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REVIEW

Magnetic Resonance Imaging is More Sensitive than Computed Tomography


Angiography for the Detection of Endoleaks after Endovascular Abdominal
Aortic Aneurysm Repair: A Systematic Review
a,*,e b,e
J. Habets , H.J.A. Zandvoort , J.B. Reitsma c, L.W. Bartels d, F.L. Moll b, T. Leiner a,e
, J.A. van Herwaarden b,e

a
Department of Radiology, University Medical Center Utrecht, Heidelberglaan 100, HP E01.132, 3508 GA Utrecht, The Netherlands
b
Department of Vascular Surgery, University Medical Center Utrecht, Utrecht, The Netherlands
c
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands
d
Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands

Objectives: The purpose of this systematic review was to examine whether magnetic resonance imaging (MRI) or
computed tomography angiography (CTA) is more sensitive for the detection of endoleaks in patients with
abdominal aortic aneurysm (AAA) after EVAR.
Design: Systematic review.
Materials and methods: A systematic electronic search was performed. Articles were included when post-EVAR
patients were evaluated by both MRI as index test and CTA as comparison. Methodological quality was assessed
with the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) tool. Primary outcome was the proportion
of patients in whom MRI detected additional endoleaks, which were not seen with CTA.
Results: Eleven articles were included. The overall methodological quality of the articles was good. In total, 369
patients with 562 MRI and 562 CTA examinations were included. A total of 146 endoleaks were detected by CTA;
MRI detected all but two of these endoleaks. With MRI 132 additional endoleaks were found.
Conclusions: MRI is more sensitive compared to CTA for the detection of post-EVAR endoleaks, especially for the
detection of type II endoleaks. MRI should be considered in patients with continued AAA growth and negative or
uncertain ndings at CTA.
2013 European Society for Vascular Surgery. Published by Elsevier Ltd. All rights reserved.
Article history: Received 17 July 2012, Accepted 21 December 2012, Available online 9 February 2013
Keywords: Magnetic resonance imaging, Computed tomography angiography, Systematic review, Endoleak,
Abdominal aortic aneurysm

Brief statement
This systematic review demonstrates that magnetic reso- and arrest of abdominal aortic aneurysm (AAA) growth.1,2 A
nance imaging (MRI) detects signicantly more endoleaks clinically important complication after EVAR is the occurrence
compared to computed tomography angiography (CTA) in of endoleak. Endoleak is dened as leakage of blood into the
patients after abdominal endovascular aneurysm repair aneurysm sac, which may result in continued aneurysm
(EVAR). These additional endoleaks detected by MRI are growth and, ultimately, rupture. Endoleaks are classied into
mainly type II endoleaks. In patients with aneurysm growth, different types (Table 1).3 Correct endoleak classication is
these type II endoleaks require treatment according to the important because there are different treatment strategies
current guidelines. MRI is a complementary imaging for different endoleak subtypes.3,4
modality to CTA that must be considered especially in For the detection of complications after EVAR, post-
patients with post-EVAR abdominal aortic aneurysm (AAA) operative surveillance is advised by performing computed
growth of unknown origin. tomography angiography (CTA) and plain radiography
The aim of endovascular aortic aneurysm repair (EVAR) is within 1 month.3 If an endoleak is detected, CTA and plain
to prevent aneurysm rupture by exclusion of the aneurysm radiography are advised after 6 and 12 months and yearly
sac from the systemic circulation. A successful endovascular thereafter. If no endoleak is detected at 1 month, CTA is
procedure will result in depressurisation of the aneurysm sac advised after 12 months followed by yearly abdominal
duplex ultrasound and plain radiography.4 In current
* Corresponding author. Tel.: 31 887556689; fax: 31 302581098. guidelines digital subtraction angiography (DSA) has no
E-mail address: J.Habets@umcutrecht.nl (J. Habets).
e
diagnostic role during EVAR follow-up.4 However, in
These authors contributed equally to this work.
1078-5884/$ e see front matter 2013 European Society for Vascular
patients with inconclusive imaging follow-up or in patients
Surgery. Published by Elsevier Ltd. All rights reserved. with an endoleak that requires treatment, DSA is recom-
http://dx.doi.org/10.1016/j.ejvs.2012.12.014 mended but often not performed.
J. Habets et al. 341

