Revista da Associação Médica Brasileira (English Edition) Revista da Associação Médica Brasileira (English Edition)
Rev Assoc Med Bras. 2013;59:557-62 - Vol. 59 Num.06

Arteriographic findings in diabetic and nondiabetic patients with critical limb ischemia

Vanessa Prado dos Santos a, Carlos Alberto Silveira Alves b, Cícero Fidelis c, José Siqueira de Araújo Filho c

a Instituto de Humanidades Artes e Ciências Professor Milton Santos, Universidade Federal da Bahia, Salvador, BA, Brazil
b Service of Vascular Surgery, Hospital Universitário Professor Edgard Santos, Universidade Federal da Bahia, Salvador, BA, Brazil
c Faculdade de Medicina da Bahia, Universidade Federal da Bahia, Salvador, BA, Brazil


Diabetes mellitus. Atherosclerosis. Ischemia. Digital subtraction angiography. Diabetes complications


Objective: To compare angiographic findings of diabetic and nondiabetic patients with critical limb ischemia.

Methods: We included 161  patients with infrainguinal critical limb ischemia (CLI). We evaluated the clinical and arteriographic (number and presence of opacification of leg arteries) of the two groups of patients. Statistical analysis was performed using EPI-INFO.

Results: Most patients were category 5 of Rutherford's Classification and had femoropopliteal disease. Seventy-two percent of nondiabetic and 67% of diabetic patients had opacification of the fibular artery (p = 0.25), which is the most present artery in both groups. Diabetic patients had less opacification of the posterior tibial artery in the univariate analysis (29% vs. 47%, p  =  0.008). But only female sex showed a significant risk for the absence of the posterior tibial artery in logistic regression (OR = 2.6; p = 0.01).

Conclusion: The peroneal artery was the most frequently found artery in angiograms of diabetic and nondiabetic patients with CLI. Diabetic and nondiabetic patients did not differ in angiographic findings of the leg.



Diabetes mellitus (DM) is considered one of the main risk factors for peripheral vascular disease.1 The overall prevalence of peripheral arterial disease (PAD) in diabetic patients is approximately 12%.2 In Brazil, the prevalence of PAD is 10% among diabetics and 2.6% among nondiabetic patients.3 Melton et al. have shown in the monitoring of diabetic patients, that the cumulative incidence of peripheral vascular disease in this population was estimated at 15% for those with more than 10 years of diagnosis, and 45% after 20 years of disease.4 Most of these patients had absence of infrapatellar pulse4 (74% without dorsalis pedis pulse and 80% without posterior tibial pulse).

Patients with critical limb ischemia, characterized by pain at rest, ulcers or gangrene secondary to peripheral vascular disease, are at high risk of cardiovascular events such as myocardial infarction and cerebrovascular accident, as well as limb loss.1 In Brazil, studies have shown the high cost of hospitalizations for diabetic foot complications,5 and peripheral vascular disease increases the risk of amputation in these patients.6

The literature reports that although diabetic patients have a lower chance of arterial reconstruction, they seem to have similar results to others with peripheral arterial occlusive disease (PAOD) in infrainguinal revascularizations.7,8 Possible differences in the arteriographic pattern may be one of the causes of the lesser opportunity of revascularization in diabetic patients. The aim of this study is to determine whether there are differences in the angiographic pattern of diabetic and nondiabetic patients with critical limb ischemia due to infrainguinal PAOD.


The study included patients consecutively admitted for treatment of critical limb ischemia due to infrainguinal PAOD, of atherosclerotic etiology, at Hospital Universitário Professor Edgard Santos (HUPES). This research project, number 292011, was approved by the Ethics Committee in Research of HUPES

Complex in August 2011. Data collection was performed retrospectively from patients' records, clinical follow-up reports and arteriographies performed and filed at the Service of Vascular Surgery of HUPES Complex of Universidade Federal da Bahia, for inpatients admitted for treatment in the period between December 2005 and December 2011 .

