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Pitfalls and artefacts in performance and interpretation of contrast-enhanced MR angiography of the lower limbs
Clinical Radiology 65 (2010) 651e658
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.elsevierhealth.com/journals/crad
Pictorial Review
Pitfalls and artefacts in performance and interpretation of contrast-enhanced MR angiography of the lower limbs P.N. Malcolm a, *, P. Craven b, D. Klass a a b
Department of Radiology, Norfolk and Norwich University Hospital, Norwich, UK Department of Radiology, Pilgrim Hospital, United Lincolnshire Hospitals NHS Trust, Boston, UK
art icl e i nformat ion Article history: Received 2 February 2010 Received in revised form 1 March 2010 Accepted 15 March 2010
Peripheral contrast-enhanced MR angiography is widely used for anatomical imaging of the arterial system of the lower limb. There are several pitfalls in the planning, acquisition, and interpretation of these studies that can result in the loss of important diagnostic information, as well as artefacts that can be misinterpreted as disease entities. This review illustrates the range of these potential sources of error and how to avoid them. Ó 2010 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Intra-arterial catheter angiography remains the reference standard for the assessment of the peripheral arterial system.1 It is a technique with high spatial resolution and the potential to progress to therapeutic intervention. It does have disadvantages, including the use of ionising radiation and potential complications arising from the use of large volumes of iodinated intravenous contrast medium and the need for arterial puncture. Peripheral contrast-enhanced peripheral magnetic resonance angiography (CE-MRA) has enabled rapid, first-pass anatomical imaging without the adverse effects of catheter angiography and is widely used as an alternative method for anatomical imaging of the lower limb vasculature. The first method to achieve general clinical acceptance was the use of an automated stepping table method using a single infusion of intravenous contrast medium with firstpass imaging at three stations progressing from lower abdomen to calves. This method is robust and simple, and
* Guarantor and correspondent: P. Malcolm, Department of Radiology, Norfolk and Norwich University Hospital, Colney Lane, Norwich NR4 7UY, UK. Tel.: þ44 1603286286; fax: þ44 1603286077. E-mail address: [email protected] (P.N. Malcolm).
studies have suggested good correlation with severity of stenosis at conventional angiography.2 The technique is relatively free of flow artefacts; however, because of the dependence on T1 shortening in contrast to the dependence on flow in two-dimensional (2D) time of flight MRA, the possibility of overestimation of severe stenoses due to dephasing artefact remains.3 This effect can be further exaggerated on maximum intensity projection (MIP) reconstructions.4 There are challenges, particularly venous contamination, which can obscure the arteries, and these occur in 8e20% of studies.2,5,6 Since introduction of this technique, there have been several advances in peripheral CE-MRA. Increases in gradient strength and the advent of multi-element array coils have enabled more rapid image acquisition, with greater signal and spatial resolution. Parallel imaging has also reduced acquisition times, reducing venous contamination.7 Successful alternative strategies to reduce venous contamination in the calf have been the use of dual injection techniques, scanning the calf before the upper stations,8 time-resolved imaging of the calf,9 or the use of subsystolic thigh compression.10,11 Imaging at 3 T has made it possible to achieve almost isotropic imaging throughout the peripheral arterial system with low doses of gadolinium.12 Continuous table
0009-9260/$ e see front matter Ó 2010 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2010.03.005
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P.N. Malcolm et al. / Clinical Radiology 65 (2010) 651e658
Table 1 Acquisition parameters for automatic moving table peripheral contrast-enhanced magnetic resonance angiography (CE-MRA) at 1.5 T with parallel imaging (iPAT)
Orientation Repetition time (ms) Echo time (ms) Flip angle Field of view (cm) Section thickness (mm) No. of sections Frequency encoding Phase encoding No. of excitations Phase field of view (%) K-space ordering Spatial resolution (mm) Imaging time (s) iPAT factor
Abdomen
Thigh
Calf/foot
Calf/foot
Coronal 2.5 1.16 20 500 1.6 80 384 261 1 90.6 Sequential 1.7 1.3 1.6 9.9 3
Coronal 3.44 1.29 25 500 1.6 60 512 250 1 81.3 Sequential 1.6 1 1.6 9.1 3
Coronal 3.8 1.44 25 500 1.4 96 512 307 1 75 Elliptic centric 1.2 1 1.4 25 2
Sagittal 4.57 1.68 25 500 1.2 80 512 384 1 75 Elliptic centric 1 1 1.2 90 2
movement also offers the potential for greater spatial resolution and extension of the field of view.13 The purpose of this review is to demonstrate the wide range of artefacts and pitfalls arising from CE-PMRA that may occur in planning and performing studies as well as interpreting images.
angiographic sequences were repeated during infusion of contrast medium. Maximum intensity projections (MIPs) were reviewed with routine reference to source data.
