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Experimental Studies |
1 From the Departments of Clinical Radiology (H.I.M., H.T.R., R.L.V., P.V.), Surgery (M.H.), and Pathology (V.M.K.), Kuopio University Hospital, Puijonlaaksontie 2, SF-70210 Kuopio, Finland, and the Department of Pathology and Forensic Medicine, University of Kuopio, Finland (V.M.K.). Received June 5, 1998; revision requested July 31; final revision received November 2; accepted February 9, 1999. Address reprint requests to H.I.M. (e-mail: hannu.manninen@kuh.fi ).
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Abstract |
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MATERIALS AND METHODS: PTA was performed in situ in one carotid artery, and stent placement was performed in the other, in ten cadavers (age range, 57–82 years; mean age, 68 years) with severe atherosclerosis by using fluoroscopic and intravascular US guidance. The carotid artery was connected to a pressurized tubing system in which a pulsatile pump circulated water. The effluent water was collected during the interventions, and after filtration and staining, the embolic material was analyzed histologically. After the interventions, the arteries were excised and 1.5-T spin-echo MR imaging was performed.
RESULTS: No difference in severity of distal embolization during stent placement versus during PTA was found. The embolic particles were composed mainly of intimal strips and cellular constituents of the atherosclerotic plaques. MR imaging accurately depicted postinterventional changes, and the findings correlated closely with those of intravascular US and histopathologic analysis.
CONCLUSION: Although stent placement and PTA were associated with equal distal embolization, the smooth surface and fully patent arterial lumen depicted at intravascular US and MR imaging postinterventionally may indicate that stent placement is preferable to PTA.
Index terms: Carotid arteries, MR, 172.121411, 904.129411 • Carotid arteries, stenosis or obstruction, 172.721, 904.721 • Carotid arteries, transluminal angioplasty, 172.126, 904.1282, 904.1286 • Carotid arteries, US, 172.1298, 904.1298 • Stents and prostheses, 172.126, 904.1268
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Introduction |
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Intravascular US is widely used in peripheral and coronary arteries (8,9) for guiding complex endovascular interventions; the technique is considered to be the standard of reference for imaging arterial wall and atherosclerotic plaque (10). Intravascular US seems to be feasible and safe for imaging carotid arteries that are "protected" with a stent (11,12) and "unprotected" carotid arteries that have mild atherosclerotic changes (13). However, intravascular US is an invasive technique that currently cannot be used to image severely diseased carotid arteries or performed during PTA of carotid arteries. Thus, there is a definite need for a noninvasive and safe imaging technique for monitoring carotid arteries after PTA or stent placement. Although magnetic resonance (MR) imaging has shown promise in quantitating and characterizing carotid atherosclerosis in vivo (14), to our knowledge, its use in evaluating carotid arteries after PTA and stent placement has not been reported on.
The present study was undertaken to (a) compare the severity of distal embolization during carotid arterial stent placement with that during PTA by means of experimental interventions in cadavers in situ, (b) correlate the distal embolization with the intravascular US appearance and histopathologic findings of the atherosclerotic arterial wall, and (c) compare T1-, T2-, and intermediate-weighted spin-echo MR imaging with intravascular US for the postinterventional evaluation of the carotid arteries.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Carotid Arterial PTA and Stent Placement
The experimental endovascular interventions were performed in conjunction with the autopsies within 48 hours after death. The aortic arch was cannulated by using visual guidance after the removal of the manubrium sterni and costal cartilages, and an 8-F introducer sheath was advanced into the proximal common carotid artery with contrast medium–enhanced digital fluoroscopic guidance (at the lateral projection). To eliminate backflow, the proximal part of the common carotid artery was tightly ligated around the sheath. Postmortem thrombi were removed by vigorously flushing the artery with water through the side port of the sheath by means of manual injections. After all friable material had been removed, the intracranial internal carotid artery was tightly cannulated at the base of the skull. The artery was connected to a circulating tubing system in which a pulsatile pump circulated water. Carotid arterial angiography was performed by manually injecting contrast medium into the side port of the introducer sheath.
