statistically significant differences between CTA, CEUS, Purpose: The aim of the study was to assess the and SMI concerning endoleak identification ability. The effectiveness of Superb Micro-vascular Imaging (SMI) weakest method in endoleak identification was CDUS. as an alternative to Contrast-Enhanced Ultrasound Conclusions: The analysis showed that SMI is effective, (CEUS) and Computed Tomography Angiography repeatable, and comparable with the CEUS modality in (CTA) for endoleak detection and classification in identification endoleaks after EVAR; it may be consid- patients followed up after endovascular abdominal aortic ered as a potential tool to monitor patients after EVAR aneurysm repair (EVAR). implantation, especially those with renal insufficiency or Materials and methods: From May 2015 to January 2017, with an allergy to any contrast media. 30 patients underwent post-EVAR follow-up with Color Doppler Ultrasound (CDUS), CEUS, SMI, and CTA Key words: Abdominal aortic aneurysm—Endovascular examinations. Aneurysmal sac diameter and graft abdominal aortic aneurysm repair—Endoleak— patency were evaluated; endoleaks were identified and Ultrasound—Superb Micro-vascular Imaging classified. Sensitivity, specificity, and accuracy values were calculated for each of the four diagnostic methods of endoleak detection. A percentage of agreement and Patients after Endovascular Aneurysm Repair (EVAR) Cohen’s Kappa coefficient were calculated for compar- require regular and strict follow-up to enable early ison of methods in terms of endoleak identification. detection of endoleaks and their treatment. The use of Results: CTA revealed fifteen endoleaks (50%): three Computed Tomography Angiography (CTA), which is type Ia, nine type II, and three type III. The sensitivity of currently recommended for the follow-up of patients CDUS, CEUS, and SMI relative to CTA was 27%, undergoing EVAR, puts the patients at risk of receiving 100%, and 100%, respectively. Specificity was 93%,93%, high doses of ionizing radiation and exposes them to the and 93%, respectively. Accuracy was 60%,97%, and repetitive impact of nephrotoxic X-ray contrast [1, 2]. 97%, respectively. There were no differences between Another method used for EVAR follow-up is ultra- SMI and CEUS in terms of sensitivity, specificity, or sound, which is a well-established and non-invasive diagnostic tool with real-time tissue harmonic imaging Correspondence to: Jolanta Tomczak; email: jolantatomczak.pte@ enabling diagnosis and prompt implementation of a gmail.com 3480 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique treatment plan; it is particularly useful in vascular CDUS, CEUS, SMI, and CTA examinations were per- imaging where precise hemodynamic data are decisive formed between May 2015 and January 2017. Our [3–5]. Endoleaks in Color Doppler Ultrasound (CDUS) institutional post-EVAR protocol consisted of CTA one appear as pulsatile color flow within or adjacent to the month after repair, followed by CDUS after 6 months, aneurysm sac . Some researchers suggest that CDUS and then CDUS once a year. The study was carried out can be used for the follow-up of patients after EVAR [6– in accordance to the Declaration of Helsinki, and its 8]. In turn, other authors state that CDUS alone is protocol was approved by the Bioethical Committee of insufficient for endoleak identification in routine clinical the Poznan University of Medical Sciences (decision no. practice [9–11]. 963/12). High-resolution contrast-enhanced ultrasound The indications to use CEUS and SMI were as fol- (CEUS) is one of the alternative methods used to detect lows: and characterize endoleaks [1, 2]. The advent of CEUS imaging utilizing sulfur hexafluoride microbubbles as a (1) Unclear CDUS results during routine follow-up; contrast agent improved the resolution and sensitivity of CEUS and SMI were used in order to verify the microvessel visualization. Moreover, the rate of adverse results and characterize the endoleak type. reactions reported for microbubbles is low, and no con- (2) Possible endoleak existence suspected intraopera- trast-induced effects on renal function have been ob- tively during the EVAR implantation. served ; notwithstanding, the method’s requirement of (3) Assessing the outcome of the secondary interven- intravenous contrast agents remains a disadvantage. tion after endoleak diagnosis. Recently, Toshiba has developed an innovative (4) Aneurysm expansion without an identifiable en- Doppler ultrasound technology called Superb Micro- doleak on CDUS. TM vascular Imaging (SMI) using the Aplio 500 ultra- Patients with inability to keep still were excluded sound system (Toshiba Medical Systems Corporation, from the study. Tochigi, Japan), which enables the visualization of slow- The CDUS, SMI, and CEUS examinations were ﬂow vessels without the need to use a contrast medium; it performed (in this order) by an experienced vascular appears to be a new promising tool for the detection of surgeon blinded to the results of CTA, using Toshiba’s endoleaks [3–5]. This advanced method offers unique TM Aplio 500 device equipped with a 4–6-MHz curved advantages, including low-velocity flow visualization, array transducer. Moreover, two additional examiners (a high-resolution imaging, minimal motion artifacts, and vascular surgeon and a radiologist) independently as- high frame rates. The technique employs a proprietary sessed the video and images. The initial examination was adaptive algorithm to remove clutter artifacts while a standard morphological investigation in 2D presenta- maintaining sensitivity to low blood flow velocities [3, tion (B-mode) followed by blood ﬂow analysis using 13]. SMI is able to visualize lower-velocity blood flows CDUS. Subsequently, cSMI and mSMI examinations without the negative influence of motion artifacts arising were conducted. Finally, CEUS was performed after the from nearby structures, which is impossible to achieve administration of an intravenous 2.5-milliliter bolus of with conventional Doppler techniques . SMI can ra- ultrasound contrast—SonoVue (Bracco, Milan, Italy); pidly confirm blood flow or detect the absence of flow in the duration of the CEUS examination is 2–3 min. CTA cases of torsion and ischemia [3, 12]. SMI works in two was performed using a GE 64 VCT Lightspeed multislice modes: the monochrome (grayscale) mode (mSMI), angiography scanner (acquisition 64 9 0.625 mm, helical which improves sensitivity by subtracting the back- mode, tube voltage 80e140 kV, tube current 300 mAs, ground information and focusing only on the vascula- CTDI Vol 14 mGy, rotation time 0.32, pitch 0.7, slice ture, and the color mode (cSMI), which demonstrates collimation 0.6, slice width 1.5 mm in retro-reconstruc- B-mode and color information simultaneously [3, 4, 13]. tion) . CTA was performed no later than 2–3 weeks The aim of the present study was to evaluate the after the CDUS, CEUS, and SMI examinations and was effectiveness of SMI as an alternative to CDUS, CEUS, used as the reference method. and CTA in the identiﬁcation and classiﬁcation of en- The ﬁndings of all four imaging modalities were re- doleaks in patients undergoing post-EVAR follow-up, corded, including the presence of endoleaks and their using CTA as the reference method. types, the types of the endoleaks’ inﬂow vessels, and the patency of the stent-graft segments. Materials and methods The maximal aneurysm sac diameter was measured The study prospectively analyzed 30 patients after from the leading edge of the anterior wall to the leading EVAR for abdominal aortic aneurysm or iliac aneur- edge of the posterior wall on the transverse plane. Con- ysms. All procedures were performed at the Department tinuous data are presented as the mean ± standard of General and Vascular Surgery of the Poznan deviation (SD) or median [interquartile range (IQR)] as University of Medical Sciences in the years 2011-2016. appropriate; qualitative parameters were expressed as 3481 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique percentages. Sensitivity, speciﬁcity, and accuracy values Endoleak identiﬁcation were estimated for all imaging modalities. To compare During the B-mode examination, the correct location of the methods in terms of endoleak identiﬁcation, the the stent graft and preserved continuity of its walls were percentage of agreement and Cohen’s Kappa coefﬁcient