Artefacts arising from scan volume selection Omission of graft from scan volume
CE-MRA protocol Peripheral CE-MRA studies were performed on 1 T (Philips NT, Philips Healthcare, Best, The Netherlands; gradient amplitude 23 mT/m, slew rate 17 mT/m/s) and 1.5 T (Siemens Magnetom Avanto, Siemens Medical, Erlangen, Germany; gradient amplitude 33 mT/m, slew rate 125 mT/m/s) MR scanners. A single infusion of intravenous gadolinium chelate with automated table movement between three stations, together with MR fluoroscopic triggering of the intravenous contrast medium infusion was used in all studies. Following localiser scans, thigh cuffs were inflated to 60 mmHg. Coronal masks of the lower abdomen, thigh, and calf were obtained using spoiledgradient echo three-dimensional (3D) angiographic sequences. The automated table step movement required intervals of approximately 4 s. On the 1.5 T unit, an additional high-resolution sagittal 3D acquisition of the calves was performed before and after contrast medium infusion. Acquisition parameters at each station are shown for the 1.5 T (Table 1) and the 1 T system (Table 2). Scanning during intravenous gadolinium chelate infusion was triggered when contrast medium was first seen in the iliac arteries using MR “fluoroscopy.” Coronal 2D volume imaging of the aorto-iliac arteries at 1 frame/s was acquired with in-line subtraction. Intravenous contrast medium [20e40 ml Gadopentate dimeglumine (Magnevist, Bayer Healthcare Pharmaceuticals, Wayne, NJ, USA) or Gadoterate meglumine (Dotarem, Guerbet, Paris, France)] was injected at 1.5e2 ml/s, followed immediately by 20e40 ml/s of 0.9% saline injected at 1.5e2 ml/s through a 20 G cannula inserted into an antecubital vein. The 3D
Limiting the scan volume reduces the total scan time. Reduction in the coronal plane (slice direction), however, may lead to the omission of subcutaneous vascular grafts (Fig. 1a). It is advisable to enquire about previous vascular surgery before scanning to alert to this possibility. Flow-dependent localisers may not show flow in a crossover graft because the flow is in the scan plane. Planning the scan volume with steady-state sequences, which are not dependent on flow, helps to detect crossover grafts before planning the scan volume. Sagittal MIPs may also help recognition of truncation of the vascular structures retrospectively. A repeat study in this case shows a patent crossover graft (Fig. 1b). Table 2 Acquisition parameters for automatic moving table peripheral contrastenhanced magnetic resonance angiography (CE-MRA) at 1 T without parallel imaging
Repetition time (ms) Echo time (ms) Flip angle Field of view (cm) Section thickness (mm) No. of sections Frequency encoding Phase encoding No. of excitations Phase field of view (%) K-space ordering Spatial resolution Imaging time (s)
Abdomen
Thigh
Calf
7.5 2.3 35 430 1.7 50 464 128 1 75 Reverse centric 0.84 0.84 1.7 21
7.5 2.3 35 430 1.7 50 464 128 1 75 Lowehigh 0.84 0.84 1.7 21
7.5 2.3 35 430 1.7 50 464 128 1 75 Highelow 0.84 0.84 1.7 21
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Figure 1 A 64-year-old man with a history of a femoro-femoral crossover graft and worsening left-sided calf claudication. (a) MIP image showing occluded left iliac system and suggesting occlusion of the crossover graft. (b) MIP image of repeat scan with a larger scan volume showing a patent femoro-femoral crossover graft.
Wraparound artefact
Immobilisation devices
Peripheral-CEMRA scan times can also be reduced by limiting the right to left field of view (phase encoding). This can result in wraparound artefact. For example, a linear, lowintensity band crossing the right common iliac artery suggested an intimal dissection flap (Fig. 2a). Examination of the baseline data revealed this band to be wraparound artefact of the patient’s forearm (Fig. 2b). The arms are preferably raised above the head to avoid fold-over artefact, although this may increase the risk of patient movement and, in this case, the arms were lowered. Examination of source data is necessary and will often demonstrate the cause of unusual artefacts.
Popliteal artery compression Hyperextension or pressure from patient immobilisation devices may occlude the popliteal artery. Immobilisation devices prevent movement during an acquisition and prevent motion-induced subtraction artefact because of movement between mask and contrast-enhanced acquisitions. In one study, 3% of examinations were degraded by motion-induced subtraction artefact.4 Fig. 3a shows an unusual appearance of bilateral short occlusions at the level of the knee joint. The appearance resolved on a repeat study with padding behind the knees
Figure 2 A 91-year-old man with severe right-sided foot pain at rest. (a) MIP image showing linear, low signal across the distal right common iliac artery (arrow), suspicious of a dissection flap. (b) Source data reveals wraparound artefact causing the low signal line (arrow) caused by the patient’s forearms (arrowheads).
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Figure 3 A 62-year-old woman with right thigh and calf claudication. (a) Appearance of the bilateral popliteal occlusions (arrows). (b) Adjustment of the immobilization device eliminates the artefact.
(Fig. 3b). Caution is necessary when using immobilisation devices, to avoid popliteal artery compression.
triggering or rapid repeated acquisitionsdtime-resolved imaging. MR “fluoroscopic” visualisation is very reliable for scan timing.
Timing of the scan acquisition Slow flow
Early triggering of contrast medium infusion Fig. 4 shows a pulmonary arterio-venous malformation with ringing artefact seen in the thoracic aorta. Ringing artefact reflects acquisition of the centre of k-space too early while the concentration of intravenous gadolinium in the aorta is still rapidly increasing. This occurs when there is premature triggering, particularly when there is early filling of central k-space with centric acquisitions.14 This can be overcome by using a test bolus, using MR fluoroscopic
Artefact may result from slow arterial flow due to increased volume of the arterial tree. A study in a patient with multiple aneurysms shows no flow in the right superficial femoral artery (Fig. 5a and b). A repeat study with greater delay between infusion and scanning was performed showing filling of the right ilio-femoral arterial tree, with venous contamination on the left due to greater delay (Fig. 5c). Asymmetrical flow is a potential pitfall. The MR fluoroscopic triggering technique helps to alert the radiologist to asymmetric iliac flow and increasing the delay before triggering may prevent under-filling of one limb. Our protocol now includes review of the automatic in-line reconstruction of the thigh acquisition. If the superficial femoral arteries are not seen, imaging of thigh and calf is repeated immediately after the study. This has helped to reduce nondiagnostic studies.
