(Stroke. 1996;27:700-705.)
© 1996 American Heart Association, Inc.
Articles |
From the Department of Neurosurgery, Shimane Medical College (R.K., K.M.), and the Department of Neurosurgery, Chugoku Rousai Hospital (T.S., Y.O.), Japan.
Correspondence to Reiko Kagawa, MD, Yokoyama Hospital, 2 5 20 Hirokoshinkai, Kure, Hiroshima, 737 01, Japan, and reprint requests to Kouzou Moritake, MD, Department of Neurosurgery, Shimane Medical College, 89-1 Enyachyou, Izumo, Shimane, 693, Japan.
| Abstract |
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Methods B-mode examinations were performed on 64 Japanese patients (68 arteries) who subsequently underwent CEA. In each case, the appearance of plaque on B-mode was classified into one of two types: heterogeneous or homogeneous; plaque echogenicity was expressed as hypoechoic, isoechoic, or hyperechoic. Surface characteristics such as ulceration also were examined, and the degree of carotid artery stenosis was calculated. The B-mode findings were compared with angiographic and pathological features.
Results B-mode accurately visualized macroscopic ulceration and surface irregularity in 93.8% of the lesions examined, which was superior to angiography. Fifty-four lesions (79.4%) were of the heterogeneous type and 14 lesions (20.6%) were of the homogeneous type on B-mode. Microscopically, 57.4% of the heterogeneous-type lesions were a mixture of atheroma and fibrosis, and all homogeneous-type lesions demonstrated fibrous change. The frequency of calcification was higher in the heterogeneous lesions than in the homogeneous lesions.
Conclusions B-mode ultrasonography findings can provide information about macroscopic and microscopic characteristics of carotid lesions.
Key Words: carotid endarterectomy carotid stenosis pathology ultrasonics
| Introduction |
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In this study, we evaluated the diagnostic value of B-mode in patients with carotid artery stenosis who subsequently underwent CEA by comparing B-mode findings with (1) those of angiography in an assessment of the preoperative location and severity of stenotic lesions, (2) intraoperative macroscopic characteristics of the lesions, and (3) microscopic findings in the lesions.
| Subjects and Methods |
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Examination With B-Mode
An 8-MHz probe (Sonobista CARO model MEU 2422, Biosound) was
used. The patients were examined in the supine position with their
heads slightly rotated to the contralateral side of the carotid artery
being studied.11 The carotid arteries were routinely
investigated in the longitudinal and axial planes and were observed
from multiple directions by shifting the probe. The visualized carotid
artery was divided into the following three segments according to the
modified Espeland classification12 : ICA, BIF, and CCA (Fig 1
). The ICA segment is defined as the portion distal to
the flow divider. The BIF segment extends from the flow divider 8 mm
proximally to the CCA. The CCA segment extends proximally from the BIF
segment. The locations of the carotid lesions were categorized into one
of five groups (ICA, ICA-BIF, BIF, BIF-CCA, and CCA) according to the
position of the most stenotic part of the lesion. For example,
a lesion located only in the ICA segment was placed in the ICA group, a
lesion with the most stenotic part extending from the ICA to
the BIF was placed in the ICA-BIF group, and a lesion located only in
the CCA segment was placed in the CCA group (Fig 1
).
|
An atherosclerotic lesion was defined as an intima-media complex
with a thickness of more than 2 mm.13 The appearance of
plaque was classified into one of the two types:
heterogeneous (type I) or homogeneous (type
II).11 14 15 Additionally, the echogenicity of the plaque
was expressed as hypoechoic, isoechoic, or hyperechoic. An isoechoic
plaque was defined as having the echogenicity of a normal
intima-media complex.11 16 A hyperechoic plaque was
brighter than an isoechoic plaque, and a hypoechoic plaque was less
bright than an isoechoic plaque. Type I lesions were composed of a
mixture of hypoechoic, isoechoic, and hyperechoic plaques. Type II
lesions consisted of only one of the three types of echogenic plaques.
Type I lesions were further divided into four subtypes: type Ia lesions
were composed of a mixture of hyper- and isoechoic plaques. Type Ib
lesions were composed of a mixture of iso- and hypoechoic plaques. Type
Ic lesions were composed of a mixture of hyper- and hypoechoic plaques.