At the beginning of the intervention, the extracranial internal carotid artery was traversed with a 0.018-inch guide wire with the aid of digital road map control. A 3.5-F, 30-MHz intravascular US catheter (Sonicath; Medi-tech/Boston Scientific, Watertown, Mass) was introduced into the distal internal carotid artery, and intravascular US (Sonos; Hewlett Packard, Andover, Mass) was performed while the catheter was slowly pulled back. The US scans were registered on super-VHS tape, as described in greater detail elsewhere (13). The mean intravascular pressure during imaging was maintained at 70–100 mm Hg to provide full expansion of the carotid artery. To register the exact longitudinal location of the US probe within the artery, several single x-ray exposures were obtained during imaging, and the corresponding time points were marked with annotations on the intravascular US videotape.
The right and left carotid arteries in each cadaver were randomized for PTA or stent placement. The sizes of the PTA balloon and the stent were determined on the basis of the measurement at intravascular US. The PTA balloon diameter was selected to match the luminal diameter of the normal internal carotid arterial segment adjacent to the diseased segment. The nominal diameter of the self-expanding stent (Wallstent; Schneider, Bulach, Switzerland) was 1–2 mm bigger than the luminal diameter of the artery. If angiographically detected residual stenosis persisted after stent placement, then complementary balloon dilation was performed. Conventional 5-F PTA balloon catheters and dilation pressures of 8–10 atmospheres were used. The results were monitored with contrast-enhanced angiography, and intravascular US was repeated at the end of the procedure.
Collection of Embolic Material
The effluent water was collected during the intervention, from the point when the lesion was traversed with the guide wire to the time of final angiography, excluding intravascular US. If the stent placement procedure ended with balloon dilation, another fraction of effluent water was collected during this stage. At the end of the intervention, 20–40 mL of water was forcefully injected by hand into the side port of the sheath to flush the remaining friable material into the tubing system. Then, a volume of 99% ethanol equivalent to the volume of water collected was added to the solution. Immediately after the intervention, the extracranial carotid arteries were excised, and the specimens were immersed in 10% buffered formalin.
MR Imaging
MR imaging of the excised arterial samples was performed at room temperature by using 1.5-T equipment (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany). A 40-mm solenoid radio-frequency coil was used as a receiver. After sagittal T1-weighted localizer images (repetition time msec/echo time msec, 15/6; flip angle, 70°) were obtained, T1-weighted spin-echo (400/14) and fast intermediate- and T2-weighted images (2,500/17–102) were obtained in the axial plane by using the following parameters: field of view, 31 x 50 mm; section thickness, 2 mm; and matrix, 160 x 256. A total length of 5–6 cm, which covered the treated area, was imaged.
Analysis of Intravascular US Findings
All of the intravascular US videotapes were analyzed at a consensus reading by two vascular radiologists (H.I.M., H.T.R.) with prior experience in intravascular US of the coronary, carotid, and peripheral arteries. The inter- and intraobserver variabilities of these two readers in interpreting carotid arterial intravascular US findings are presented elsewhere (13). The percentage diameter of stenosis before and after the intervention was measured at intravascular US by using the analysis program provided with the equipment software. The morphology of the atherosclerotic plaques was classified at intravascular US on the basis of established criteria as soft, fibrotic, or mixed (13,15,16). The intravascular US appearance of the surface of the plaques was classified as smooth, irregular, or ulcerated. Hyperechoic intralesional areas with acoustic shadowing were interpreted as calcifications. The total number of macroscopic calcifications at the treated segments were calculated. The degree of lesion calcification was visually assessed on a four-point scale as not calcified, minimally calcified, moderately calcified, or heavily calcified.
The postinterventional intravascular US scans were analyzed for the presence of dissections, which were defined as separations of the components of the arterial wall. The site of the dissection in relation to the atherosclerotic plaque and the extension of the dissection were graded as minor or major. We also searched for fractures in the inner parts of the plaque. Partly loosened intimal flaps and other components of the atherosclerotic arterial wall floating inside the arterial lumen were registered.
