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Jornal Vascular Brasileiro

versão impressa ISSN 1677-5449

J. vasc. bras. vol.9 no.1 Porto Alegre  2010 



Prevalence of atherosclerotic stenosis of celiac trunk and superior mesenteric artery in occlusive arteriopathy of lower limbs



Wenes Pereira ReisI; Josileide GaioII; César Reis JúniorIII; Daniel Reis WaisbergIV; Marly KlugV; Robson Barbosa MirandaVI; Jaques WaisbergVII

ICirurgião Vascular, Serviço de Ultrassonografia, Centro de Terapia e Diagnóstico por Imagem (CIM), Hospital Beatriz Ramos, Indaial SC
IIPsicóloga, Universidade Regional de Blumenau, Blumenau, SC
IIIMédico residente, Serviço de Cirurgia Geral, Loma Linda University Medical Center, Califórnia, EUA
IVAcadêmico de Medicina, Faculdade de Medicina da Universidade de São Paulo (FMUSP), São Paulo, SP
VAcadêmica de Enfermagem, Universidade Regional de Blumenau, Blumenau, SC
VICirurgião Vascular, Faculdade de Medicina da Fundação ABC, Santo André, SP
VIICirurgião, Serviço de Gastroenterologia Cirúrgica, Instituto de Assistência Médica ao Servidor Público Estadual (IAMSPE), São Paulo, SP





Background: The occasional relationship between arterial atherosclerosis of lower limbs and atherosclerosis of intestinal arteries has not been fully studied yet.
Objective: To assess the presence of lesions with ≥ 70% stenosis in the superior mesenteric artery and/or in the celiac trunk in patients with chronic obstructive arteriopathy of the lower limbs, using vascular ultrasound (Doppler).
Method: Two groups were involved, a treatment group and a control group, each comprising 60 patients (40 men and 20 women). The treatment group consisted of patients with chronic obstructive arterial disease of the lower limbs, limiting intermittent claudication or rest pain, and/or trophic lesions of the extremities but no gastrointestinal complaints. The control group comprised patients without obstructive arterial disease of the lower limbs or gastrointestinal complaints. Diabetes mellitus, arterial hypertension, obesity, angina/infarct, smoking or dyslipidemia were considered risk factors. All the patients were submitted to vascular ultrasound of the celiac trunk and superior mesenteric artery. The patients in the treatment group were divided according to the presence of limiting intermittent claudication (n = 12) or trophic lesion and/or rest pain (n = 48).
Results: A significant association was found between age (p = 0.04) and presence of ischemic cardiopathy (p = 0.04) with atherosclerosis of the superior mesenteric artery. The risk factors showed no significant association with the presence of stenosis of the celiac trunk. A significant association was found between the presence of arteriopathy of the lower limbs and stenotic lesion of the superior mesenteric artery (p = 0.006) and the celiac trunk (p < 0.001).
Conclusions: On vascular ultrasound, a finding of peripheral arteriopathy of the lower limbs suggests the presence of stenotic lesion in the superior mesenteric artery and /or the celiac trunk. The atherosclerosis in the superior mesenteric artery is associated with ischemic cardiopathy and advanced age.

Keywords: Stenosis, vascular ultrasound, superior mesenteric artery, celiac trunk.




Although the presence of atherosclerosis of digestive arteries is a frequently observed condition, it is common to encounter asymptomatic patients with marked stenosis or even complete occlusion of digestive arteries. This is due to the development of a profuse circulatory system of replacement of digestive arteries among themselves.1-3

The systemic nature of the atherosclerotic process contributes for the development of concomitant disease in other territories, such as cerebral and cardiac.4 Consequently, patients with lower limbs atherosclerosis present a higher risk of myocardial ischemia and infarct, besides cerebral stroke; these conditions may result in death.4,5 Moreover, atherosclerosis is responsible for approximately 90% of renal stenotic lesions.6,7

Patients with chronic mesenteric ischemia frequently present atherosclerotic disease in lower limbs and coronary and carotid arteries.8 However, the relation between intestinal arteries atherosclerosis with lower limbs atherosclerosis have received little attention.

