Limb Revascularization in Patients with Diabetes Mellitus

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The review describes morbidity, mortality and possible complication rates for diabetic patients with peripheral arteries disease. The article demonstrates the modern tendency in the surgical treatment of peripheral arteries atherosclerosis, shows and compares worldwide results of endovascular and open revascularization. The authors have assessed the risk of amputation for patients with diffuse peripheral arteries disease and described basic treatment principals for better chronic ischemic ulcer healing.

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Up to date, more than 170 million people worldwide suffer from diabetes mellitus (DM). By 2030, according to the vast majority of experts, in the coming years the number of patients will increase up to 300 million [1]. DM is the main risk factor for the development of peripheral arterial disease (PAD) [2]. It is proved that the presence of diabetes increases the risk of vascular complications 5 times relative to patients without it. In this regard, all patients with diabetes need to conduct diagnostic tests of all vascular arterial pools in case of damage to at least one of them. This approach helps to reduce the frequency of complications from surgical interventions [3]. If the patient complains of classic pains in the lower extremities when walking, it is necessary to conduct tests not only for ischemia, but also for neuropathy in the legs, since the latter can cause similar clinical symptoms [4]. In a number of studies it has been demonstrated that an elevation in the concentration of glycated hemoglobin up to 1% increases the risk of developing PAD by 28% [5]. Approximately 25% of patients with DM suffer from chronic arterial insufficiency and neuropathy contributes to the clinical picture of trophic changes in the leg in 80% of these patients [6]. The pathogenesis of the development of critical lower limb ischemia in patients with DM is quite complicated. Initially, patients with DM develop atrophy of the connective tissues. At the same time, the proliferation of skin fibroblasts is reduced [7]. Further, in the presence of an inflammatory process or minimal limb injury, increases the production of matrix metalloproteinases, which leads to a disruption in the synthesis of collagen fibers [8]. Against the background of the initial changes, hyperglycemia contributes to increased production of superoxide radical, which damages the vascular endothelium. This leads to the suppression of NO, and, accordingly, retreatment in these patients. The absence of angiogenesis during the repair phase slows the healing of wounds in the leg [9]. Subsequently, the number of proteases and cytokines in the wound increases and this intensifies damage of the small vessels of the leg. Due to the presented mechanism, it is quite difficult to differentiate the primary cause of the development of critical ischemia - micro- or macroangiopathy. Damage develop in vascular system in all area of inflammatory changes. Due to this in patients with DM changes in the arteries of the lower leg are more often diagnosed, which does not allow for adequate revascularization and reduced macroangiopathy. A decrease in ankle-brachial index (ABI) to 0.50 in patients with diabetes in case of moderate stenosis of the main arteries often already leads to the need for amputation [10]. This is primarily associated with a high risk of migration of blood cells into the damaged area, which leads to micro and macro thrombosis [1, 11]. By itself, an increase in blood glucose levels reduces the ABI in patients even with minimal manifestations of PAD. Approximately 30% of patients do not have an adequate assessment of the vascular bed due to the presence of neuropathy, which reduces clinical manifestations until the onset of critical lower limb ischemia [4]. It should be noted that in patients with diabetes, the distal extremities (lower leg arteries) are more often affected, unlike patients without this disease. In smoking patients the risks of developing PAD increase by 3.5 times in men and 8.6 times in women compared to non-smokers [12]. Moreover, high amputation in this lesion has to be performed 5-15 times more often than in patients without diabetes [13]. In the clinical picture of PAD in diabetes, the same factors can be traced as for patients without diabetes. However, in most cases, there is a more distal level of damage that affects the tibial arteries [14]. DM itself enhances the inflammatory response in vascular cells and leads to their alteration. All patients with PAD have an abnormal increase in protein C, which indicates chronic inflammation. In individuals with diabetes, the values of this protein are often higher in comparison with patients without it [15]. Protein C is a risk factor for thrombosis; it enhances the procoagulant activity of hemostasis due to increased excretion of tissue factors [16]. Also, its effect is associated with the suppression of NO and plasminogen-1 activation inhibitor [13, 17]. Due to the violation of NO-mediated vasodilation, diabetes leads to severe endothelial dysfunction [18]. Of the mechanisms of this lesion, a decrease in the concentration of NO and a violation of its bioavailability for cells should be noted. This is achieved both due to impaired cell susceptibility to glucose, and due to the increased content of lipoproteins in the blood of patients with diabetes [19]. Also in the vessels there is an increase in