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(Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:1393-1398.)
© 1996 American Heart Association, Inc.

Articles

Coronary Artery Restenosis After Balloon Angioplasty in Humans Is Associated With Circumferential Coronary Constriction

Huai Luo; Toshihiko Nishioka; Neal L. Eigler; James S. Forrester; Michael C. Fishbein; Hans Berglund; Robert J. Siegel

the Division of Cardiology, Cedars-Sinai Medical Center, Los Angeles, Calif.

Correspondence to Robert J. Siegel, MD, Division of Cardiology, Room 5335, Cedars-Sinai Medical Center, 8700 Beverly Blvd, Los Angeles, CA 90048.

	Abstract

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Therapies that inhibit intimal hyperplasia do not prevent restenosis after coronary artery balloon angioplasty, suggesting that additional mechanisms may be responsible for restenosis in humans. Using an intravascular ultrasound (Hewlett-Packard Sonos Intravascular Imaging System), 3.5F, 30-MHz (Boston Scientific) monorail imaging catheter, we studied 17 patients with clinical and angiographic restenosis at an average (mean±SD) of 7±6 months after balloon angioplasty (13 men: age, 71±10 years; 12 left anterior descending coronary arteries, 4 right coronary arteries, and 1 left circumflex coronary artery). The lumen area (LA), vessel wall area (VWA), and total cross-sectional area (CSA) within the external elastic lamina were measured at the restenosis site and at proximal and distal reference sites, which were defined as adjacent segments with the least amount of plaque. Consistent with coronary angiography findings, decreased LA at the restenotic site was detected in all 17 patients. The unique finding was that total CSA at the restenotic site was significantly decreased compared with both proximal and distal reference sites (10.1±2.4 versus 14.8±3.2 mm² and 10.1±2.4 versus 13.8±3.1 mm², respectively, P<.001), whereas VWA (intima plus media) was slightly increased at the angioplasty site compared with both proximal and distal reference sites (8.0±2.3 versus 7.6±2.3 mm² and 8.0±2.3 versus 6.7±2.3 mm², respectively, P=NS). Eighty-three percent of the loss in LA at the restenotic site was due to constriction of the total CSA, while the increase in VWA at the restenotic site accounted for only a 17% loss in LA. We then compared these results with the morphology of coronary artery segments in 14 patients without restenosis. These coronary artery segments had been previously treated with balloon angioplasty (7±5 months). Unlike that in restenotic lesions, the total CSA within the external elastic lamina at the sites of previous angioplasty was similar to that in distal and proximal reference sites (P=NS). Significant and consistent reduction in arterial CSA, with a minor increase in VWA, characterizes human coronary lesions that cause angiographic restenosis. These data suggest that in humans, "recoil" and/or vascular contraction with healing in response to balloon injury is a major contributor to restenosis after balloon angioplasty.

Key Words: coronary restenosis • balloon angioplasty • intravascular ultrasound

	Introduction

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Balloon injury to arteries in animals causes intimal hyperplasia, which within weeks partially obstructs the vessel lumen.¹ Autopsy studies of restenosis in humans^{2 3} and atherectomy samples of tissue from restenotic sites ⁴ typically show intimal hyperplasia. For this reason, restenosis in humans has been attributed to injury-induced intimal hyperplasia.⁵ However, clinical studies to date, which have been focused on inhibiting SMC proliferation to prevent restenosis, have not reduced the frequency of restenosis.^{6 7} These data suggest that either the therapies to reduce intimal hyperplasia are ineffective or that additional mechanisms are responsible for restenosis in humans.^{7 8} Arterial remodeling has been reported to be one such important determinant, in both animal studies after peripheral arterial balloon angioplasty^{9 10 11} and patients after multiple coronary transcatheter therapies.^{12 13 14} Previous IVUS studies on coronary arterial remodeling after restenosis have compared mean values in a large number of patients but have not evaluated the relationship between LA and VWA in individual vessels. The purpose of this IVUS study was to (1) compare the LA, VWA, and total CSA at the restenotic site with distal and proximal reference sites in the same vessel and (2) determine whether these relationships were different in restenosis versus nonrestenosis lesions.

	Methods

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Patients
Seventeen consecutive, symptomatic patients with restenosis 7±6 months after PTCA underwent IVUS examination in the cardiac catheterization laboratory from October 1992 to September 1995 (13 men and 4 women; age, 71±10 years; 12 left anterior descending coronary arteries, 4 right coronary arteries, and 1 left circumflex coronary artery). Only patients in whom the precise location of the previous PTCA could be ascertained by multiple orthogonal angiographic views and with lesions far enough from side branches (1 to 2 cm) to allow both proximal and distal reference sites to be measured were selected. Patients with insulin-dependent diabetes mellitus or severe familial hypercholesterolemia with premature coronary atherosclerosis were excluded. At the time of the initial PTCA procedure, 13 patients had stable angina, 2 had unstable angina, and 2 had a recent myocardial infarction (1 day old). At the time of follow-up angiography and IVUS, all 17 patients had clinical evidence of recurrent ischemia. All 17 had recurrent exertional chest pain, and 9 of 10 patients had positive ECG/TI or echocardiographic stress tests.