Table 1. Endoleak classication.3 well as the number and type of endoleaks detected by MRI
Endoleak type Description and CTA was collected.
I Attachment site leak e IA proximal, Studies were assessed for quality based on the criteria as
IB is distal, IC Iliac occluder proposed by the Quality Assessment of Diagnostic Accuracy
II Branch vessel retrograde ow e Studies (QUADAS) checklist.9 The QUADAS items for each
IIA IMA; IIB Lumbar arteries included study were scored as yes, no and unclear
III Graft Failure (Appendix II).
IV Graft-wall porosity
V Endotension
IMA Inferior Mesenteric Artery. Data analysis
Currently, tri-phasic CTA with unenhanced, arterial and On MRI examinations, endoleak was dened as a high-intensity
delayed phases is considered to be the most appropriate signal within the aneurysm sac on post-contrast T1-weighted
method for detection of endoleaks after EVAR. Neverthe- images, not present on pre-contrast T1-weighted images.
less, it is known that CTA sometimes fails to detect the The outcome in the rst set of analyses was the proportion
presence of endoleaks.5,6 In patients with aneurysm growth of patients in whom an endoleak was detected by MRI, which
post-EVAR, it is important to detect these missed endoleaks was not detected by CTA, divided by the total number of
with alternative imaging strategies because they may patients examined. In case a study reported results of MRI
require treatment.4,7,8 Because of its excellent soft-tissue versus CTA examination during follow-up from multiple time
contrast, magnetic resonance imaging (MRI) is of high points, we used all available data.10 A Forest plot was
interest for this purpose. On the other hand, it is conceiv- generated to depict the proportion of additional endoleaks
able that susceptibility artefacts associated with the stent- detected by MRI and corresponding 95% condence intervals
graft material limit assessment of post-EVAR AAA with MRI. (CIs) for all studies. To evaluate if data could be pooled, we
At present, the diagnostic capabilities of MRI for the calculated I2 and the Cochrans Q test to examine how
detection of endoleak after EVAR remain to be determined. consistent the proportion of additionally detected endoleaks
The purpose of this systematic review is to examine by MRI was across studies. I2 represents the percentage of
whether MRI is more sensitive than CTA for the detection of variability in the estimates of additionally detected endoleaks
endoleaks in patients with AAA after EVAR. by MRI, which is attributable to heterogeneity between
studies rather than sampling error.
MATERIALS AND METHODS Furthermore, we examined the types of endoleaks that
were detected by MRI, but not seen at CTA. If available, data
Literature search were extracted on the ve subtypes of endoleaks (Table 1).
A systematic electronic search was performed in the PubMed
and Embase databases for original articles published until 1 RESULTS
November 2011. The language was restricted to English arti-
cles. Key search terms were magnetic resonance imaging, Search results
endoleak, endovascular treatment and corresponding The electronic search yielded a total of 218 publications after
synonyms. The exact search terms are shown in Appendix I. removal of duplicates. Nineteen full-text versions of studies
that matched the inclusion criteria were obtained. Six studies
Selection of publications were excluded: two case reports, two publications that
contained the same patient population, one article that did
After removal of duplicates, two reviewers independently
not meet the language restriction (German article) and one
screened titles and abstracts of the remaining studies. Arti-
study that discussed thoracic EVAR (TEVAR) patients. Cross-
cles were included if: (1) patients after EVAR of an abdominal
referencing of all included articles did not yield additional
aortic aneurysm were studied; (2) examination during follow-
articles. The nal selection of articles consisted therefore of
up for the detection of endoleaks included assessment with
11 studies (Fig. 1). The detailed results of the quality
MRI; and (3) a comparison between ndings at MRI and CTA
assessment for each study are given in Appendix II.
was performed. Full-text versions of studies that matched the
All included studies (Table 2) reported on the detection
inclusion criteria were obtained. The reference lists of all
of endoleaks in patients during follow-up after EVAR and
included articles were scanned by the rst authors for any
compared MRI with CTA ndings. These 11 studies included
relevant publication not identied by the electronic searches
369 patients, who underwent at least one MRI and CTA
(cross-referencing); if present, these articles were included.
examination, with 562 MRI and 562 CTA examinations. The
All full-text publications were examined by two reviewers
interval between CTA and MRI should ideally be restricted
independently and in cases of disagreement consensus was
to 1 month. Most studies (n 7) reported a mean time
reached during a consensus meeting.
between MRI and CTA of 1 month or shorter. Two studies
exceeded the 1 month mean interval time between MRI
Quality assessment and CTA modality.5,11 Furthermore, two studies did not
Information on study design characteristics, sample size and explicitly report the time interval between both examina-
type of patient population, MRI protocol, CTA protocol as tions.10,12 The latter four studies were also included in the
342 European Journal of Vascular and Endovascular Surgery Volume 45 Issue 4 April/2013

Pubmed Embase
N = 121 N = 178

N = 299

Removal of duplicates
N = 81

Excluded after screening title + abstract N = 218


N = 201

Inclusion criteria:
- Patients who underwent EVAR for AAA.
- Imaging for the detection of endoleaks during follow up
- Comparison of MRA with CTA.