During this period, the treatment records of 213 patients admitted for treatment of critical ischemia due to infrainguinal atherosclerotic disease were found and reviewed. On physical examination, all patients had normal femoral pulses, characterizing infrainguinal disease, with absence of dorsalis pedis and posterior tibial pulses. We included only those cases in which the ischemic limb arteriography was filed in the Service, with digital subtraction arteriography performed through ipsilateral femoral puncture at HUPES.

Due to the absence of documented angiographic study, 52 patients were excluded. Therefore, this study included 161 patients, which meant the treatment of 175 ischemic lower limbs. Critical bilateral ischemia was found in 14 patients during the period considered for the study, but the lower extremities with less severe disease in these cases were excluded from the analysis, totaling 161 lower limbs for final analysis.

All patients' data are recorded in the clinical follow-up files, which belong to the Service, containing detailed information on the patients. A protocol was designed to collect data from the medical records in the outpatient clinic and angio-radiology unit. The arteriographies were evaluated together by two vascular surgeons, blinded to the diagnosis of diabetes, presence of opacification of any segment of the lower-limb arteries [popliteal, anterior tibial (AT), posterior tibial (PT) and peroneal].

Patients were divided into two groups (diabetic and nondiabetic), with the aim of comparatively analyzing the arteriographic pattern in both groups. Patients were considered diabetic when they had a prior diagnosis of the disease and received treatment for it. This was also the criterion used for systemic arterial hypertension. The history of ischemic heart disease and chronic renal failure was considered according to the medical record notes of such a diagnosis, through the patient's clinical history. The patient was considered a smoker if he or she had the habit of smoking at the time of treatment.

The two groups of patients were comparatively evaluated regarding the following aspects: Rutherford Classification of the lower limb with critical ischemia,1 number of lower-limb opacified arteries at the arteriography (0 or none, 1, 2 or 3), and the presence of opacification of any segment of the AT, PT and peroneal arteries. The Rutherford classification for chronic ischemia of the lower limbs consists of the categories: (0)  asymptomatic, (1) mild claudication, (2) moderate claudication, (3) severe claudication, (4) ischemic rest pain, (5) minor tissue loss and (6) major tissue loss. Patients in categories 4, 5 and 6 are considered as having critical limb ischemia, and are at higher risk of limb loss.1

The presence of refilling of the popliteal artery was evaluated in the 117 limbs that showed occlusive disease of the femoropopliteal sector during physical assessment of pulses with absent popliteal pulse. It was considered for the analysis the presence of any opacified segment of lower-limb arteries due to the presence of advanced occlusive disease and critical ischemia in all cases, with no popliteal pulse in 117 cases and absence of both distal pulses (posterior tibial and dorsalis pedis) in all cases.

Data were tabulated in Microsoft Excel® and analyzed using Epi-info software, release 3.3.2, February 2005. The Chi-square (x2) test was used to test the association between diabetes mellitus and other qualitative variables, correlating them to the arteriographic assessment. Mean age was compared by analysis of variance (ANOVA). Logistic regression was used to analyze the risk factors that were significantly correlated to the absence of opacification of a certain artery, when they reached statistical significance (p < 0.05) in the Chi-square test, which occurred only with posterior tibial artery. The significance level was set at 5% (p < 0.05) for rejection of the null hypothesis, i.e., that there is no statistical difference between the groups regarding the studied variables.


Of the 161 patients studied, 54% were diabetic, 73% hypertensive, 67% were smokers and 53% were male. As for the topographic diagnosis of arterial obstruction through pulse examination, 73% had femoropopliteal occlusive disease, with absence of popliteal and distal pulse at physical examination, and the remaining 27% had infrapatellar disease, with normal popliteal pulse. The mean age of patients was 70.08 years, ranging between 44  and 93  years. As for the Rutherford classification1 for chronic critical ischemia, 80% of limbs were in Category 5, 15% in Category 6 and 5% in Category 4. A comparative analysis of the clinical characteristics of diabetic and nondiabetic patients is shown in Table 1. More than 90% of the cases had necrotic tissue (gangrene) and the presence of some degree of opacification of the leg arteries was studied because impacts in revascularization surgical procedures in these cases.