For a long time, the study of digestive arteries was performed through autopsies9,10 and arteriographies.5,11 There are, notwithstanding, some restrictions to the latter due to its invasiveness and possible complications.12,13

Studies on intestinal circulation comparing vascular arteriography and Doppler ultrasound have granted this exam credibility to assess arterial circulation of lower limbs and, more recently, of intestinal arteries.14-16 Vascular Doppler ultrasound is considered a simple performance, non-invasive and inexpensive method,6,12,17 which permits the study of intestinal arteries circulation in a less invasive manner and assess the flow in celiac trunk (CT) and superior mesenteric artery (SMA), in addition to flow direction and speed in these arteries. The performance of the exam may be hindered by obesity, intestinal loops superposition or by the presence of ascites.18-20

In accordance with most authors,6,12,1,21 the most widely accepted criterion for diagnosing stenosis of 70% or more of digestive arteries' lumen with vascular Doppler ultrasound is the one adopted by Moneta et al.,16 who considers the degree of stenosis important when, in the patient systolic peak speed is ≥ 200 cm/s at CT and ≥ 275 cm/s at SMA. Moneta et al.16 have observed that the absence of flow or systolic peak speed ≥ 200 cm/s at CT and the absence of flow or systolic peak speed ≥ 275 cm/s at SMA reveal arterial segment with significant stenosis.

This study aimed at assessing, through Doppler vascular ultrasound, the prevalence of occlusive lesions at the CT and SMA in patients with lower limbs occlusive arteriopathy.



The research project was approved by the Research Ethics Committee of the Hospital do Servidor Público Estadual, São Paulo, SP, and by the Research Ethics Committee of the Beatriz Ramos Hospital, Indaial SC. The study was performed in accordance with ethical standards accepted by the Declaration of Helsinki of the World Medical Association, adopted in 1869 and amended in 1996.

Two series of patients were studied, one designed as treatment group and the other as control group, both consisting of 60 patients. The treatment group comprised patients presenting occlusive arteriopathy of the lower limbs. Control group was represented by patients who did not have diagnosed intestinal disease or arteriopathy of the lower limbs and were invited to participate in the current study as volunteers.

Both groups were paired according to sex and age. In each group, 40 male and 20 female individuals were assessed. Mean age of the treatment group patients was 66±11 years (39-93 years), while in control group it was 65±10 years (36-91 years).

In each group clinical-demographic data (age, sex, ethnicity and presence of pre-existing diseases) and risk factors for arteriopathy (diabetes mellitus, systemic hypertension, obesity, angina/infarct, smoking and dyslipidemia) were assessed.

Individuals who presented Body Mass Index > 30 (weight/height2) were considered obese.22

Individuals with total cholesterol serum level > 200 mg/dL, LDL cholesterol > 100 mg/dL, HDL cholesterol < 40 mg/dL and triglycerides serum level > 150 mg/dL were considered dyslipidemic.23 Individuals with systolic or diastolic hypertension ≥ 140 and ≥ 90 mm Hg, respectively were considered hypertensive.24 Individuals with glycaemia > 126 mg/dL after an 8 hours fasting were considered diabetic.25,26

All the patients in the treatment group presented lower limbs arteriopathy symptoms as intermittent claudication or trophic lesions at the extremities, with or without rest pain, but no symptoms related to digestive arterial alterations. Control group had lower limb occlusive arterial disease and their members were also asymptomatic in relation to arterial occlusive disease of digestive circulation.

At vascular physical exam the intensity of arterial pulses in the lower limbs was assessed using the subjective criterion of 0 to 3 intensity crosses, thus considered: 0 = absence of pulses; + = significant decrease of pulses; ++ = mild decrease; +++ = normal pulses.27 The pathway of lower limbs arteries was auscultated in order to detect occasional presence of souffles.

Individuals in the treatment group were classified according to the presence, in the general clinical picture, of intermittent claudication or, on the other hand, trophic lesion and/or rest pain. The former was constituted by 12 (20%) patients (8 men and 4 women), and the latter by 48 patients (32 men and 16 women).