Venous contamination
Figure 4 A 57-year-old woman patient with OslereWebereRendu syndrome. MIP image shows aortic ringing artefact (arrowheads) on study triggered early for pulmonary arterio-venous malformation imaging (arrow).
This is the most common artefact in peripheral CE-MRA and despite many advances in MRA technology has not been eliminated. This predominantly affects the calf (Fig. 6) and increases with the length of delay following infusion. Methods to limit this artefact include thigh compression and bolus timing injection to predict the interval between starting infusion and arrival time at the calf.14 High-resolution imaging improves distinction of arteries from veins on source data. Time-resolved imaging of the calves is another successful approach, although in some patients with severe arterial disease, venous contamination is seen before optimal enhancement of the calf arteries. Thigh cuff
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Figure 5 A 61-year-old man with multiple aneurysms and pain at rest in the right leg. (a) Extensive proximal aneurysmal disease and an ectatic left superficial femoral artery. No flow is seen in the right superficial femoral artery (arrow). (b) Flow is seen in a femoro-popliteal graft (arrow) on the left, but no flow on the right. (c) Delayed imaging demonstrates right femoral arteries (arrow).
venous compression increases the arterio-venous transit time.10 In a recent series of 131 studies using thigh cuffs, interpretation of 5% of stations was limited and 1% of stations were non-diagnostic because of venous contamination. Prolongation of the arterio-venous transit time has the additional advantage of enabling repeat scanning of the calves at higher spatial resolution.15 Even with measurement of aorta to lower limb transit times using a timing bolus and the use of sub-systolic thigh compression, venous contamination is not entirely eliminated.16
Thigh compression
(40 mmHg) has been proposed in patients with femoropopliteal grafts because of theoretical risk of occlusion.3 Artefactual occlusion of the thigh arteries is sometimes seen in patients with aorto-iliac occlusions [15, unpublished data]. This example demonstrates sharp termination of branches of the profunda femoris artery and superficial femoral artery (Fig. 7a) in a patient with aorto-iliac occlusion. A repeat study without thigh cuffs demonstrated patency (Fig. 7b). Our protocol is to deflate the cuffs immediately and repeat the thigh and calf stations without compression at the end of the study if the superficial femoral artery appears occluded at in-line reconstructions.
Pseudo-occlusion artefact
Movement resulting from thigh cuff inflation
The use of thigh cuffs inflated to 60 mmHg reduces venous contamination.10,11 A lower inflation pressure
The study depicted in Fig. 8 suggested occlusion of the left femoro-popliteal arteries, but correlation with the planning scan after the study showed that there had been change in thigh position. This is usually attributable to patient movement. This study, however, was performed under general anaesthesia and the movement resulted from inflation of thigh cuffs after the planning scan. There is the risk of change in position if cuffs are inflated after precontrast medium masks. Cuff inflation should be performed before the mask sequences are acquired so that appropriate positioning of the scan volume is confirmed on the mask and there is no risk of movement due to cuff inflation between mask and contrast-enhanced scan.3 It is also necessary to monitor cuff pressure to ensure the cuff pressure is maintained during the study.
Abnormalities obscured by MIP images Unrecognised aneurysm Figure 6 A 83-year-old man with heart failure, diabetes, and bilateral foot ulcers. MIP image showing venous contamination bilaterally obscuring the arterial run-off.
The study depicted in Fig. 9a suggested a 1 cm left internal iliac aneurysm and no flow in the right internal iliac artery on the MIP images. However, source data reveals a 2.7 cm left internal iliac aneurysm and a thrombosed 5 cm
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Figure 7 A 60-year-old man with pain at rest in the left leg. (a) Pseudo-occlusion of the left superficial (arrow) and profunda femoral arteries (arrowheads). (b) The occlusions resolve when thigh cuff inflation is not used.
right iliac aneurysm not visible on MIP data. The T1 intense rim of the right internal iliac aneurysm visible on source data is subtracted on the MIP images (Fig. 9b). Thrombus and vessel wall thickness are not seen on subtracted images. Unsubtracted source data should be examined routinely when reviewing CE-MRA studies. Otherwise aneurysms, most commonly aortic, may be undetected or underestimated. If an aneurysm is suspected, T1 weighted or balanced gradient-echo sequences will demonstrate both vessel wall and lumen.17
Obscured soft-tissue abnormalities The study depicted in Fig. 10a showed ill-defined enhancement in the right thigh. This is frequently seen at sites of inflammation where there is early enhancement of soft tissues (T1 shine-through), which may obscure vessels. In this case, enhancement was attributable to treatment for a soft-tissue sarcoma. However, examination of the source data reveals enhancement in the rim of a collection that was not seen on the MIP (Fig. 10b). Review of source data may demonstrate soft-tissue or intraluminal abnormalities, such as dissection flaps, that are obscured by MIP reconstructions.
Metal artefacts Susceptibility effects The MIPs from this study show large signal voids and vessel distortion due to bilateral hip and knee prostheses (Fig. 11). The appearance of the MIPs might suggest arterial stenoses of the common femoral arteries and occlusion of the popliteal arteries. The source data demonstrated signal void consistent with susceptibility effect due to the prostheses. The particularly intense high signal dot (Fig. 11) suggests susceptibility artefact and review of source data will clarify this.
