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Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 1  |  Issue : 1  |  Page : 6-13

Limb salvage following successful infra-inguinal revascularization in diabetic patients


Vascular and Endovascular Research Center, Johns Hopkins Bayview Medical Center, Johns Hopkins University, Baltimore, MD, USA

Date of Web Publication10-Jul-2018

Correspondence Address:
Mahmoud B Malas
Professor of Surgery, Johns Hopkins University, Director of The Center for Research Excellence and Surgical Trials, Johns Hopkins Hospital, Director of Endovascular Surgery, Johns Hopkins Bayview Medical Center, 4940 Eastern Avenue, Baltimore, MD 21224
USA
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/VIT.VIT_4_18

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  Abstract 

BACKGROUND: Diabetes is a major risk factor for peripheral artery disease (PAD). Infrainguinal bypass surgery (IBS) has been the modality of choice for limb salvage in PAD patients. It is well known that diabetic patients have different disease progression than nondiabetics. Therefore, it is important to assess the outcomes and to determine the efficacy of current surgical practices for limb salvage in the diabetic population. The aim of this study is to evaluate short-term and long-term outcomes after IBS in diabetic patients.
MATERIALS AND METHODS: We identified all patients who underwent IBS at our hospital from 2007 to 2014. Explanatory analysis using Pearson's Chi-square test, Fischer's exact test, and Student's t-test was performed. Kaplan–Meier analysis was used to evaluate primary patency, primary-assisted patency, and limb loss. Multivariate Cox regression analysis was implemented to examine loss of patency and amputation after adjusting for patients' demographics and comorbidities.
RESULTS: A total of 428 IBSs were performed. Out of those, 264 (62%) were diabetic. Diabetic patients presented on average of 3 years earlier than nondiabetics (66.3 [11.0] vs. 68.9 [11.9], P = 0.03) and had significantly higher comorbidities including dyslipidemia (58% vs. 45% P = 0.01), coronary artery disease (70% vs. 46%, P = 0.01), and chronic kidney disease (20% vs. 2%, P = 0.001). There were more diabetics who presented with critical limb ischemia (CLI) (92% vs. 80%, P < 0.001). There was no difference in all-cause mortality over the study period between the two groups (35% vs. 27%, P = 0.11), but diabetics had three times higher major amputation rates (17% vs. 6%, P = 0.001). After adjusting for potential confounders, the risk of amputation was 2.7 times higher in diabetics (hazard ratio [HR] =2.66, 95% confidence interval [CI]: 1.24–5.72, P = 0.001) with no statistically significant difference in loss of primary patency (HR = 1.23, 95% CI: 0.78–1.94, P = 0.37) or primary-assisted patency (HR = 0.98, 95% CI: 0.58–1.64, P = 0.94).
CONCLUSIONS: In this study, we found no significant difference in graft patency between diabetic and nondiabetic patients; however, limb loss was almost four folds higher in diabetics with CLI after IBS. This suggests that additional factors after revascularization play an important role in limb salvage in diabetics. Further prospective study in a larger cohort of patients is suggested to evaluate the outcomes of IBS and endovascular therapy in diabetic patients.

Keywords: Diabetes, infrainguinal bypass surgery, peripheral artery disease


How to cite this article:
Rizwan M, Nejim B, Aridi HD, Locham SS, Reifsnyder T, Malas MB. Limb salvage following successful infra-inguinal revascularization in diabetic patients. Vasc Invest Ther 2018;1:6-13

How to cite this URL:
Rizwan M, Nejim B, Aridi HD, Locham SS, Reifsnyder T, Malas MB. Limb salvage following successful infra-inguinal revascularization in diabetic patients. Vasc Invest Ther [serial online] 2018 [cited 2018 Aug 21];1:6-13. Available from: http://www.vitonline.org/text.asp?2018/1/1/6/236294


