|Year : 2018 | Volume
| Issue : 3 | Page : 1050-1057
Comparative study between Doppler ultrasound and computed tomography angiography in diabetic lower limb arterial insufficiency
Zeinab A Ali1, Rehab M Habib1, Mahmoud A. M Abo Hendy2
1 Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Radiology, El Sahel Teaching Hospital, Cairo, Egypt
|Date of Submission||24-Mar-2017|
|Date of Acceptance||09-May-2017|
|Date of Web Publication||31-Dec-2018|
Mahmoud A. M Abo Hendy
Department of Radiology, El Sahel Teaching Hospital, Cairo
Source of Support: None, Conflict of Interest: None
This work aimed to highlight the role of color Doppler ultrasound in the assessment of lower limb arterial insufficiency in patients with diabetes as well as the characteristics of lower limb arterial disease in diabetic patients.
Diabetic lower limb arterial insufficiency is a major health problem affecting the individuals and community health. Doppler ultrasound is a widespread relatively cheap examination with no health hazards of radiation. Hence, we considered studying the role of Doppler ultrasound in determining the characteristics of lower limb arterial diabetic insufficiency and its level of accuracy.
Patients and methods
One hundred diabetic patients with clinically suspected lower limb arterial insufficiency were examined using Doppler ultrasound and computed tomography angiography (CTA), and the characteristics of diabetic lower limb arterial disease and accuracy of Doppler results in relation to CTA were determined.
Diabetic lower limb arterial disease was characterized by being bilateral and multisegmental in the majority of cases with more affection of the distal (below knee) arteries. There was no significant difference between Doppler and CTA results at the above knee arteries as regards detection of significant arterial stenosis (luminal narrowing ≥ 50% of artery diameter); P values were as follows: common iliac artery segment, 0.695; external iliac artery, 0.776; common femoral artery, 0.563; and superficial femoral artery, 0.599. Further, a low significant difference at below knee arteries was found; P values were as follows: popliteal artery segment, 0.033; anterior tibial artery, 0.025; posterior tibial artery, 0.019; and peroneal artery, 0.031. The overall sensitivity of Doppler in evaluating lower limb arteries was 90.46%, the specificity was 92.05%, and the accuracy was 91.81% when CTA was taken as a standard.
Duplex ultrasound provides high-resolution, precise anatomical and physiological information of the peripheral arteries. It should be first-line investigation for lower limb arterial assessment and also be combined with other arterial imaging modalities to obtain better diagnostic accuracy.
Keywords: arterial insufficiency, computed tomography angiography, diabetes, Doppler, lower limb, ultrasound
|How to cite this article:|
Ali ZA, Habib RM, Abo Hendy MA. Comparative study between Doppler ultrasound and computed tomography angiography in diabetic lower limb arterial insufficiency. Menoufia Med J 2018;31:1050-7
|How to cite this URL:|
Ali ZA, Habib RM, Abo Hendy MA. Comparative study between Doppler ultrasound and computed tomography angiography in diabetic lower limb arterial insufficiency. Menoufia Med J [serial online] 2018 [cited 2019 Jan 20];31:1050-7. Available from: http://www.mmj.eg.net/text.asp?2018/31/3/1050/248727
| Introduction|| |
Lower limb arterial disease resulting from long-standing diabetes mellitus (DM) is an important health problem of present time. DM is a common pathological condition with a higher prevalence rate in developing countries. Egypt is included among the countries with the highest prevalence of diabetes.
DM is a metabolic disorder characterized by hyperglycemia and dyslipidemia. The abnormalities in nutrient metabolism and vascularity resulting from DM lead to lower limb arterial diseases and ischemia, and this leads to infection, foot ulcers, and impairment of wound healing. Diabetic lower limb ischemia often leads to limb necrosis.
Color Doppler ultrasound is a widely available noninvasive technique in the assessment of arterial affection of lower limbs that occur with DM. Color Doppler ultrasound has lots of advantages over other diagnostic imaging modalities; it is a feasible modality available in nearly all hospitals, being cheap, accurate, and safe.
It also uses nonionizing radiation, and hence is safe in all cases with no limitations. Color Doppler ultrasound technique is not used with contrast agents, and hence it has no hazards of allergic or nephropathic effects. Color Doppler ultrasound competes with magnetic resonance angiography, and some studies show same or better results compared with magnetic resonance angiography but with much less cost.