The control group of nonrestenotic lesions was obtained in 14 patients (without insulin-dependent diabetes mellitus or familial hypercholesterolemia) in whom PTCA of 2 separate lesions in the same vessel had been performed 7±5 months previously (11 men and 3 women; age, 65±17 years; 4 left anterior descending coronary arteries, 7 right coronary arteries, and 3 left circumflex coronary arteries). In these patients 1 prior balloon angioplasty site had no angiographic evidence of restenosis. When IVUS was performed on a treated restenotic lesion, the previous angioplasty site without angiographic restenosis also was imaged by IVUS. At the time of initial PTCA in the control group, 12 patients had stable angina, 1 had unstable angina, and 1 had a recent acute myocardial infarction (1 day old). Of the 7 patients who underwent ECG/TI or echocardiographic stress testing, all were positive for myocardial ischemia. At the time of restudy, 8 of 8 patients had positive stress tests.

IVUS System, Imaging Procedure, and Image Analysis
IVUS imaging of restenotic lesions was performed immediately after diagnostic angiography. All patients gave written, informed consent before the procedure. A 3.5F, 30-MHz ultrasound catheter (Boston Scientific Corp) was used to provide two-dimensional tomographic images. The imaging catheter was inserted through a guiding catheter over a 0.014-in. guide wire to 2 cm beyond the stenotic lesion. Images were recorded on 0.5-in. super VHS videotape as the catheter was pulled back slowly (1 mm/s) from the distal segment through the lesion into the proximal vessel. While IVUS recordings were obtained on a continuous pullback, IVUS measurements were made at a single cross-sectional imaging plane at the angioplasty site as well as at proximal and distal reference sites. Before and after the ultrasound procedure, 100 to 200 µg IC nitroglycerin was given. Coronary angiography of the imaged vessel was repeated after IVUS. Images were analyzed off-line with a Hewlett-Packard Sonos System. Because acoustic "shadowing" can make IVUS measurements difficult, patients with calcified plaque deposits in >60° of the 360° of arterial circumference were excluded.¹⁵ Proximal and distal reference sites were defined as those segments adjacent to the restenotic lesion site with the least amount of plaque and that were 1 to 2 cm from side branches. The minimal lumen diameter was used for calculation of diameter stenosis.

LAs and total CSAs (both in millimeters squared) within the EEL were measured at the restenotic site and proximal and distal reference sites. VWA was defined as total CSA minus LA. The lumen loss at the restenotic site could be due to an increase in VWA and/or a reduction in total CSA. Under the assumption that the blood vessel gradually tapers from its proximal to its distal end, the lumen loss (difference) at the restenotic site was defined as the mean LA at the proximal and distal reference sites minus LA at the restenotic site. "VWA difference" at the restenotic site was defined as the VWA at the restenotic site minus mean VWA at proximal and distal reference sites. The total "CSA difference" was defined as the mean total CSA at the proximal and distal reference sites minus total CSA at the restenotic site. The relative contributions of remodeling and intimal hyperplasia to lumen loss were calculated as [(total CSA difference/lumen loss)x100] and [(VWA difference/lumen loss)x100], respectively.

Interobserver and intraobserver reproducibility of such measurements has been previously demonstrated in our laboratory to have correlation coefficients (r) .96^{16 17} and a 1.6% to 3.1% mean difference.¹⁸ The accuracy of IVUS for our laboratory^{16 17 18 19} agrees with the reports of others.^{20 21 22 23} We have previously shown by microdissection techniques that IVUS can delineate the EEL.²⁴ Blinded measurements of restenotic, proximal, and distal vessel segments were made by consensus of three observers.

Coronary Angiographic Analysis
Quantitative coronary angiography was performed on 17 patients at the time of the initial PTCA and at follow-up, with identification of the restenosis. Images were magnified, acquired by a video camera (Vanguard Instrument), and digitized on an Imagecomm Systems Processor. The image of the guide catheter was used for calibration. Percent diameter stenoses were obtained by measuring minimal diameter and mean diameter of the closest, most disease-free segment, and this segment was used as a "normal" reference.²⁵ Angiographic restenosis was defined as a previously treated lesion with either >50% stenosis or >50% loss of the initial angiographic diameter gain.⁴

Statistics
Differences between mean IVUS values among the three sites (angioplasty, proximal, and distal) were tested by repeated-measures ANOVA with appropriate contrasts. A paired t test was performed to compare angiographic changes on distal and proximal reference vessel sizes between the initial procedure and follow-up. All data are presented as mean±SD.