Type Id lesions were composed of a mixture of hypo-, iso-, and
hyperechoic plaques. Type II lesions were further divided into three
subtypes: type IIa, IIb, and IIc lesions were hyper-, iso-, and
hypoechoic, respectively. A typical example of a type Id lesion is
shown in Fig 2A
, and a typical example of a type IIb
lesion is shown in Fig 2B
.
|
Surface characteristics of the plaque were classified into three categories: ulcerated, irregular/uncertain ulceration, or smooth/no ulceration.17 An ulcerated plaque was characterized by the absence of visualization of the intimal layer and presence of a crater in the plaque surface.11 An irregular lesion was defined as a lesion lacking surface smoothness and having an intimal layer. A smooth lesion was defined as a lesion without ulceration and surface irregularity.
The degree of carotid stenosis was measured on the longitudinal
section demonstrating the most severe stenosis (Fig 3A
). We measured the distance from the near
media-adventitia interface to the far media-adventitia
interface (A) and the distance from the near intimal surface to the far
intimal surface (B) at the most stenotic point of the
artery.9 13 The degree of carotid stenosis on
B-mode was calculated as (A-B)/Ax100.
|
Angiography
Selective carotid angiography was performed using
anteroposterior, lateral, and oblique views.8
Arterial lumen diameters were measured in the most
stenotic view at the most stenotic site (Fig 3B
),2 and the normal arterial lumen was
extrapolated at this site. The appearance of the lesion was classified
into one of three categories: ulcerated, irregular/uncertain
ulceration, or smooth/no ulceration.8 Briefly, an
ulcerated plaque was defined as a lesion seen in profile as a crater
penetrating into a stenotic plaque.8 An irregular
lesion was defined as wall irregularity or multiple small
craters.8
The degree of stenosis was calculated using the extrapolated diameter of the artery (A) and the residual lumen (B) as (A-B)/Ax100 (linear method).2 18
Macroscopic and Microscopic Examination
CEA was performed on patients under general
anesthesia, widely exposing the carotid arteries from the
ICA to the CCA. An internal shunt system was applied in all cases
during cross-clamping of the carotid arteries.19 After
arteriotomy, the involved site was macroscopically investigated to
clarify the surface characteristics.8 Then the
stenotic lesion was carefully removed en bloc. The surface of
the excised specimens and the axial sections were macroscopically
examined and then photographed. The first 20 CEA specimens were not
macroscopically evaluated by the pathologist. Hence, the macroscopic
correlations were obtained only from 48 CEA specimens. These surface
characteristics of the lesions were classified into three
categories: ulcerated, irregular/uncertain ulceration, and
smooth/no ulceration. Macroscopic ulcerations were defined by both the
surgeon and the pathologist as either disruptions in the surface of the
plaque or pits and depression in the plaque, often with a sharply
delineated color difference between the base of the pit and the
adjacent luminal surface.8 Irregular lesions were defined
as plaques with surface pits and plaques without disruptions and color
changes.
The specimens were fixed in a 10% formalin solution and stained with hematoxylin-eosin for microscopic examination. Pathological examination was performed in tissue from the main stenotic lesion, including at least four axial sections.10 The existence of intraplaque hemorrhage and calcification was examined in detail. The lesions were microscopically classified into one of five categories: (1) atheromatous lesions composed mainly of lipid material, (2) fibrous lesions composed of fibrotic proliferation over 70% of the lesion, (3) complicated lesions of atheroma and fibrosis, (4) intraplaque hemorrhage within complicated lesions, and (5) miscellaneous lesions.20 21 A calcified plaque was defined as having macroscopic evidence of calcification or more than five calcified deposits of >1 mm in diameter.
| Results |
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B-Mode Findings of Carotid Stenotic Lesions
Echogenicity classification of stenotic lesions is shown
in Table 1
. Fifty-four (79.4%) of the 68 carotid
stenotic lesions were classified as type I and the remaining 14
(20.6%) as type II. The most common type I subtype lesion was type Id
(22 lesions, 40.7%), consisting of hypoechogenic, isoechogenic, and
hyperechogenic plaques. The most common type II subtype lesion was type
IIb (7 lesions, 50.0%), consisting of isoechoic plaques.
|
Relationship Between Carotid Lesion Location and
Echogenicity
The relationship between location of lesions and their
echogenicity is shown in Table 2
. Type I lesions were
observed in 3 (60.0%) of 5 ICA lesions, 47 (81.0%) of 58 ICA-BIF
lesions, and 4 (80.0%) of 5 CCA lesions. In the 58 ICA-BIF lesions,
type Id and type Ib were seen in 22 (37.9%) and 15 (25.9%) lesions,
respectively. Additionally, type Id lesions were detected only in the
ICA-BIF. Eleven of 14 type II lesions were observed in the ICA-BIF.
