Assessment of Coronary Artery Distensibility by Intravascular Ultrasound
Application of Simultaneous Measurements of Luminal Area and Pressure
Background Atherosclerotic change in the coronary artery is associated with an impaired vessel wall distensibility. However, there are few data regarding the relation between vessel wall morphology and distensibility. Therefore, with intravascular ultrasound, we assessed coronary artery distensibility in angiographically normal coronary segments of humans.
Methods and Results Data were analyzed at 35 angiographically normal coronary sites where circumferential or noncircumferential lesions were demonstrated by ultrasound in 22 patients (mean age, 55 years). After intracoronary injection of 500 μg nitroglycerin (NTG), coronary luminal area was measured with intravascular ultrasound (30 MHz, 3.5F to 4.3F, 1800 rpm). Intracoronary pressure was simultaneously measured with a 2F micromanometer-tipped catheter located at the left main coronary artery. The coronary distensibility index was calculated as 10-fold the ratio of luminal area change to intracoronary pressure change during a cardiac cycle. Another pressure-independent vascular stiffness index, β, was derived by the following formula: β=[ln(SBP/DBP)]/(dD/diastolic mean diameter), where SBP is systolic intracoronary pressure, DBP is diastolic intracoronary pressure, and dD is the difference between systolic and diastolic diameters. At the sites where luminal areas were measured, thickness of intima-media complex, defined as the distance between the intimal leading edge and the adventitial leading edge, was determined as an index of the severity of atherosclerosis. In seven segments, distensibility index was determined before and after NTG injection to examine the effect of NTG on coronary distensibility. In all examined sites, including circumferential and noncircumferential lesions, the luminal area was 12.6±5.0 mm2 during systole and 11.6±4.6 mm2 during diastole, and the calculated coronary distensibility index ranged from 0 to 0.83 mm2/mm Hg. The thickness of the intima-media complex ranged from 0.12 to 1.30 mm, suggesting the presence of various grades of atherosclerosis even in the absence of angiographic lesions. There was a poor inverse correlation between thickness of the intima-media complex and distensibility index (r=.19, y=−0.17x+0.41, P=.29). However, when noncircumferential lesions were excluded for evaluation, there was a significant inverse correlation between them (r=.58, y=−0.50x+0.72, P<.01). Under these conditions, the thickness of the intima-media complex also correlated with the value of β (×10−1), which ranged from 0.28 to 3.99 (r=.70). After NTG injection, coronary distensibility increased by an average of 71% in the segments with a thin intima-media complex, whereas it did not substantially change in those with a relatively thick intima-media complex.
Conclusions These results suggest that coronary distensibility is impaired in the coronary sites accompanying occult atherosclerosis, none of which can be detected by the conventional angiography. NTG can augment coronary distensibility in the segments without a markedly thickened intima-media complex. We suggest that thickness of the intima-media complex can contribute to determining the coronary distensibility in clinical settings.
Because atherosclerotic changes in large coronary arteries play a central role in the pathogenesis of myocardial ischemia in coronary heart disease, early detection of the vessel atherosclerosis is of great importance. However, as conventional angiography provides only a silhouette of the vascular lumen, it may be somewhat difficult to assess the early stage of atherosclerosis by this method.1 2
Atherosclerosis of the vessel is a combination of two pathological processes: atheromatous change and sclerotic change. These changes are closely related, and the atheromatous changes in the coronary artery are directly associated with an increase in the vascular wall stiffness.3 Thus, quantitative assessment of vessel stiffness would be an alternative method of predicting the extent of atherosclerotic damage of coronary arteries. Shimazu et al4 reported that with magnified cine coronary angiography, the elastic property of the left main coronary artery (LMCA) could be determined and the elasticity was impaired even in the absence of angiographically significant stenosis. However, angiography requires contrast injection, and continuous observation of a vessel lumen is difficult. Therefore, there might be an inaccurate determination of coronary luminal diameter or cross-sectional area that is essential in the assessment of coronary artery distensibility. In addition, evaluation of the wall morphology is somewhat difficult with angiography.