Table 1 - Comparative analysis of the clinical characteristics of diabetic and nondiabetic patients with critical ischemia due to infrainguinal PAOD.

When performing the evaluation of digital arteriographies of the 161 lower limbs regarding the number of leg arteries identified, most patients in both groups had only one artery at the examination (Table 2).

Table 2 - Comparative analysis of the number of opacified leg arteries in the digital angiograms of diabetic and nondiabetic patients with critical ischemia due to infrainguinal PAOD.

The 117 limbs with femoropopliteal disease were studied separately in relation to the opacification of the popliteal artery, comparing data from diabetic and nondiabetic patients, with no significant differences (Table 3).

Table 3 - Comparative analysis of the presence of opacification of leg arteries in the digital angiography of diabetic and nondiabetic patients with critical ischemia due to infrainguinal PAOD.

The peroneal artery was the one identified in most cases in both diabetics and nondiabetics (Table 3). When studying the AT artery, diabetics and nondiabetics did not differ significantly regarding its presence (Table 3). The opacification of the peroneal and AT arteries did not differ significantly between genders, and were not associated alone to SAH or smoking.

The posterior tibial (PT) artery was significantly more present in angiographic examinations of nondiabetic patients (Table 3). However, diabetic patients had a significantly higher percentage of women and hypertensive patients. Thus, using the x2 test, we evaluated the possibility of correlation of other risk factors for atherosclerosis and non-opacification of the PT artery. The female sex (21% vs. 52%, p = 0.00002), SAH (30% vs. 57%, p = 0.001), DM (Table 3) and smoking (44% vs. 25%, p = 0.009) were significantly correlated in the univariate analysis using the x2 test with opacification of the PT artery. The patients with PT opacification were also significantly younger (67 vs. 72 years, p = 0.0048). The multivariate logistic regression analysis was performed, including the variables that had statistical significance (female gender, age, smoking, diabetes and SAH), and only the female gender was significant, showing to be a risk factor for non-opacification of the posterior tibial artery in the lower-limb angiograms (p = 0.01) (Table 4).

Table 4 - Multivariate logistic regression analysis of risk factors related to the absence of opacification in the posterior tibial artery in leg angiographies.


Cardiovascular disease is the leading cause of death in the Brazilian population,9 and diabetes mellitus is one of its risk factors. A recent study shows an increase in mortality by diabetes in most Brazilian cities.10 Diabetes is also an important risk factor for peripheral vascular disease and patients with critical limb ischemia have a mortality rate of around 20% as early as in the first year after disease presentation.1 The literature shows particularities of atherosclerotic disease in diabetic patients, such as the fact that it occurs earlier, being more frequent and more severe, with diabetes being the leading cause of lower limb amputations in the world.11,12 To find characteristics and peculiarities of peripheral vascular disease in Brazil may demonstrate which population groups are more exposed to the disease, helping research on the disease treatment and prevention.

In this study, we compared diabetic and nondiabetic patients with critical limb ischemia due to PAOD and found no difference between the mean age of the two groups, which was around 70 years for both. Although the literature reports that peripheral vascular disease in diabetic patients occurs earlier,13-15 perhaps the advanced form of the disease, leading to critical ischemia, occurs later, at a similar age range of nondiabetic patients.