	Results

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IVUS Imaging
Fig 1A shows quantitative IVUS images from a coronary artery restenotic lesion from which measurements were derived. There is a fibrous plaque with focal calcification at the site of restenosis. The total coronary artery CSA measured at the EEL is smaller at the restenotic site than at proximal and distal reference sites. The case example in Fig 1B shows findings for a patient in the control group without restenosis after PTCA. Here, the LA, VWA, and total artery CSA at the previous angioplasty site are similar to those at proximal and distal reference sites.

View larger version (119K): [in this window] [in a new window]   Figure 1. A, IVUS images of the left anterior descending coronary artery from patient No. 11, 10 months after balloon angioplasty. Left, Proximal reference site; middle, restenosis site; and right, distal reference site. Images show a fibrous plaque with heavy calcification at the restenosis site. Area within the EEL (arrows) was 13.4 mm2 at the proximal reference site, 7.6 mm2 at the restenotic site, and 11.3 mm2 at the distal reference site. "C" identifies the IVUS catheter within the arterial lumen. B, IVUS images of the right coronary artery from patient No. 9, 3 months after balloon angioplasty. Left, Proximal reference site; middle, previous angioplasty site; and right, distal reference site. Images show a concentric, fibrous plaque inside the vessel lumen. Area within the EEL was 14.9 mm2 at the proximal reference site, 13.3 mm2 at the previous angioplasty site, and 13.0 mm2 at the distal reference site.

Fig 2A shows the data for all 17 restenosis patients. The LA at the restenotic site is significantly (P<.001) smaller than that at reference proximal (2.1±0.8 versus 7.2±1.8 mm²) and distal (2.1±0.8 versus 7.1±2.1 mm²). sites. The total artery CSA is less compared with that at the proximal reference site (10.1±2.4 versus 14.8±3.2 mm², P<.001) and distal reference site (10.1±2.4 versus 13.8±3.1 mm², P<.001). There was a trend for VWA at the restenosis site to be slightly greater than that at either proximal (8.0±2.3 versus 7.6±2.3 mm², P=NS) or distal (8.0±2.3 versus 6.7±2.3 mm², P=NS) reference site.

View larger version (52K): [in this window] [in a new window]   Figure 2. A, IVUS assessment of coronary arteries with restenosis and comparison of LA, VWA, and total CSA within the EEL at the proximal reference site, restenotic site, and distal reference site. B, IVUS assessment of coronary arteries without restenosis and comparison of LA, VWA, and total CSA within the EEL at the proximal reference site, restenotic site, and distal reference site.

Fig 2B shows data for the 14 control patients. The LA at the previous angioplasty site is not significantly smaller than that at either the proximal (8.0±2.4 versus 9.4±2.7 mm², P=NS) or distal (8.0±2.4 versus 9.2±2.0 mm², P=NS) reference site; the VWA at the angioplasty site is not significantly greater than that at the proximal (6.8±2.8 versus 6.4±2.6 mm², P=NS) or distal (6.8±2.8 versus 5.3±3.0 mm², P=NS) reference site; and the total artery CSA at the previous angioplasty site is similar to that at both the proximal (14.8±3.9 versus 15.8±3.7 mm², P=NS) and distal (14.8±3.9 versus 14.5±4.2 mm², P=NS) reference sites.

Table 1 lists the clinical and IVUS measurements for all 17 patients with clinical and angiographic restenosis. In each patient arterial CSA at the restenosis site was smaller than that at both proximal and distal reference sites. The mean reduction in LA at the restenotic site was 5.1 mm². Of this total lumen loss, 4.2 mm², or 83%, was due to a reduction in total CSA (constriction), whereas the increase in VWA accounted for only 0.9 mm², or 17%, of the loss in LA. For comparison, clinical and IVUS measurements for all 14 control patients are shown in Table 2. After the IVUS procedure and subsequent administration of intracoronary nitroglycerin, there was no measurable change in coronary angiographic percent diameter stenosis at the restenosis site in any of the 17 patients.

View this table: [in this window] [in a new window]   Table 1. Clinical and IVUS Findings in 17 Patients With Coronary Artery Restenosis

View this table: [in this window] [in a new window]   Table 2. Clinical and IVUS Findings in 14 Patients Without Coronary Artery Restenosis

Quantitative Coronary Angiography
For the 17 restenosis patients, at initial PTCA the mean pretreatment diameter stenosis was 90±7%, with a residual stenosis of 25±13% after initial angioplasty. At follow-up angiography, there was a 75±8% angiographic diameter stenosis. In comparison, the mean diameter stenosis by IVUS was 65±5% and the area stenosis by IVUS 87±7%.