Intravascular ultrasound is a new method that enables two-dimensional visualization of coronary arteries in real time. Both in vitro and in vivo studies have shown that this method provides accurate determination of coronary artery luminal dimension, cross-sectional area, wall thickness, and wall morphology.5 6 7 8 9 Therefore, with intravascular ultrasound, it is possible to evaluate changes in vascular lumen size, facilitating the quantitation of vascular stiffness of human coronary arteries. In the present study, we attempted (1) to establish a method to quantify the severity of coronary artery sclerosis using intravascular ultrasound and (2) to determine the vascular distensibility associated with circumferential or noncircumferential atherosclerotic lesions in angiographically normal coronary segments. We also examined the effect of nitroglycerin (NTG) on coronary distensibility in the presence or absence of occult atherosclerosis.
The research protocol was approved by the Hospital Medical Ethics Committee of the National Cardiovascular Center (no. 92-04-4), and written informed consent was obtained from all patients. Thirty-three patients who had angiographically normal or minimally irregular segments in the LMCA and in the proximal left anterior descending coronary artery (LAD) were entered into the present study. All were in sinus rhythm. Two patients with an extremely curved LMCA, 3 patients with a small lumen of the LMCA, and 3 patients with critical stenoses in both the left circumflex and the right coronary arteries were excluded from the study. One patient with an extremely tortuous abdominal aorta, which could hamper catheter manipulations, also was excluded. Therefore, 24 patients (22 men and 2 women) comprised the study population. No patient had previously had a myocardial infarction. The age range was 34 to 67 years (mean, 55 years).
Because Zeiher et al10 demonstrated that blood level of HDL could affect the coronary reactivity to vasoactive drugs, plasma levels of total cholesterol and HDL were determined before the examination.
Catheterization was performed with patients in the fasting state. All antianginal drugs were discontinued at least 12 hours before catheterization. After intravenous administration of heparin (3000 U), left and right coronary angiograms were obtained by the standard Judkins method with 5F catheters (Softip; Schneider) inserted from the right femoral artery.
After routine diagnostic angiography from multiple projections, an additional 100 U/kg heparin was administered, and the 5F catheter in the right femoral artery was replaced with an 8F left Judkins-type guiding catheter (Softip, Superflow; Schneider). This catheter was used for insertion of a 3.5F or 4.3F, 30-MHz, 1800-rpm intravascular imaging catheter (Boston-Scientific Corp or Cardiovascular Imaging System Inc) (Fig 1⇓). The imaging catheter was preloaded with a 0.014-in, very flexible, steerable guide wire (USCI). The guide wire was extended beyond the tip of the imaging catheter, and the entire system was passed through the guiding catheter into the left coronary artery.
Measurement of regional pressure in the coronary artery is important for calculation of vessel distensibility. The estimation of intracoronary pressure through the guiding catheter may not be accurate because variations in positioning of the guiding catheter may alter coronary flow and pressure characteristics. Thus, another 5F left Judkins-type catheter was inserted from the left femoral artery, and a 2F micromanometer-tipped catheter (Millar Mikro-Tip Model SPC-320; Millar Instruments) was inserted through this catheter, with its tip located at the LMCA (not at the LAD) for measurement of intracoronary pressure (Fig 1⇑). Therefore, LMCA pressure recordings were acquired while the LAD was imaged.