N = 17
Excluded after reading Full text

N=6 Included after cross


referencing
Reasons of exclusion:
Case report N=2
N=0
Double publication N=2
Non-English article N=1
Thoracic aortic aneurysm N=1
N = 11
Figure 1. Flowchart demonstrating search results and number of included and excluded studies.

systematic review because of the limited number of studies Patient population


providing data on this topic. One study reported similar In the analysis two different study populations were distin-
proportions of additional endoleaks detected by MRI than guished: (1) an unselected patient population (n 10) and (2)
the other included studies. By contrast, the other study patients with no discernible endoleaks at CTA (n 1). One
detected relatively more additional endoleaks but this study study consisted of both unselected patients and patients with
had a limited sample size (n 6).11 All MRI examinations known endoleaks on CTA.13 We considered pooling the
were performed on 1.5-T MRI systems, except in one study extracted data of the individual studies by examining an
in which a 1.0-T MRI system was used in some patients.13 unselected patient population. However, we refrained from
All included studies performed arterial-phase imaging. pooling because of large clinical heterogeneity based on the
Delayed-phase CTA (60 s after contrast administration) QUADAS assessment and large statistical heterogeneity as
was performed in eight of 11 (73) studies (Table 2). In one demonstrated by the I2 test in the unselected population e
study not all patients received delayed-phased imaging. 81.1% (P value of Cochrans Q statistic < 0.001). Therefore,
Delayed-phase imaging was performed only in 13 patients only estimates from individual studies are shown in Fig. 2. In
(13/28; 46%) with suspected endoleaks.14 One study did not the single study that included patients with non-shrinking
report the time interval between contrast administration AAA without visible endoleaks on CTA (population 2), MRI
and delayed-phase imaging.11 Finally, in one study delayed detected six endoleaks (55%) (Fig. 2).16
phase imaging was not performed.12 Detailed individual
information on patient characteristics and stent-graft type
was inconsistently reported in the different studies. The Endoleak types
available information is shown in Table 3. Overall, MRI The proportion of additional endoleaks detected by MRI was
detected 278 endoleaks while CTA detected 146 endoleaks. classied into the different endoleak subtypes. In the unse-
Thus, MRI detected 132 additional endoleaks compared to lected patient population MRI detected a total of 128 addi-
CTA. MRI failed to detect two type I endoleaks: one prox- tional endoleaks. The study of Insko et al. detected four
imal type IA endoleak and one distal type IB endoleak.10,15 additional endoleaks with MRI in nine patients, but did not
In Table 4, the number of additional endoleaks detected by specify which types of endoleaks were found.12 Therefore,
MRI in the different studies is presented. 124 additional endoleaks detected by MRI could be classied
Table 2. Included studies.

J. Habets et al.
Author, journal, Number of Study MRI Reference Delayed phase Mean time No. and type of endoleaks No. and type of endoleaks
year patients population mModality CTA (acquisition between detected by MRI detected by CTA
included time after start MRI and
(number of contrast injection) CTA (range)
scans)
Haulon, Eur. J. 31 (31) Unselected MRI DSA Yes (60 s) 2.6 months Total MRA: 18 Total CTA: 10
Vasc. Endovasc. (1.5 T) (1e6 Type I:1 Type I: 1
Surg., 20015 months) Type II: 17 Type II: 9
Cejna, Eur. Radiol., 32 (40) Unselected MRI CTA Yes (60e70 s) 6.6 days Total: 18 Uniphasic (n
200213 (1.0 T or (0e28 Type I/III: 6 22 scans)
1.5 T) days) Type II: 12 Total: 7
Type I/III: 3
Type II: 4
Biphasic (n
18 scans)
Total: 8
Type I/III: 3
Type II: 5
Insko, Acad. Radiol., 9 (9) Unselected MRI CTA No Not Total:6 Total: 4
200312 (1.5 T) reported Type I:2 Type I: 2
Type II:4 Type II: 2
Ayuso, J. Magn. Reson. 27 (27) Unselected MRI CTA Yes (20e30 s after 1e30 days Total: 21 Total: 16
Imaging, 200426 (n 17) (1.5 T) arterial phase) Type II: 15 Type II: 12
Endoleaks Type III: 3 Type III 3
present Indeterminate: 3 Indeterminate: 1
on CTA
(n 10)
Ersoy, Am. J. 6 (6) Unselected MRI CTA Yes (NR) 90 days (5e Total: 6 Total: 2
Roentgenol., 200411 (1.5 T) 203 days)
Pitton, Am. J. 52 (252) Unselected MRI Consensus Yes (90 s) Not Total MRA: 131 Total CTA: 62
Roentgenol., 200410 (1.5 T) reading of reported Type I: 7 Type I: 8
CTA and Type II: 93 Type II: 42
MRI Type III: 21 Type III: 10
Complex: 10 Complex 2
Van der Laan, 28 (35) Unselected MRI CTA Yes (120 and Max 1 Total: 23 Total: 11
Eur. J. Vasc. (1.5 T) 240 s) in month Type I: 2 Type I: 2
Endovasc. patients Type II: 6 Type II: 3
Surg., 200614 with Type III: 1 Type III: 1
suspected Indeterminate 14 Indeterminate: 5
endoleak
Alerci, Eur. Radiol., 43 (43) Unselected MRI Consensus Yes (60 s) Max 1 Observer 1 Observer 2 Observer 1 Observer 2
200815 (1.5 T) reading of week Total: 22 Total: 24 Total: 11 Total: 12
CTA CTA and Type II: 19 Type II: 13 Type II: 10 Type I: 1
MRI Indeterminate: 3 Indeterminate: 11 Type V: 1 Type II: 7

343
Indeterminate: 4
Continued
344 European Journal of Vascular and Endovascular Surgery Volume 45 Issue 4 April/2013

per endoleak type. This resulted in the following distribution


of additional endoleaks detected by MRI: 86 type II (69%); 12
No. and type of endoleaks

type III (10%) and 26 indeterminate endoleaks (21%). Data on


type II subtype (IIa and IIb) were not provided in most studies
and therefore not addressed in this meta-analysis. A total of
detected by CTA

two endoleaks were detected by CTA and missed by MRI.