To depict the degree of ischemia of the studied limb, blood pressure (BP) was measured in lower and upper limbs, thus obtaining the ankle-arm index, in which the numerator is the ankle's systolic BP, and the denominator, the upper limb systolic BP. The normal value was considered to be 0.9.28

All the patients, both in the treatment group and the control group, were submitted to ultrasound of intestinal arterial circulation using a vascular ultrasound device equipped with Doppler (model HDI 5000, ATL®, Bothell, WA, USA) and 2-5 MHz convex transducers.

The patients were examined in supine position after 12 hours fasting with the ultrasound device's transducer at the position corresponding to the cutaneous projection of the CT and the SMA in the epigastric region in longitudinal insonation. Assessment with Doppler was performed in the most representative segment of the flow of the artery studied. Ostium and the first CT and SMA centimeters were studied for flow analysis. Speeds ≥ 200 cm/s at CT and ≥ 275 cm/s at SMA characterized stenosis ≥ 70% in these arteries.16 In treatment and control group individuals who did not present any sign of arterial blood flow at ultrasound assessment, the presence of vase occlusion was configured. Ultrasound exams had a mean duration of 14±1,5 minutes.



Comparison between treatment and control groups

The treatment and control groups were homogeneous in age and sex. The treatment group presented a higher proportion of patients with diabetes mellitus, hypertension and smoking if compared to the control group (p < 0.05). There was no significant difference in the proportion of obese, dyslipidemic patients and those carrying angina or previous stroke between treatment and control groups (p > 0.05) (Table 1).



None of the patients in the control group presented SMA or CT lesion. The treatment group presented a higher proportion of patients with SMA or CT lesion than the control group (p = 0.006 and p < 0.001, respectively). It was observed that, regardless of the level of impairment of the patient's peripheral circulation, most of them (70%) did not present lesion in any of the two arteries assessed and, thus, there was no significant association between peripheral impairment and intestinal arterial lesion (p = 0.55) (Table 2).



Among the 60 patients with lower limbs arteriopathy (treatment group) SMA lesion was observed in 8 (13.3%) [confidence interval 95% (CI95%) 5.9-24.6%]. In relation to CT, it was observed that of the 60 lower limb arteriopathy patients, 14 (23.3%) presented CT lesion (CI95% 13.3-36%) (Table 3).



It was also observed that 42 lower limb arteriopathy patients (70%) presented SMA or CT lesion (Table 3). Approximately four patients (7%) presented lesion in both arteries assessed. Despite the higher proportion of patients with CT lesion (23%) observed when compared to the proportion of SMA lesion (13%), this difference did not show to be significant (p = 0.18).

Superior mesenteric artery

Sex, diabetes mellitus, hypertension, obesity, smoking, dyslipidemia and presence of clinical picture did not seem associated with the presence of SMA lesion (p > 0.05) (Table 4). In relation to age, patients who had SMA lesion presented a significantly higher age median (p = 0.04) than that found in patients in which SMA lesion was absent, pointing that, whenever the lower limb arteriopathy patient's age increases in 1 year, the possibility of SMA lesion increases in approximately 11%. A significant association (p = 0.043) was observed between SMA lesion and angina/infarct, which is, the presence of SMA lesion in patients with lower limbs arteriopathy who presented angina/infarct was 7.2 times higher than that of patients with no angina/infarct.



To assess if age and angina/infarct appeared as independently associated to SMA lesion, a multivariate analysis was performed through adjustment of logistic regression multivariate model. In this model, in addition to age and angina/infarct, variables with p < 0.20 were inserted.

With this adjustment, the presence of diabetes mellitus appeared as a variable independently associated to the presence of SMA lesion (p = 0.42). And in the adjustment, taking into consideration only age and angina, none of the two variables showed to be independent of the SMA lesion (p = 0.118 and 0.119, respectively). It was observed that both age and the presence of angina increased the possibility of SMA lesion (p = 0.04 for both variables).

