OriginalORIGINAL Article ARTICLE ISSN 1738-5520 Korean Circulation J 2005;35:795-800 ⓒ 2005, The Korean Society of Circulation

Correlation between the Carotid Intima-Media Thickness and the Plaque Burden of the Left Main Coronary Using Ultrasonography

Dae Woo Hyun, MD1, Kee Sik Kim, MD2 and Seung Ho Hur, MD2 1Division of Cardiology, Cardiovascular Center, College of Medicine Konyang University, Daejeon, 2Department of Cardiology, Keimyung University Dongsan Medical Center, Daegu, Korea

ABSTRACT

Background and Objectives：It has been reported that the common carotid artery (CCA) intima-media thickness (IMT) correlates to angiographically determined coronary artery . The aim of this study was to evaluate the correlation between the carotid IMT and left main (LM) plaque using ultrasonography. Subjects and Methods：In fifty patients (mean age 59.6±9.9, males 35 (70%)) with (CAD), the risk factors of were evaluated and coronary angiographs obtained. The carotid IMT was measured in the far wall of both CCAs, with a 10 MHz linear probe, and the value of the IMT was automatically calculated using programmed software (M’ATH, METRIS Co., Argenteuil, France). The LM plaque was measured by intravascular . The maximal thickness, ratio of the maximal thickness, cross-sectional area (CSA) and burden of the plaque were measured at 2 mm intervals, and the average values calculated. Results：In the right common carotid artery, the maximal IMT significantly correlated with the mean plaque CSA and plaque burden of the LM (r=0.375. p=0.007, r=0.408. p=0.003, respectively). The mean IMT significantly correlated with the plaque burden of the LM, but not with the mean plaque CSA of the LM (r=0.357. p=0.011, r=0.264. p=0.063, respectively). In the left common carotid artery, the maximal IMT was not significantly correlated with the mean plaque CSA and plaque burden of the LM (p=0.251, p=0.218, respectively). The mean IMT was not correlated with the mean plaque CSA and plaque burden of the LM (p=0.249, p=0.078, respectively). Conclusion：There was a significant correlation between the right CCA IMT and plaque burden of the LM in patients with CAD. (Korean Circulation J 2005;35:795-800)

KEY WORDS：Ultrasound；Coronary disease；Carotid .

Introduction IMT of the carotid artery has been used as the primary variable in the evaluation of the progression/regression The ultrasonographic assessment of peripheral arte- of atherosclerosis during lipid-lowering or antihyper- ries has evolved as a promising technique for non-in- tensive treatment.4)5) The atherosclerotic process can vasive evaluation of atherosclerosis.1)2) Assessment of the be studied at an earlier phase through measurement of carotid artery intima-media thickness(IMT), using B- the carotid IMT. Determination of the carotid IMT mode ultrasound, is a useful clinical and research tool allows for a direct, non-invasive, repeatable measure- for the measurement of atherosclerosis.3) An increased ment. It has been reported that the common carotid IMT is considered as a sign of early atherosclerosis of IMT is correlated to the angiographically determined the carotid artery, and is associated with future car- coronary artery stenosis in coronary ,6-9) diovascular events, asymptomatic myocardial ischemia, this correlation is only weak.10) In contrast to coronary coronary risk factors and a change in the coronary risk angiography, which investigates the vascular contour factors after therapeutic intervention. The effect of the and , (IVUS) imaging

Received：April 25, 2005 depicts the structural morphology of the arterial wall Revision Received：June 23, 2005 itself. Despite being angiographically silent, left main Accepted：July 28, 2005 (LM) disease, as detected by IVUS, is an independent Correspondence：Kee Sik Kim, MD, Department of Cardiology, Keimyung predictor of future cardiac events and may serve as a University Dongsan Medical Center, #194 Dongsan-dong, Jung-gu, marker for such events.11) The aim of this study was to Daegu 700-721, Korea Tel: 82-53-250-7379, Fax: 82-53-250-7434 evaluate the correlation between the carotid IMT and E-mail: [email protected] the plaque burden of the left main coronary artery(LM),