Both these leaks were type 1 endoleaks.10,15
Type II: 12

Type II: 18
Type III: 2
Total: 12

Total: 20
Total: 0

DISCUSSION
The principal nding of this systematic review is that MRI
detects signicantly more endoleaks compared to CTA in
patients after EVAR, especially type II endoleaks. The detec-
tion of these additional type II endoleaks is clinically relevant
No. and type of endoleaks

because these endoleaks require treatment in patients with


aneurysm growth according to both the Society for Vascular
Surgery (SVS) as well as European Journal of Vascular and
Indeterminate: 5
detected by MRI

Endovascular Surgery (EJVES) guidelines.4,8


Type II: 21

Methodological quality assessment revealed several


Type II: 21
Type III: 3
Type II: 1

7.5 days (1e Total: 21

Max 1 week Total: 24


23 days (13e Total: 6

potentially relevant differences between included studies.


First, mean time interval between CTA and MRI exceeded 1
month in two studies5,11 and was unclear in two studies.10,12
Longer time interval between CTA and MRI may increase the
CTA (range)
Mean time

detection of additional endoleaks by MRI because during this


30 days).
between
MRI and

49 days)

time interval new endoleaks could have developed or


increased in volume or severity. We decided to include these
studies because of the limited available data on this topic.
contrast injection)

Second, in the majority of included studies (8/11; 73%), the


CTA (acquisition
time after start
Delayed phase

presence of endoleak was assessed on delayed-phase CTA.


Yes (120 s)

For the detection of type II endoleaks, delayed-phase imaging


Yes (90 s)

Yes (70 s)

is crucial and the absence of delayed-phase imaging could


have resulted in overestimation of the additional value of MRI
for the detection of endoleaks. Three other QUADAS items
CTA, MRI and

deserve to be mentioned (Appendix II). The rst item (item 12,


mModality

Consensus
reading of
Reference

Appendix II) concerns the availability of clinical data during


available

MRI assessment. This item was scored unclear in nine studies


DSA if
CTA

CTA

and no in two studies. However, for accurate MRI and CTA


assessment, the availability of clinical data is not a strict
necessity. The second item (reporting of uninterpretable and
(1.5 T)

(1.5 T)

(1.5 T)

CDUS
CEUS
MRI
MRI

No endoleaks MRI

MRi

CTA

intermediate test results; item 13, Appendix II) was scored


yes in three studies and no in eight studies. Appropriate
reporting of these results is relevant because in clinical
Unselected

Unselected
population

practice it is important to know if image quality is adequate to


on CTA

assess endoleak presence because it may guide treatment


Number of Study

decisions. The last item (explanation on withdrawals from the


study; item 14, Appendix II) was scored yes in three studies
(number of

and no in eight studies. Reporting of withdrawals is impor-


108 (108)
included

12 (11)

32 (32)
patients

scans)

tant because, for clinical implementation of MRI in EVAR


follow-up, it is important to know if patients tolerate the MR
examination and administration of MR contrast agents.
Endovasc. Surg., 201127
Interv. Radiol., 201017

Overall, MRI examinations demonstrated 126 additional


Cantisani, Eur. J. Vasc.
Wieners, Cardiovasc.

endoleaks compared to CTA. However, MRI missed two type


Cornelissen, Invest.

I endoleaks that were detected by CTA.10,12 One distal type I


Table 2-continued

Radiol., 201016
Author, journal,

endoleak (IB) was masked because of vessel-wall calcica-


tions and platinum markers of the distal limb stent graft. This
type I endoleak was detected with a triphasic CT protocol. On
year

the unenhanced scan, calcications were identied and


could be differentiated from the endoleak present on the
J. Habets et al. 345

Table 3. Study characteristics.