Nitinol stents
Figure 8 A 64-year-old woman with limiting left calf claudication. MIP image showing apparent occlusion of left femoro-popliteal arteries (arrow) and poor flow in the superficial femoral artery on the right (arrowheads) resulting from movement because of cuff inflation between mask and contrast study.
Stainless steel endovascular stents result in marked susceptibility effect and are usually easily identified. Nitinol stents, such as a left iliac stent, cause much less susceptibility effect. Fig. 12 shows some attenuation of luminal signal at the site of the stent, but there is relatively little artefact3 and source data allows some interpretation of flow within it. Even on T2*-weighted imaging, susceptibility effect was minimal in this case. The relatively smooth narrowing and homogeneous mild
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Figure 9 A 75-year-old man with multiple aneurysms imaged to determine run-off. (a) A 1 cm left internal iliac aneurysm is seen on the MIP image (arrow). (b) Bilateral internal iliac aneurysms are revealed on source data (arrows). The T1 intense rim of the right aneurysm, concealed on the MIP image because of subtraction, is seen on the source data (arrowhead).
reduction in signal are typical of a nitinol stent,11 but may be harder to recognize because of the mild susceptibility effect. Any history of vascular stenting is important to elicit.
Teaching points A history of any vascular surgery, stents, or joint replacements is helpful at the time of scanning and the scan volume should be planned to include any arterial grafts.
Appropriate immobilisation will prevent motion subtraction artefacts, but popliteal compression must be avoided. Thigh cuffs should be inflated before the acquisition of the mask series to ensure that positioning will include the arteries. Cuffs may cause pseudo-occlusion in patients with aorto-iliac occlusions. During the contrast scan, review of in-line reconstructions will assist recognition of absence of flow in the superficial femoral artery due to slow flow, occlusion, or pseudo-occlusion. This enables repeat scanning of the thigh and calf when the lower stations are complete avoiding repeat studies.
Figure 10 A 59-year-old woman with a history of excision and radiotherapy of a soft-tissue sarcoma in the right thigh. (a) MIP image shows high signal in the right mid thigh (arrowhead) due to the T1 shine-through. (b) The source data demonstrates a low signal collection (arrowheads) in right thigh not seen on MIP images.
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Conclusion Peripheral CE-MRA is now a routine and reliable way to assess the lower limb arterial tree. This technique is now challenging conventional angiography in spatial resolution as well as convenience and safety. Technical improvements have substantially reduced venous contamination, which remains the major limitation in practice. Nevertheless, technical advances have not negated the need for attention to detail if this technique is to provide accurate diagnostic information.
References
Figure 11 A 92-year-old woman with rheumatoid arthritis and multiple joint prostheses with pain at rest in the right foot. MIP images demonstrate a severely attenuated distal left common femoral artery (arrowhead), absent popliteal artery signal bilaterally and an attenuated, possibly occluded right common and superficial femoral artery (arrows). This is due to signal voids created by the caused by the metal prostheses (susceptibility artefact). The high-intensity dot (arrowhead) at the right groin is a further indication of susceptibility artefact.
Source data should be routinely scrutinized, in addition to MIP images, to characterise luminal and extraluminal abnormalities as well as artefacts, such as susceptibility effects.
Figure 12 A 76-year-old woman with a history of a femoro-femoral crossover graft, right femoro-popliteal bypass graft, and a left iliac stent presented with pain at rest in the left foot. MIP image demonstrating smooth narrowing and reduced intensity of the external iliac artery (arrow) due to mild field distortion caused by nitinol endovascular stents (susceptibility effect).
1. Poschreinder FP, Hamer OW, Herold T, et al. Diagnostic accuracy of intra-arterial and IV MR angiography for the detection of stenosis of the infra-inguinal arteries. AJR Am J Roentgenol 2009;192:117e21. 2. Meaney JFM, Ridgway JP, Chakraverty S, et al. Stepping-table gadoliniumenhanced digital subtraction MR angiography of the aorta and lower extremity arteries: preliminary experience. Radiology 1999;211:59e67. 3. Ersoy H, Zhang H, Prince M. Peripheral MR angiography. J Cardiovasc Magn Reson 2006;8:517e28. 4. Low G, Mizzi A, Ong K, et al. Technical inadequacies of peripheral contrast-enhanced magnetic resonance angiography: incidence, causes and management strategies. Clin Radiol 2006;61:937e45. 5. Ho KY, Leiner T, de Haan MW, et al. Peripheral vascular tree stenoses: evaluation with moving bed infusion-tracking MR angiography. Radiology 1998;206:683e92. 6. Wang Y, Winchester PA, Khilnani NM, et al. Contrast-enhanced peripheral MR angiography form the abdominal aorta to the pedal arteries: combined dynamic two-dimensional and bolus-chase threedimensional acquisitions. Invest Radiol 2001;36:170e7. 7. Maki JH, Wilson GJ, Eubank WB, et al. Utilizing SENSE to achieve lower station sub-millimeter isotropic resolution and minimal venous enhancement in peripheral MR angiography. J Magn Reson Imaging 2002;15:484e91. 8. Pereles FS, Collins JD, Carr JC, et al. Accuracy of stepping-table lower extremity MR angiography with dual-level bolus timing and separate calf acquisition: hybrid peripheral MR angiography. Radiology 2006;240: 283e90. 9. Swan JS, Carroll TJ, Kennell TW, et al. Time-resolved three-dimensional contrast-enhanced MR angiography of the peripheral vessels. Radiology 2002;225:43e52. 10. Zhang HL, Ho BY, Chao M, et al. Decreased venous contamination on 3D gadolinium-enhanced bolus chase peripheral MR angiography using thigh compression. AJR Am J Roentgenol 2004;183:1041e7. 