foot or its residuum in the MVR group was 55.5 days and NMVR group was 96.5 days (P = 0.045). Other data are given in [Table 1], [Table 2], [Table 3]. In our series after minimizing the background differences with the propensity score method, the positive effect of [Graph 1] and [Graph 2] MVR for the secondary RVI was evident. Thirty-nine propensity-matched pairs with identical baseline characteristics were detected and analyzed statistically. Lower limb salvage rate in 2 years in the MVR group was 87% and NMVR group was 68% (P = 0.082). By statistical analysis, the MVR group [Table 1] had lesser latent period (P = 0.042), lesser ulcer recurrences (P = 0.044), and lesser flap and reconstruction failures leading to amputation (P = 0.0345). This study conforms to STROBE epidemiological observational study. Microsoft Excel for Mac 2011 version 14.7.2 was used for statistical analysis [Table 3].
|Table 3: Results in both microvascular reconstruction group and nonmicrovascular reconstruction group|
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| Discussion|| |
Armstrong et al. and Margolis et al., had shown in their study that critical ischemia of lower extremity combined with infection was responsible for major limb loss. Several studies ,,, have established that by the dedicated multispecialty integrated approach by angiosome-directed revascularization and reconstructions of the critically ischemic diabetic foot a shoeable and stable foot or its residuum was possible. Author has also established in his study that IPDDR could reduce the amputation rate of the neuroischemic diabetic foot. Despite advanced and successful revascularization procedures that produce conducive environment for wound healing, wounds do not proceed in an orderly fashion of healing culminating in the establishment of effective skin barrier as shown by several studies.,,
Rhodes and King  had shown in their study that following successful distal revascularization there existed a latency period before the periwound transcutaneous oxygen pressure returns to a normal level and for the granulation to appear. Wound healing studies , had shown that oxygen supply to the wound and wound oxygen tension were main factors in determining the wound healing. Although the successful revascularization procedure brings normal blood flow in the pedal vessels, there existed a definitive period when the wound recuperates from the local perfusion failure. This pathology–local wound perfusion failure was seen as a common feature by the author, following successful IPDDR (secondary RVI). Rarely, there were few patients seen by the author with bounding pedal pulse with ulcers exhibiting no granulation (primary RVI). Hence, author believes that RVI - a nonocclusive microvascular disease sometimes precedes and always coexists with a characteristic atherosclerotic obstructive tibial disease that occurs in the diabetic foot. Draznin et al. called this pathology behind the RVI as “functional microangiopathy.” They described sluggish microcirculation, failure of capillaries to dilate and proliferate when exposed to oxygen gradient as the contributing cause of wound failure. Author's pivotal study on the RVI is first of its nature to unravel the factors that can prod failing ischemic wound to the healing process. The valid reason  why one should go for the IPDDR is the involvement of intercommunicating vessels between the axial vessels of the leg and foot. Despite this several studies ,, revealed RVI as the cause for prolonged healing after successful involved angiosome or perforosome-directed distal revascularization. The author had done adjuvant internal offloading procedures as an integral part of reconstruction in both groups. Author by this study had established that the microvascular reconstruction using the hip or above hip level perforosomal flaps that brought tissues free from the microangiopathy, resulted in the early and stable reconstructions. On analyzing the reasons for the better outcome and better healing of secondary RVI in the MVR group, the following factors were considered by the authors.
- The high failure rate for locoregional flaps (average overall failure rate in the NMVR group is 15%) could be due to latent secondary RVI in the penumbra regions of the defects that were uncovered in these locoregional flaps
- Unrecognized stenosis and occlusions in the adjacent perforators and source vessels could also contribute to the high failure rate of locoregional flaps
- However in MVR, distant tissues (hip and above hip level) which were free from microangiopathy  and with homogenized supra normal blood supply  effectively heals the secondary RVI as it is bringing the direct blood supply from the IPDDR treated source vessels
- In the NMVR group, the definitive reconstruction is delayed until the healing potential is well established by the confluent granulation and bacteriological balance of the wound. Whereas in the MVR group, definitive reconstruction was encouraged early (by virtue of free flap hemodynamics) even in the stubborn ischemic wound with secondary RVI as the independent homogenized blood supply  was established following the anastomosis to the disease-free segment of the source blood vessel. This explains why there was less latency in the MVR group
- Furthermore, the durable tissue reconstructions were easily possible with MVR that brought less recurrences and lasting results in the MVR group.
Drying, desiccation, and death of ischemic tissues are the common phenomenon seen in the diabetic. Balanced debridements with an aim to salvage potentially salvageable ischemic tissues following IPDDR reinforced by early MVR would be the most prudent step in the limb salvage for limb-threatening ischemia. Limitation of the author study is a small-scale retrospective study. However, the strength of the study is the lucid statistical illustration of the benefits of MVR for secondary RVI.
| Conclusion|| |
The MVR by bringing tissue from above or at the level of hip area produces sound and early healing of secondary RVI following the successful revascularization of neuroischemic diabetic foot. The durable and lasting results can be achieved with MVR reinforced with adjuvant surgical internal offloading procedures. The Kaplan–Meier estimation showed very encouraging results regarding a 2-year limb salvage rate in the MVR group. With the prevalent exponential increase in the aged diabetic population, the present study findings will be applicable for physicians dealing with the reconstruction of chronic limb-threatening ischemia.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Narres M, Kvitkina T, Claessen H, Droste S, Schuster B, Morbach S, et al.