Color Doppler ultrasound technique can identify the condition of arterial wall, whether healthy or diseased, atheromatous plaques, and calcification through gray scale. Areas of stenosis, turbulence, and defect of blood flow can be seen with the help of color. Moreover, a major advantage for Doppler ultrasound over other imaging modalities is that it can identify hemodynamic changes that occur with arterial stenosis.
| Aim|| |
Because of these much advantages of Doppler ultrasound we aimed to highlight its role in the assessment of lower limb arterial insufficiency in patients with diabetes as well as the characteristics of lower limb arterial disease in diabetic patients. In addition, the value and diagnostic accuracy of Doppler ultrasound were evaluated when compared with computed tomography angiography (CTA).
| Patients and Methods|| |
This study was a retrospective one, conducted from July 2015 to July 2016 with patient's referral from both the medical and surgical units. One hundred patients were included in this study by means of purposive nonrandomized sampling. The selected participants provided consent for participation in the study before they were subjected to examinations and investigations, and the study was approved by the Ethics Committee of Menoufia University Hospital.
Adult diabetic patients irrespective of the type of diabetes and sex with clinically suspected peripheral arterial insufficiency were included. Patients with a previous history of trauma to the arterial vasculature, those who underwent previous arterial interventions, patients with excessive scarring or skin injury interfering with ultrasound Doppler assessment, patients with renal insufficiency (creatinine level above 1.5), patients with lower limb metallic internal fixation, and pregnant women were excluded from the study.
Radiological workup of these patients was carried out within 2 days from their referral. All patients were subjected to history taking, clinical examination, color Doppler ultrasonography, and CTA.
History taking and clinical examination included the following: age, history of DM and type of diabetes (I or II), duration and medications, smoking, hypertension, cardiac troubles, central nervous system troubles, and a history of ischemic pain (claudication and rest pain). Inspection for color changes and gangrene, trophic changes, and palpation for leg temperature and peripheral pulses and renal function tests were carried out to all patients.
Ultrasound color and Doppler examinations were performed with Toshiba Xario 200 ultrasound machine (Toshiba, Akasaka, Minato-ku, Tokyo 107-6205 Japan), which can combine a real-time B-mode imaging system with pulsed and continuous wave Doppler facilities together with the availability of color coding of signals. Patients were asked not to eat for 8 h before examination to diminish the bowel gases and enhance visualization of the abdominal aorta and common iliac arteries (CIAs). The arterial supply of lower extremities was divided into these segments: CIA, external iliac artery (EIA), common femoral artery (CFA), superficial femoral artery (SFA), popliteal artery, anterior tibial artery (ATA), posterior tibial artery (PTA), and peroneal artery [Figure 1].
|Figure 1: Lower limb arterial segments. ATA, anterior tibial artery; CFA, common femoral artery; CIA, CIA, common iliac artery; EIA, external iliac artery; Per A, peroneal artery; Pop A, popliteal artery; PTA, posterior tibial artery; SFA, superficial femoral artery.|
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Iliac segments were examined with 3–5 MHz probe with the patient supine. A 4–7 MHz probe was used for the femoropopliteal segments, which were examined with the legs relaxed in mild external rotation. Examination of the popliteal arteries and the origins of the tibial arteries was performed in lateral or prone position with the knees partially flexed. The infrapopliteal arteries were similarly scanned using 4–7 MHz probe with the patient lying prone or in lateral position.
Each segment was examined first using gray scale ultrasound for the detection of atheromatous plaques and then using color flow imaging transversely and longitudinally to size the colored flow in the lumen with respect to the arterial wall and to detect areas of flow disturbances or increased velocity. Arterial lesions were located by changes in vessel caliber, changes in color flow patterns, and broadening of Doppler waveform, quantified by measuring the peak systolic velocity (PSV) ratio across a lesion and by comparing the PSV within stenosis with that proximal to the lesion; this ratio was independent of individual variations in blood pressure, vascular compliance, and cardiac function. The segment was considered normal if no stenotic lesion or Doppler spectral changes were found. The stenotic lesion was considered hemodynamically significant if there was doubling of the PSV ratio or more across the lesion (PSV ratio). Therefore, the stenosis was considered hemodynamically significant if PSV ratio greater than or equal to 2, whereas the stenosis was considered hemodynamically nonsignificant if PSV ratio of 1–2. Occlusions were diagnosed when no color flow or Doppler spectral signal was detected despite the variations in the sensitivity by increasing the Doppler gain, decreasing the scale, and increasing the sample volume size in order to detect any slow flow within the lesion. Thereafter, patients were examined using CTA on the next day.