clearly visible in all studied patients. No stent-graft were calculated. The differences in endoleak identiﬁca- deformation was observed. In all cases, CDUS, SMI, and tion between the studied methods were considered sta- CEUS revealed the presence of blood ﬂow in the stent- tistically signiﬁcant when the observed P value for graft lumen. We did not observe any adverse reactions or proportionate agreement was < 0.05. The level of sta- complications during the use of either CTA or the tistical significance has been determined using the v test microbubble contrast agent. or Fisher’s exact test and GraphPad Prism software CDUS identiﬁed endoleaks in 17% of the enrolled (version 6.04). patients (5/30 cases), CEUS and SMI in 53% of patients (16/30 cases), and CTA (the gold standard) identiﬁed Results endoleaks in 50% of patients (15/30 cases). The majority Patient characteristics of the identiﬁed endoleaks were type II (Fig. 1), then three type Ia (Fig. 2), and three type III. No type IV or This prospective study included 30 patients (27 males and type V (endotension) endoleaks were diagnosed in the 3 females) at the mean age of 70.1 years (SD ± 10.3) who study group. had undergone EVAR procedures; the mean aneurysm The detailed ﬁndings were as follows. Fifteen en- diameter was 6.41 cm (SD ± 1.9, range 3.8 –10.5 cm). doleaks were correctly detected by CEUS and SMI as Patient characteristics are presented in Table 1. well as CTA. One additional endoleak was detected by The median period of time between the procedure and both CEUS and SMI; however, it was not conﬁrmed by the imaging studies was 165 days (IQR 52, 839). The CTA (the gold standard). This means that CEUS and analyzed patients underwent different EVAR proce- SMI yielded only one false-positive result each. All en- dures. In 24 patients, EVAR implantation was per- doleaks identiﬁed by SMI were conﬁrmed by both cSMI formed to treat infrarenal abdominal aortic aneurysms and mSMI. CDUS revealed only ﬁve endoleaks, and one (23 bifurcated stent grafts and one Nellix device were of these results was a false positive; the method failed to implanted). Another three patients had isolated common detect endoleaks in as many as 11 patients. The number iliac artery aneurysms and were implanted with uni-iliac and types of the endoleaks are presented in Table 2. devices. Finally, three patients were treated with fenes- The sensitivity, speciﬁcity, and accuracy of SMI and trated endografts (using from 1 up to 4 branches). The CEUS were the same (100%,93%, and 97%, respec- procedures were performed with the following devices: tively). The sensitivity, speciﬁcity, and accuracy of Zenith (Cook Medical, Bloomington, IN, USA): n = 21; CDUS, CEUS, and SMI in identifying endoleaks are Excluder (W.L. Gore and Associates, Flagstaff, AZ, summarized in Table 3. It is worth noting that CEUS USA): n = 6; E-vita (JOTEC, Hechingen, Germany): and SMI were distinctly more accurate than CDUS in n = 2, and Nellix (Endologix, Irvine, CA, USA): n =1. the identification of endoleaks, and their accuracy was The choice of the specific stent graft depended on the similar to CTA. morphology of the abdominal aortic aneurysm and was There were no statistically signiﬁcant differences be- made in accordance with the manufacturer’s guidelines tween CTA, CEUS, and SMI concerning their ability to in all cases. identify endoleaks (Table 4). However, the results indi- cate that CDUS is the least reliable method in endoleak identification. We observed that the percentage of agreement between CDUS and CTA was only 66.7% (P = 0.006, Cohen’s Kappa coefficient was 0.333), and this proportion was similar when CDUS was compared Table 1. Patient characteristics to SMI/CEUS (63.3% at P = 0.003 and 0.477, respec- tively). Patient characteristics n = 30 Percentage Smoking (present) 36.7 Discussion Obesity BMI > 30 [(kg/m ) 40.0 Diabetes 36.7 EVAR procedures require close lifelong imaging Hypertension 83.3 surveillance to quickly detect any possible complications Hyperlipidemia 30.0 Coronary artery disease 63.3 such as endoleaks, fractures, graft migration, kinking, or Renal insufficiency 23.3 enlargement of the aneurysm sac with probable aneur- ysm