Author, journal, Mean max AAA Stentgraft Male/female Mean age in MRI contrast MRI T1-weighted
year diameter (range) type ratio years (range) agent type sequence type
Haulon, Eur. J. 49 mm 25 Vanguard; 30/1 64 (47e77) Gadolinium Spin echo
Vasc. Endovasc. 4 AneuRx; 2 based
Surg., 20015 Talent extracellular
Cejna, Eur. Not reported 3 Talent; 7 29/3 72 (58e84) Gadolinium Gradient echo
Radiol., 200213 Excluder; 30 based
Stentor and extracellular
Vanguard
Insko, Acad. Not reported 8 Medtronic Not reported Not reported Gadolinium Gradient echo
Radiol., 200312 nitinol; 1 based
elgiloy extracellular
Guidant
Ayuso, J. Magn. CTA: 56.7 mm 4 Talent; 20 Not reported Not reported Gadolinium Gradient echo
Reson. Imaging, (39e93) Excluder; 2 based
200426 MRA: 58.8 mm Vanguard; 2 extracellular
(37e96) AneuRx
Ersoy, Am. J. 50 mm (44e65) AneuRx; 6/1 62e83 Albumin- Not reported
Roentgenol l., Ancure binding
200411
Pitton, Am. J. Not reported Talent; 48/4 71.1 (55e82) Gadolinium Gradient echo
Roentgenol., Vanguard based
200410 extracellular
Van der Laan, Not reported 3 Excluder; 26/2 72.3 Gadolinium Spin echo
Eur. J. Vasc. 25 Ancure based
Endovasc. extracellular
Surg., 200614
Alerci, Eur. 58 mm (50e74) 13 Talent; 41/2 Not reported Albumin- Gradient echo
Radiol., 200815 30 Excluder binding
Cornelissen, 60 mm (41e87) 9 Talent; 1 10/2 76.6 (62e90) Albumin- Spin echo
Invest. Radiol., Excluder; 2 binding
201016 Guidant (1
AUI and 1
Ancure)
Wieners, CTA: 52.5 mm 25 Excluder; 4 Not reported 76 (64e86) Albumin- Gradient echo
Cardiovasc. (24e84) Talent; 3 binding
Interv. Radiol., MRI: 52.8 mm Anaconda
201017 (24e86)
Cantisani, 54 mm (39e87) 55 Talent; 50 92/31 63.0 Gadolinium Gradient echo
Eur. J. Vasc. Excluder; 12 based
Endovasc. Powerlink; extracellular
Surg., 201127 6 Jomed

CTA images. Alerci et al. reported on the second missed type nitinol stent grafts, longer overlap zones between the
I endoleak (only one of two observers mentioned this modular components and stronger polyester fabrics. MRI
endoleak).15 However, their consensus reading (MRI CTA) detected all type III endoleaks detected by CTA. However,
concluded that there was no type I endoleak on both CTA Pitton et al. detected 11 additional type III endoleaks with
and MRI. We chose to use the numbers of endoleaks of the MRI compared to CTA.10 Type III endoleaks are fast-ow
second observer because they were most close to the endoleaks that require appropriate treatment. In this study,
consensus reading. In clinical practice, it is crucial to detect only two patients who underwent re-intervention had
type I endoleaks because they often result in AAA growth a negative biphasic CTA examination and an additional
and may even lead to aneurysm rupture. Besides these two endoleak on MRI.10 These two patients had a type II endoleak
type I endoleaks, MRI and CTA detected both all type I that was embolised and a type III endoleak (dislodgement
endoleaks. Furthermore, we would like to emphasise that we due to kinking of the stent graft) that required late conver-
view MRI as a complementary technique to CTA in the case sion. Although 11 additional type III endoleaks were found by
of aneurysm growth. Therefore, the missed type I endoleaks MRI, treatment of a type III endoleak was only reported in
are less relevant because in our proposed diagnostic strategy one patient. This is in contrast to current guidelines that
CTA would probably have detected these endoleaks (Fig. 3). recommend treating all type III endoleaks.4,8 However, it is
Nowadays, type III endoleaks due to graft failure are unclear how many times this patient was imaged because
infrequently encountered because of the new-generation MRI was a part of the standard follow-up protocol.
Table 4. Endoleaks detected by different studies, specied by type (unselected patients).

346
Author Year Patients (N) Scans (n) MRI: total MRI: endoleaks by type Reference: total Reference: endoleaks by type
endoleaks I II III IV V Indeter- endoleaks I II III IV V Indeter-
minate minate
Haulon et al.5 2001 31 31 18 1 17 0 0 0 10c 1 9 0 0 0 0 0
13 b
Cejna et al. 2002 32 18 9 1 6 1 0 0 8b 1 5 1 1 0 0 1
Insko et al.12 2003 9 9 6 2 4 0 0 0 4 2 2 0 0 0 0 0
Ayuso et al.26 2004 17 17 10 0 6 1 0 0 5 0 3 3 1 0 0 1
Ersoy et al.11 2004 6 6 6 NR NR NR NR NR 2 NR NR NR NR NR NR NR
Pitton et al.10 2005 52 252 131 7 93 21 0 0 62c 8 42 10 10 0 0 2
14
Van der Laan et al. 2006 28 35 23 2 6 1 0 0 11 2 3 14 1 0 0 5
Alerci et al.15,a 2009 43 43 24 0 13 0 0 0 12c 1 7 11 0 0 0 4
Wieners et al.17 2010 32 32 21 0 21 0 0 0 12 0 12 0 0 0 0 0
Cantisani et al.27 2011 108 108 24 0 21 3 0 0 20c 0 18 0 2 0 0 0
Total 358 551 272 13 187 27 0 0 146 15 101 39 15 0 0 13
NR: Not reported.