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796·Korean Circulation J 2005;35:795-800 using B-mode ultrasound and IVUS, respectively. Vivid 7 echocardiograph(General Electronics Corp., Horten, Norway). The patients were examined in the Subjects and Methods supine position. The operator directed the sound beam perpendicularly to the arterial surface of the far wall of Study population the common carotid artery(CCA) to obtain two pa- Fifty consecutive patients with ischemic disease, rallel echogenic lines, corresponding to the -in- undergoing percutaneous coronary intervention on tima and media-adventitia interfaces. The right and left the left anterior descending or left circumflex artery, CCA IMT were measured at least 10 mm proximal to were enrolled. All had angiographically normal or mild the bifurcation. The values of the maximal and mean LM disease by visual assessment(<20% diameter ste- IMT were automatically calculated by the programmed nosis). The diagnosis of stable angina was defined as a software(M’ATH, METRIS Co., Argenteuil, France) clinically constant pattern of severity for more than two (Fig. 1). The presence of a plaque was evaluated in months. Unstable angina was diagnosed if the patient’s the carotid artery. The plaque was defined as a distinct chest pain, which was accompanied by electrocardio- area, with an IMT exceeding twice that of the neighbo- graphic ST-T changes, was either new or worse in fre- ring sites, so an IMT > 1.3 mm was consequently not quency, severity or duration, superimposed on a pre- included in the calculation of the carotid IMT. existing pattern of anginal pain. Patients were diagnos- ed as having according to the Measurement of the LM plaque and coronary an- presence of chest pain lasting more than 30 minutes, giography accompanied by ST-T segment elevation in two or more Coronary angiography was performed using the stan- related electrocardiographic leads, pathologic Q waves, dard Judkins technique, and significant coronary artery or elevation of serum levels of creatine kinase- MB stenosis was diagnosed when the coronary angiogram fraction(CK-MB)(more than twice the upper normal showed a ≥50% reduction in the lumen diameter. The limit) or cardiac troponin-I. Hypertension was defined LM plaque was measured using IVUS(CLEARVIEW. as a blood pressure ≥140/90 mmHg or the use of anti- Boston Scientific Corp., San Jose, California, USA), hypertensive medications. Diabetes was defined as being with a 30 MHz probe, at 2 mm intervals. In each cross present when previously diagnosed by a physician. Smo- section, the maximal thickness, ratio of thickness, cross- king was estimated from the patient’s history. Hyper- sectional area(CSA) and burden of the LM plaque cholesterolemia was defined as a total-cholesterol level were measured. These variables were calculated by the of ≥200 mg/dL. Obesity was defined as a body mass following formulae: ratio of the thickness=(maximal index(BMI)(weight in kilograms divided by the square plaque thickness/vessel diameter)×100, plaque CSA of the height in meters) of ≥25. =vessel CSA-lumen CSA, plaque burden=(plaque CSA/vessel CSA)×100(Fig. 2). For each variable the Measurement of the carotid IMT B-mode ultrasound measurements were performed with a 10-MHz linear- array transducer, connected to a

D C

B

A

Fig. 2. Measurement of the plaque of the left main coronary artery. Fig. 1. Measurement of the carotid intima-media thickness (IMT). The The plaque of the left main coronary artery was measured at 2 mm values of the maximal (Max) and mean (Mean) intima-media thickness intervals, and the average value calculated. Maximal thickness (A), is automatically calculated using programmed software (M’ATH, ME- Ratio of thickness (%)=Maximal plaque thickness (A)/Vesseldiame- TRIS Co., Argenteuil, France). Q.I.: qualitative index, Std D: stan- ter (B) ×100, Plaque CSA=Vessel CSA (D)-Lumen CSA (C), Burden dard deviation. (%)=Plaque CSA/Vessel CSA (D) ×100. CSA: cross sectional area.