In the arterial segments treated with stents, we evaluated the contact between the stent and arterial wall and searched for protrusion of the plaque material through the stent. The extension of the stent over the whole diseased segment was assessed.
Analysis of MR Imaging Findings
The axial MR images were analyzed by one radiologist (H.I.M.) 2 months before the intravascular US analysis by using a classification similar to that used in the analysis of the postinterventional intravascular US videotapes. Furthermore, T1-, T2-, and intermediate-weighted MR images were compared side by side and given a grade of 1–3 relative to each other for the depiction of the following anatomic and diagnostic details: calcifications, dissections, demarcation of the arterial wall from the periadventitial tissues, demarcation of the atherosclerotic plaque from the arterial wall, and absence of artifacts due to the stent.
Histologic Analysis of the Embolic Material
The histologic analyses were performed by an experienced pathologist (V.M.K.). The effluent fluid collected during each intervention was micropore filtered, and the sediment was stained with Papanicolaou stain. To characterize the distal embolism, the material captured by the filters was analyzed under a light microscope. The composition of the filtered particles was classified into the following three categories: clusters of unspecified cells, lipid-filled foam cells or other material of the fragmented atherosclerotic plaque, and intimal strips. The number of these elements in each sample was calculated, and the dimensions of the largest particles were measured with an image analyzer (Quantimet 570; Leica, Cambridge, England) operated in an interactive mode. In addition, the relative amounts of lipid-filled foam cells or other fragmented atherosclerotic plaque material were classified as scanty (less than 10), numerous, or abundant (unmeasurable). On the basis of the abundance of the components described above, the overall severity of embolism was assessed on a three-point scale as mild, moderate, or severe. Finally, in each cadaver, the severity of embolism between the right and left carotid arteries, with consideration of the amount of embolic material and the particle size, was compared pairwise by using a rating system in which a score of -2 indicated the embolism was much more severe on the stent-treated side; -1, the embolism was slightly more severe on the stent-treated side; 0, the embolism was equal on both sides; 1, the embolism was slightly more severe on the PTA-treated side; and 2, the embolism was much more severe on the PTA-treated side.
Histopathologic Analysis of Arterial Specimens
To locate the anatomic landmarks, fine-resolution native film hard-copy images of the air-filled carotid arterial specimens were obtained at 30 kVp in the lateral projection. On the basis of findings on these images, the MR images, and the intravascular US scans, two or three anatomic locations were selected in the area of the treated (with stent placement or balloon dilation) segment. The stents were carefully removed from the excised, formalin-buffered arteries. Five-micrometer-thick slices were cut in the marked locations. The slices were stained with either hematoxylin-eosin or Masson trichrome stain and analyzed under a light microscope. Other constituents of the plaques that were registered included the presence of a necrotic core, hemorrhage or remarkable neovascularity, and intraplaque calcifications (hematoxylin-eosin stain). The calcifications were classified as microscopic (punctate) or large (either deep or superficial).
Plaques with a fibrotic superficial part and middle and basal cell layers that contained foam cells, cellular debris, and cholesterol crystals were classified as fibrous cap lesions (13). The fibrous cap was further classified as complete, thin, or incomplete. Dissections, which were defined and classified analogously to those on the imaging studies, were registered. Plaque disruption was defined as intraplaque material protruding outside the plaque.
Statistical Analyses
The Spearman correlation coefficient for the continuous and ordinal scale variables between the two treatment groups was calculated. The differences between the two groups were tested by using the Wilcoxon rank sum W test for the continuous and ordinal scale variables and the Fisher exact test for the dichotomized variables. The Wilcoxon matched pairs signed rank test was used to perform paired comparisons between the right and left carotid arteries in each cadaver. The Friedman two-way analysis of variance was used to test differences between the three MR imaging sequences. Differences with a P value of less than .05 were considered to be statistically significant.