Incidence of lower extremity amputations in the diabetic compared with the non-diabetic population: A systematic review. PLoS One 2017;12:e0182081.
International Diabetes Federation. IDF Diabetes Atlas. 7th
ed. Belgium: International Diabetes Federation; 2016.
Trautner C, Haastert B, Spraul M, Giani G, Berger M. Unchanged incidence of lower-limb amputations in a German city, 1990-1998. Diabetes Care 2001;24:855-9.
Almaraz MC, González-Romero S, Bravo M, Caballero FF, Palomo MJ, Vallejo R, et al.
Incidence of lower limb amputations in individuals with and without diabetes mellitus in Andalusia (Spain) from 1998 to 2006. Diabetes Res Clin Pract 2012;95:399-405.
Laclé A, Valero-Juan LF. Diabetes-related lower-extremity amputation incidence and risk factors: A prospective seven-year study in Costa Rica. Rev Panam Salud Publica 2012;32:192-8.
Ang Y, Yap CW, Saxena N, Lin LK, Heng BH. Diabetes-related lower extremity amputations in Singapore. Proc Singapore Healthc 2017;26:76-80.
Moxey PW, Gogalniceanu P, Hinchliffe RJ, Loftus IM, Jones KJ, Thompson MM, et al.
Lower extremity amputations – A review of global variability in incidence. Diabet Med 2011;28:1144-53.
Prompers L, Schaper N, Apelqvist J, Edmonds M, Jude E, Mauricio D, et al.
Prediction of outcome in individuals with diabetic foot ulcers: Focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE study. Diabetologia 2008;51:747-55.
Ryu HM, Kim JS, Ko YG, Hong MK, Jang Y, Choi DH. Comparison of clinical outcome of infrapopliteal angioplasty between Korean diabetic and non-diabetic patients with critical limb ischemia. Circ J 2012;76:335-41.
Armstrong DG, Cohen K, Courric S, Bharara M, Marston W. Diabetic foot ulcers and vascular insufficiency: Our population has changed, but our methods have not. J Diabetes Sci Technol 2011;5:1591-5.
Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, et al.
High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study. Diabetologia 2007;50:18-25.
Adler AI, Boyko EJ, Ahroni JH, Smith DG. Lower-extremity amputation in diabetes. The independent effects of peripheral vascular disease, sensory neuropathy, and foot ulcers. Diabetes Care 1999;22:1029-35.
Limperopoulou D, Bates M, Petrova NL, Me E. The epidemic of neuroischaemic foot. In: Diabetic Foot Study Group. Chalkidiki; 2005.
Jeffcoate WJ, Harding KG. Diabetic foot ulcers. Lancet 2003;361:1545-51.
Akbari CM, LoGerfo FW. Microvascular changes in the diabetic foot. In: Veves A, Giurini J, LoGerfo FW, editors. The Diabetic Foot. Totowa: Humana; 2002.
Balakrishnan TM, Ilayakumar P. Microvascular reconstruction in the revascularised diabetic foot: A perforosome approach. Clin Res Foot Ankle 2016;4:1000206.
Flynn MD, Tooke JE. Aetiology of diabetic foot ulceration: A role for the microcirculation? Diabet Med 1992;9:320-9.
Conrad MC. Large and small artery occlusion in diabetics and nondiabetics with severe vascular disease. Circulation 1967;36:83-91.
Rayman G, Williams SA, Spencer PD, Smaje LH, Wise PH, Tooke JE, et al.
Impaired microvascular hyperaemic response to minor skin trauma in type I diabetes. Br Med J (Clin Res Ed) 1986;292:1295-8.
Akbari CM, LoGerfo FW. Microvascular Changes in the Diabetic Foot. In: Veves A, Giurini JM, LoGerfo FW (eds). The Diabetic Foot. Humana Press, Totowa, NJ. 2002.
Azuma N, Koya A, Uchida D, Saito Y, Uchida H. Ulcer healing after peripheral intervention-can we predict it before revascularization? Circ J 2014;78:1791-800.
Attinger CE, Evans KK, Bulan E, Blume P, Cooper P. Angiosomes of the foot and ankle and clinical implications for limb salvage: Reconstruction, incisions, and revascularization. Plast Reconstr Surg 2006;117:261S-93S.
Hoffmann U, Schulte KL, Heidrich H, Rieger H, Schellong S. Complete ulcer healing as primary endpoint in studies on critical limb ischemia? A critical reappraisal. Eur J Vasc Endovasc Surg 2007;33:311-6.