Overall, there was a slight male predominance. However, when comparing the groups, females were statistically more prevalent among diabetics, as shown in studies by other authors who focused on diabetic foot complications.5,16-18 This finding may be explained by a parallel with coronary heart disease, in which the protective effect of the female sex is eliminated by diabetes, as well as the fact that diabetes doubles the risk of cardiovascular disease in men and triples it in women.19,20 The higher prevalence of hypertension among diabetic patients with PAOD found in our sample has also been mentioned by other authors.6,18,21

As for the arterial territory affected by PAOD, diagnosed by physical examination of pulses, most of our patients in both groups had femoropopliteal disease. The infrapatellar disease, with normal popliteal pulse was little prevalent in our sample and the difference was not significant between diabetics and nondiabetics.

Atherosclerotic disease in diabetics, according to the literature, is prone to involvement of infragenicular arteries, with reports of a greater proportions of tibioperoneal illness among diabetic patients when compared to nondiabetic ones and lower propensity to aortoiliac disease in diabetics.8,18,22 However, histological studies have shown that atherosclerotic lesions in the lower limbs appear to have indistinguishable morphology and distribution in both groups.18,23

Our study found no differences in the angiographic patterns of diabetic and nondiabetic patients in relation to opacification of the leg arteries, except for the PT artery, with both groups having similar behavior in relation to the number of visualized arteries. However, other authors, who also performed arteriographic studies, showed differences between diabetic and nondiabetic patients, reporting that diabetics have greater infrapatellar involvement by atherosclerotic disease.21,24  A possible explanation for this may be the fact that we only included cases with critical limb ischemia, predominantly patients in category 5 of the Rutherford classification,1 with advanced atherosclerotic disease, different from the study by Jude et al.,21 who also included in their series patients with claudication.

We also differed regarding the methodology from the study by Rueda et al.,24 as we did not measure the arterial stenotic lesions in our patients, choosing to assess only the presence of opacification in some arterial segments, as we believe that the presence of this refilling has a more objective meaning, directly influencing the type of revascularization of the ischemic limb. We searched the arteriographies for the presence of any refilling of leg arteries, unlike Graziani et al.,25  who created a morphological classification of the lesions based on arteriographies only in diabetic patients with critical limb ischemia. However, the study by Graziani et al.25 is similar to ours as it found a high prevalence of combined occlusive disease in the femoropopliteal and infrapatellar sectors in diabetic patients, with high rates of occlusion in the AT and PT arteries.

Our patients also showed multisegmental peripheral vascular disease, and it is noteworthy that we termed the disease "femoropopliteal" when there was no femoral pulse on physical examination, but atherosclerosis was not exclusive in this sector. The obstructive disease was diffuse in both groups, with a minority of patients showing refilling of the three leg arteries. In cases with femoropopliteal disease, there was no difference between diabetic and nondiabetic patients in relation to the popliteal artery refilling. The presence of this refilling can mean the chance of a lower-complexity revascularization. However, this study did not consider the length of the opacified segment of the arteries.

The peroneal artery was the only one of the leg arteries that was present in most of the angiograms, in both diabetics and nondiabetics. Graziani et al.25  reported a greater incidence of occlusions, when compared to the stenosis, in the AT and PT arteries of diabetic patients, but not in the fibular artery, which showed significantly more stenoses than occlusions, which, we believe, corroborates our findings. In the 1960s, the anatomopathological study by Strandness et al.26 found that diabetics had the PT, AT and fibular arteries more frequently affected than nondiabetic patients, whereas other histological studies showed a similar pattern of atherosclerotic disease between diabetics and nondiabetics.18,27-29 While the arteriographic studies do not determine the morphological characteristics of the atherosclerotic plaque and may fail to detect it, either due to the examination technique or the presence of lesions that do not lead to significant stenoses,30 histological studies often do not analyze the entire length of the artery in question, but only sections of selected fragments.

The influence of the female gender on the arteriographic pattern of PAOD deserves to be highlighted. Women had lower percentage of PT artery opacification when compared to men. This difference remained significant after logistic regression. Nguyem et al., in a multicenter study with over 1000 patients, found that among patients with critical limb ischemia submitted to revascularization, women of black ethnicity had a higher risk of graft failure and limb loss.31 It was not the purpose of our study to establish a correlation between the angiographic pattern in women and the risk of limb loss, but such angiographic characteristics may have significance in the prognosis and treatment of these patients, which needs to be further studied. The women from our sample smoked less, but had more diabetes, more arterial hypertension and were older. These particularities of the female gender are likely to influence the pattern of PAOD and will be further studied in our research.