Celiac trunk

None of the variables assessed presented significant association with the presence of CT lesion (p > 0.05) (Table 5). The variables age and obesity tended to be associated with CT lesion (p = 0.06 and p = 0.09, respectively). Although patients with celiac trunk lesion presenting a median of age higher than that of patients without this lesion, there was no significant difference (p = 0.06). There was a higher proportion of obese patients among those with CT lesion (43%) when compared to the observed proportion between those without the lesion (20%), but this difference was not significant.



Due to the significance lower than 20% in the assessment of these variables (age and obesity) with CT lesion, multivariate adjustment was chosen considering both variables in the model. This adjustment showed that none of the two variables was independently associated with CT lesion (p = 0.17 for age and p = 0.13 for obesity).



Atherosclerotic process is the main etiological agent of chronic mesenteric ischemia, as well as that of its impairment in other vascular territories simultaneously dependent on risk factors.4-6,8,10,21 Despite mesenteric atherosclerotic disease being a frequent condition, its clinical manifestation is rare.29

The current study analyzed two distinct groups: treatment group and control group. In the treatment group, all the patients had symptoms related with lower limbs arterial circulation and presented intermittent claudication or trophic lesions in the extremities and/or rest pain, but they were asymptomatic in relation to intestinal arterial circulation. In the control group patients had no symptoms related with lower limbs arterial circulation and intestinal arterial circulation.

The vascular ultrasound (Doppler) study was limited to the initial centimeters of digestive arteries because this was the most affected region.10

The proposal of using Doppler vascular ultrasound to measure intestinal arteries flow occurred initially in 198230 and, according to Perko,17 Doppler ultrasound allows the recognition of the speed and direction of the flow by measuring the luminal diameter and blood speed inside the vases.

Concomitant to lower limbs' vascular alterations in the treatment group patients, a marked stenosis (≥ 70%) in the SMA was observed in 8 (13.6%) of them with lower limbs arteriopathy and SMA lesion (CI95%). With respect to the CT, 23.7% of the 60 patients with arteriopathy of the lower limbs presented marked stenosis (≥ 70%) (CI95%) in the CT. Similar results were found in literature and they indicate the CT as the most frequent site for lesions.5,6,9-11,13 Other authors, on their turn, found the inferior mesenteric artery31 or the SMA32 to be the most frequent site for lesions. The studies by Valentine et al.11 and Widman et al.5 used selected groups of patients with peripheral arteriopathy and cited a frequency of CT impairment of 25 and 16.1%, and SMA impairment of 6 and 8%, respectively. These stenoses, despite asymptomatic due to circulatory replacement, have little interference in the digestive arteries' normal functioning,5 but present an evolutive potential for complete obstruction. However, for this picture to be actualized, two sequential arterial trunks have to be obstructed.5 In this study, despite the occurrence of 30% of significant stenosis in one of the intestinal arteries, none of these patients presented digestive symptoms. According to Waibel,33 there is no difference in abdominal symptomatology of patients with stenoses of two or more visceral branches when compared with patients without stenoses. Jarvinen et al.10 found 15% of cases in which at least two digestive arteries were affected not accompanied by symptomatology.

In the current series, 70% of the patients did not present SMA or CT lesion. Approximately 7% of the patients presented lesion in both arteries assessed. Despite the higher proportion of patients with CT lesion (24%) in relation to the proportion of SMA lesion (14%), this difference did not prove significant (p = 0.18).

The increase of risk factors present in patients with mesenteric stenosis was reported by Moawad et al.8 These authors have observed that, of the chronic mesenteric ischemia patients, 75% were smokers, 55% had peripheral vascular diseases, 43% presented coronary ischemic disease, 37% were hypertensive and 10% were dyslipidemic.

In this study, in the treatment group, around 80% of the patients had trophic lesion and/or rest pain, and diabetes mellitus was present in 48% of the subjects, hypertension in 67% and around 52% of them were smokers.