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RESULTS |
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Comparison of MR Imaging Sequences
Table 4 shows the main results of comparisons between T1-, T2-, and intermediate-weighted MR imaging sequences for the depiction of the postinterventional status of the carotid arteries. The differences in usefulness between the sequences were small. Overall, the T1-weighted images depicted best the calcifications of the plaques (Figs 1, 4), but in one artery, the depiction of a deep calcification was poorest on the T1-weighted image (Fig 6c). The stent mesh caused minimal artifacts with all three sequences, and T2- and intermediate-weighted images in particular were almost free of artifacts (Fig 4).
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DISCUSSION |
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Distal Embolization during Carotid Arterial Interventions
The frequency of complications, especially ischemic stroke caused by distal embolization, is of fundamental importance when selecting the therapeutic intervention. Transcranial Doppler US of the middle cerebral artery has been reported (20) to register more microembolic signals during PTA than during surgical carotid endarterectomy. However, transcranial Doppler US cannot enable differentiation between microembolic signals caused by particulate and those caused by contrast media injections or inflation and deflation of the angioplastic balloon, and it does not offer any information about the pathologic type of the emboli.
An in vitro model with specimens of carotid plaque encased in a vascular graft wrap was used to quantitate embolic material during experimental stent placement (21). Unfortunately, in such models, when the intervention is not performed in situ, the atherosclerotic lesions are exposed to mechanical handling during surgical excision, and the normal elasticity of human carotid adventitia and periadventitial tissues is missing. Our experimental setup, in which the endovascular therapies were performed in situ in fresh cadavers, simulates better a clinical intervention and thus facilitates the accurate collection and histologic analysis of embolic constituents. The interventions were performed under pressurized conditions that provided an opportunity to assess the imaging findings after carotid arterial PTA with intravascular US. Intravascular US cannot be used to guide carotid angioplasty in living humans because of the risk of embolization.
The most common stent currently used in carotid arteries is the self-expandable Wallstent. One might expect the distal embolization during self-expanding stent placement to occur less frequently than that during balloon dilation. First, the Wallstent has the ability to expand during placement, beginning from the distal end and encompassing the atherosclerotic plaque and possibly the embolic fragments against the vessel wall. Second, the results of intravascular US and autopsy studies (22,23) on peripheral and coronary arteries have shown that the inner surface of vessels treated with stents is smooth, whereas extensive irregularity due to plaque ruptures and dissections are frequently encountered after PTA. Although intravascular US and MR imaging confirmed this in the present study, the severity of distal embolization was similar in the stent and PTA groups. Because the atherosclerotic lesions and other characteristics of the arterial wall (ie, vulnerability to catheter and/or guide-wire manipulation) of the two carotid arteries in each cadaver were interrelated, a paired analysis of the stent-treated arteries compared with the PTA–treated arteries in each cadaver also was performed. Not even the pairwise comparison revealed definite differences.
We did not perform predilation of any arteries in the stent group, but we performed balloon dilation inside the stent after stent placement in four arteries because of residual stenosis. It seems to be commonly assumed that embolization occurs most often during balloon dilation. However, although we found some embolic material during the complementary balloon dilation in each case, the overall severity of distal embolization in these arteries did not clearly differ from those in which dilation inside the stent was not performed. It should be noted that dilation inside the stent is a part of the placement of balloon-expanding stents and commonly is mandatory after the clinical deployment of self-expanding stents in carotid atherosclerotic lesions (6).
The most potentially dangerous embolic constituents encountered in the present study were intimal strips, the largest of which were several millimeters long. Similar particles have been found in experimental atheroablations of lower limb arteries with the Kensey atherectomy catheter (24). On the other hand, the embolic particles found by Ohki et al (21) during experimental carotid arterial stent placement did not include intimal strips. In the present study, the three cases with the greatest numbers of embolic intimal strips were encountered in the PTA group, but the mean numbers of intimal strips in the two study groups were almost equal (Table 3).