  Introduction Top


The prevalence of peripheral arterial disease (PAD) is on the rise.[1],[2] Diabetes is a strong risk factor for PAD along with other factors such as old age, male gender, smoking, obesity, hypertension (HTN), and hyperlipidemia.[1],[3],[4],[5],[6],[7] In diabetics, PAD has a subtle presentation and patients may not present until an advanced stage of the disease due to diabetes-related complications, such as neuropathy, which complicates the disease course and its treatment.[8],[9] Moreover, the presence of PAD suggests a more complex diffuse atherosclerotic disease and higher cardiovascular morbidity and mortality. Foot ulcer is a common complication of diabetic foot and a strong risk factor for major and minor lower extremity amputation in diabetic patients.[10],[11] Diabetes is also associated with rapid and more diffuse disease progression of atherosclerotic vascular disease.[12] In this era of increasing trend toward minimally invasive endovascular revascularization treatment strategies for PADs, infrainguinal bypass surgery (IBS) remains the modality of choice for the treatment of advanced PAD. These treatment strategies are sometimes combined when needed. Although many studies have reported the fast progression and poor outcomes of PAD in diabetics, data about its course in these patients after IBS are controversial.[3],[5],[12],[13],[14] The purpose of this study is to evaluate the outcomes of contemporary surgical practices in the treatment of advanced PAD in diabetic patients. This study compares short- and long-term outcomes after lower extremity bypass between diabetics and nondiabetics including overall survival, reintervention, amputation-free survival, primary and primary-assisted patencies, and predictors of mortality, amputation, and patency.


  Materials and Methods Top


The Johns Hopkins Institutional Review Board approved this study. The need for patients' informed consent was waived due to the use of de-identified data. A retrospective analysis was performed for all PAD patients who underwent IBS using autogenous vein conduits at our institution from January 2007 to July 2014. Patients who received prosthetic conduits for bypass were excluded.

Covariates

Electronic medical records at the time of surgery were abstracted for patient demographics (age, race, and gender), comorbidities (diabetes mellitus [DM], HTN, coronary artery disease [CAD], myocardial infarction [MI], stroke, chronic kidney disease, hemodialysis [HD], and hyperlipidemia), clinical presentation (claudication and critical limb ischemia [CLI]), type of anesthesia (general, spinal, and regional), level of bypass (femoropopliteal, femorotibial, popliteal-tibial/pedal), and type of bypass conduit (reversed and nonreversed saphenous vein and arm veins).

Operative selection and vein mapping

Our institution practices favor IBS over endovascular interventions for patients presenting with TransAtlantic Inter-Society Consensus II (TASC II) C lesions and for all patients with TASC D lesion and those with diffuse multilevel disease or have failed prior multiple endovascular treatments. Autogenous veins are the preferred bypass conduits. We maximize our efforts to obtain autogenous vein conduit including small saphenous and upper limb veins if the greater saphenous vein is not available or unsuitable. Prosthetic bypass conduits are the very last option after failing to obtain any autogenous vein. To assure identifying suitable vein, we routinely perform vein mapping. Our cutoff vein diameter is 3–3.5 mm. The size is confirmed intraoperatively. These efforts toward the use of autogenous vein conduits for IBS have resulted in the use of autogenous veins in 95% of all our bypasses. Only 5% of IBSs were done with prosthetic conduits over the study period and were excluded from the study cohort.

Follow-up and outcomes

Main outcomes of this study are mortality, limb salvage, amputation-free survival, and primary and primary-assisted patencies.

Primary and secondary patencies were defined in accordance with the Society for Vascular Surgery reporting standard.[15] Reintervention is defined as open or endovascular measures to maintain the patency. Postoperative routine follow-up visits are held every 3 months in the 1st year and yearly thereafter. Physical examination and arterial Doppler and duplex scans are performed routinely on every visit. Angiography is performed for significant graft stenosis (defined as spectrum broadening with peak systolic velocity >350 cm/s, ratio >3.5 to prelesion velocity, and velocity <50 cm/s distal to stenosis). Relevant data including graft thrombosis, graft stenosis, interventions for thrombosis or stenosis, number of interventions, medications including aspirin and statins, minor and major amputation, and death were collected. Death was confirmed with social security death index. Selection of interventions to maintain the patency of the bypass graft depends on the presentation and associated factors. We usually use endovascular approach first, whereas open procedures are performed when endovascular interventions fail to maintain the patency.

