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ORIGINAL ARTICLE
Year : 2018  |  Volume : 31  |  Issue : 2  |  Page : 508-513

Role of computed tomography angiography and color Doppler ultrasonography in the evaluation of diabetic foot


1 Department of Radiodiagnosis, Faculty of Medicine, Menoufia University, Shebin Elkom, Egypt
2 Radiodiagnosis Department, Quesna General Hospital, Quesena, Menoufia Governorate, Egypt

Date of Submission06-Dec-2016
Date of Acceptance27-Feb-2017
Date of Web Publication27-Aug-2018

Correspondence Address:
Ameer M Eltelwany
Radiodiagnosis Department, Quesna General Hospital, Quesena, Menoufia Governorate
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_670_16

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  Abstract 


Objective
The aim of this study was to highlight the role of computed tomography angiography (CTA) and color Doppler ultrasonography (DUS) in the evaluation of patients with diabetic foot disease.
Background
The risk for ulceration and amputation is much higher in diabetics compared with nondiabetics. CTA is more frequently used to assess peripheral vascular disease of the diabetic foot.
Patient and methods
This prospective study included 30 diabetic patients who presented with diabetic foot vascular lesions and referred from outpatient clinics of vascular surgery to the Radiology Department, National Liver Institute, Menoufia University Hospital and Private Center. The present study was performed in the period between January 2015 and January 2016. Their ages ranged from 47 to 86 years; 22 of them were men and eight were women. All cases underwent Doppler examination as a rapid, noninvasive complementary diagnostic tool, and the findings were compared with those of CTA.
Results
In the present study, the number of segments was 399 for 57 limbs, and each arterial tree of one limb was divided into seven segments (common femoral, superficial femoral, popliteal, anterior tibial, posterior tibial, peroneal, and dorsalis pedis arteries). In this study, the number of stenotic segments was 38 (9.5%) and 42 (10.5%) on multidetector computed tomography angiography (MDCTA) and DUS, respectively. The number of occluded segments with distal collateral refilling was 16 (4%) on both MDCTA and DUS. The number of segments with total occlusion was 65 (16.2%) and 63 (15.7%) on MDCTA and DUS, respectively.
Conclusion
The use of CTA and DUS increases the ability to better delineate vascular anatomy, localize the obstruction, assess the severity of stenosis, and detect the presence of collaterals and distal run-off.

Keywords: computed tomography angiography, diabetic foot, occlusion, stenosis


How to cite this article:
Elsayed EE, Zytoon AA, Eltelwany AM. Role of computed tomography angiography and color Doppler ultrasonography in the evaluation of diabetic foot. Menoufia Med J 2018;31:508-13

How to cite this URL:
Elsayed EE, Zytoon AA, Eltelwany AM. Role of computed tomography angiography and color Doppler ultrasonography in the evaluation of diabetic foot. Menoufia Med J [serial online] 2018 [cited 2018 Nov 16];31:508-13. Available from: http://www.mmj.eg.net/text.asp?2018/31/2/508/239764




  Introduction Top


The risk for ulceration and amputation is much higher in diabetics compared with nondiabetics. The lifetime risk of a diabetic individual to develop an ulcer is as high as 25%. Peripheral neuropathy, arterial disease, and foot deformities are the main factors accounting for this increased risk. Age and sex as well as social and cultural status are contributing factors [1].

Delayed wound healing in diabetic patients without large-vessel disease has been attributed to microvascular dysfunction and abnormal cellular and inflammatory responses [2].

The computed tomography angiography (CTA) is more frequently used to assess peripheral vascular disease of diabetic foot as it is less invasive than digital subtraction angiography (DSA) and can provide three-dimensional images. Multidetector computed tomography (MDCT) can decrease acquisition time and increase spatial resolution. This method can produce high-spatial resolution images of the entire extremity in several seconds [3].

Color Doppler ultrasonography (DUS) is a widely available, noninvasive, cheap, and accurate diagnostic technique. In most cases of diabetic foot, color duplex examination results in accurate diagnosis of the status of the underlying arterial tree and consequent decision making, either conservative, interventional, or surgical [4].

This study aimed to highlight the role of CTA and color DUS to better delineate vascular anatomy, localize the obstruction, assess the severity of stenosis, and detect the presence of collaterals and distal run-off in patients with diabetic foot disease.