Dae Woo Hyun, et al: Coronary Atherosclerosis is Correlated with Carotid IMT·797 average value was calculated. tion. Hypertension was present in 20(40%), diabetes mellitus in 9(18%), smoking in 27(54%), hypercho- Statistical analysis lesterolemia in 15(30%) and obesity in 16(32%) of All results were expressed as the mean±standard the patients. error of the mean. SPSS 11.0 was used for all statistical Twenty-seven patients(54%) had a one-vessel disease, calculations. Statistical comparisons were performed 17(34%) a two-vessel disease and 6(12%) a three- using Student’s t-tests. Correlations between the varia- vessel disease(Table 1). bles of the carotid IMT and plaque of the LM were evaluated using the Pearson correlation coefficient. A Effect of the risk factors for carotid IMT and LM probability value of <0.05 was taken as statistically sig- plaque nificant. Multiple linear regression analysis was used to With regard to a difference between the genders, test for an association between the plaque burden of the plaque CSA and burden of the LM were 10.9±4.2 the LM and male, hypertension, diabetes, smoking, hy- mm2, 40.9±12.0% in males and 8.2±1.7 mm2, 32.9 percholesterolemia, obesity and the mean right CCA ±6.9% in females, respectively. The plaque CSA and IMT. burden were significantly larger in the males compared to those in the females(p=0.023, p=0.019). In the hy- Results pertensive and normotensive patients, the right maximal and mean carotid IMTs were 1.04±0.17 and 0.82± Baseline characteristics 0.14 mm, and 0.91±0.14 and 0.71±0.11 mm, respec- The mean age of the patients in this study was 59.6 tively. The right maximal and mean carotid IMT were ±9.9 years; 70% were male. The diagnoses of the pa- larger in the hypertensive than normotensive patients tients were 16(32%) with stable angina, 10(20%) with (p=0.005, p=0.006). For diabetes mellitus, there was unstable angina and 24(48%) with myocardial infarc- no significant difference between the patients with and those without in the carotid IMT and plaque of the Table 1. Baseline characteristics LM(Table. 2A). For smoking, the maximal thickness, Age (years) 59.6±9.9 ratio of the thickness, CSA and burden of the LM pla- Male 35 (70%) que were 1.67±0.56 mm, 23.3±7.5%, 11.5±4.4 mm2 2 BMI (kg/m ) 23.9±2.3 and 43.4±11.9%, respectively, in the smokers and Risk factors 1.17±0.29 mm, 16.9±5.4%, 8.4±2.0 mm2 and 32.8 Hypertension 20 (40%) Diabetes mellitus 09 (18%) ±7.2%, respectively, in the non-smokers. The maxi- Smoking 27 (54%) mal thickness, ratio of the thickness, CSA and burden Hypercholesterolemia 15 (30%) of the plaque were larger in the smokers than in the Obesity 16 (32%) nonsmokers(p=0.000, p=0.002, p=0.003 and p= Diagnosis 0.000, respectively)(Table. 2B). In a multiple linear Stable angina 16 (32%) regression analysis, the plaque burden of the LM was Unstable angina 10 (20%) significantly associated with smoking and the right mean Acute myocardial infarction 24 (48%) CCA IMT(p=0.042, p=0.029, respectively)(Table 3). Number of stenotic coronary artery 1 27 (54%) 2 17 (34%) Plaque of the LM related to the presence or absence 3 06 (12%) of carotid plaque BMI: body mass index A carotid plaque was present in 14(28%) patients;

Table 2A. The effects of risk factors in the carotid intima-media thickness and plaque of the left main coronary artery Sex Hypertension Diabetes Male Female (+) (-) (+) (-) Carotid IMT Right max (mm) 0.96±0.18 0.98±0.14 1.04±0.17* 0.91±0.14* 1.07±0.17 0.94±0.16 Right mean (mm) 0.75±0.13 0.76±0.14 0.82±0.14* 0.71±0.11* 0.84±0.15 0.74±0.12 Left max (mm) 0.97±0.12 1.02±0.17 1.00±0.14* 0.98±0.13* 1.06±0.10 0.97±0.14 Left mean (mm) 0.76±0.11 0.76±0.13 0.78±0.13* 0.75±0.10* 0.82±0.09 0.75±0.12 Plaque of LM Max thickness (mm) 1.53±0.56 01.21±0.30 1.54±0.50* 1.37±0.53* 1.58±0.48 1.41±0.53 Ratio of thickness (%) 21.6±7.40 17.5±6.30 20.9±7.10* 20.0±7.5** 22.0±5.8* 20.0±7.60 CSA (mm2) 10.9±4.2* 08.2±1.7* 10.5±3.8** 9.8±3.8* 10.7±3.4* 9.9±3.9 Burden (%) *40.9±12.0* 32.9±6.9* 38.6±11.3* 38.5±11.5* 40.7±7.0* 38.1±12.0 IMT: intima-media thickness, LM: left main coronary artery, Max: maximal, CSA: cross-sectional area. *: p<0.05