Statistical methods

Explanatory analysis using Pearson's Chi-square test, Fischer's exact test, and Student's t-test was performed. Kaplan–Meier analysis was used to evaluate primary patency, primary-assisted patency, limb loss, and amputation-free survival at 5 years of follow-up. Multivariate Cox hazard regression analysis was implemented to examine loss of patency and amputation while adjusting for patients' demographics, comorbidities, medications, graft type, and bypass level. The analysis was performed using STATA Statistical Software Version 14.1 (StataCorp, College Station, Texas, USA). Statistical significance was accepted at P 0.05.


  Results Top


Patients' characteristics

A total of 428 lower extremity IBSs using autogenous vein grafts were performed in 367 patients over a period of 7.5 years. Of these, 264 (62%) were diabetic. Mean age of diabetic and nondiabetic patients was 66.3 years (standard deviation [SD]: 11.0) and 68.9 years (SD: 11.9), respectively (P = 0.02). Diabetic patients had significantly more comorbidities such as HTN (94.3% vs. 87.2%, P = 0.01), CAD (70.1% vs. 46.3%, P < 0.001), history of MI (37.5% vs. 23.2%, P = 0.002), history of stroke (21.2% vs. 11.0%, P = 0.006), dyslipidemia (58.3% vs. 45.1%, P = 0.008), and HD (19.7% vs. 2.4%, P < 0.001) as compared to nondiabetics. CLI was present in 92.1% of diabetics compared to 79.9% (P < 0.001) of nondiabetics. Saphenous vein grafts were used in 83.7% of diabetics versus 84.2% of nondiabetics (P = 0.91). IBSs were 27.7% femoropopliteal, 38.3% femorotibial, and 34.1% popliteo-tibial/pedal in diabetics. Detailed patient characteristics and other procedural details are shown in [Table 1].
Table 1: Patient demographics and characteristics

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Outcomes

Mean follow-up time of this cohort was 1.8 ± 1.8 years. Absolute all-cause mortality was 34.9% in diabetics versus 27.4% in nondiabetics over the study period (P = 0.11). The majority of patients in both groups did not have any secondary intervention (71.6% vs. 70.1%, P = 0.06). Rates of surgical wound infection requiring antibiotics were 1.5% in diabetics compared to 1.2% in nondiabetics (P = 0.80). The rate of major amputation was found to be almost three folds higher in diabetic patients compared to nondiabetic patients (16.7% vs. 5.5%, P = 0.001) [Table 2].
Table 2: Absolute outcomes after infrainguinal bypass surgery in diabetics versus nondiabetics

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In diabetic patients, overall primary patency was 70.5%, 59.4%, and 44.3% compared to 74.1%, 64.1%, and 52.4% in nondiabetics at 1, 3, and 5 years, respectively [Figure 1]. Primary-assisted patency in diabetics was 81.5%, 67.3%, and 54.1% versus 83.5%, 73.5%, and 58.8% in nondiabetics at 1, 3, and 5 years, respectively [Table 3] and [Figure 2]. On univariate analysis, no difference in overall primary and primary-assisted patencies was noted between the two groups (P = 0.32 and 0.41, respectively). However, when stratified with respect to different bypass levels, primary and primary-assisted patencies were different between the two groups at femorotibial and popliteal-tibial levels [Table 4]. At 5 years, femorotibial bypass in diabetics had significantly lower primary patency (30.7%, 95% confidence interval [CI]: 8.9–56.2) versus in nondiabetics (49.3%, 95% CI: 10.5–80.2, P = 0.02) and primary-assisted patency (34.6%, 95% CI: 7.7–64.4) versus in nondiabetics (56.0%, 95% CI: 9.5–86.7, P = 0.03). Amputation-free survival in diabetics was 82.6%, 77.9%, and 73.5% versus 95.5%, 91.6%, and 91.6% in nondiabetics at 1, 3, and 5 years, respectively (P = 0.0005) [Table 3] and [Figure 3].
Figure 1: Kaplan–Meier curve estimating the primary patency