European Journal of Vascular and Endovascular Surgery


a
Only results of observer 2.
b
Endoleaks detected on biphasic CTAs and compared to MRI. Endoleaks detected on uniphasic CTAs are not shown in this table.
c
Number of endoleaks detected on CTA (Reference standard in this studies was dened as consensus reading between MRI and/or CTA and/or DSA).
patients with aneurysm growth.
Figure 3. Proposed diagnostic algorithm for post-EVAR imaging in

review demonstrates that MRI has a higher sensitivity


of endoleak during post-EVAR follow-up. This systematic
commonly used imaging technique to evaluate the presence

* studies with albumin-binding MRI contrast agents.


Figure 2. Proportion (%) of additional endoleaks detected by MRI.
We compared MRI with CTA because CTA is the most

Volume 45 Issue 4 April/2013


J. Habets et al. 347

compared to CTA for the detection of endoleaks, especially determine the exact value of albumin-binding contrast
type II endoleaks. The main reason for this nding is prob- agents and T1-weighted spin-echo sequences.
ably the superior MRI soft-tissue contrast and, subsequently, Besides CTA, contrast-enhanced ultrasound is used to detect
the improved contrast sensitivity for small and slow-ow endoleaks in patients after EVAR. A meta-analysis by Mirza
endoleaks. Furthermore, in four studies (4/11; 36%), et al. reported a good pooled sensitivity (98%) and specicity
albumin-binding contrast agents were administered, which (88%) of contrast-enhanced ultrasound with CTA used as
are characterised by a higher relaxivity (2e5 times higher) a reference standard.21 This meta-analysis shows that contrast-
compared to conventional extracellular agents.11,15e17 enhanced ultrasound is a clinically interesting alternative to
These contrast agents have a prolonged intravascular CTA. However, for the evaluation of stent-graft position and
retention in the circulation that allows a longer time interval fractures, contrast-enhanced ultrasound is inferior to CTA.22
between contrast administration and post-contrast Time-resolved MR angiography (MRA) sequences can also
imaging.18,19 Both higher relaxivity and prolonged intravas- be used to detect endoleaks. The advantage of this type of
cular retention could have improved the sensitivity of MRI. sequence is the superior temporal resolution, which enables
The bulk of additional endoleaks detected with MRI con- better assessment of contrast dynamics over time. The disad-
cerned type II endoleaks. Unfortunately, individual data on vantage of this sequence is the generally inferior spatial reso-
aneurysm growth was lacking, which is crucial for treatment lution compared to conventional post-contrast T1-weighted
decisions because type II endoleaks which cause AAA diameter imaging, which can potentially result in missing small endo-
growth require treatment according to current guidelines.4,8 leaks. Furthermore, time-resolved acquisitions are based on
Although Wieners et al. reported that six of nine (67%) addi- gradient echo sequences, which are more sensitive to
tional endoleaks on MRI occurred in patients with AAA growth, susceptibility artefacts that can degrade image quality.
further prospective studies are required to determine the exact However, time-resolved MRA may have an additional diag-
value of MRI in patients with AAA growth.17 Furthermore, nostic value to T1-weighted post-contrast imaging in the clas-
Cornelissen et al. detected two additional type II endoleaks in sication of endoleaks and can be combined with conventional
patients with AAA growth with MRI among 11 patients with T1-weighted imaging without signicant time penalty.23e25
non-shrinking AAA after EVAR and no endoleak at CTA.16 For MRI imaging of endoleaks with blood pool agents, no
standard MRA sequences are reported in the literature. For
comparability of studies and to reduce heterogeneity, it is
Limitations important that in prospective studies MRA sequences are
Meta-analysis was not meaningful because of the large standardised to extrapolate results to clinical practice.
heterogeneity in the included studies. Besides the previously In this review, studies were included that compared CTA to
mentioned AAA growth, several other interesting covariates MRI T1-weighted post-contrast imaging. Verication with an
(stent-graft type, the use of albumin-binding contrast agents independent reference standard (e.g., digital subtraction
and the use of T1 spin-echo sequences) could not be analysed angiography, DSA) was not systematically performed in the
because of the large heterogeneity and the lack of individual included studies. However, DSA may also miss endoleaks
data in the study reports. Most studies concerned patients especially when non-selective DSA is performed. Prospective
with nitinol stent grafts that generally did not hamper studies are required to compare CTA and MRI to selective DSA.
assessment (Table 3). It is well known that other stent-graft Finally, it is important to mention that metal-induced
types (Elgiloy and stainless steel) can hamper diagnostic MR susceptibility artefacts due to surgical clips and stainless-steel
assessment because of metal-induced susceptibility artefacts, coils can also hamper MRI assessment of post-EVAR patients.
even when T1 spin-echo sequences are used. These stent- MR-compatible clips and coil material (i.e., platinum) are
graft types are not good candidates for MR evaluation. Prior in advisable if MRI follow-up is considered. It is also important to
vitro work demonstrated that Zenith (Stainless Steel; Cook, mention that not all patients are good candidates for MRI due
Bloomington, IN, USA) and Lifepath (Elgiloy; Baxter, Morton to contraindications such as claustrophobia, certain other
Grove, IL, USA) stent grafts are not assessable by MRI.20 For types of metal implants and the presence of implanted
these stent-graft types, CTA and contrast-enhanced ultra- pacemakers or internal cardioverter/debrillators.
sound remain the preferred imaging modalities.
The use of albumin-binding high-relaxivity contrast agents CONCLUSION
as well as T1-weighted spin-echo post-contrast MR imaging
MRI is more sensitive than CTA for the detection of post-
seem to increase sensitivity for the detection of endoleak.15e
17 EVAR endoleaks, especially for the detection of type II
Albumin-binding contrast agents could be promising for
endoleaks which has treatment consequences in patients
the detection of slow-ow endoleaks in patients with aneu-
with AAA growth. MRI is therefore an interesting comple-
rysm growth and no endoleaks on CTA because of the pro-
mentary imaging modality to CTA that must be considered,
longed intravascular retention as well as the higher relaxivity.
especially in patients with post-EVAR AAA growth of
In the included studies, mainly nitinol stent grafts were
unknown origin.
imaged and especially for other stent-graft types (e.g., Elgiloy
and stainless steel) T1-weighted spin-echo sequences may be
preferable because images are less affected by susceptibility CONFLICT OF INTEREST/FUNDING
artefacts.20 Nevertheless, prospective studies are required to None.
348
APPENDIX I.
Exact search terms used in literature search.
Pubmed: 121 articles
((MRA[Title/Abstract] OR MRI[Title/Abstract] OR Magnetic Resonance Imaging[Title/Abstract] OR Magnetic Resonance Angiography[Title/Abstract] OR Magnetic Resonance
Angiographies[Title/Abstract] OR Magnetic Resonance Imaging[Mesh] OR Magnetic Resonance Angiography[Mesh])
AND
(endoleak[Title/Abstract] OR endoleaks[Title/Abstract] OR Perigraft Leak[Title/Abstract] OR perigraft leaks[Title/Abstract] OR endotension[Title/Abstract] OR endoleak[Mesh]))
AND
((EVAR[Title/Abstract] OR endovascular[Title/Abstract] OR aneurysm repair[Title/Abstract] OR aneurysm surgery[Title/Abstract]
OR aortic stent[Title/Abstract]) OR aortic stent graft[Title/Abstract] OR AAA[Title/Abstract] OR aortic aneurysm[Title/Abstract]
OR aortic aneurysms[Title/Abstract] OR aorta aneurysm[Title/Abstract] OR aorta aneurysms[Title/Abstract] OR Aortic Aneurysm, Abdominal[Mesh] OR Aortic Aneurysm[Mesh])
Embase: 178 articles
(nuclear magnetic resonance imaging/exp OR magnetic resonance angiography/exp OR mra:ab,ti OR mri:ab,ti OR (magnetic AND resonance AND imaging:ab,ti) OR (magnetic AND
resonance AND angiography; ab,ti) OR (magnetic AND resonance AND angiographies; ab,ti))
AND
(endoleak; ab,ti OR endoleaks:ab,ti OR (perigraft AND leak:ab,ti) OR (perigraft AND leaks:ab,ti) OR endotension:ab,ti OR endoleak/exp)