11. Vogt FM, Ajaj W, Hunold P, et al. Venous compression at high-spatialresolution three-dimensional MR angiography of peripheral arteries. Radiology 2004;233:913e20. 12. Nael K, Krishnam M, Nael A, et al. Peripheral contrast-enhanced MR angiography at 3.0 T, improved spatial resolution and low dose contrast: initial clinical experience. Eur Radiol 2008;18:2893e900. 13. Vogt FM, Zenge MO, Ladd ME, et al. Comparison of continuous MR angiography and conventional MR angiography. Radiology 2007;243:229e38. 14. Maki JH, Prince MR, Londy FJ, et al. The effects of time varying intravascular signal intensity and k-space acquisition order on three-dimensional MR angiography image quality. J Magn Reson Imaging 1996;6:642e51. 15. West AT, Toms AP, Malcolm PN. The effectiveness of thigh cuff venous compression in peripheral MRA and description of an unintended effect: the femoral pseudo-occlusion artefact. 2009. RSNA December 2009;1100 [abstract no.: LL-VI4366-D10]. 16. Potthast S, Wilson JG, Wang MS, et al. Peripheral moving-table contrastenhanced magnetic resonance angiography (CE-MRA) using a prototype 18-channel peripheral vascular coil and scanning parameters optimized to the patient’s individual hemodynamics. J Magn Reson Imaging 2009;29:1106e15. 17. Lee VS, Martin DJ, Krinsky GA, et al. Gadolinium-enhanced MR angiography. artefacts and pitfalls. AJR Am J Roentgenol 2000;175:197e205.
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.elsevierhealth.com/journals/crad
Pictorial Review
Pitfalls and artefacts in performance and interpretation of contrast-enhanced MR angiography of the lower limbs P.N. Malcolm a, *, P. Craven b, D. Klass a a b
Department of Radiology, Norfolk and Norwich University Hospital, Norwich, UK Department of Radiology, Pilgrim Hospital, United Lincolnshire Hospitals NHS Trust, Boston, UK
art icl e i nformat ion Article history: Received 2 February 2010 Received in revised form 1 March 2010 Accepted 15 March 2010
Peripheral contrast-enhanced MR angiography is widely used for anatomical imaging of the arterial system of the lower limb. There are several pitfalls in the planning, acquisition, and interpretation of these studies that can result in the loss of important diagnostic information, as well as artefacts that can be misinterpreted as disease entities. This review illustrates the range of these potential sources of error and how to avoid them. Ó 2010 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Intra-arterial catheter angiography remains the reference standard for the assessment of the peripheral arterial system.1 It is a technique with high spatial resolution and the potential to progress to therapeutic intervention. It does have disadvantages, including the use of ionising radiation and potential complications arising from the use of large volumes of iodinated intravenous contrast medium and the need for arterial puncture. Peripheral contrast-enhanced peripheral magnetic resonance angiography (CE-MRA) has enabled rapid, first-pass anatomical imaging without the adverse effects of catheter angiography and is widely used as an alternative method for anatomical imaging of the lower limb vasculature. The first method to achieve general clinical acceptance was the use of an automated stepping table method using a single infusion of intravenous contrast medium with firstpass imaging at three stations progressing from lower abdomen to calves. This method is robust and simple, and
* Guarantor and correspondent: P. Malcolm, Department of Radiology, Norfolk and Norwich University Hospital, Colney Lane, Norwich NR4 7UY, UK. Tel.: þ44 1603286286; fax: þ44 1603286077. E-mail address: [email protected] (P.N. Malcolm).
studies have suggested good correlation with severity of stenosis at conventional angiography.2 The technique is relatively free of flow artefacts; however, because of the dependence on T1 shortening in contrast to the dependence on flow in two-dimensional (2D) time of flight MRA, the possibility of overestimation of severe stenoses due to dephasing artefact remains.3 This effect can be further exaggerated on maximum intensity projection (MIP) reconstructions.4 There are challenges, particularly venous contamination, which can obscure the arteries, and these occur in 8e20% of studies.2,5,6 Since introduction of this technique, there have been several advances in peripheral CE-MRA. Increases in gradient strength and the advent of multi-element array coils have enabled more rapid image acquisition, with greater signal and spatial resolution. Parallel imaging has also reduced acquisition times, reducing venous contamination.7 Successful alternative strategies to reduce venous contamination in the calf have been the use of dual injection techniques, scanning the calf before the upper stations,8 time-resolved imaging of the calf,9 or the use of subsystolic thigh compression.10,11 Imaging at 3 T has made it possible to achieve almost isotropic imaging throughout the peripheral arterial system with low doses of gadolinium.12 Continuous table
0009-9260/$ e see front matter Ó 2010 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2010.03.005
652
P.N. Malcolm et al. / Clinical Radiology 65 (2010) 651e658
Table 1 Acquisition parameters for automatic moving table peripheral contrast-enhanced magnetic resonance angiography (CE-MRA) at 1.5 T with parallel imaging (iPAT)
Orientation Repetition time (ms) Echo time (ms) Flip angle Field of view (cm) Section thickness (mm) No. of sections Frequency encoding Phase encoding No. of excitations Phase field of view (%) K-space ordering Spatial resolution (mm) Imaging time (s) iPAT factor
Abdomen
Thigh
Calf/foot
Calf/foot
Coronal 2.5 1.16 20 500 1.6 80 384 261 1 90.6 Sequential 1.7 1.3 1.6 9.9 3
Coronal 3.44 1.29 25 500 1.6 60 512 250 1 81.3 Sequential 1.6 1 1.6 9.1 3
Coronal 3.8 1.44 25 500 1.4 96 512 307 1 75 Elliptic centric 1.2 1 1.4 25 2
Sagittal 4.57 1.68 25 500 1.2 80 512 384 1 75 Elliptic centric 1 1 1.2 90 2
movement also offers the potential for greater spatial resolution and extension of the field of view.13 The purpose of this review is to demonstrate the wide range of artefacts and pitfalls arising from CE-PMRA that may occur in planning and performing studies as well as interpreting images.