In three cases with large numbers of embolic strips, postinterventional intravascular US revealed partly loosened intimal flaps floating in the vessel lumen. One of these flaps was on the normal side of the arterial wall (Fig 3), and another was adjacent to the segment treated with a stent, which implied that the balloon dilation or stent deployment was not necessarily the reason for the strips, but rather guide-wire and/or catheter manipulation may have been the causative factor. The behavior of cadaveric arteries may not be identical to that of in vivo arteries, and postmortem autolysis probably contributed to the vulnerability of the arterial intima and increased friability of the plaque. Our experimental setup may have therefore overestimated the abundance of embolic intimal strips and other embolic constituents that manifest during clinical endovascular carotid interventions.
Recognition of the imaging features that correspond to the histopathologic constituents of carotid plaques associated with increased risk of distal embolization during endovascular intervention would be very useful before deciding on the therapy in individual cases. We correlated the histopathologic and intravascular US characteristics of such plaques with the distal embolism. The presence of histopathologic intraplaque hemorrhage and/or remarkable neovascularity was associated with a greater abundance of lipid-filled foam cells in the embolic filtrate. Intraplaque hemorrhage indicates an unstable lesion, which is prone to spontaneous rupture (25). One could postulate that the compression of such plaques makes the inner constituents more prone to disperse as embolic particles.
Ohki et al (21) found an increased risk of distal embolization in lesions that were hypoechoic at external US and "soft" at histopathologic analysis. We did not find such correlation; however, it should be noted that only about one-fifth (four of 19) of the lesions in the present study were "soft" at intravascular US (Table 1), whereas almost three-fourths (14 of 19) of the lesions had a fibrous cap at histopathologic analysis (Table 2). On the other hand, in the present study the abundance of unspecified cells in the embolic filtrate correlated positively with the number of calcifications at intravascular US. Ohki et al (21) found that plaques with a more than 90% diameter of stenosis produced a higher number of embolic particles during experimental stent placement. The embolic material in our study did not include such tight lesions: The diameter of stenosis at intravascular US in the arteries treated with interventions ranged from 32% to 85%.
Postinterventional Changes at Intravascular US and MR Imaging
The intravascular US appearance of the arterial wall after coronary and peripheral arterial PTA and stent placement in vivo has been established by several authors (9,22,26). Our findings during ex vivo, in situ interventions in human carotid arteries were very similar: There was substantial residual stenosis in every case, and the surface of the arterial plaque was mainly irregular or the plaque was fractured after PTA, with dissections in the majority of the arteries. The lumen was fully patent and the surface of the treated segment was smooth in all arteries after stent placement. It should be noted that the long-term patency of carotid arteries treated with stents compared with that of arteries treated with PTA is still unknown.
Neither intravascular US nor MR imaging depicted any dissections or plaque fractures at the area of segments treated with stents, even though the histopathologic specimens revealed dissection in five cases and plaque disruption in three. Although it is possible that these damages were partly due to excision of the vessels and removal of the stent from the formalin-buffered artery, it is evident that they were mainly caused by the active radial expansion force of the self-expanding Wallstent and/or the additional balloon dilation. It remains uncertain whether these damages, which were isolated by the stent mesh, were the cause of the distal embolization.
Reports on the use of MR imaging for postinterventional evaluation of PTA are sparse. Although time-of-flight MR angiography accurately depicts the degree of stenosis with reference to x-ray angiography, its poor soft-tissue contrast reduces its potential to enable assessment of postinterventional morphologic changes in the treated lesion (27). Toussaint et al (28) used spin-echo sequences at 9.4-T to image samples of atherosclerotic arteries treated with balloon compression and found fibrous cap lesions to be resistant to compression; however, substantial reduction and redistribution occurred in the lipid cores of the fatty plaques. We did not find any association between the histopathologic type of the lesion and the post-PTA status at MR imaging or intravascular US. This might be owing to the small total number of lesions in our study and to the fact that the majority of the plaques had a fibrous cap (Table 2). Toussaint et al (28) reported that the compression often dissected the calcified plaques at shoulder level; we also encountered this finding (Fig 6).