European Journal of Vascular and Endovascular Surgery


AND
(abdominal aorta aneurysm/exp OR abdominal aorta aneurysm OR endovascular surgery/exp OR endovascular surgery OR aorta aneurysm/exp OR aorta aneurysm OR evar:ab,ti
OR endovascular:ab,ti OR (aneurysm/exp OR aneurysm AND repair:ab,ti) OR (aneurysm/exp OR aneurysm AND surgery:ab,ti) OR (aortic AND stent:ab,ti) OR (aortic AND (stent/exp OR
stent) AND graft:ab,ti) OR aaa:ab,ti OR (aortic AND aneurysm:ab,ti) OR (aortic AND aneurysms:ab,ti) OR (aorta/exp OR aorta AND aneurysm:ab,ti) OR (aorta/exp OR aorta AND
aneurysms:ab,ti))

APPENDIX II.
Quality of the studies based on the criteria as proposed by the QUADAS checklists.
Author, journal, year Item 1 Item 2 Item 3 Item 4 Item 5 Item 6 Item 7 Item 8 Item 9 Item 10 Item 11 Item 12 Item 13 Item 14
Haulon, Eur. J. Vasc. Endovasc. Surg., 2001 Yes Yes Yes (DSA) No No Yes Yes Yes Yes Yes Yes Unclear No No
Cejna, Eur. Radiol., 2002 Yes Unclear Yes (CTA) Yes Unclear Yes Yes Yes Yes Yes Yes Unclear No Yes
Insko, Acad. Radiol., 2003 Yes No Yes (CTA/DSA) Yes Yes No Yes Yes Yes Unclear Unclear Unclear No No
Ayuso, J. Magn. Reson. Imaging, 2004 Yes/No Yes Yes (CTA) Yes Yes Yes Yes Yes Yes Yes Yes Unclear No No
Ersoy, Eur. J. Radiol., 2004 Yes Yes Yes (CTA) No Yes Yes Yes Yes No Unclear Unclear Unclear No Yes