The baseline vascular motor tone can affect coronary distensibility.4 In the present study, individual variation of the vascular tone was minimized by the administration of NTG. After 1 minute of NTG (500 μg) injection into the left coronary artery, the tip of the imaging catheter was positioned at several angiographically normal sites in the LMCA and/or the proximal portion of the LAD. Minor manipulation of the catheter placement was implemented to position the tip at the center of the lumen. When necessary, a small dose of contrast media was injected through a guiding catheter during imaging to assist in the identification of the lumen-intima boundary.8 This procedure also ensured that insertion of the ultrasound catheter probe had not induced coronary vasospasm. All recordings were completed within 3 minutes after NTG injection, while its vasodilatory effect lasted.11 12
Sites of side branches and vessel bifurcations were not examined. The angular segments also were not examined because in these segments, the ultrasound beam could slice the wall at an oblique angle and, under these conditions, the vessel contour sometimes gets distorted and the blood-intimal boundaries become obscure. In the present study, the sites with calcified lesions also were excluded since the presence of calcification sometimes hampered the measurements due to its acoustic shadowing effect. Ultrasound gain settings were adjusted for optimal visualization of the lumen-intima boundary, and luminal images were acquired without frame averaging.
In seven segments from 7 patients, examinations were performed before and 3 minutes after NTG injection for evaluation of the effect of NTG on coronary distensibility. However, no additional maneuvers to increase or decrease the baseline blood pressure and determine the distensibility at different blood pressure levels were performed.
The ultrasound equipment was modified to display ECGs and pressure waveforms superimposed on the ultrasound image, which ensures coincident pressure and ultrasound dimension measurements (Fig 1⇑). With this system, luminal images as well as ECG (lead II) and intracoronary pressure were recorded on high-quality (sVHS) -in videotape for off-line analysis. Intracoronary pressure was also recorded on a strip chart at 200 mm/s.
The measured segments were divided into subgroups according to the distribution of wall thickening: circumferential if the entire 360 degrees were homogeneously thickened and noncircumferential if the vessel wall was inhomogeneously thickened or only part of the vessel perimeter was involved.
The largest luminal area (systolic luminal area) was determined by tracing the lumen-intima interface at the time of peak intracoronary pressure, and the smallest luminal area (diastolic luminal area) was traced at the time of minimal intracoronary pressure in one cardiac cycle (Fig 1⇑). Although a single frame was used for measurement, review of the dynamic imaging sequence was routinely used to confirm the location of the intimal leading edge.
The systolic and diastolic mean diameters were calculated from those areas with the assumption that the cross section was circular (diameter=2[area/π]1/2). Changes in intracoronary pressure during one cardiac cycle (dP) at the identical beat were measured from the strip-chart recording. The distensibility index of the coronary artery was defined as (dA/dP)×10, where dA is the difference between the largest and the smallest areas. The dA/dP could be influenced by a change in blood pressure. Therefore, another index, β, which is considered to be independent of the changes in blood pressure,13 14 15 was obtained, essentially by normalizing dimension change to the diastolic mean diameter according to the following formula: β=[ln (SBP/DBP)]/(dD/diastolic mean diameter), where SBP is systolic intracoronary pressure, DBP is diastolic intracoronary pressure, and dD is the difference between systolic and diastolic mean diameters.
The severity of vascular atherosclerosis was assessed by the thickness of the intima-media complex in systole.16 17 18 The thickness of the intima-media complex was defined as the distance between the blood-intima interface (the intimal leading edge) and the media-adventitia interface (the leading edge of the next bright layer) (Fig 1⇑). At the segments with circumferential lesions, thickness of the intima-media complex was derived by averaging the values from the two different sites of the same slice. At the segments with noncircumferential lesions, thickness was measured at the site with minimal thickness of the intima-media complex. Area and thickness measurements were performed with an off-line computer system (PC-9801, NEC) equipped with a digitizer. All reported measurements represent the average of three consecutive beats.
Interobserver and Intraobserver Variabilities
Cross-sectional areas of 10 randomly selected sites were measured by two independent observers and by one observer at two separate times. These data were used in the assessment of interobserver and intraobserver variabilities. The results were expressed as a linear regression between the two measurements and as a percent error that was derived as the absolute difference between measurements divided by the initial measurements.19
Data are expressed as mean±SD. The relation between two parameters was evaluated with a linear regression analysis. Paired Student’s t test was used to compare the data in the different conditions of the same segments. We considered the results significant when P<.05.