798·Korean Circulation J 2005;35:795-800

Table 2B. The effects of risk factors in the carotid intima-media thickness and plaque of the left main coronary artery Smoking Hypercholesterolemia Obesity (+) (-) (+) (-) (+) (-) Carotid IMT Right max (mm) 0.98±0.18 0.95±0.15 1.00±0.18 0.95±0.16 0.98±0.16 0.96±0.17 Right mean (mm) 0.77±0.13 0.74±0.14 0.78±0.17 0.74±0.12 0.77±0.13 0.75±0.13 Left max (mm) 0.99±0.12 1.98±0.15 1.03±0.16 0.97±0.12 1.03±0.15 0.97±0.13 Left mean (mm) 0.77±0.10 0.75±0.12 0.81±0.14 0.74±0.10 0.78±0.11 0.75±0.11 Plaque of LM ± ± ± ± ± ± Max thickness (mm) 01.67 0.56* 01.17 0.29* 1.31 0.31 1.49 0.58 1.40 0.54 1.46 0.52 ± ± ± ± ± ± Ratio of thickness (%) 23.3 7.5* 16.9 5.4* 19.3 5.60 20.8 7.90 20.3 7.40 20.4 7.40 11.5±4.4* 08.4±2.0* 8.6±2.1 10.7±4.20 9.5±2.5 10.4±4.30 CSA (mm2) *43.4±11.9* 32.8±7.2* 36.8±9.10 39.3±12.1 38.3±11.0 38.6±11.5 Burden (%) IMT: intima-media thickness, LM: left main coronary artery, Max: maximal, CSA: cross sectional area. *: p<0.05

Table 3. Stepwise multiple linear regression analysis for the plaque Correlation between the carotid IMT and plaque of burden of the left main coronary artery as a dependent variable the LM B SE (B) p In the right common carotid artery(CCA), the ma- Male 2.814 04.038 0.490 ximal IMT was significantly correlated to the plaque Hypertension -0.546 03.298 0.869 CSA and burden of the LM(r=0.375. p=0.007, r= Diabetes 0.247 03.923 0.950 0.408. p=0.003, respectively)(Fig. 4A, B). The mean Smoking 8.088 03.849 0.042 IMT was significantly correlated to the plaque burden Hypercholesterolemia -0.319 03.276 0.923 (Fig. 4C), but not with the plaque CSA of the LM Obesity -1.036 03.062 0.737 (r=0.357. p=0.011, r=0.264. p=0.063, respectively). Mean IMT, right CCA 28.535 12.625 0.029 In the left CCA, the maximal IMT was not signifi- IMT: intima-media thickness, CCA: cross-sectional area, B: regres- sion coefficient, SE (B): standard error of regression coefficient cantly correlated to the plaque CSA and burden of the LM(p=0.251, p=0.218, respectively). The mean IMT

) was not correlated with the plaque CSA and burden of

p=NS ) p=NS % ( mm the LM(p=0.249, p=0.078, respectively). ( 19.6 22.3 1.38 1.58 Ratio of Ratio Maximal Discussion thickeness

thickeness (-) CCA plaque (+) (-) CCA plaque (+) Carotid artery disease and coronary artery disease

p<0.05 p<0.05 (CAD) are primary manifestations of generalized athe-

)

2 rosclerosis. An association between carotid atheroscle- )

% ( mm 12.2 rosis and coronary atherosclerosis has been demons- ( 43.5 9.3 36.6 1)3)12-14) Plaque CSA trated in several epidemiologic and clinical studies. Plaque burden An increased IMT and plaque development in the (-) CCA plaque (+) (-) CCA plaque (+) extracranial carotid arteries were correlated with the Fig. 3. The plaque of the left main coronary artery (LM) related to the prevalence of coronary artery disease.6-9) Our study in- presence or absence of a carotid plaque. CCA: common carotid artery, CSA: cross sectional area, NS: not significant. vestigated the correlations between coronary atheroscle- rosis, as and carotid atherosclerosis, as detected by a right carotid plaque in 8(16%), a left plaque in 11 IVUS and ultrasonography, respectively. (22%), and both left and right plaques in 5(10%). The IMT was defined as the maximum measurement For the thickness and ratio of the thickness of the LM determined at the far wall between the leading edges plaque, there was no significant difference between the of the lumen-intima and the media-adventitia inter- patients with carotid plaque and those without. The faces. There are many different methods for measuring plaque CSA and burden were 12.2±4.3 mm2 and the carotid IMT. In previous studies, measurement of 43.5±10.7%, respectively in the patient with carotid the IMT was subjective as the operator and the points plaque and 9.3±3.3 mm2 and 36.6±11.0%, respecti- of measurement were poor(less than 10 points).5)6)15) vely, in those patient without. The plaque CSA and In our study, the value of the IMT was automatically burden of the LM were larger in patients with than calculated using programmed software(M’ATH, ME- without carotid plaques(p=0.014, p=0.048)(Fig. 3). TRIS Co., Argenteuil, France)(Fig. 1); thus, the mea- surement of the IMT was objective and the points of