CTA was performed with Philips Brilliance 64 slice multidetector CT scanner (Philips, Amsterdam, the Netherlands). Patients were placed in supine position with feet entering the gantry first. Scanogram and plain study were taken. Spiral acquisitions were performed in a single scanning pass from the level of the diaphragm down to the ankles. The average length of scanning for a patient was about 1500 mm. Patients were asked to hold their breath during the first part of the scanning pass.
After saline check, 100 ml volume of iodinated contrast material 320 mg of iodine/ml was administered through a 20-G cannula in an antecubital vein at a rate of 4.5 ml/s through pressure injector followed by saline chase. The scanning parameters were as follows: 120 kV, 200 mA effective, and section thickness of 2 mm. Scanning was begun when the contrast opacification of descending thoracic aorta reached 100 HU, determined using the automated bolus tracking technique. Images were reconstructed with an effective section thickness and an increment of 1mm by using the smooth algorithm. All transverse source images were transferred to workstations for the preparation of reconstructions. Slicing maximum intensity projections were obtained with coronal and sagittal projections of each data set. Whole-volume maximum intensity projections with segmentation of bone and vessel wall calcifications and volume-rendered images were obtained. The images were analyzed on the basis of transverse images, maximum intensity projection, multiplanar reformats, and volume-rendering images for stenosis, occlusion, calcification, plaque morphology, and collaterals. Stenosis was graded as follows: grade I (nonsignificant stenosis): luminal narrowing less than 50% of artery diameter; grade II (significant stenosis): luminal narrowing greater than or equal to 50% of artery diameter; and grade III: total occlusion.
For each arterial segment results were obtained and data were collected, tabulated, and statistically analyzed using computer using statistical package for the social sciences program (SPSS, version 10, SPSS Inc., Chicago, Illinois, USA).
Two types of statistics were performed: descriptive statistics included number and percent, and analytical statistics included the χ2 test, which was used to compare between two or more qualitative variables. contingency table or r × c comple × 2 × 2 in table. P value less than 0.05 indicates significant difference. P value less than 0.01 indicates high significant difference. Receiver operating characteristic curve analysis was performed. The sensitivity of a diagnostic test is the probability that the test results will be positive when the disease is present (true-positive rate, expressed as a percentage). The specificity of a diagnostic test is the probability that the test results will be negative when the disease is absent (true-negative rate, expressed as a percentage). Positive predictive value of a diagnostic test is a probability that the disease is present when the test is positive. Negative predictive value of a diagnostic test is a probability that the disease is present when the test is negative). Accuracy is the ratio of true-positive and true-negative results on all patients.
| Results|| |
In this study 100 diabetic patients with suspected lower limb arterial insufficiency were examined using Doppler ultrasound and CTA. Of these 100 patients, 66% were male and 34% were female. The majority of examined cases were from 50 to 70 (78%) years [Table 1] and [Figure 2].
Foot ulcers were the most common complaint for which patients needed medical advice in our study (45% of patients). Claudication and rest pain were the second common complaints [Figure 3].
There was a strong association between lower limb arterial-related complaints and other arterial-related diseases. Twenty-three percent of patients had a history of ischemic heart disease, 19% had brain ischemia, and 14% had hypertension [Figure 4].
|Figure 4: Associated comorbidities of examined patients. HTN, hypertension; IHD, ischemic heart disease.|
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Of 72 patients with significant lower limb arterial disease (luminal narrowing ≥50% of artery diameter), the majority of cases (43 patients) had bilateral disease. There was no difference between the right and left limbs in disease distribution. In total, 47.22% of patients with significant arterial disease (luminal narrowing ≥50% of artery diameter) had some degree of plaque calcification [Table 2]. Distal small arteries and anterior and PTAs were the most commonly affected ones both on Doppler and CTA, and stenosis was more common compared with occlusion [Table 3] and [Figure 5].