vasoconstriction due to the synthesis of endothelin-1, impaired migration of the ovary muscle cells and activation of cytokines. All this enhances atherogenesis [20]. The altered structure of atherosclerotic plaques in patients with diabetes is considered a consequence of the induction of hyperglycemia of apoptosis of smooth muscle cells of the arterial wall, which leads to a higher frequency of their destruction and violation of the integrity of the capsule [21]. The results of surgical revascularization in patients with diabetes depend on many factors: concomitant diseases, the presence of trophic changes in the legs, neuropathy and human immune status [22]. A high level of glycated hemoglobin also increases the risks of the distal lesion and worsens the results of revascularization in situations where it is possible, and the worse long-term results in such a situation are described for both shunt operations and endovascular interventions [23]. For patients with diabetes, it is extremely important to change the lifestyle after revascularization. This allows to affect the pathophysiological changes leading to PAD. Increased physical activity, weight loss, normalization of glucose levels, adequate therapy aimed at reducing blood atherogenicity can improve long-term results of the intervention [24]. An individual selection of the method of surgical intervention, taking into account comprehensive features, the state of health of a patient with diabetes is the most important point in treatment. In this category of patients, the incidence of arthrosis (or arthritis) of the knee joint is high, in connection with this, the results of surgical revascularization in the long term are better, in comparison with endovascular procedures. Until recently, it was believed that with proximal femoral artery damage, stenting is the surgery of choice, however, recent studies show the best long-term results of bypass surgery in patients with both proximal and distal lesions of the lower limb arteries [13]. A large retrospective study examined the effects of fasting glucose on long-term surgical outcomes. Patients were divided into 2 groups: glucose level for therapy in normal values and inadequate hypoglycemic therapy. According to the study, avoidance from restenosis after 1 year of observation in group 1 was 46%, in 2-16%. The same pattern was observed in the effect on the frequency of limb amputation. In this case, the appointment of insulin in the postoperative period and the normalization of glucose did not lead to an improvement in long-term results. The authors concluded that an adequate metabolic status of an organism during an intervention is the best predictor of long-term results [25]. Critical ischemia of the lower extremities (CILE) in patients with diabetes develops more often than in people with occlusive lesions of the lower extremities without diabetes. A number of researchers demonstrate the incidence of diabetes in patients hospitalized for CILE as high as 76% [26]. To date, it is recommended that arteries be reconstructed in patients with diabetes with an estimated shunt patency of over 75% for 1 year [27]. Often, patients with CILE on the background of diabetes require more than one intervention. Regardless of tactics simultaneous reconstruction of several levels of the arteries of the lower extremities or sequential operations in these regions give a high probability of preserving the limb [26]. The correct comprehensive multidisciplinary approach to the surgical and medical treatment of patients with diabetes allowed us to obtain a similar incidence of complications and amputations in the long term compared with people without diabetes. In the presence of ulcerative defects or diabetic foot, the fact of revascularization is important, and not the method of treatment of the patient. Healing of trophic defects and preservation of the limb have similar results in patients with surgical revascularization and endovascular interventions [28]. The main goal of treating patients with CILE and diabetes is normalization of arterial inflow to the vessels of the foot using surgical and/or endovascular technologies [29]. The main problems associated with the surgical treatment of these patients are: - a distal-diffuse form of atherosclerotic lesion, which does not allow performing radical interventions with a good long-term distant result; - violation of microcirculation and microangiopathy; - increased risks of infection of a surgical wound; - lack of adequate collateral blood supply due to the high growth rate of atherosclerotic plaques [30]. Based on the above features, for a long time patients with diabetes have been denied surgical treatment, only in recent years the number of reconstructive operations in this category of patients has begun to increase worldwide [31]. Currently, reconstructive methods are the operation of choice in PAD, even in patients with diabetes. In the presence of a distal receiving bed, patients with diabetes need and justified to perform shunt operations on the femoral-tibial segment. Patency of shunts after 5 years in such patients reaches 57-93% [32]. Unfortunately, satisfactory results are shown only for auto-veins. Synthetic materials in patients with diabetes are prone to the rapid growth of neo-intima in the anastomotic zone. This led to the formation of shunt thrombosis and relapse of ischemia [33]. To date, it is generally accepted that the presence of at least one passable artery on the lower leg is an acceptable outflow pathway for performing reconstructive surgery [34]. The results of distal bypass operations vary widely in the literature. F.M. Pomposelli et al. [35] presented the experience of treating more than 1000 patients with revascularization at the level of the dorsal artery of the foot for 10 years. The primary patency of shunts was registered at the level of 56.8%, the secondary - 62.7%. Other authors reported that after a year the patency of such shunts was only 58.1%, and after 3 years - 39.5% [36]. As can be seen from these reports, the results of such interventions vary significantly, but they allow you to save the limb and/or heal the trophic arterial ulcer. The main objective for the treatment of trophic diabetic ulcers is the restoration of blood flow in the foot. In most patients with a clinic of trophic ulcers, lesions of the superficial femoral artery (SFA), popliteal artery (PA) and tibial arteries (TA) were noted. With the defeat of the latter, open surgical interventions are severely limited in technical performance. Endovascular interventions are complex due to the long occlusions that are observed in these patients (150-300 mm). For greater convenience, the “passage” of occlusion by the conductor uses retrograde tibial access. Of the minuses of the approach, an increase in the area of the ulcer should be noted if the recanalization is not successful. Often, another ulcer forms in the access area, as access is essentially a violation of the integrity of the skin, and there is no adequate perfusion in this case. In modern artery surgery, patients with diabetes increasingly use the concept of angiosomes. Due to the accumulated practical experience, areas have been identified that are supplied with various TA. Based on the data obtained, an isolated arterial revascularization is performed, which is responsible for this area. Due to normalization of blood flow, it is in the angiosomal region that the healing rate of trophic ulcers increases and the frequency of amputations decreases [37]. It is worth noting that X-ray endovascular methods allow you to save the limb on average in 86% of cases, while it is enough to perform revascularization of one artery. In diabetes mellitus, the revascularization by the presented method has higher technical success in comparison with patients without diabetes and distal lesions of the arteries of the lower extremities [38]. In an experimental study, it was shown that revascularization based on the angiosomal approach can lead to “robbing” of other parts of the leg and reduce perfusion in them [39]. Thus, it cannot be argued that endovascular revascularization is by far the most effective treatment method, it is probably one of the key tools for healing trophic ulcers and preserving the limb. It is important to note that in TA, only angioplasty should be used predominantly. Special cylinders 20-30 cm long have been developed, which allows revascularization of long stenoses and occlusions. The use of stents is justified only in complicated cases (dissection, residual stenosis of more than 50%). Given the fact that TAs have a diameter of 2.0-3.5 mm, coronary balloon expandable stents are used in case of need for stenting. Large randomized trials demonstrate that the use of drug-coated cylinders gives better long-term results compared to simple stenting [40]. One study demonstrated a lower rate of amputation in the absence of a stent in TA[41]. Modern devices for atheroectomy did not show significant positive results in the treatment of patients of this category; on the contrary, the implementation of endovascular atheroctomy led to an increase in the number of thromboses of the reconstructed artery [42, 43]. Despite the achievements of endovascular treatment methods, bypass surgery remains the best reconstruction method in terms of long-term results [44]. Arterial bypass grafting of the lower extremities has an increased risk of developing transoperative complications (myocardial infarction or stroke). At the same time, the two-year survival rate after open surgery was higher [45]. In some cases, the possibility of performing a shunt operation is described even in situations where endovascular methods have proven to be ineffective. The main factor in the impossibility of reconstruction is the lack of an adequate vein on the legs for the formation of a shunt. An adequate diameter of a filled vein is considered to be 3.5-5.0 mm, while the best long-term results are observed when using one vein, in comparison with the formation of a shunt from several sections or veins from two legs. When using a single vein, the frequency of thrombosis in the first 30 days was less than 2%, and patency during the year was above 90% [46]. In one study [47], surgery was performed using a microscope, which allowed the shunting of arteries with a diameter of less than 2 mm. Revacularization of the two leg arteries was performed in only 9.6% of cases. In the presence of a site of vein hypoplasia, resection and reversion were performed so that the site of narrowing was in the distal direction. The authors formed a “natural” decrease in diameter in the anastomotic zone. This technique made it possible to obtain 72.6% possibility of the shunt for 1 year and about 60% by the 4th year of observation. The main task of revascularization of the arteries of the lower extremities is the restoration of adequate perfusion in the tissues of the foot. With critical ischemia, the perfusion pressure of oxygen decreases to about 20 mmHg. Art. The only objective method for restoring blood flow is considered to be an increase in