Dae Woo Hyun, et al: Coronary Atherosclerosis is Correlated with Carotid IMT·799

70 22 65 r=0.408 r=0.375 r=0.357

) 60 ) ) p=0.003 2 18 p=0.00 55 p=0.011 % % ( 50 ( mm ( 14 45 40 10 35 30 Plaque burden Plaque CSA 6 25 20 Plaque burden

10 2 15 0.5 0.6 0.7 0.8 0.9 1.0 1.1 1.2 1.3 1.4 0.6 0.7 0.8 0.9 1.0 1.1 1.2 1.3 0.5 0.6 0.7 0.8 0.9 1.0 1.1

A Right maximal IMT (mm) B Right maximal IMT (mm) C Right mean IMT (mm)

Fig. 4. A: correlation between the right carotid intima-media thickness (IMT) and the plaque burden of the left main coronary artery. B: correlation between the right maximal value of the carotid IMT and plaque cross-sectional area (CSA) of the left main coronary artery. C: correlation between the right mean value of the carotid IMT and the plaque burden of the left main coronary artery. measurement were larger(more than 100 points) than vestigates the vascular contours and lumen, ultrasound in previous studies. imaging depicts the structural morphology of the arte- Carotid plaques are related to the risk of cardiovas- rial wall itself. Despite being angiographically silent, cular death or myocardial infarction.15) Kato et al.5) the LM disease detected by IVUS is an independent reported that the prevalence of soft and hard plaques predictor of future cardiac events, which may serve as a was higher in the patients with multiple coronary pla- marker for such events.11) The LM was selected from ques than in those with single plaques. In ACS, they among the coronary arteries, because the evaluation of demonstrated that multiple coronary plaques are asso- whole segments is possible in the left main coronary ciated with positive carotid remodeling. Honda et al.16) artery using IVUS. reported that echolucent carotid plaques, with low in- There are many studies about the relationship bet- tegrated backscatter values, predicted the coronary pla- ween coronary atherosclerosis detected angiographi- que complexity and development of future coronary cally and carotid atherosclerosis.6-9) Carotid IMT mea- complications in patients with stable CAD. These fin- surements can give a comprehensive picture of the da- dings5)15-17) may suggest that carotid plaques may reflect mage caused on the arterial wall by several coronary heart vulnerable coronary lesions. Giral et al.18) reported that disease risk factors over time23) and are an indicator of echographic evaluation of the carotid plaque signifi- generalized atherosclerosis.3) Adams et al.10) reported cantly improved the diagnostic specificity of the exercise that although the carotid IMT is significantly correlated electrocardiography. There are usefulness in predicting with the extent and severity of coronary artery disease, CAD by ultrasonic evaluation of the carotid plaque.17)18) the relationship is only weak. Usually, both CCAs In our study, carotid plaques were found in 28% of were used to evaluate the carotid IMT.3)4)12)13)18)23)24) Some patients. The plaque burden of the LM was larger in the reports25)26) have described that one of the CCAs IMT patient with carotid plaques than in those without(Fig. was correlated with CAD, and was used to evaluate the 4). This finding suggests that the evaluation of the carotid IMT. Ogata et al.27) reported that the average of carotid plaque appears to provide information on the the maximum CCA IMT was significantly correlated diagnosis of CAD. with the LM atherosclerosis evaluated by IVUS. In this An increased carotid IMT is regarded as an early study, the right carotid IMT was more correlated with sign of atherosclerosis. The IMT increases if the vas- the LM plaque than the left carotid IMT. It may seem cular walls are exposed to cardiovascular risk factors, that the right CCA is a shorter distance from the LM such as age, hypercholesterolemia, hypertension and than the left CCA. smoking.19-22) The reduction of the cardiovascular risk This study had some limitations; the sample size was factors inhibits the progression of increases in the small and the patients were a consecutive group under- IMT.4) Because B-mode ultrasound imaging of arterial going . This selection bias means walls is a noninvasive and “patient-friendly” technique, that the correlations between the carotid IMT and CAD it allows for repeated measurements over time in large may not be applicable to the general population. groups of patients. Therefore, the method has become a powerful tool in studies of atherosclerosis. Conclusion Coronary angiography can only indirectly measure There was a significant correlation between the right the degree of atherosclerosis by assessing the lumen carotid IMT and plaque burden of the LM in the pa- size. Therefore, coronary angiography can only quan- tient with CAD. The presence of plaques in the CCAs tify the atherosclerosis at a relatively later stage of in- provides information for diagnosing CAD. These fin- trusive lesion formation. Unlike angiography, which in- dings suggest that the evaluation of the CCA by ultra-

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