|Table 2: Correlation between calcified atheromatous plaques and significant arterial stenosis|
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|Table 3: Distribution of arterial segmental affection by means of Duplex examination|
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|Figure 5: Distribution of arterial segmental affection by Duplex examination. ATA, anterior tibial artery; CFA, common femoral artery; CIA, CIA, common iliac artery; EIA, external iliac artery; Per A, peroneal artery; POP A, popliteal artery; PTA, posterior tibial artery; SFA, superficial femoral artery.|
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We concentrated in the study on the detection of segments with significant arterial stenosis (luminal narrowing ≥ 50% of artery diameter), as these lesions are of clinical importance and may need intervention, and smaller lesions are mainly of no major clinical importance and usually need no intervention. We also compared between Doppler ultrasound and CTA as regards difference in the detection of segments with significant stenosis (luminal narrowing ≥50% of artery diameter).
There was no major difference between the results of Doppler ultrasound and CTA. The Doppler examination results had some trend of stenosis overestimation, but it was unlikely to miss significant stenosis in different segments. There was no significant difference between Doppler and CTA results at the above knee arteries as regards detection of significant arterial stenosis (luminal narrowing ≥50% of artery diameter); P values were as follows: CIA segment, 0.695; EIA, 0.776; CFA, 0.563; and SFA, 0.599. Further, a low significant difference was found at below knee arteries; P values were as follows: popliteal artery segment, 0.033; ATA, 0.025; PTA, 0.019; and peroneal artery, 0.031 [Table 4].
|Table 4: Comparison between Doppler ultrasound and computed tomography angiography results|
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Although catheter angiography was considered the gold standard for lower limb arterial disease evaluation for many years, because of its invasive technique with much complication, it is now mainly limited to therapeutic options, and high-degree CTA has replaced it for diagnostic purposes.
Case no. 1
History: A 60-year-old male patient presented with bilateral claudication pain for 5 years and trophic changes and coldness in both legs. Duplex findings were as follows [Figure 6]a and [Figure 6]b: patent diffusely atherosclerotic aorta, iliac, and CFAs on both sides with no significant stenotic lesions; occluded left SFA by intraluminal adherent thrombus with distal patent attenuated arteries showing poststenotic damped flow; and right SFA significant stenosis with distal monophasic low velocity flow. There were no other significant stenotic segments. CTA findings were as follows [Figure 6]c: confirmed diagnosis with occluded left SFA with distal patent attenuated arteries showing refilling through collaterals with no other significant stenotic segments, and significant right SFA stenosis at its upper and lower thirds with no other distal significant stenotic lesions.
|Figure 6: (a) Absent color flow at superficial femoral artery (SFA) because of intraluminal thrombosis (black arrow) with normal color filling of the SFA (white arrow) and noted collaterals beside the SFA (arrowhead). (b) Distal SFA monophasic low velocity flow Doppler (arrow). (c) Left SFA thrombosis showing absent opacification with distal collateral refilling (white arrows). Right SFA stenotic segments (blue arrows) computed tomography angiography.|
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Case no. 2
History: A 62-year-old male patient with ischemic heart disease presented with nonhealing left foot ulcer and trophic changes. Duplex findings were as follows [Figure 7]a and [Figure 7]b: diffuse atherosclerotic changes in both lower limb arteries from the iliac down to the popliteal arteries with no significant stenotic segments, and bilaterally attenuated tibial and peroneal arteries with low velocity monophasic flow. CTA findings were as follows [Figure 7]c: confirmed diagnosis with diffuse atherosclerotic changes in both lower limb arteries from the iliac down to the popliteal arteries with no significant stenotic segments, and bilaterally attenuated tibial and peroneal arteries with multiple segments of wall calcification.