Metallic stents are a concern during MR imaging, especially during the immediate postinterventional period, because they can theoretically move, induce electrical currents, or heat tissues (29,30). The key determinant in the safeness of a metallic stent in MR imaging is its ferromagnetic properties. According to the manufacturer, the self-expanding Wallstent used in our study is made of an alloy of cobalt and tantalum and hence is nonferromagnetic and safe for MR imaging. However, to our knowledge, the safeness of MR imaging immediately after the deployment of a Wallstent in a human carotid artery in vivo has not been assessed. Minimal artifacts were seen at spin-echo MR imaging in the present study (Figs 1, 4), but they did not interfere with the diagnostic quality of the images. On the contrary, the diagnostic value of external US for assessment after stent placement was considerably deteriorated by the acoustic shadowing caused by the stent mesh. However, our experimental setup with MR imaging of excised carotid arteries was highly contrived; greater degradation of image quality would be expected at clinical spin-echo MR imaging owing to flow and motion artifacts.
T2-weighted MR imaging has shown promise in differentiating lipid-rich, necrotic, hemorrhagic, and fibrotic constituents of atherosclerotic plaque in vivo (14). Because our study focused on the evaluation of post-PTA and post–stent placement changes, we did not correlate in detail the MR imaging findings and histopathologic constituents of the lesions. Overall, MR imaging depicted accurately most of the postinterventional changes after stent placement and PTA and correlated well with intravascular US imaging: The residual stenosis, extent of the plaques and stents, and surface of the treated segments were precisely assessed. However, it appears that intravascular US is superior to MR imaging for depicting dissection; intravascular US depicted eight dissections in the PTA group, whereas MR imaging depicted five. In addition, the findings were often more subtle at MR imaging than at intravascular US. It should be noted that the arteries were not pressurized during imaging, and this may have contributed to the findings being more subtle at MR imaging.
The T1-weighted images were slightly superior to the T2- and intermediate-weighted images, especially in the depiction of calcifications; the deep, hypointense calcifications in particular were demarcated better, because the adventitia has high signal intensity on T1-weighted images but low signal intensity on intermediate- and T2-weighted images (Fig 4) (31). In one case (Fig 6c), however, the calcification was almost isointense on the T1-weighted image, whereas a distinct signal intensity void was seen on the T2- and intermediate-weighted images. In this particular focus, this phenomenon, which is familiar in intervertebral disks, probably indicates a relatively low concentration of calcium, which occurs when the simultaneously shortened T1 and T2 relaxation times due to the calcium are in equilibrium (32).
Practical application: Distal embolization was common during both PTA and stent placement in situ in the carotid arteries of cadavers, and there was no substantial difference in the severity of distal embolization between the treatments. Intravascular US and MR imaging revealed substantial residual stenosis, dissections, plaque fractures, and irregularity on the surface of the treated segments after PTA, but showed fully patent lumens and smooth surfaces after stent placement; these findings might lead us to favor stent placement over PTA. MR imaging with spin-echo sequences, because of its noninvasiveness, clarity of image presentation, and ability to depict the whole extension of the atherosclerotic plaque despite calcifications or stent mesh, has potential for postinterventional imaging.
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Acknowledgments |
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, H.I.M.; study concepts, H.I.M., H.T.R.; study design, H.I.M., H.T.R., M.H.; definition of intellectual content, H.I.M.; literature research, H.I.M.; experimental studies, H.I.M., H.T.R., R.L.V., P.V., M.H.; data acquisition, H.I.M., H.T.R., R.L.V., P.V.; data analysis, H.I.M., P.V., V.M.K.; statistical analysis, H.I.M.; manuscript preparation, H.I.M., H.T.R., V.M.K.; manuscript editing, R.L.V., P.V.; manuscript review, M.H.
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