|
Degree of Stenosis
The degree of carotid stenosis as determined with
B-mode ranged from 15% to 97.4% (mean, 49.0%) and that by
angiography from 22.6% to 99.5% (mean, 65.4%) (Fig 4
). B-mode tended to underestimate the degree of
stenosis compared with angiography. In the 68 stenotic
carotid lesions, there was no significant linear correlation between
the degree of stenosis as determined by B-mode compared with
angiography (r=.15).
|
Comparison of B-Mode, Angiographic, and Macroscopic
Findings
Macroscopic examinations were performed on 48 stenotic
carotid lesions by both a surgeon and a pathologist. B-mode,
angiographic, and macroscopic findings of the surface characteristics
are summarized in Table 3
.
|
In these 48 carotid lesions, B-mode diagnosed ulcerations and/or
surface irregularities in 38 (79.2%) and angiography in 24 (50.0%).
B-mode and angiographic findings of ulcerations and/or surface
irregularities correlated with macroscopic features in 45 (93.8%) and
29 (60.4%) of the 48 carotid lesions, respectively. The correlation
rate of B-mode was significantly higher than that of angiography
(
2 test, P<.01).
Comparison of B-Mode and Microscopic Examinations
The microscopic features of the stenotic carotid lesions
are summarized in Table 4
. Mixed lesions with
atheroma and fibrosis were most frequently seen (34
[50.0%] of 68 lesions). Fibrosis alone was seen in 15 carotid
lesions and atheroma alone in 7. Calcification was observed
in 21 carotid lesions and intraplaque hemorrhage in 8. Of the
21 lesions with calcification, 19 (90.5%) showed
heterogeneous echogenicity (type I). Thirty-one
(57.4%) of the 54 type I lesions were composed of atheroma
and fibrosis microscopically. Calcification was found in 12 (54.5%) of
the 22 type Id lesions and in 3 (15.8%) of the 19 type Ib
lesions. The frequency of calcification was significantly higher in the
type Id lesions than in the type Ib lesions (
2
test, P<.05). Fig 5A
shows a typical example
of a type Id lesion with a mixture of hypo-, iso-, and
hyperechogenicity at the ICA-BIF. Microscopic examination of the
surgical specimen demonstrated an atheromatous lesion
with calcification.
|
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Intraplaque hemorrhage was more frequently seen in type Ib and Id lesions. Only one type II lesion indicated intraplaque hemorrhage.
A typical example of a type II lesion is shown in Fig 5B
. B-mode
demonstrated a homogeneous isoechoic lesion that was
macroscopically composed of fibrous thickening of the intimal layer.
Microscopically, it was composed of hyalinized fibrosis. Type II
lesions did not contain solely atheroma, but all had
fibrosis.
| Discussion |
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Location of Stenotic Carotid Lesions and Degree of
Stenosis
In this study, the ICA-BIF was the most frequently involved site,
which agrees with a previous report.23 The main lesions at
the ICA-BIF extended into the CCA, and the border between lesions and
normal arteries was not well defined. We therefore thought that careful
observation and management of lesions in the CCA would be
important.
Agreement of lesion location between B-mode and angiography was observed in 61 of 68 lesions (nearly 90%). Disagreement between the two methods (7 lesions, 10.3%) may have been attributable to the following reasons. First, measurement of the stenotic site tends to be inaccurate with angiography because only the internal wall of the carotid artery is visualized. In contrast, B-mode visualizes changes throughout the carotid artery wall, such as thickening of the intima and thrombus formation. Second, detection of high lesions distal to the mandibular edge by B-mode is difficult, especially in our series of patients, because the probe cannot visualize the distal ICA. Because of this, B-mode could not detect the seven distal lesions depicted by angiography.