rupture [2, 10]. Variables expressed as % 3482 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique Fig. 1. Cross section through an abdominal aortic aneurysm C color Superb Micro-vascular Imaging; D monochrome showing a type IIb endoleak (green arrow). A Computed Superb Micro-vascular Imaging. Tomography Angiography, B Contrast-Enhanced Ultrasound, CTA is currently considered to be the gold standard CDUS is an inexpensive and non-invasive imaging for monitoring during post-EVAR follow-up. CTA modality with no risk of radiation exposure or contrast- imaging is widespread and provides precise aneurysm sac induced renal insufﬁciency, and it has been, therefore, measurements. Moreover, it enables rapid and repro- investigated as an alternative to CTA for post-EVAR ducible acquisition of data (ensuring homogeneous re- monitoring . On the other hand, CDUS has major sults among institutions) with high diagnostic value. limitations, including the notable rates of false-positive CTA also provides superior information related to the and false-negative results as well as significant operator stent graft, such as patency, the presence of endoleaks dependency . Additionally, CDUS imaging seems to and their type, anchoring, or kinking [10, 11]. be impeded by unfavorable body habitus (e.g., obesity), Furthermore, a systematic review by Karthike- ascites, or excessive intervening bowel gas, as well as salingam et al. pointed out that the mean sensitivity and graft factors such as echo reflection from the stent graft, speciﬁcity of CTA in endoleak detection is 70% and 98%, stent-graft failure, kinking of the limbs, or slow endoleak respectively . However, the method has a number of flow [9, 19]. significant disadvantages. One example is the high and In recent years, numerous studies and a meta-analysis cumulative dose of ionizing radiation (more than have shown the increasing role of CEUS in post-EVAR 20 mGy per one thoraco-abdominal CT scan), which surveillance. The results demonstrated that CEUS is significantly increases the risk of cancer. Moreover, the highly diagnostic and comparable to CTA with regard to nephrotoxic contrast agent load causes a significant de- detecting and characterizing endoleaks; moreover, it is cline in renal function during long-term EVAR moni- not associated with renal impairment or ionizing radia- toring. Finally, the method is associated with high costs. tion. Additionally, CEUS is more cost-effective than These drawbacks prompted the search for a diagnostic CTA . A systematic review by Karthikesalingam et al. technique that would be better suited for long-term emphasized that CEUS, with its specificity of 90%–97% surveillance [10, 15–17]. Because of these factors, a safer and sensitivity of 62%–83%, is useful in endoleak detec- and more cost-effective alternative to CTA is required [2, tion . In the present study, the specificity of CEUS in 14, 16]. endoleak detection was 93%, while its sensitivity was 3483 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique Fig. 2. A type I endoleak (yellow arrow) according to four Ultrasound, C monochrome Superb Micro-vascular Imaging, different imaging methods of an abdominal aortic aneurysm: D Contrast-Enhanced Ultrasound. A Computed Tomography Angiography, B Color Doppler Table 2. The number of endoleaks detected by each imaging modality Accordingly, several authors considered CEUS as the ﬁrst imaging tool for post-EVAR surveillance as it ap- Variable Imaging modality pears to be more speciﬁc than CTA for low-ﬂow en- CDUS CEUS SMI CTA doleaks [10, 23]. Their results also indicate that CEUS enables better classification of endoleaks because of its No endoleak detected: 25 14 14 15 Endoleak detected: 5 16 16 15 ability to obtain real-time hemodynamic information I0 3 3 3 about the direction of blood flow [10, 23], which is par- Ia 0 3 3 3 ticularly helpful in planning redo procedures, especially Ib 0 0 0 0 II 5 10 10 9 in patients with, type II endoleaks . IIa (IMA) 1 2 2 2 The EFSUMB guidelines of 2011 recommend the use IIb (LA) 3 7 7 5 of CEUS in post-EVAR follow-up (level of evidence: 1a). IIa + IIb 1 1 1 2 III 0 3 3 3 The main obstacle for the widespread use of CEUS is