Volume 45 Issue 4 April/2013


Pitton, Am. J. Roentgenol., 2004 Yes Yes Yes (CTA) Unclear Yes Yes No Yes Yes Yes No Unclear Yes No
Vd Laan, Eur. J. Vasc. Endovasc. Surg., 2006 Yes Yes Yes (CTA) Yes Yes Yes Yes Yes Yes Yes Yes Unclear No No
Alerci, Eur. Radiol., 2008 Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes No Yes No
Cornelissen, Invest. Radiol., 2010 No Yes Yes (CTA) Yes No Yes Yes Yes Yes Yes Yes No Yes Yes
Wieners, Cardiovasc. Interv. Radiol., 2010 Yes No Yes (CTA) Yes Yes Yes Yes Unclear Unclear Yes Yes Unclear No No
Cantisani, Eur. J. Vasc. Endovasc. Surg., 2011 Yes Yes Unclear Yes Unclear Unclear Yes Yes Yes Yes Yes Unclear No No
J. Habets et al. 349

Questions according to the different items: 7 Koole D, Moll FL, Buth J, Hobo R, Zandvoort HJ, Bots ML, et al.
Annual rupture risk of abdominal aortic aneurysm enlargement
1. Was the spectrum of patients representative of the without detectable endoleak after endovascular abdominal
patients who will receive the test in practice? aortic repair. J Vasc Surg 2011;54:1614e22.
2. Were selection criteria clearly described? 8 Chaikof EL, Brewster DC, Dalman RL, Makaroun MS, Illig KA,
3. Is the reference standard likely to correctly classify the Sicard GA, et al. The care of patients with an abdominal aortic
aneurysm: the Society for Vascular Surgery practice guidelines.
target condition?
J Vasc Surg 2009;50:S2e49.
4. Is the time period between reference standard and 9 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The
index test short enough to be reasonably sure that development of QUADAS: a tool for the quality assessment of
the target condition did not change between the two studies of diagnostic accuracy included in systematic reviews.
tests? BMC Med Res Methodol 2003;3:25.
5. Did the whole sample or a random selection of the 10 Pitton MB, Schweitzer H, Herber S, Schmiedt W, Neufang A,
sample, receive verication using a reference Kalden P, et al. MRI versus helical CT for endoleak detection
standard of diagnosis? after endovascular aneurysm repair. Am J Roentgenol
6. Did patients receive the same reference standard 2005;185:1275e81.
regardless of the index test result? 11 Ersoy H, Jacobs P, Kent CK, Prince MR. Blood pool MR angi-
7. Was the reference standard independent of the index ography of aortic stent-graft endoleak. Am J Roentgenol
2004;182:1181e6.
test (i.e., the index test did not form part of the
12 Insko EK, Kulzer LM, Fairman RM, Carpenter JP,
reference standard)? Stavropoulos SW. MR imaging for the detection of endoleaks in
8. Was the execution of the index test described in recipients of abdominal aortic stent-grafts with low magnetic
sufcient detail to permit replication of the test? susceptibility. Acad Radiol 2003;10:509e13.
9. Was the execution of the reference standard described 13 Cejna M, Loewe C, Schoder M, Dirisamer A, Holzenbein T,
in sufcient detail to permit its replication? Kretschmer G, et al. MR angiography vs CT angiography in the
10. Were the index test results interpreted without follow-up of nitinol stent grafts in endoluminally treated aortic
knowledge of the results of the reference standard? aneurysms. Eur Radiol 2002;120:2443e50.
11. Were the reference standard results interpreted 14 van der Laan MJ, Bartels LW, Viergever MA, Blankensteijn JD.
without knowledge of the results of the index test? Computed tomography versus magnetic resonance imaging of
12. Were the same clinical data available when test results endoleaks after EVAR. Eur J Vasc Endovasc Surg 2006;32:361e5.
15 Alerci M, Oberson M, Fogliata A, Gallino A, Vock P,
were interpreted as would be available when the test
Wyttenbach R. Prospective, intraindividual comparison of MRI
is used in practice? versus MDCT for endoleak detection after endovascular repair
13. Were uninterpretable/intermediate test results of abdominal aortic aneurysms. Eur Radiol 2009;19:1223e31.
reported? 16 Cornelissen SA, Prokop M, Verhagen HJ, Adriaensen ME,
14. Were withdrawals from the study explained? Moll FL, Bartels LW. Detection of occult endoleaks after
endovascular treatment of abdominal aortic aneurysm using
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