|Figure 7: (a) Irregular beaded color flow at the distal part of the right posterior tibial artery (PTA) (white arrow) with normal color filling at its venae commitants (blue arrow). (b) Beaded attenuated left anterior tibial artery (ATA) with monophasic reduced velocity flow on Doppler (arrow). (c) Bilateral ATA (blue arrows) and PTA (white arrows) beaded attenuated opacification with multiple segmental plaque calcification computed tomography angiography.|
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Case no. 3
History: A 50-year-old male patient presented with left calf claudication pain. Duplex findings were as follows [Figure 8]a and [Figure 8]b: mild diffuse atherosclerotic changes in both lower limb arterial system with mild intima/media complex thickening, and left popliteal artery significant stenosis with no calcified concentric atheromatous plaque with distal monophasic low velocity (damped) flow. CTA findings were as follows [Figure 8]c: confirmed diagnosis of significant stenosis of the left popliteal artery. No other significant stenotic segments were present.
|Figure 8: (a) Left popliteal artery significant stenosis color flow (white arrow) with poststenotic turbulence flow showing color aliasing (blue arrow). (b) Left popliteal artery significant stenosis Doppler showing markedly increased velocity flow (blue arrow). (c) Left popliteal artery significant stenosis with markedly reduced diameter (arrow) with normal proximal and distal arterial opacification computed tomography angiography.|
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| Discussion|| |
The complications of diabetic vasculopathy commonly include two categories: microvascular and macrovascular complications. Macrovascular disease is the most common reason of mortality and morbidity in diabetes and is responsible for high incidence of vascular diseases such as stroke, myocardial infarction, and peripheral vascular diseases.
Epidemiological evidence has confirmed an association between diabetes and increased the prevalence of lower limb arterial disease. The duration and severity of diabetes correlate with the incidence and extent of lower limb arterial insufficiency.
In our study we examined 100 diabetic patients with symptoms suggestive of lower limb arterial insufficiency; 72% of patients were affected by significant lower limb arterial stenosis. There was male predominance as regards the lower limb diabetic arterial affection; 66% of patients were male and 34% were female. Male predominance was also encountered in a previous similar study by Das et al.. Of 60 patients they examined for diabetic lower limbs arterial disease, 60% were male and 40% were female.
In our study the lower limb arterial disease in the diabetic patients was characterized by being bilateral and multisegmental in the majority of cases; 47% of patients with significant arterial stenosis had bilateral affection and 58% had multisegmental distribution. This is in agreement with previous studies by Guo et al., who found higher results than ours as regards bilateral and multisegmental diabetic lower limbs arterial affection. Fifty-three percent of patients they examined were affected by bilateral lower limb arterial disease and 70% had multisegmental distribution.
In our study diabetic lower limb arterial disease had more affection of the distal (below knee) arteries in 66% of patients. The ATA was the most commonly involved artery with significant stenosis in our study (23%); the PTA and the popliteal artery were the second most commonly affected at 20 and 13%, respectively. There were similar results of arterial stenotic characteristics and segmental distribution of diabetic lower limb arterial disease in previous studies. In a study made by Das et al., the ATA (in 31%) and PTA (in 30%) were the most commonly involved arteries with luminal narrowing. The arterial affection was characterized by incidence of plaque calcification in our study in 53% of cases. There were similar results in their study that found plaque calcification at 58% of identified stenotic lesions.
In our study there was a strong association of lower limb arterial diseases with coronary heart disease (19%) and cerebral arterial disease (19%) as diabetic arterial pathology is global throughout the body. A strong association between diabetic lower limb arterial disease and coronary heart disease was noted by He et al. in 28% of cases and with cerebral ischemia in 33% of cases.
In our study when we compared Duplex ultrasound results with CTA, Duplex ultrasound was by far of great value with comparable results. In the CIA segments, Doppler was able to pick up 92% hemodynamically significant stenotic lesions. It missed significant stenosis only in one patient who had a calcific plaque. In the EIA segments, Doppler failed to detect hemodynamically significant stenosis in two patients. In the CFA segments, Doppler was able to detect all hemodynamically significant stenoses. In the SFA, Doppler was able to detect 90.9% of hemodynamically significant stenotic lesions. The distal SFA in the adductor canal was a challenging area during examination, in which some differences in the results between Doppler and CTA were more obvious. The overall sensitivity and specificity of Doppler at iliofemoral segments were 93.10 and 97.62%, respectively.