oxygen pressure after revascularization. The level of transcutaneous oxygen tension (TCT) is today considered a predictor of wound healing, as well as a criterion for adequately performed lower limb revascularization. With a TCT value of 40 mm Hg and higher, the trophic ulcer heals without additional surgical intervention; most surgeons seek to achieve this indicator after reconstruction of the arteries [48]. The TCT level rises after revascularization of the lower limb, regardless of the method of surgical correction [49]. However, there are a number of differences. With isolated arterial recanalization, perfusion often improves only in the region of revascularized angiosoma, with artery bypass grafting, an increase in TCTs is also observed in other angiosomes, this is especially well seen with a normally functioning plantar arch [50]. An increase in the frequency of use of the hybrid approach to surgical treatment to date has demonstrated that after initial shunting with an inadequate distal bed (on the foot), repeated angioplasty showed a higher perfusion rate and TCT level during recanalization of the foot arteries than with isolated endovascular treatment [51]. When describing the surgical treatment of PAD in patients with diabetes, all authors pointed to the need for distal reconstructions. Indeed, in practice, people with diabetes are quite rare in whom the cause of severe lower limb ischemia was the defeat of the aortic-femoral segment. According to various authors, lesions of the iliac arteries in patients with diabetes were found in no more than 20% of cases, and the femoral segment was affected in 70% of cases, of which about 15% affected the common and deep femoral artery [52]. With the initial passable aortic-femoral segment, the choice of reconstruction leaves no doubt. It is necessary to restore the distal blood flow, since there are no adequate collateral paths at the level of the knee and below. Other issues arise with stenosis above the bifurcation of the femoral artery or with lesions of both the superficial and deep femoral arteries. In such patients, microcirculation often persists, however, trophic ulcers develop due to insufficient influx along the collateral path from the iliac to the femoral arteries. When blood flow is restored to the superficial femoral artery, perfusion pressure increases and there is no need to perform distal reconstructions [53]. Thus, minimally invasive procedures, such as plasty of the deep femoral artery and endarterctomy from the common femoral artery, are of interest. Profundoplasty was described in the 60s of the last century [54]. As an isolated procedure, they have long been used only in patients with chronic lower limb ischemia and the “lack” of adequate outflow paths to the lower legs. As an element of treatment, it is used everywhere when performing femoral-distal bypass surgery. In recent years, this surgical intervention has “revived” and changed its purpose. Most patients with aortic-femoral lesions present stenosis of the deep femoral artery (DFA). A hybrid approach to treatment involves stenting the iliac arteries and performing profundoplasty to improve collateral blood supply. The freedom from restenosis with profundoplasty and plastic of the common femoral artery is 96% for 8 years [55]. To perform revascularization in patients with critical lower limb ischemia, it is possible to apply this method of surgical intervention, however, it is associated with a relatively high frequency of need for additional intervention in the future (freedom from amputations of 40% for 10 years in the presence of trophic changes in the leg). At the same time, within two years, limb preservation was noted in 70% of patients, which is comparable with distal reconstructions [56]. The study of frequency of repeated interventions for bifurcation of the FA demonstrated that 17-28% of patients had hemodynamically significant restenoses for 5 years [57]. A.V. Akhmetov [57] offers to perform extended profundoplasty to branches of the 3rd order, which improves long-term results and enhances collateral blood flow. Of the advantages of surgery only in the upper third of the thigh in patients with infected or potentially infected trophic ulcers, one should note lower risks of infection (17%), which are often represented by marginal skin necrosis and infiltration in the surgical area, while in the presence of shunts there is 3% risk of infection [58, 59]. Based on the data presented in this review, it can be concluded that modern integrated approaches to the treatment of patients with peripheral arterial disease and diabetes mellitus provide adequate long-term results for limb preservation. An important point is the restoration of the achievement of the target values of the transcutaneous oxygen tension on the lower leg and foot over 40 mm Hg after the reconstruction. None of the methods showed an “ideal” results. In this regard, we believe that comprehensive treatment is the most justified and promising for further study.


About the authors

L. A. Bokeria

Sechenov University

Author for correspondence.
Moscow, Russian Federation

V. S. Arakelyan

Sechenov University

Moscow, Russian Federation

V. G. Papitashvili

Sechenov University

Moscow, Russian Federation

Sh. Sh. Tsurtsumiya

Bakulev Scientific Center of Cardiovascular Surgery

Moscow, Russian Federation


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Copyright (c) 2019 Bokeria L.A., Arakelyan V.S., Papitashvili V.G., Tsurtsumiya S.S.

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