  Patients and Methods Top


Study population

This prospective study included 30 diabetic patients who presented with diabetic foot vascular lesions and were referred to the Radiology Department, National Liver Institute, Menoufia University Hospital and Private Center. The present study was carried out in the period between January 2015 and January 2016. Their ages ranged from 47 to 86 years; 22 of them were men, and eight of them were women [Figure 1], [Figure 2], [Figure 3].
Figure 1: Case no. 1. (a–c) Multidetector computed tomography (MDCT), maximum intensity projection, and three-dimensional images of the infragenicular arteries show total occlusion of the left popliteal artery (red arrows), which is seen extending for a segment measuring 8.7 cm in length, poor collateral circulation is seen with only a short segment of the left posterior tibial artery (PTA) seen patent with contrast, and absent flow in the anterior tibial artery. Almost no flow could be seen in the left foot. (d–g) Corresponding MDCT axial images: (d) axial image at the level of the popliteal artery; (e) axial image at the level of the anterior tibial artery, PTA, and peroneal artery; (f and g) axial images at the level of foot. All these images confirm total occlusion of the left popliteal artery (red arrow) and absent flow in the anterior tibial and peroneal arteries. Almost no flow could be seen in the left dorsalis pedis; however, the corresponding arteries in the contralateral side are seen patent (orange, green, and yellow arrows, respectively).

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Figure 2: Case no. 2. (a) Multidetector computed tomography angiography, maximum intensity projection (MIP) image, and anterior view of infragenicular arteries showing nonfilling of both popliteal arteries, and no vessels could be seen beyond the distal superficial arteries on both sides with total lack of any contrast filling in the infragenicular vessels on both sides. (b and c) Axial images at the level of the polpilteal (yellow arrows) and foot arteries (red arrows) confirm the findings. (d) Duplex of the right superficial femoral artery shows attenuated caliber of the whole course with monophasic waveform and dumped velocity. (e and f) MIP and axial images at the level of the common iliac arteries show a soft atheroma (orange arrow), which is near totally occluding the right common iliac artery just proximal to its bifurcation, and associated nonfilling of the right internal iliac artery.

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Figure 3: Case no. 3. (a) Multidetector computed tomography, maximum intensity projection (MIP) image, left anterior oblique of the whole lower limb arteries. (b and c) Anterior and oblique view of infragenicular arteries showing occluded left popliteal artery (white circle), bilateral occluded anterior tibial arteries (red arrows), bilateral occluded posterior tibial arteries except for tiny, short, faint, skipped stenotic segments. (d) MIP image and magnified infragenicular view showing the left posterior tibial artery (yellow arrow) filled with good collateral from the left superficial femoral artery (orange arrow).

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Inclusion criteria

Inclusion criteria were as follows: diabetic patients with symptoms of ischemia (intermittent claudication and rest pain), patients with ischemic ulcers and gangrene, patients with foot cellulitis, and patients with past history of any vascular surgical intervention of the lower limb (previous debridement, drainage, and amputations).

Exclusion criteria

Patients with history of trauma, chronic renal failure, and lactic acidosis were excluded.

All patients were subjected to the following:

  • Personal history taking, including name, age, sex, and occupation; history of the present condition, including onset, duration before presentation, history of trauma (type and mechanism); past history of diabetes mellitus (onset, duration, control, and treatment), hypertension, heart disease (ischemic or rheumatic) or renal disease, and symptoms of ischemia (intermittent claudication or rest pain); and past history of any vascular surgical intervention of the lower limb (previous debridement, drainage, and amputations)
  • Clinical examination including general examination with special emphasis on lower-limb vascularity with regard to pulse and vascular refilling
  • Routine laboratory investigations (blood urea, serum creatinine, and fasting blood glucose level)
  • All patients were informed about the technique, and they were ensured that their anonymity will be carefully protected. Informed consent was obtained from all patients. The study was approved by the ethical committee of the hospital faculty of medicine menoufia university and the patients gave an informed consents.


Protocol of the multidetector computed angiography

Multidetector computed angiography imaging

First, we explained the protocol to patients. Total immobilization of the patient during the examination is of vital importance, and anesthesia may be required in claustrophobic patients.

Scan parameters

The examinations were performed mainly on Siemens 128 MDCT (Siemens Healthcare GmbH, Henkestr. 127, 91052 Erlangen, Germany), with slice thickness of 1.5 mm.

Before starting the imaging study, the following steps were considered:

  • For the display of soft tissues, a window level of 40 HU and a window width between 400 and 700 HU were selected; these parameters provide enough contrast between fat and air. A window level between 40 and 300 HU and a window width between 2400 and 3200 HU were selected for imaging bony structures
  • Patients were placed in the supine position
  • Scanning was started at the abdomen and proceeded in a craniocaudal direction
  • A total of 100–120 ml of nonionic contrast material (iopromide 300) was administered at a rate of 3–4 ml/s by using a power injector and a 20-G intravenous catheter inserted into an antecubital vein followed by 20-ml normal saline injection.