angiographic sequences were repeated during infusion of contrast medium. Maximum intensity projections (MIPs) were reviewed with routine reference to source data.
Artefacts arising from scan volume selection Omission of graft from scan volume
CE-MRA protocol Peripheral CE-MRA studies were performed on 1 T (Philips NT, Philips Healthcare, Best, The Netherlands; gradient amplitude 23 mT/m, slew rate 17 mT/m/s) and 1.5 T (Siemens Magnetom Avanto, Siemens Medical, Erlangen, Germany; gradient amplitude 33 mT/m, slew rate 125 mT/m/s) MR scanners. A single infusion of intravenous gadolinium chelate with automated table movement between three stations, together with MR fluoroscopic triggering of the intravenous contrast medium infusion was used in all studies. Following localiser scans, thigh cuffs were inflated to 60 mmHg. Coronal masks of the lower abdomen, thigh, and calf were obtained using spoiledgradient echo three-dimensional (3D) angiographic sequences. The automated table step movement required intervals of approximately 4 s. On the 1.5 T unit, an additional high-resolution sagittal 3D acquisition of the calves was performed before and after contrast medium infusion. Acquisition parameters at each station are shown for the 1.5 T (Table 1) and the 1 T system (Table 2). Scanning during intravenous gadolinium chelate infusion was triggered when contrast medium was first seen in the iliac arteries using MR “fluoroscopy.” Coronal 2D volume imaging of the aorto-iliac arteries at 1 frame/s was acquired with in-line subtraction. Intravenous contrast medium [20e40 ml Gadopentate dimeglumine (Magnevist, Bayer Healthcare Pharmaceuticals, Wayne, NJ, USA) or Gadoterate meglumine (Dotarem, Guerbet, Paris, France)] was injected at 1.5e2 ml/s, followed immediately by 20e40 ml/s of 0.9% saline injected at 1.5e2 ml/s through a 20 G cannula inserted into an antecubital vein. The 3D
Limiting the scan volume reduces the total scan time. Reduction in the coronal plane (slice direction), however, may lead to the omission of subcutaneous vascular grafts (Fig. 1a). It is advisable to enquire about previous vascular surgery before scanning to alert to this possibility. Flow-dependent localisers may not show flow in a crossover graft because the flow is in the scan plane. Planning the scan volume with steady-state sequences, which are not dependent on flow, helps to detect crossover grafts before planning the scan volume. Sagittal MIPs may also help recognition of truncation of the vascular structures retrospectively. A repeat study in this case shows a patent crossover graft (Fig. 1b). Table 2 Acquisition parameters for automatic moving table peripheral contrastenhanced magnetic resonance angiography (CE-MRA) at 1 T without parallel imaging
Repetition time (ms) Echo time (ms) Flip angle Field of view (cm) Section thickness (mm) No. of sections Frequency encoding Phase encoding No. of excitations Phase field of view (%) K-space ordering Spatial resolution Imaging time (s)
Abdomen
Thigh
Calf
7.5 2.3 35 430 1.7 50 464 128 1 75 Reverse centric 0.84 0.84 1.7 21
7.5 2.3 35 430 1.7 50 464 128 1 75 Lowehigh 0.84 0.84 1.7 21
7.5 2.3 35 430 1.7 50 464 128 1 75 Highelow 0.84 0.84 1.7 21
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Figure 1 A 64-year-old man with a history of a femoro-femoral crossover graft and worsening left-sided calf claudication. (a) MIP image showing occluded left iliac system and suggesting occlusion of the crossover graft. (b) MIP image of repeat scan with a larger scan volume showing a patent femoro-femoral crossover graft.
Wraparound artefact
Immobilisation devices
Peripheral-CEMRA scan times can also be reduced by limiting the right to left field of view (phase encoding). This can result in wraparound artefact. For example, a linear, lowintensity band crossing the right common iliac artery suggested an intimal dissection flap (Fig. 2a). Examination of the baseline data revealed this band to be wraparound artefact of the patient’s forearm (Fig. 2b). The arms are preferably raised above the head to avoid fold-over artefact, although this may increase the risk of patient movement and, in this case, the arms were lowered. Examination of source data is necessary and will often demonstrate the cause of unusual artefacts.