Quantifiable luminal images were obtained at 17 sites in the LMCA and at 18 sites in the proximal LAD. All sites were angiographically normal. The luminal area in systole is larger than that in diastole, as observed by other methods.4 20 Systolic luminal area ranged from 3.4 to 22.6 mm2 (mean, 12.6±5.0 mm2), and diastolic luminal area ranged from 3.0 to 21.3 mm2 (mean, 11.6±4.6 mm2) (Figs 2⇓, 3⇓, and 4⇓).
Thickness of the intima-media complex varied from 0.12 to 1.30 mm (mean, 0.57±0.29 mm), even in the absence of angiographically significant lesions. It was interesting that the changes in the luminal area during a cardiac cycle appeared to be greater at the sites with a thin intima-media complex (Fig 2⇑) than that at the sites with a relatively thickened intima-media complex, which distributed circumferentially (Fig 3⇑).
Coronary Distensibility Indexes
At the time of imaging, systolic intracoronary pressure ranged 70 to 154 mm Hg, and diastolic intracoronary pressure ranged from 47 to 86 mm Hg. Thus, the calculated distensibility index showed wide variation among each segment with circumferential (n=26) or noncircumferential (n=9) disease (0 to 0.83 mm2/mm Hg). When these values were correlated with thickness of the intima-media complex, there was poor inverse correlation (r=.19, y=−0.17x+0.41, P=.29; Fig 5⇓). Since heterogeneous distribution of atherosclerosis in noncircumferential lesions can affect the whole vessel compliance, noncircumferential lesions were excluded for evaluation. As a result, there was significant inverse correlation between thickness of the intima-media complex and coronary distensibility (r=.58, y=−0.50x+0.72, P<.01; Fig 5⇓). Under these conditions, the value of the pressure-independent stiffness index, β (×10−1), of the circumferential lesions varied from 0.28 to 3.99. Thickness of the intima-media complex showed significant correlation with β, suggesting that an increase in vessel wall thickness could result in a decrease in vessel distensibility (r=.70, y=2.23x−0.31, P<.001; Fig 6⇓).
Plasma levels of total cholesterol and HDL were 221±46 and 36±12 mg/dL, respectively, and there was no significant correlation between these values and coronary distensibility index.
Effect of NTG on Coronary Distensibility
In seven segments from 7 patients, the ultrasound examination was performed before and after NTG injection. All quantitative data are summarized and given in the Table⇓. Before NTG injection, the coronary luminal areas were 10.2±4.7 mm2 in diastole and 11.0±5.2 mm2 in systole. Systolic and diastolic coronary pressures were 114±50 and 72±30 mm Hg, respectively, and the calculated distensibility index was 0.20±0.12 mm2/mm Hg. Three minutes after NTG injection, both systolic and diastolic coronary pressures significantly declined to 93±40 mm Hg and 65±27 mm Hg (P<.01). Under these conditions, the luminal area in diastole was 11.4±5.2 mm2 (P<.05), and that in systole was 12.6±5.7 mm2 (P<.01). Thus, the overall coronary distensibility index increased to 0.39±0.27 mm2/mm Hg (P<.01), or by an average of 71%. However, it should be pointed out that in the segments that exhibited a markedly thickened intima-media complex (patient 7 in the Table⇓), the coronary distensibility index was substantially unchanged after NTG injection.
Interobserver and Intraobserver Variabilities
Interobserver correlation coefficient and the percent error were .96 and 5.6±3.3% for systolic luminal area and .98 and 4.3±2.2% for diastolic luminal area. Intraobserver correlation coefficient and the percent error were .98 and 3.6±3.2% for systolic luminal area and .98 and 3.8±2.4% for diastolic luminal area.
No complications occurred during the catheterization procedures.