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Table 3: Primary patency, primary-assisted patency, and amputation-free survival in diabetics versus nondiabetics following infrainguinal bypass surgery

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Figure 2: Kaplan–Meier curve estimating the primary-assisted patency

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Table 4: Primary and primary-assisted patency in diabetics versus nondiabetics stratified by bypass level

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Figure 3: Kaplan–Meier curve for amputation-free survival

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After adjusting for potential confounders, diabetes was not significantly associated with loss of primary or primary-assisted patency [Tables 5] but was significantly associated with an increased hazard of major amputation (hazard ratio [HR] =2.66, 95% CI: 1.24–5.72, P = 0.001) [Table 6]. Male gender was associated with lower hazards of limb loss. Popliteo-tibial/pedal bypass was also associated with higher hazards of limb loss in diabetic population (HR = 2.81, 95% CI: 1.28–6.21, P = 0.01). Hyperlipidemia was another factor that was associated with the loss of primary-assisted patency (HR = 1.62, 95% CI: 1.00–2.6, P = 0.05) [Table 6]. Nonsaphenous vein graft did not increase the hazard of major amputation compared to saphenous veins (HR = 2.22, 95% CI: 0.88–5.58, P = 0.09).
Table 5: Cox regression of the predictors of loss of primary and primary assisted patency

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Table 6: Predictors of amputation, Cox regression

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  Discussion Top


Patients with diabetes have a fast progression of their PAD and are more likely to have additional risk factors such as HTN and hyperlipidemia.[3],[5],[16],[17] The presence of PAD suggests more advanced and diffuse atherosclerotic disease in the coronary and carotid arteries, leading to increased risk of MI and stroke.[18],[19] In this study, diabetic patients had significantly higher prevalence of coronary and cerebrovascular events, suggesting a more aggressive and complex disease.

In our prior analysis of all patients, the primary and primary-assisted patency rates were 55% and 64%, respectively, at 5 years.[20] In the current study, the overall primary patency at 1 year was 70.5% in diabetic patients compared to 74.1% of nondiabetics. After 5 years, those rates were 54.2% versus 59.0%, respectively (P = 0.33). Similarly, for primary-assisted patency, the rates at 1 and 5 years were 81.5% and 60.1% for diabetics compared to 83.5% and 66.1% for nondiabetics, respectively (P = 0.39). However, when stratified by bypass-level diabetic patients had lower 5-year primary and primary-assisted patencies of femorotibial and popliteal-tibial/pedal bypasses compared to nondiabetics patients on univariate analysis ([primary patency at 5 years for femoropopliteal bypass in diabetics vs. nondiabetics, 52.7% vs. 54.3%, P = 0.83] and [primary patency at 5 years for femorotibial bypass: diabetics vs. nondiabetics 30.7% vs. 49.3%, P = 0.02]) ([primary-assisted patency at 5 years for femoropopliteal bypass in diabetics vs. nondiabetics, 52.7% vs. 54.3%, P = 0.52] and [primary-assisted patency at 5 years for femorotibial bypass: diabetics vs. nondiabetics 30.7% vs. 49.3%, P = 0.03]). However, after adjusting for patient's demographics, comorbidities, and conduit types in the regression model, there is no significant difference in the rates of primary and primary-assisted patencies between the two groups. This suggests that advanced disease and aggressive comorbidities in diabetic patients are contributing to lower long-term patency for distal bypasses in diabetic patients. Our patency rates are comparable to many previously published studies showing similar graft patency in diabetics vs. nondiabetics after IBS [13],[21],[22] and are in line with the ACC/AHA 2005 Practice Guidelines for the Management of Patients with PAD, where the overall 5-year patency ranges from 66% to 80% depending on the different levels of bypass.[23] However, our patency rates were higher than few prior studies, especially those who did not use autogenous vein exclusively as a bypass conduit.[22],[24] The discrepancy in patency among different bypass conduit types further strengthens the evidence of the superiority of autogenous vein conduit in patients undergoing IBS.[14],[25],[26] Our study emphasizes the importance of maximizing the efforts on using autogenous vein conduits to achieve better patency and overall outcomes of the IBS procedures in PAD patients, especially in diabetic patients who are at inherited higher risk of graft failure and wound infection.