Scan delay was monitored through bolus-tracking technique

A single, low-dose computed tomography (CT) image was obtained, without contrast administration, at the level of the celiac axis. A 10–15-mm 2 circular region of interest was placed at the center of the aortic lumen, and this subsequently measured the Hounsfield units of the aortic lumen on subsequent scanning. At 10 s following intravenous contrast administration, serial low-dose monitoring CT scans were obtained at the same table position (celiac axis level) at 2-s intervals. When the region of interest detects a preset contrast enhancement level (usually a 100–150 HU value), there is automatic triggering of the scanner to acquire images in the desired scan range, from the level of the celiac axis to the feet. This time-efficient method ensures optimal arterial enhancement within the region of interest.

In the scanning protocol of the present study, the second run or 'late phase' acquisition was performed for all patients.

Image reconstruction and manipulation were performed on a workstation. Many postprocessing techniques such as multiplanar reconstruction, maximum intensity projection (MIP), and volume rendering technique were used in most of the cases. However, inspection of the axial source images remains an essential part of the assessment.

Doppler ultrasonography

The examination was mainly performed using GE (Yorba Linda, CA 92887, USA) S7 expert ultrasound machines with combined gray-scale and color-flow duplex and Doppler spectral mode by a superficial probe (7.5 MHz) to scan the arterial tree starting from the common femoral to the dorsalis pedis artery.

Statistical methods

Data were analyzed using IBM SPSS statistics version 23 (IBM Corp., Armonk, New York, USA) and MedCalc version 15 (MedCalc Software BVBA, Ostend, Belgium).

The study assessed the agreement between CTA findings and DUS findings regarding arteries of the lower limbs on both sides. The studied arterial segments were classified into normal, stenotic, occluded, and occluded with collaterals formation. Degrees of κ agreement were classified into very good agreement (0.81–1.00), good agreement (0.61–0.80), moderate agreement (0.41–0.60), fair agreement (0.21–0.40), poor agreement (0.0–0.20), and no agreement (<0) [Table 1].
Table 1: Agreement between color Doppler and computed tomography angiography in evaluating lower-limb arterial stenosis and occlusion

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  Results Top


The present study included 30 diabetic patients referred to the Radiology department, National Liver Institute, Menoufia University Hospital and Private center. Among our 30 patients, 22 (73.3%) were males and eight (26.7%) were females. Their ages ranged from 47 to 86 years, with a mean age of 59 ± 11 years [Table 2].
Table 2: Patients' demographic data

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All 30 patients had type II diabetes mellitus and had uncontrolled hyperglycemia with mean glucose levels of 262 ± 70 mg/dl [Table 2].

The duration of diabetes since diagnosis ranged from 4 months (accidentally discovered on admission with previous toe gangrene) to 18 years, with a mean of 10.13 ± 7.27 years. The median diabetes duration in the studied patients was 9.50 years [Table 2].

Smoking or history of smoking was present in 19 out of 30 patients. Hypertension was present in 25 out of 30 patients. Hyperlipidemia was present in 25 out of 30 patients [Table 2].

Clinical presentation of our patients was as follows: claudication in nine (30.0%) cases, rest pain in six (20.0%) cases, redness and edema in 30 (100.0%) cases, minor tissue loss in six (20.0%) cases, and major tissue loss in 12 (40.0%) cases.

Sixteen patients (53.3%) had bilateral complaint, and 14 (46.7%) patients had unilateral affection [Table 2].

The reported clinical presentation in the 30 patients included rest pain in six patients, intermittent claudication pain in nine patients, minor tissue loss “ulceration” in six patients, and major tissue loss in twelve patients [Table 2].

The number of segments was 399 for 57 limbs, and each arterial tree of one limb was divided into seven segments (common femoral, superficial femoral, popliteal, anterior tibial, posterior tibial, peroneal, and dorsalis pedis arteries). In the present study, the number of segments with stenosis was 38 (9.5%) out of 399 on multidetector computed tomography angiography (MDCTA). The number of segments diagnosed as occluded with distal collateral refilling was 16 (4%) out of 399 on MDCTA. The number of segments with total occlusion was 65 (16.2%) out of 399 on MDCTA.

The number of stenotic segments was 42 (10.5%) on DUS. The number of occluded segments with distal collateral refilling was 16 (4%) on DUS. The number of segments with total occlusion was 63 (15.7%) on DUS.

Twenty-five cases out of 30 had arterial wall calcification ranging from mild arterial calcification (20 cases) to severe arterial wall calcification (five cases).