Popliteal artery compression Hyperextension or pressure from patient immobilisation devices may occlude the popliteal artery. Immobilisation devices prevent movement during an acquisition and prevent motion-induced subtraction artefact because of movement between mask and contrast-enhanced acquisitions. In one study, 3% of examinations were degraded by motion-induced subtraction artefact.4 Fig. 3a shows an unusual appearance of bilateral short occlusions at the level of the knee joint. The appearance resolved on a repeat study with padding behind the knees
Figure 2 A 91-year-old man with severe right-sided foot pain at rest. (a) MIP image showing linear, low signal across the distal right common iliac artery (arrow), suspicious of a dissection flap. (b) Source data reveals wraparound artefact causing the low signal line (arrow) caused by the patient’s forearms (arrowheads).
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Figure 3 A 62-year-old woman with right thigh and calf claudication. (a) Appearance of the bilateral popliteal occlusions (arrows). (b) Adjustment of the immobilization device eliminates the artefact.
(Fig. 3b). Caution is necessary when using immobilisation devices, to avoid popliteal artery compression.
triggering or rapid repeated acquisitionsdtime-resolved imaging. MR “fluoroscopic” visualisation is very reliable for scan timing.
Timing of the scan acquisition Slow flow
Early triggering of contrast medium infusion Fig. 4 shows a pulmonary arterio-venous malformation with ringing artefact seen in the thoracic aorta. Ringing artefact reflects acquisition of the centre of k-space too early while the concentration of intravenous gadolinium in the aorta is still rapidly increasing. This occurs when there is premature triggering, particularly when there is early filling of central k-space with centric acquisitions.14 This can be overcome by using a test bolus, using MR fluoroscopic
Artefact may result from slow arterial flow due to increased volume of the arterial tree. A study in a patient with multiple aneurysms shows no flow in the right superficial femoral artery (Fig. 5a and b). A repeat study with greater delay between infusion and scanning was performed showing filling of the right ilio-femoral arterial tree, with venous contamination on the left due to greater delay (Fig. 5c). Asymmetrical flow is a potential pitfall. The MR fluoroscopic triggering technique helps to alert the radiologist to asymmetric iliac flow and increasing the delay before triggering may prevent under-filling of one limb. Our protocol now includes review of the automatic in-line reconstruction of the thigh acquisition. If the superficial femoral arteries are not seen, imaging of thigh and calf is repeated immediately after the study. This has helped to reduce nondiagnostic studies.
Venous contamination
Figure 4 A 57-year-old woman patient with OslereWebereRendu syndrome. MIP image shows aortic ringing artefact (arrowheads) on study triggered early for pulmonary arterio-venous malformation imaging (arrow).
This is the most common artefact in peripheral CE-MRA and despite many advances in MRA technology has not been eliminated. This predominantly affects the calf (Fig. 6) and increases with the length of delay following infusion. Methods to limit this artefact include thigh compression and bolus timing injection to predict the interval between starting infusion and arrival time at the calf.14 High-resolution imaging improves distinction of arteries from veins on source data. Time-resolved imaging of the calves is another successful approach, although in some patients with severe arterial disease, venous contamination is seen before optimal enhancement of the calf arteries. Thigh cuff
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Figure 5 A 61-year-old man with multiple aneurysms and pain at rest in the right leg. (a) Extensive proximal aneurysmal disease and an ectatic left superficial femoral artery. No flow is seen in the right superficial femoral artery (arrow). (b) Flow is seen in a femoro-popliteal graft (arrow) on the left, but no flow on the right. (c) Delayed imaging demonstrates right femoral arteries (arrow).
venous compression increases the arterio-venous transit time.10 In a recent series of 131 studies using thigh cuffs, interpretation of 5% of stations was limited and 1% of stations were non-diagnostic because of venous contamination. Prolongation of the arterio-venous transit time has the additional advantage of enabling repeat scanning of the calves at higher spatial resolution.15 Even with measurement of aorta to lower limb transit times using a timing bolus and the use of sub-systolic thigh compression, venous contamination is not entirely eliminated.16
Thigh compression
(40 mmHg) has been proposed in patients with femoropopliteal grafts because of theoretical risk of occlusion.3 Artefactual occlusion of the thigh arteries is sometimes seen in patients with aorto-iliac occlusions [15, unpublished data]. This example demonstrates sharp termination of branches of the profunda femoris artery and superficial femoral artery (Fig. 7a) in a patient with aorto-iliac occlusion. A repeat study without thigh cuffs demonstrated patency (Fig. 7b). Our protocol is to deflate the cuffs immediately and repeat the thigh and calf stations without compression at the end of the study if the superficial femoral artery appears occluded at in-line reconstructions.
Pseudo-occlusion artefact
Movement resulting from thigh cuff inflation
The use of thigh cuffs inflated to 60 mmHg reduces venous contamination.10,11 A lower inflation pressure
The study depicted in Fig. 8 suggested occlusion of the left femoro-popliteal arteries, but correlation with the planning scan after the study showed that there had been change in thigh position. This is usually attributable to patient movement. This study, however, was performed under general anaesthesia and the movement resulted from inflation of thigh cuffs after the planning scan. There is the risk of change in position if cuffs are inflated after precontrast medium masks. Cuff inflation should be performed before the mask sequences are acquired so that appropriate positioning of the scan volume is confirmed on the mask and there is no risk of movement due to cuff inflation between mask and contrast-enhanced scan.3 It is also necessary to monitor cuff pressure to ensure the cuff pressure is maintained during the study.
Abnormalities obscured by MIP images Unrecognised aneurysm Figure 6 A 83-year-old man with heart failure, diabetes, and bilateral foot ulcers. MIP image showing venous contamination bilaterally obscuring the arterial run-off.