The literature has shown that the angiographic pattern of occlusive arterial disease has prognostic value for the limb, being a risk factor for amputations in diabetics.32 In our study, we found no differences in the angiographic pattern between diabetics and nondiabetics; it only shows the limitations inherent to a retrospective study and we did not assess whether the opacified arteries were eligible for revascularization. However, it shows new aspects of a disease with high prevalence and high rates of morbimortality. Future researches are needed aiming at the in-depth study of the peculiarities of peripheral atherosclerotic disease in diabetics and in the female gender.


In our sample of patients with advanced vascular disease of the lower limbs, diabetic and nondiabetic patients did not differ regarding the angiographic pattern of the extremity. The fibular artery was the best preserved artery in the leg arteriographies in both groups. Female patients were more likely to have PT artery involvement.

Conflicts of interest

The authors declare no conflicts of interest.

Article history:
Received 2 May 2012
Accepted 6 July 2013

Study conducted at Complexo Hospitalar Universitário Professor Edgard Santos, Universidade Federal da Bahia, Salvador, BA, Brazil.

* Corresponding author.
E-mail:"> (V.P. Santos).


1. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-society consensus for the management of peri pheral arterial disease (TASC II). J Vasc Surg. 2007;45(Suppl S): S5-67.
2. Lavery LA, Armstrong DG, Wunderlich RP, Trendwell J, Boulton AJM. Diabetic Foot Syndrome: evaluating the prevalence and incidence of foot patology in Mexican Americans and non-hispanic whites from a diabetes disease management cohort. Diabetes Care. 2003;26:1435-8.
3. Brasil. Ministério da Saúde. Diabetes mellitus como problema de saúde pública. In: Manual de Diabetes. 2nd ed. Brasília: Ministério da Saúde;1993. 92 p.
4. Melton LJ III, Macken M, Palumbo PJ, Elveback LR. Incidence and prevalence of clinical peripheral vascular disease in a population-based cohort of diabetic patients. Diabetes Care. 1980;3:650-4.
5. Rezende KF, Nunes MAP, Melo NH, Malerbi D, Chacra AR, Ferraz MB. Internações por Pé Diabético: Comparação entre o Custo Direto Estimado e o Desembolso do SUS. Arq Bras Endrocrinol Metab. 2008;52:523-30.
6. Santos VP, Silveira DR, Caffaro RA. Risk factors for primary major amputation in diabetic patients. São Paulo Med J. 2006;124:66-70.
7. Fratezi AC, Albers M, De Luccia N, Pereira CA. Outcome and quality os life of patients with severe chronic limb ischemia: a cohort study on the influence of diabetes. Eur J Vasc Endovasc Surg 1995;10:459-65.
8. Mueller MP, Wright J, Klein SR. Diabetes and peripheral vascular disease. In: Vascular surgery: principles and practice. 2nd ed. New York: McGraw Hill;1994. p. 514.
9. Schmidt MI, Duncan BB, Azevedo e Silva G, Menezes AM, Monteiro CA, Barreto SM, et al. Doenças crônicas não transmissíveis no Brasil: carga e desafios atuais. Lancet. 2011;4: 61-74. (Série Saúde no Brasil).
10. Mattos PE, Luz LL, Santiago LM, Mattos IE. Tendência da mortalidade por diabetes melito em capitais brasileiras, 1980-2007. Arq Bras Endrocrinol Metab. 2012;56:39-46.
11. Slovenkai MP. Foot problems in diabetes. Med Clin North Am. 1998;82:9948-70.
12. De Luccia N. Doença vascular e diabetes. J Vasc Bras. 2003;2: 49-60.