that equipment for contrast imaging is not available in all CDUS Color Doppler ultrasound, CEUS Contrast-Enhanced Ultra- centers . Moreover, the time of examination is limited sound, SMI Superb Micro-vascular Imaging (cSMI & mSMI), CTA Computed Tomography Angiography, IMA Inferior Mesenteric Ar- to only a few minutes, and extensive operator experience tery, LA Lumbar Arteries is required. Both CEUS and SMI are vascular imaging methods that provide outstanding detectability and classiﬁcation 100%. Furthermore, in a meta-analysis published by of endoleaks, visualizing them in real time. However, Mirza et al., the authors confirmed that CDUS had SMI provides continuous, real-time scanning without insufficient sensitivity for endoleak detection and praised any time constraints. No intravenous contrast agent is CEUS as a highly sensitive diagnostic tool . On the needed with SMI, which is one reason why it is better other hand, CTA is unsuitable for detecting some types suited for detecting or monitoring endoleaks in patients of slow endoleaks which can be visualized with CEUS, with renal failure. In particular, the fact that SMI can be MRA [20–22], or, as we have shown in the present study, used separately or in combination with contrast agents SMI. makes it a novel and promising tool for visualizing en- 3484 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique Table 3. Sensitivity, specificity, and accuracy of the analyzed imaging modalities in detecting post-EVAR endoleaks Imaging modality True positives False positives False negatives True negatives Sensitivity (%) Specificity (%) Accuracy (%) CDUS 4 1 11 14 27 93 60 CEUS 15 1 0 14 100 93 97 SMI 15 1 0 14 100 93 97 CDUS Color Doppler Ultrasound, CEUS Contrast-Enhanced Ultrasound, SMI Superb Micro-vascular Imaging (cSMI & mSMI) Table 4. Comparison of methods in terms of endoleak identification Endoleak identification SMI vs. CTA CEUS vs. CTA SMI vs. CEUS CDUS vs. CTA CDUS vs. SMI/CEUS Agreement [%], P value 96.7, 0.796 96.7, 0.796 100.0, 1.000 66.7, 0.006 63.3, 0.003 Cohen’s Kappa coefficient 0.935 0.935 1.000 0.333 0.477 CDUS Color Doppler Ultrasound, CEUS Contrast-Enhanced Ultrasound, SMI Superb Micro-vascular Imaging (cSMI & mSMI), CTA Computed Tomography Angiography doleaks [12, 13, 25]. SMI can also save time, increase According to the results, SMI was more accurate than sensitivity, and improve diagnostic accuracy as well as CDUS, but less accurate than CEUS and CTA in iden- treatment planning. Compared with conventional Dop- tifying endoleaks. This led the authors to recommend pler techniques, SMI offers better detail resolution, faster SMI for post-EVAR follow-up, especially in cases when frame rates, less clutter, and fewer flash artifacts [3, 12]. CEUS or CTA cannot be used . The difference in the The existing Doppler modes are unable to distinguish number of endoleaks reported by Cantisani et al. and our motion artifacts from actual blood flow. With SMI, it is study may influence the difference in sensitivity in both possible to analyze the characteristics of such motion studies (75% vs. 100%, respectively). Despite the large artifacts and extract only the clinically relevant infor- number of patients participating in the Cantisani et al. mation . investigation, the authors have observed a small number In addition, the proper performance of an SMI of endoleaks. Moreover, they encountered only type II examination requires several conditions to be met. Dur- endoleak, which is the most frequent type of endoleak. ing the scanning of individual vascular sections, the Accordingly, not all types of endoleaks were represented probe must be maintained in a stable position, without in mentioned study. Contrary to the findings showed by shifting or vibrating. When small endoleaks are exam- Cantisani et al., in our study we observed type Ia, II, and ined, it may be helpful to ask the patient to temporarily III endoleaks. refrain from breathing. It should be taken into account The recent study presents the currently largest case that, at least in some cases, the test is time-consuming. series of endoleaks examined with CTA, SMI, and CEUS The presence of intestinal gases or increased peristaltic (n = 15), showing that the three modalities have nearly movements may result in the occurrence of artifacts that the same sensitivity, specificity, and accuracy in endoleak impede vascular assessment. The amount of gases in the detection. In the present study, CEUS and SMI detected examined area can be reduced by massaging the area a higher number of endoleaks compared to CTA, yield- with the probe to displace the gas to other abdominal ing only one false-positive result each. As a reference regions. In the case of increased peristalsis, it may be method, CTA still allows for better classification of en- helpful to change the position of the body or to take a doleaks compared to CEUS and SMI. However, the high few-minute break. sensitivity and specificity found in this study lead to the The ﬁrst case report about the use of SMI for EVAR conclusion that CEUS and SMI may be equivalent to surveillance comes from our research team; we demon- CTA, especially in long-term EVAR follow-up. strated promising results of using SMI for endoleak According to the still scant literature about the detection, comparing the method with CDUS, CEUS, application of SMI, the method appears to have signiﬁ- and CTA . Cantisani et al. compared SMI with cant clinical value in terms of early diagnosis and treat- CDUS, CEUS, and CTA. The authors examined 57 ment planning in patients with cancer and tumors, patients after EVAR procedures and confirmed the facilitating the evaluation of the shape and density of the presence of 8 endoleaks (all type II). The study demon- tumor vessels. Other potential clinical applications of SMI include gynecological and obstetric imaging, eval- strated that the sensitivity of CTA, CEUS, CDUS, and SMI was 88%, 100%,63%, and 75%, respectively. uation of lymph nodes and abdominal areas, as well as 3485 M. Gabriel et al.: Superb Micro-vascular Imaging (SMI): a Doppler ultrasound technique Development (Grant Number INNOMED/I/17/NCBR/2014) from the diagnosis of skin lesions, rheumatoid arthritis, and many Innovative Economy Operational Programme founds, in the frame- other medical conditions [4, 5, 13, 27, 28]. work of the European Regional Development Fund. As is the case with CDUS, CEUS, and CTA, SMI has some disadvantages. The SMI technology available only Conflict of interest The authors declare that they have no conflict of interest. uses the Toshiba ultrasound system. Besides the draw- backs mentioned in the earlier discussion of CDUS, a Ethical Approval This article does not contain any studies with ani- crucial issue related to SMI is that it requires substantial mals performed by any of the authors. All procedures performed in studies involving human participants were in accordance with the eth- experience from the operator performing the examina- ical standards of the institutional and/or national research committee tion. Like CEUS, SMI is an examination with high and with the 1964 Helsinki declaration and its later amendments or operator dependency and requires a learning curve. comparable ethical standards. Additionally, interpreting SMI results is particularly Informed consent Informed consent was obtained from all individual difﬁcult for inexperienced operators. Neither CEUS  participants included in the study. nor SMI should be used as the only imaging technique for EVAR surveillance, particularly when reintervention is required. Nevertheless, these methods can certainly Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecom replace most CTA examinations and act as a first-line mons.org/licenses/by/4.0/), which permits unrestricted use, distribution, modality filtering which patients should undergo CTA if and reproduction in any medium, provided you give appropriate credit an endoleak is detected. Thus, the use of SMI and CEUS to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. would significantly reduce the number of CTA exami- nations and, in consequence, decrease the load of ioniz- References ing radiation and the risk of renal insufficiency . 1. 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Abdominal Radiology – Springer Journals
Published: Jun 6, 2018
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