Arterial Wall Thickening in Angiographically Normal Sites
Intravascular ultrasound imaging can detect intimal thickening and is suitable for detection of early atherosclerosis, which cannot be detected by conventional angiography.21 22 23 However, when the intimal layer is below the ultrasound resolution, intimal thickness is unmeasurable by intravascular ultrasound.9 22 In addition, because the acoustic property of early intimal thickening is similar to that of media, differentiation of intima from media might be difficult, particularly in the early stage of atherosclerosis.8 24 Under these conditions, thickness of the intima-media complex is considered to represent arterial wall thickness16 17 25 and is used to assess the degree of atherosclerotic change.17 18 26 27
In the present study, the severity of coronary atherosclerosis was assessed according to thickness of the intima-media complex. Even in the circumferential lesion, we observed a wide range in thickness of the intima-media complex (0.12 to 1.30 mm). Fitzgerald et al24 reported that mean values of intimal and medial thickness in mildly diseased coronary segments were 0.243 and 0.210 mm, respectively. On the basis of their findings, more than two thirds of the examined sites in the present study were diseased, although angiography did not reveal such early changes in vessel walls. Thus, as observed by others,8 22 occult atherosclerosis, which could not be assessed by contrast angiography, was present in the examined coronary segments.
Elastic Property of the Coronary Artery
Because the elastic property of the arterial wall has been evaluated by analysis of the relation between luminal diameter and the pressure,14 28 29 precise information on luminal diameter and the pressure at the same site is required. Thus, in the present study, we determined coronary cross-sectional area and mean luminal diameter using a high-frequency intravascular ultrasound system, which allowed continuous observation of luminal images.
It is also important to measure the pressure changes at the sites where the dimension changes are determined because intracoronary pressure has been reported to be higher than the aortic pressure, particularly during systole, although they are identical during diastole.4 Also, positioning of the two guiding catheters may alter regional pressure in the coronary artery. Therefore, for accuracy, we measured intracoronary pressure at the LMCA with a high-fidelity catheter-tip manometer. These procedures should enable us to determine the elastic property of the human coronary artery as precisely as possible.
When we correlated thickness of the intima-media complex with the coronary distensibility index [(dA/dP)×10] in all segments with circumferential or noncircumferential lesions, there was poor correlation. However, after excluding the segments with noncircumferential lesions, there was significant inverse correlation between thickness of the intima-media complex and coronary distensibility. It is possible that the heterogeneous plaque distribution at the site with noncircumferential lesions may alter regional vessel compliance, resulting in inaccurate estimation of total coronary distensibility by the present method. Local vessel wall distensibility should be determined in these noncircumferential lesions.30
It is possible that even in the segments with circumferential lesions, the changes in blood pressure may affect the measured dA/dP. However, the value of another index, β, which is relatively independent of the pressure changes, also correlated with thickness of the intima-media complex. This suggests that the mechanical properties of the coronary artery can be influenced by thickening of the intima-media complex associated with or not associated with occult atherosclerosis, which cannot be identified by angiography.
Recently, Zeiher et al10 reported that the degree of abnormal local vascular reactivity to acetylcholine is closely related to the extent of atherosclerosis and that elevated serum HDL can ameliorate abnormal vasoconstriction at any given extent of atherosclerotic lesions. However, the mechanical property of vessel wall, which can be represented by distensibility index, appears to be independent of the blood level of HDL, as observed in the present study. These lipids may react with extrinsic stimuli such as acetylcholine to alter the vessel wall function, although we did not examine the effect of acetylcholine in the present study.
Shimazu et al4 indicated that with angiography, coronary distensibility was altered by NTG. In the present study, we also observed that NTG could increase coronary distensibility in normal or mildly diseased segments. However, in the segments with a markedly thickened intima-media complex, distensibility was substantially unchanged after NTG. In these segments, NTG-induced vasodilation also was impaired (Table⇑). Thus, the impaired increase in coronary distensibility after NTG in severely diseased segments may be caused, in part, by the effect of medial smooth muscle atrophy, a feature characteristic of advanced atherosclerotic lesions.31
We found that distensibility of the vessel was reduced even if the coronary angiography did not show any luminal abnormalities. Also, changes in the distensibility indexes were more prominent than those in arterial wall thickness. Therefore, one might speculate that vessel distensibility shown in the present study could be an alternate index representing the pathological process of atherosclerosis.