13. Pratt TC. Gangrene and infection in the diabetics. Med Clin North Am. 1965;49:987-1004.
14. Lo Gerfo FW, Coffman JD. Vascular and microvascular disease of the foot in diabetes: implications for foot care. N Engl J Med. 1984;311:1615-9.
15. Drouet L. Atherothrombosis in diabetes - its evolution and management. Diabetes Obes Metab. 1999;1:37-47.
16. Cameron HC, Leonard J, Robinson MP. Amputations in the diabetic: outcome and survival. Lancet. 1964;2:605-7.
17. Lira JRS, Castro AA, Pitta GBB, Figueiredo LFP, Lage VMM, Miranda Júnior F. Prevalência de polineuropatia sensitive-motora nos pés no momento do diagnóstico do diabetes melito. J Vasc Bras. 2005;4:22-6.
18. Santos VP, Caffaro RA, Pozzan G, Saieg MA, Castelli Jr V. Comparative histological study of atherosclerotic lesions and microvascular changes in amputated lower limbs of diabetic and nondiabetic patients. Arq Bras Endrocrinol Metab. 2008;52:1115-23.
19. Nathan DM. Long-term complications of diabetes mellitus. N Engl J Med. 1993;328:1676-84.
20. Kannel WB, Daniel LM. Diabetes and cardiovascular disease: the Framinghan Study. JAMA. 1979;241:2035-8.
21. Jude, EB, Oyibo SO, Chalmers N, Boulton AJ. Peripheral arterial disease in diabetic and nondiabetic patients. Diabetes Care. 2001;24:1433-7.
22. Langer B, Aguiar ET, Wolosker N. Complicações vasculares do diabetes. In: Tratado de Endocrinologia Clínica. São Paulo: Roca;1992. p. 787-97.
23. Cowell JA, Lopes-Virela M, Haluska PV. Pathogenesis of atherosclerosis in diabetes mellitus. Diabetes Care. 1981;4: 121-33.
24. Rueda CA, Nehler MR, Perry DJ, McLafferty RB, Casserly IP, Hiatt WR et al. Patterns or artery disease in 450 patients undergoing revascularization for critical limb ischemia: implications for clinical trial design. J Vasc Surg. 2008;47:995-1000.
25. Graziani L, Silvestro A, Bertone V, Manara E, Andreini R, Sigala A, et al. Vascular involvement in diabetic subjects with ischemic foot ulcer: a new morphologic categorization of disease severity. Eur J Vasc Endovasc Surg. 2007;33:453-60.
26. Strandness Junior DE, Priest RE, Gibbons GE. Combined clinical and pathologic study of diabetic and nondiabetic peripheral arterial disease. Diabetes. 1964;13:366-72.
27. Goldenberg S, Alex M, Joshi RA, Blumenthal HT. Nonatheromatous periferal vascular disease of the lower extremity in diabetes mellitus. Diabetes. 1959;8:261-73.
28. Conrad MC. Large and small artery occlusion in diabetics and nondiabetics with severe vascular disease. Circulation. 1967;36:83-91.
29. Ferrier TM, Q´Land MRACP. Comparative study of arterial disease in amputated lower limbs from diabetics and nondiabetics (with special reference to feet arteries). Med J Australia. 1967;1:5-11.
30. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull Junior W, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Circulation. 1995;92:1355-74.
31. Nguyem LL, Hevelone N, Rogers SO, Bandyk DF, Clowes AW, Moneta G L, et al. Disparity in outcomes of surgical revascularization for limb salvage. Circulation. 2009;6:123-30.
32. Faglia E, Favales F, Quarantiello A, Calia P, Clelia P, Brambiella G, et al. Angiographic evaluation of peripheral arterial oclusive disease and it´s role as a prognostic determinant for major amputation in diabetic subjects with foot ulcers. Diabetes Care. 1998;21:625-30.
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