  Discussion Top


In the present study, the number of segments was 399 for 57 limbs, and each arterial tree of one limb was divided into seven segments (common femoral, superficial femoral, popliteal, anterior tibial, posterior tibial, peroneal, and dorsalis pedis arteries). In the present study, the number of segments with stenosis was 38 (9.5%) out of 399 on MDCTA. The number of segments diagnosed as occluded with distal collateral refilling was 16 (4%) out of 399 on MDCTA. The number of segments with total occlusion was 65 (16.2%) out of 399 on MDCTA.

In the present study, the number of segments diagnosed as occluded with distal collateral refilling was 16 (4%) out of 399 on MDCTA; therefore, visualization of collaterals was easy using MIP images, which appeared at sites of severe stenosis or occluded arteries, leading to refilling of the arteries distal to the occluded segment. Collaterals are indicative of chronic arterial disease.

In the present study, 25 out of 30 cases had arterial wall calcification ranging from mild arterial calcification (20 cases) to severe arterial wall calcification (five cases).

In this study, all cases underwent Doppler examination as a rapid, noninvasive complementary diagnostic tool, and the findings were compared with CTA.

Lingegowda et al. [5] by studying imaging modalities for diabetic ischemic foot stated that when a diabetic patient presents with a nonhealing ulcer, the investigation of choice should be duplex ultrasound.

In the present study, DUS was performed for all patients with diabetic foot infection, which helped primary mapping of the vessels, which was not accurate as the results of MDCT, because of some disadvantages such as patient status, presence of calcification, and a deeply seated peroneal artery.

In this study, the number of stenotic segments was 38 (9.5%) and 42 (10.5%) on MDCTA and DUS, respectively. The number of occluded segments with distal collaterals refilling was 16 (4%) on both MDCTA and DUS. The number of segments with total occlusion was 65 (16.2%) and 63 (15.7%) on MDCTA and DUS, respectively.

Kayhan et al. [6] in their study of 43 patients by both Doppler and MDCTA showed that the number of segments with stenosis greater than 50% was 27 (3.49%) and 35 (4.52%) on DUS and MDCTA, respectively. The number of segments with occlusion was 59 (7.62%) and 95 (12.27%) on DUS and MDCTA, respectively. Overall, these results showed that when DUS and MDCTA are compared, MDCTA detects more stenotic or occluded arteries in the suprapopliteal, infrapopliteal, and whole leg comparison. These results are in agreement with the present study regarding occlusion and are not in agreement with the present study regarding stenosis; this is mostly attributed to the small sample size.

This study showed that color Doppler and CT angiography are more widely available, easier to perform, less costly, and also can be performed on almost all patients; on the other hand, MRA was not performed because of its high cost and it cannot be performed on patients with pacemakers and metallic stents.

MDCT angiography of the aorta and lower-extremity arteries in this study demonstrated that the technique is highly accurate and has potential to substitute DSA and MRA. As CT scan is generally easier to perform, more widely available, and can be obtained more rapidly than MRA and DSA, it is usually preferred in the emergent setting.


  Conclusion Top


The use of CTA and DUS increases the ability to better delineate vascular anatomy, localize the obstruction, assess the severity of stenosis, and detect the presence of collaterals and distal run-off. CTA scan is generally noninvasive, easy to perform, widely available, and can be obtained more rapidly than MR and DSA.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Richard JL, Schuldiner S. Epidemiology of diabetic foot problems. Rev Med Interne 2008; 29:222–230.  Back to cited text no. 1
    
2.
Krishnan ST, Quattrini C, Jeziorska M, Malik RA, Rayman G. Neurovascular factors in wound healing in the foot skin of type II diabetic subjects. Diabetes Care 2007; 30:3058–3062.  Back to cited text no. 2
    
3.
Dakshin GD, Perry H, Robert LG. The diabetic foot – imaging options and considerations. US Endocrinol 2007; 2:75–78.  Back to cited text no. 3
    
4.
Elgzyri T, Ekberg G, Peterson K, Lundell A, Apelqvist J. Can Duplex arterial ultrasonography reduce unnecessary angiography? J Wound Care 2008; 17:497–500.  Back to cited text no. 4
    
5.
Lingegowda D, Moorthy S, Sreekumar KP. Imaging in diabetic ischemic foot. Int J Diabetes Dev Ctries 2012; 30:179–185.  Back to cited text no. 5
    
6.
Kayhan A, Palabıyıkb F, Serinsöz S, Kırış AB, Bayramoğlu S, Williams JT, Cimilli T. Multidetector angiography versus arterial duplex USG in diagnosis of mild lower extremity peripheral arterial disease: is multidetector CT a valuable screening tool? Eur J Radiol 2012; 81:542–546.  Back to cited text no. 6
    


    Figures

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

  [Table 1], [Table 2]



 

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