Hansen et al.6 have affirmed that abdominal pain due to atherosclerotic occlusion of the SMA reflects coronary disease and myocardial ischemia. Jarvinen et al.,10 in analyzing 120 consecutive autopsies in traffic collision victims, have observed that coronary atherosclerosis was significantly the most important modality of atherosclerosis associated with mesenteric atherosclerosis. Equally in the current study a significant association (p = 0.04) was found between the presence of SMA lesion and angina/infarct: the possibility of SMA lesion in lower limbs arteriopathy patients who presented angina and/or infarct is 7.1 times higher than in patients who did not present these events. No significance was observed in relation to the presence of CT lesion.

Age was also associated with the presence of mesenteric atherosclerosis.6,10,11,13 In this series, the lower limbs arteriopathy age median was 67 years (39-93 years). It was observed that SMA lesion presented a median of age significantly higher (p = 0.04) than that presented by the patients without lesion in this artery, which means that when the age of lower limbs arteriopathy patients increases in one year, the possibility of SMA lesion increases in 11%. No significant association was found in the CT lesions. Studies conducted in necropsies showed that lesions of digestive arteries tended to grow progressively as the age of the patient increases. This suggests that, with the advancing of the patients' age, a depletion of organic capacity of meeting digestive arterial circulatory needs appeared, with these arteries being progressively limited by the stenoses.5

There is a disagreement in literature in relation to the frequency of stenoses of digestive arteries in patients of both sexes, showing a higher incidence in men,29 in women2 and equal in both.34,35 In this study, male sex was more frequently affected (67%), but this trend did not prove significant.

It is accepted that diabetes mellitus,36 smoking,37 hypertension38 and the increase in cholesterol levels represent risk factors for atherosclerosis.39 However, in this series, the risk factors sex, diabetes mellitus, hypertension, obesity, smoking, dyslipidemia, intermittent claudication and trophic lesion did not show any association with the presence of SMA lesion. It was also observed that none of the risk factors assessed presented a significant association with the presence of CT lesion. Lesion in both arteries – CT and SMA – occurred with unexpressive frequency, a fact also observed by Roboottom and Dubbins.13

It was observed that the treatment group presented a significantly higher proportion of individuals with diabetes mellitus, hypertension, and smoking if compared to control group. This result is probably due to the fact that the treatment group is constituted by patients selected for obstructive atherosclerotic arteriopathy of the lower limbs.

There was no significant difference between the treatment and the control groups in the proportion of obese, dyslipidemic, patients, with previous episodes of angina or stroke. None of the control group patients presented SMA or CT lesion. This way, it can be said that the treatment group presented a significantly higher proportion of SMA or CT lesion if compared to the control group (p < 0.001). The presence of asymptomatic stenosis in intestinal arteries and associated to peripheral vascular disease was also observed by Valentine et al.11 These authors have cited the presence of mesenteric atherosclerosis in 29% of the patients with atherosclerotic vascular lesions in lower limbs. Reiner et al.32 saw the association between mesenteric atherosclerosis and peripheral vascular disease as important.

In this series, it was discovered that, in relation to peripheral vascular impairment – claudication and trophic lesion and/or rest pain – observed, regardless of symptoms presented, 70% of the patients did not present significant lesion in none of the two arteries assessed (SMA and CT) and, thus, there was no significant association between the presence of peripheral arterial symptomatology and the presence of mesenteric arterial lesion.

The current study also found that Doppler vascular ultrasound is simply and rapidly performed, not invasive and presents a high diagnostic index of lesions with stenosis ≥ 70% of the SMA or CT lumen.



The finding of vascular arteriopathy of the lower limbs suggests the presence of SMA and CT stenotic lesion. The finding of SMA atherosclerosis in Doppler vascular ultrasound is associated with the presence of ischemic cardiopathy and advanced age.



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Wenes Pereira Reis
Rua das Nações, 77, Nações
CEP 89130-000 - Indaial, SC
Tel.: (47) 3394-2952
Fax: (47) 3382-2587

Manuscript received April 19 2009, accepted for publication Nov 11 2009.



No conflicts of interests declared concerning the publication of this article.
Research conducted at the Beatriz Ramos Hospital , Indaial, SC, and at the Institute of Medical Care for the State Server (Instituto de Assistência Médica ao Servidor Público Estadual - IAMSPE), São Paulo, SP.

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