We previously reported that atherosclerosis is present at the site of focal vasospasm, even in the absence of angiographic disease.32 The quantitative analysis of the effect of vasoactive drugs such as ergonovine on vessel distensibility can provide further information about the correlation between the extent of atherosclerosis and vessel wall reactivity, although positioning of the intracoronary catheter at the time of the ergonovine provocative test is somewhat difficult in clinical settings.
In the present study, vessel distensibility in the LAD as well as in the LMCA was evaluated. Although measurements of intracoronary pressure in the LAD may be necessary to assess coronary distensibility of the LAD, we measured the pressure in the LMCA instead of in the LAD. However, because the data-obtaining site in the LAD was close to the LMCA, intracoronary pressure in the LAD would be almost identical to that in the LMCA. The use of a pressure-manometer catheter with a movable guide wire33 may have reduced the technical difficulties associated with measurement of distal coronary pressure.
We did not determine regional vessel distensibility but rather total vessel distensibility. However, as shown at the sites with noncircumferential lesions, distensibility in the diseased arc can be different from that in the relatively normal arc. This regional difference in distensibility may induce cardiac cycle-related plaque deformation, resulting in plaque rupture and acute coronary events associated with myocardial infarction or unstable angina.34 Determination of regional wall distensibility in noncircumferential lesions may provide further insight into the mechanism of acute coronary events.30
The present data indicated that thickness of the intima-media complex could be one of the determinants of human coronary distensibility. However, an intrinsic vessel wall property also should be considered, because an increase in the stiffness of arteries can be related to not only increased wall thickness but also structural changes, such as an increased ratio of collagen to elastin, associated with deficiency of the vessel wall elements.35 Combination of the intravascular ultrasound study with tissue characterization of the arterial wall36 will be necessary to define the role of intrinsic factors in determining vessel distensibility.
Other factors that might influence the distensibility also should be considered. These factors include patient age,37 the absolute levels of intracoronary pressure, and the presence of calcification. Further studies, in which a large number of patients should be studied with the multivariate analysis method, will be necessary to consider the role of these variables in determining coronary distensibility.
Coronary artery distensibility was assessed in angiographically normal sites with the use of intravascular ultrasound. It is evident that coronary artery distensibility can in part depend on thickness of the intima-media complex associated with or not associated with occult disease. We suggest that measurements of the coronary distensibility can provide further quantitative estimation of the extent of atherosclerosis in coronary artery disease.
This work was supported in part by grants from the Japan Heart Foundation (Dr Yamagishi), Tokyo; Shimadzu Scientific Foundation (Dr Yamagishi), Kyoto; and Takeda Medical Research Foundation (Dr Miyatake), Osaka, Japan. We thank Sachiko Suzuki and Yoriko Hashimoto for their skillful secretarial assistance.
Presented in part at the 42nd Annual Scientific Sessions, American College of Cardiology, Anaheim, Calif, March 1993.
- Received October 12, 1994.
- Revision received December 8, 1994.
- Accepted December 27, 1994.
- Copyright © 1995 by American Heart Association
Caro CG, Pedley TJ, Schroter RC, Seed WA. The systemic arteries. In: Caro CG, Pedley TJ, Schroter RC, Seed WA, eds. The Mechanics of the Circulation. New York, NY: Oxford University Press; 1978:243-349.
Nissen SE, Grines CL, Gurley JC, Sublett K, Haynie D, Diaz C, Booth DC, DeMaria AN. Application of a new phased-array ultrasound imaging catheter in the assessment of vascular dimensions: in vivo comparison to cineangiography. Circulation. 1990;81:660-666.
Nissen SE, Gurley JC, Grines CL, Booth DC, McClure R, Berk M, Fischer C, DeMaria AN. Intravascular ultrasound assessment of lumen size and wall morphology in normal subjects and patients with coronary artery disease. Circulation. 1991;84:1087-1099.