The study depicted in Fig. 9a suggested a 1 cm left internal iliac aneurysm and no flow in the right internal iliac artery on the MIP images. However, source data reveals a 2.7 cm left internal iliac aneurysm and a thrombosed 5 cm
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Figure 7 A 60-year-old man with pain at rest in the left leg. (a) Pseudo-occlusion of the left superficial (arrow) and profunda femoral arteries (arrowheads). (b) The occlusions resolve when thigh cuff inflation is not used.
right iliac aneurysm not visible on MIP data. The T1 intense rim of the right internal iliac aneurysm visible on source data is subtracted on the MIP images (Fig. 9b). Thrombus and vessel wall thickness are not seen on subtracted images. Unsubtracted source data should be examined routinely when reviewing CE-MRA studies. Otherwise aneurysms, most commonly aortic, may be undetected or underestimated. If an aneurysm is suspected, T1 weighted or balanced gradient-echo sequences will demonstrate both vessel wall and lumen.17
Obscured soft-tissue abnormalities The study depicted in Fig. 10a showed ill-defined enhancement in the right thigh. This is frequently seen at sites of inflammation where there is early enhancement of soft tissues (T1 shine-through), which may obscure vessels. In this case, enhancement was attributable to treatment for a soft-tissue sarcoma. However, examination of the source data reveals enhancement in the rim of a collection that was not seen on the MIP (Fig. 10b). Review of source data may demonstrate soft-tissue or intraluminal abnormalities, such as dissection flaps, that are obscured by MIP reconstructions.
Metal artefacts Susceptibility effects The MIPs from this study show large signal voids and vessel distortion due to bilateral hip and knee prostheses (Fig. 11). The appearance of the MIPs might suggest arterial stenoses of the common femoral arteries and occlusion of the popliteal arteries. The source data demonstrated signal void consistent with susceptibility effect due to the prostheses. The particularly intense high signal dot (Fig. 11) suggests susceptibility artefact and review of source data will clarify this.
Nitinol stents
Figure 8 A 64-year-old woman with limiting left calf claudication. MIP image showing apparent occlusion of left femoro-popliteal arteries (arrow) and poor flow in the superficial femoral artery on the right (arrowheads) resulting from movement because of cuff inflation between mask and contrast study.
Stainless steel endovascular stents result in marked susceptibility effect and are usually easily identified. Nitinol stents, such as a left iliac stent, cause much less susceptibility effect. Fig. 12 shows some attenuation of luminal signal at the site of the stent, but there is relatively little artefact3 and source data allows some interpretation of flow within it. Even on T2*-weighted imaging, susceptibility effect was minimal in this case. The relatively smooth narrowing and homogeneous mild
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Figure 9 A 75-year-old man with multiple aneurysms imaged to determine run-off. (a) A 1 cm left internal iliac aneurysm is seen on the MIP image (arrow). (b) Bilateral internal iliac aneurysms are revealed on source data (arrows). The T1 intense rim of the right aneurysm, concealed on the MIP image because of subtraction, is seen on the source data (arrowhead).
reduction in signal are typical of a nitinol stent,11 but may be harder to recognize because of the mild susceptibility effect. Any history of vascular stenting is important to elicit.
Teaching points A history of any vascular surgery, stents, or joint replacements is helpful at the time of scanning and the scan volume should be planned to include any arterial grafts.
Appropriate immobilisation will prevent motion subtraction artefacts, but popliteal compression must be avoided. Thigh cuffs should be inflated before the acquisition of the mask series to ensure that positioning will include the arteries. Cuffs may cause pseudo-occlusion in patients with aorto-iliac occlusions. During the contrast scan, review of in-line reconstructions will assist recognition of absence of flow in the superficial femoral artery due to slow flow, occlusion, or pseudo-occlusion. This enables repeat scanning of the thigh and calf when the lower stations are complete avoiding repeat studies.
Figure 10 A 59-year-old woman with a history of excision and radiotherapy of a soft-tissue sarcoma in the right thigh. (a) MIP image shows high signal in the right mid thigh (arrowhead) due to the T1 shine-through. (b) The source data demonstrates a low signal collection (arrowheads) in right thigh not seen on MIP images.
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Conclusion Peripheral CE-MRA is now a routine and reliable way to assess the lower limb arterial tree. This technique is now challenging conventional angiography in spatial resolution as well as convenience and safety. Technical improvements have substantially reduced venous contamination, which remains the major limitation in practice. Nevertheless, technical advances have not negated the need for attention to detail if this technique is to provide accurate diagnostic information.
References
Figure 11 A 92-year-old woman with rheumatoid arthritis and multiple joint prostheses with pain at rest in the right foot. MIP images demonstrate a severely attenuated distal left common femoral artery (arrowhead), absent popliteal artery signal bilaterally and an attenuated, possibly occluded right common and superficial femoral artery (arrows). This is due to signal voids created by the caused by the metal prostheses (susceptibility artefact). The high-intensity dot (arrowhead) at the right groin is a further indication of susceptibility artefact.
Source data should be routinely scrutinized, in addition to MIP images, to characterise luminal and extraluminal abnormalities as well as artefacts, such as susceptibility effects.
Figure 12 A 76-year-old woman with a history of a femoro-femoral crossover graft, right femoro-popliteal bypass graft, and a left iliac stent presented with pain at rest in the left foot. MIP image demonstrating smooth narrowing and reduced intensity of the external iliac artery (arrow) due to mild field distortion caused by nitinol endovascular stents (susceptibility effect).
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