Barshes NR, Chambers JD, Cohen J, Belkin M; Model To Optimize Healthcare Value in Ischemic Extremities 1 (MOVIE) Study Collaborators. Cost-effectiveness in the contemporary management of critical limb ischemia with tissue loss. J Vasc Surg 2012;56:1015-240.
Nabuurs-Franssen MH, Huijberts MS, Nieuwenhuijzen Kruseman AC, Willems J, Schaper NC. Health-related quality of life of diabetic foot ulcer patients and their caregivers. Diabetologia 2005;48:1906-10.
Rashid H, Slim H, Zayed H, Huang DY, Wilkins CJ, Evans DR, et al.
The impact of arterial pedal arch quality and angiosome revascularization on foot tissue loss healing and infrapopliteal bypass outcome. J Vasc Surg 2013;57:1219-26.
Varela C, Acín F, de Haro J, Bleda S, Esparza L, March JR. The role of foot collateral vessels on ulcer healing and limb salvage after successful endovascular and surgical distal procedures according to an angiosome model. Vasc Endovascular Surg 2010;44:654-60.
Kawarada O, Fujihara M, Higashimori A, Yokoi Y, Honda Y, Fitzgerald PJ. Predictors of adverse clinical outcomes after successful infrapopliteal intervention. Catheter Cardiovasc Interv 2012;80:861-71.
Alexandrescu VA, Hubermont G, Philips Y, Guillaumie B, Ngongang C, Vandenbossche P, et al.
Selective primary angioplasty following an angiosome model of reperfusion in the treatment of Wagner 1-4 diabetic foot lesions: Practice in a multidisciplinary diabetic limb service. J Endovasc Ther 2008;15:580-93.
Armstrong DG, Lavery LA, Harkless LB. Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 1998;21:855-9.
Margolis D, Malay DS, Hoffstad OJ, Leonard CE, MaCurdy T, Lopez de Nava K, et al
. Prevalence of Diabetes, Diabetic Foot Ulcer, and Lower Extremity Amputation among Medicare Beneficiaries, 2006 to 2008. Rockville: Quality AfHRa; 2011.
Neville RF, Attinger CE, Bulan EJ, Ducic I, Thomassen M, Sidawy AN, et al.
Revascularization of a specific angiosome for limb salvage: Does the target artery matter? Ann Vasc Surg 2009;23:367-73.
Clemens MW, Attinger CE. Angiosomes and wound care in the diabetic foot. Foot Ankle Clin 2010;15:439-64.
Clemens MW, Attinger CE. Functional reconstruction of the diabetic foot. Semin Plast Surg 2010;24:43-56.
Carsten CG 3rd
, Taylor SM, Langan EM 3rd
, Crane MM. Factors associated with limb loss despite a patent infrainguinal bypass graft. Am Surg 1998;64:33-7.
Berceli SA, Chan AK, Pomposelli FB Jr., Gibbons GW, Campbell DR, Akbari CM, et al.
Efficacy of dorsal pedal artery bypass in limb salvage for ischemic heel ulcers. J Vasc Surg 1999;30:499-508.
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;31:1110-8.
Rhodes GR, King TA. Delayed skin oxygenation following distal tibial revascularization (DTR). Implications for wound healing in late amputations. Am Surg 1986;52:519-25.
Hunt TK, Hopf HW. Wound healing and wound infection. What surgeons and anesthesiologists can do. Surg Clin North Am 1997;77:587-606.
Sheffield PJ. Tissue oxygen measurements. In: Hunt TK, Davis JC, editors. Problem Wounds: The Role of Oxygen. New York: Elsevier; 1988. p. 17-52.
Draznin M, Eison R, Maverakis E, Huntley A. Levin and O'Neal's The Diabetic Foot. 7th
ed. Mosby Elsevier. Philadelphia;2008.
Goshima KR, Mills JL Sr., Hughes JD. A new look at outcomes after infrainguinal bypass surgery: Traditional reporting standards systematically underestimate the expenditure of effort required to attain limb salvage. J Vasc Surg 2004;39:330-5.
Söderström M, Arvela E, Albäck A, Aho PS, Lepäntalo M. Healing of ischaemic tissue lesions after infrainguinal bypass surgery for critical leg ischaemia. Eur J Vasc Endovasc Surg 2008;36:90-5.
Faglia E, Clerici G, Clerissi J, Mantero M, Caminiti M, Quarantiello A, et al.
When is a technically successful peripheral angioplasty effective in preventing above-the-ankle amputation in diabetic patients with critical limb ischaemia? Diabet Med 2007;24:823-9.
Rubino C, Coscia V, Cavazzuti AM, Canu V. Haemodynamic enhancement in perforator flaps: The inversion phenomenon and its clinical significance. A study of the relation of blood velocity and flow between pedicle and perforator vessels in perforator flaps. J Plast Reconstr Aesthet Surg 2006;59:636-43.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3]