Zeiher AM, Schachinger V, Hohnloser SH, Saurbier B, Just H. Coronary atherosclerotic wall thickening and vascular reactivity in humans: elevated high-density lipoprotein levels ameliorate abnormal vasoconstriction in early atherosclerosis. Circulation. 1994;89:2525-2532.
Hausmann D, Mügge A, Fitzgerald PJ, Yock PG, Daniel WG. Nitroglycerin-induced coronary vasodilation in heart transplant patients is impaired by intimal thickening. J Am Coll Cardiol. 1993;21:334A. Abstract.
Hayashi K, Sato M, Handa H, Moritake K. Biomechanical study of the constituitive laws of vascular walls. Exp Mechan. 1974;14:440-444.
Hirai T, Sasayama S, Kawasaki T, Yagi S. Stiffness of systemic arteries in patients with myocardial infarction: a noninvasive method to predict severity of coronary atherosclerosis. Circulation. 1989;80:78-86.
Pignoli P, Tremori E, Poli A, Oreste P, Paoletti R. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation. 1986;74:1399-1406.
Poli A, Tremori E, Colombo A, Sirtori M, Pignoli P, Paoletti R. Ultrasonographic measurement of the common carotid artery wall thickness in hypercholesterolemic patients: a new model for the quantitation and follow-up of preclinical atherosclerosis in living human subjects. Atherosclerosis. 1988;70:253-261.
Handa N, Matsumoto M, Maeda H, Hougaku H, Ogawa S, Fukunaga R, Yoneda S, Kimura K, Kamada T. Ultrasonic evaluation of early carotid atherosclerosis. Stroke. 1990;21:1567-1572.
Vatner SF, Pagani M, Manders WT, Pasipoularides AD. Alpha adrenergic vasoconstriction and nitroglycerin vasodilation of large coronary arteries in the conscious dog. J Clin Invest. 1980;65:5-14.
St Goar FG, Pinto FJ, Alderman EL, Valantine HA, Schroeder JS, Gao SZ, Stinson EB, Popp RL. Intracoronary ultrasound in cardiac transplant recipients: in vivo evidence of ‘angiographically silent’ intimal thickening. Circulation. 1992;85:979-987.
Fitzgerald PJ, St Goar FG, Connolly AJ, Pinto FJ, Billingham ME, Popp RL, Yock PG. Intravascular ultrasound imaging of coronary arteries: is three layers the norm? Circulation. 1992;86:154-158.
Kawano S, Yamagishi M, Nakatani S, Tamai J, Kawaguchi A, Hao H, Yutani C, Miyatake K. Comparison of intravascular ultrasound images of human coronary arteries obtained by mechanical rotating and synthetic aperture array systems—in vitro and in vivo observations. J Am Coll Cardiol. 1993;21:449A. Abstract.
Wendelhag I, Wiklund O, Wikstrand J. Arterial wall thickness in familial hypercholesterolemia: ultrasound measurement of intima-media thickness in the common carotid artery. Arterioscler Thromb. 1992;12:70-77.
Imura T, Yamamoto K, Satoh T, Kanamori K, Mikami T, Yasuda H. In vivo viscoelastic behavior in the human aorta. Circ Res. 1990;66:1413-1419.
Umeno T, Yamagishi M, Nakatani S, Uematsu M, Goto Y, Miyatake K. Intravascular ultrasound evidence for importance of plaque distribution in determining regional coronary vessel distensibility. Circulation. 1994;90(suppl I):I-164. Abstract.
Mizushige K, DeMaria AN, Matsuo H. Evaluation of coronary arterial morphology using intravascular ultrasound. Jpn Circ J. 1995;58:1177-1180.
Learoyd BM, Taylor MG. Alterations with age in the viscoelastic properties of human arterial walls. Circ Res. 1966;18:278-292.
Fitzgerald PJ, Koren J, McKenzie JR, Beyhan NU, Moore TC, Yock PG. Combined catheter ultrasound imaging with on-line tissue characterization: feasibility study. Circulation. 1991;84(suppl II):II-372. Abstract.