B-mode has been suggested to cause underestimation of the degree of stenosis compared with angiography, and no statistically significant correlation was observed between the degree of stenosis as determined by B-mode and angiography. The following difference in measurement between the two methods could account for this result: B-mode accurately shows the outer arterial wall being used for calculation of the stenotic rate. Angiography, however, extrapolates lines from an uninvolved site to obtain the normal arterial lumen at the involved site, which may vary because of poststenotic dilatation in the distal ICA.7
Echogenicity of Stenotic Carotid Lesions
In this study, heterogeneous (type I) lesions were
found more frequently than homogeneous (type II) ones. This
result was consistent with that of Hennerici et
al.25 Type Ib lesions (a mixture of iso- and
hypoechogenicities) and type Id lesions (a mixture of hypo-, iso-, and
hyperechogenicities) were predominant, which might reflect the
multifarious nature of stenotic carotid lesions. It has been
suggested that many embolic events coincide with recent intraplaque
hemorrhage, which gives heterogeneity to the
lesion.7 26 Lipid lesions, demonstrated by low
echogenicity, have a high tendency to develop thrombosis, embolism, and
ulceration.10 Therefore, accurate information about lesion
echogenicity is important in planning therapeutic strategies for
stenotic carotid lesions. Type Id lesions were most frequently
observed at the ICA-BIF and were not detected at either the ICA or the
CCA. This preference suggests that microscopic features of the
stenotic lesions are closely related to the site of the
lesion.
Relationship Between B-Mode and Angiography in Comparison With
Macroscopic Features
B-mode is known to diagnose ulceration in 50% to 95% of patients
with carotid artery stenosis7 23 and to have a
higher sensitivity than angiography in the detection of ulceration and
intraplaque hemorrhage.7 27 False-negative
results with B-mode may increase unless lesions are observed from
multiple directions.23 Our B-mode examinations
demonstrated ulcerations and/or surface irregularities in 38 (79.2%)
of 48 macroscopically diagnosed lesions. B-mode examination of surface
characteristics was significantly superior to angiography: the B-mode
findings were 93.8% accurate, but the angiographic findings were
60.4% accurate.
Relationship Between B-Mode and Microscopic Features
It has been reported that fatty tissue and hemorrhage are
hypoechoic, fibrosis is isoechoic or slightly hyperechoic, and
calcification is hyperechoic with acoustic
shadowing.7 16 26 28 The majority of
heterogeneous (type I) lesions in this study were composed
of a mixture of atheroma and fibrosis. More than 90% of
all calcified lesions were type I lesions. Calcification therefore
should be accompanied by a mixture of atheroma and
fibrosis. Calcification was significantly more frequent in type Id
lesions than in type Ib lesions, which suggests that hyperechoic
components were closely related to calcification.
Intraplaque hemorrhages can be seen as echolucent areas with caps of echodense material.15 26 28 Intraplaque hemorrhage was more frequent in type I lesions than in type II lesions. All lesions with intraplaque hemorrhage, except two, contained hypoechoic components. These results suggest that hypoechoic components are closely related to hemorrhage. Differentiation between intraplaque hemorrhage, indicated by hypoechogenicity, and ulceration of echolucent areas has been difficult with B-mode.15
Homogeneous type lesions have been shown to consist most often of fibrosis.7 Hyperechoic and isoechoic homogeneous (type II) lesions were found to have mainly fibrotic changes in our study. This result was consistent with that of Matalanis and Lusby.26
From this study, we suggest that B-mode and angiographic findings have considerable differences in estimations of the degree of stenosis and surface and plaque characteristics of carotid lesions. Furthermore, the echogenicity of carotid lesions is closely related to the macroscopic and microscopic features of the lesions.
| Selected Abbreviations and Acronyms |
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| Acknowledgments |
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Received August 3, 1995; revision received December 14, 1995; accepted December 14, 1995.
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M. Yasaka, K. Kimura, R. Otsubo, K. Isa, K. Wada, K. Nagatsuka, K. Minematsu, and T. Yamaguchi Transoral Carotid Ultrasonography Stroke, July 1, 1998; 29(7): 1383 - 1388. [Abstract] [Full Text] [PDF] |
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V. Y. Beletsky, R. E. Kelley, M. Fowler, and T. Phifer Ultrasound Densitometric Analysis of Carotid Plaque Composition: Pathoanatomic Correlation Stroke, December 1, 1996; 27(12): 2173 - 2177. [Abstract] [Full Text] |
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N. Suwanwela, U. Can, K. L. Furie, J. F. Southern, N. R. Macdonald, C. S. Ogilvy, C. J. Hansen, F. S. Buonanno, W. M. Abbott, W. J. Koroshetz, et al. Carotid Doppler Ultrasound Criteria for Internal Carotid Artery Stenosis Based on Residual Lumen Diameter Calculated From En Bloc Carotid Endarterectomy Specimens Stroke, November 1, 1996; 27(11): 1965 - 1969. [Abstract] [Full Text] |
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