In the popliteal artery segments, Doppler detected 83.3% of hemodynamically significant stenotic lesions. The sensitivity and specificity were somewhat decreased at the popliteal artery. The decreased sensitivity and specificity at this level were due to the overestimated stenosis that was more at this level probably due to patients who had long-segment disease in SFAs with resultant monophasic flow in the popliteal arteries, which was mistaken for hemodynamically significant stenosis.
Similar results were found in a previous study by Kandasamy et al., who compared the results of Doppler ultrasonography with CTA in 34 patients. The sensitivity of Doppler in evaluating aortoiliac segments and femoropopliteal segments was 87.5 and 100%, respectively, and the specificity in evaluating aortoiliac segments and femoropopliteal segments was 100 and 96.01%, respectively. CTA was taken as standard. The agreement between the two modalities in the evaluation of the aortoiliac region and the femoropopliteal region was very good. Other studies by Chidambara et al. found that ultrasound gives valuable information as regards the vessel wall in atherosclerotic arterial disease in addition to evaluation of vascular lumen abnormalities causing stenosis, thrombus, etc. However, dense calcification hinders the evaluation of lumen due to acoustic shadowing. Moreover, they reported that, as regards the iliac segments, the sensitivity, specificity, and accuracy of Doppler ultrasound were 96.55, 94.79, and 95.2%, respectively. In femoropopliteal segments, the sensitivity, specificity, and accuracy of Doppler ultrasound were 88.88, 92.95, and 91.58%.
In our study, the overall specificity was decreased in below knee levels, being 84.25% in the ATA segments, 83.87% in the PTA segments, and 82.43% in the peroneal artery segments, but the sensitivity was fairly good in these levels, being 96.30, 91.11, and 90.6%, respectively. This can be attributed to the fact that in the infrapopliteal arteries Doppler detected false-positive stenosis at 23.6% of ATA segments, 26.3% in PTA segments, and 27.3% in peroneal arterial segments. CTA determined that those patients (with false-positive Doppler stenosis) mainly had occlusions of the femoropopliteal region with reformation of the infrapopliteal vessels at their mid or distal parts and it was difficult to find the reformation of these vessels by Doppler ultrasound as there were many collateral vessels seen in the leg. The overall sensitivity and specificity of Doppler at the popliteal and infrapopliteal segments were 88.96 and 85.91%, respectively.
The sensitivity and specificity of Doppler ultrasound in below knee arteries were similarly reported to be reduced in previous studies that compared Doppler ultrasound with other imaging modalities. In the study made by Kandasamy et al., Doppler sensitivity in evaluating the infrapopliteal segments was relatively lower in comparison with more proximal segments, being 75.32%, and the specificity was 83.06% when CTA was taken as standard. The agreement between the two modalities in infrapopliteal vessels was only moderate. In the study by Chidambara et al., they also reported some valuable variation between Doppler and CTA in the distal arteries with a sensitivity, specificity, and accuracy of 96.15, 61.53, and 78.84%, respectively.
In this study the overall sensitivity of Doppler in evaluating lower limb arteries was 90.46%, the specificity was 92.05%, and the accuracy was 91.81% when CTA was taken as a standard.
This study showed various advantages of Doppler. When extensive calcifications are present in the vessel, the end product of CTA is of questionable diagnostic value as it overstages the lesion. Doppler is able to demonstrate this overstaging of CTA by showing that the calcific plaque, which appears to have produced more than 50% stenosis, has actually not resulted in hemodynamically significant stenosis. It is able to show the duration of occlusion, as acute thrombus distends the vessels while chronic occlusion narrows the vessel caliber. As no iodinated contrast is required, it is safely performed in patients with nephropathy. Moreover, Doppler could be performed in cases of emergencies such as traumatic/iatrogenic injuries to rule out arterial obstruction at any time, whereas CTA is not easily available at all time and is available only at apex institutions. Doppler is also cost-effective when compared with CTA.
| Conclusion|| |
Duplex ultrasound is unlikely to misclassify a whole limb as normal when it has a significant pathology and thus inappropriately screen out a patient from further investigation. Duplex ultrasound was found to have a high negative predictive value and could exclude a significant lesion; thus, it should be used to help avoiding other costly diagnostic modalities in a mildly symptomatic patients and should be combined with CTA to obtain better diagnostic accuracy.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
[Table 1], [Table 2], [Table 3], [Table 4]