Although limited by the small numbers when stratified by the bypass level, the primary and primary-assisted patencies were particularly worse for diabetic patients receiving femorotibial bypass. The distal repair is generally associated with worse outcomes, but apparently, this association was intensified in the presence of DM.[20],[27]

Diabetic patients had similar primary and primary-assisted patencies to nondiabetics over the study period; however, they had three times higher amputation rates (17% vs. 6%, P = 0.001) after IBS compared to nondiabetics. After adjusting for comorbidities and graft characteristics, the hazard of amputation was 2.6 times higher in diabetics (HR = 2.7, P = 0.01). Overall, these rates are in line with prior studies reporting limb salvage rates following IBS. Results from the Bypass versus Angioplasty in Severe Ischemia of the Leg Trial showed 91% amputation-free survival at 2 years in patients who underwent lower extremity bypass.[28] Amputation-free survival in our study was significantly different in diabetics and nondiabetics. Amputation-free survival in diabetics was 82.6% and 73.5% versus 95.5% and 91.6% in nondiabetics at 1 and 5 years, respectively (P = 0.0005). Several other studies have also previously shown that diabetics have higher rates of amputation compared to nondiabetics after lower extremity bypass surgery,[29],[30],[31],[32] while few other studies have shown similar rates of limb salvage in diabetics and nondiabetics following lower extremity bypass.[21],[22],[33] In a single-institutional retrospective study, Hertzer et al. showed similar results to our analysis with diabetes not affecting the patency but adversely affected the limb salvage following the bypass (amputation HR = 1.5, 95% CI: 1.0–2.1, P = 0.026).[29] In another prior study using nationwide vascular registry by Virkkunen et al., 30-day postoperative amputation rates were twice as much in diabetics as compared to nondiabetics (6.5% vs. 3.3%, P < 0.001).[31] Other factors associated with higher amputation rates in our study were the female gender, distal versus proximal level of the bypass, and hyperlipidemia. On multivariate analysis, male gender was shown to reduce the risk of amputation by 37% (odds ratio = 0.63, 95% CI: 0.38–1.02). This finding is in line with a prior large multicenter study by Egorova et al., which showed that the female gender was associated with poor outcomes of amputation and mortality.[34] In that study, females were more likely to undergo emergent admissions which can partly explain the higher amputation rates. Higher amputation rates in diabetics after successful revascularization of lower limb in this study and prior literature suggest the importance of better control of diabetes and its related complications for limb salvage even after revascularization. Use of a multidisciplinary approach for PAD in diabetic patients is warranted to maximize the limb salvage.

This study should be considered in the light of certain limitations. The single-center retrospective nature of this study might limit the generalizability of the results. Moreover, the mean follow-up time was 1.8 ± 1.8 years; thus, long-term outcomes should be interpreted with caution. In addition, no sufficient information about glycemic control was available for the entire period of the study, which might have provided some insights about the impact of diabetes control on outcomes. Nonetheless, we believe that this study was successful in accomplishing its aim in adding to the current evidence that limb salvage in diabetic patients is multifactorial and relies on additional factors after successful revascularization.


  Conclusions Top


This study suggests the similar effectiveness of infrainguinal bypass in diabetic and nondiabetic patients with advanced PAD. However, compared to nondiabetics, diabetic patients are at a higher risk of secondary amputation after infrainguinal bypass. Better control of diabetes and its related complications are needed to maximize the effectiveness of limb revascularization and reduce secondary amputation rates.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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