For the 14 control patients, at initial PTCA the mean pretreatment diameter stenosis was 85±5%, with a residual stenosis of 25±4% after angioplasty. At the time of IVUS imaging 7±5 months later, there was a 25±7% angiographic diameter stenosis. In comparison, the mean diameter stenosis by IVUS was 30±9% and the area stenosis by IVUS 45±13%.

For the entire group of 31 patients (17 with restenosis and 14 control cases), from the initial procedure to follow-up there was no significant angiographic change in distal reference vessel size (2.26 versus 2.33 mm, P=NS) or proximal reference vessel size (2.42 versus 2.44 mm, P=NS).

	Discussion

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This study shows that the magnitude of reduction in total coronary artery CSA greatly exceeds the magnitude of increase in VWA in patients with restenosis. Restenotic lesions were associated with a 29% decrease in total CSA compared with adjacent (angiographically normal) reference sites. This total CSA reduction accounted for 83% of LA loss. Although VWA at the restenotic site was not significantly greater than that at either the proximal or distal reference segment, it accounted for 17% of LA loss. Since total CSA reflects the external circumference of the vessel and VWA reflects intimal hyperplasia, the data suggest that the loss of external circumference is quantitatively more important than intimal hyperplasia in the pathogenesis of restenosis.

Experimental data in rabbits support our findings. Post et al⁹ found that lumen narrowing after balloon injury predominantly resulted from a reduction in the circumferential dimension of the entire artery and that intimal hyperplasia was only a minor factor. Kakuta et al¹⁰ showed that differences in compensatory enlargement, not intimal hyperplasia, accounted for restenosis in a hypercholesterolemic rabbit model. Furthermore, Lafont et al¹¹ found that late residual stenosis was correlated with chronic constriction (P=.003) but not with neointimal-medial growth or adventitial growth. These findings suggest that factors related to arterial remodeling rather than neointimal-medial growth dominate the response to angioplasty.

Mintz et al¹³ compared plaque burden and vessel size in de novo and restenotic lesions in a pooled study that included plaque debulking procedures, ie, directional coronary atherectomy, rotational atherectomy, and excimer laser angioplasty, with and without balloon angioplasty. They did not find large amounts of myointimal tissue in restenotic lesions and concluded that elastic recoil and changes in vessel geometry might play a proportionately greater role than intimal hyperplasia in restenosis.

There may, however, be differences in the mechanisms responsible for restenosis after balloon-induced stretch and atheroma debulking. Di Mario et al¹⁴ compared serial IVUS findings after directional coronary atherectomy with those after balloon angioplasty alone. IVUS images were obtained during the initial intervention and at 6-month follow-up whether or not restenosis was present. In the directional coronary atherectomy–treated lesions, plaque growth predominated, whereas in the post–balloon angioplasty group, remodeling appeared to account for most of the restenosis. However, the average percent diameter stenosis in this group was only 45±11% at follow-up, and the clinical restenosis rate was not reported. In our study all 17 patients had clinical restenosis with a mean angiographic diameter stenosis of 74±9%, and all had restenosis by IVUS. Our study is the first to show that in patients with clinical coronary restenosis after isolated balloon angioplasty, there is a consistent reduction in total CSA as shown by IVUS.

In de novo coronary artery stenoses, compensatory enlargement frequently occurs in response to intimal hyperplasia, thus preserving the LA.^{26 27 28} However, McPherson et al²⁹ found that 20% of de novo coronary artery stenoses had a smaller arterial area at the lesion site than at the reference site. Nishioka et al³⁰ from our laboratory found similar results in 26% of de novo lesions. These studies suggest that in a significant minority of cases, constriction of arterial size occurs in de novo stenoses and precedes the appearance of circumferential narrowing with restenosis.

In our study, although we were unable to determine the mechanisms responsible for the arterial narrowing associated with restenosis, there are several possibilities. Intracoronary nitroglycerin did not affect the angiographic appearance of any of the 17 restenotic segments, suggesting that an increase in coronary vascular tone or artifactual local vasoconstriction induced by the imaging procedure is unlikely. A second possible cause of circumferential narrowing is fibrotic constriction. While there are no published histological data from human studies that document postangioplasty fibrosis in the region of the EEL or adventitia, recent data from animal studies now support this concept.^{9 10 11} In a histopathological study in rat common carotid arteries, Clowes et al³¹ showed that luminal narrowing 2 weeks after balloon injury was largely due to contraction associated with the proliferation of arterial SMCs. These authors suggested that this phenomenon might be analogous to scar contraction caused by myofibroblasts in skin wounds. The histopathological findings after balloon-induced arterial injury reported by Lafont et al,¹¹ Post et al,⁹ and Kakuta et al¹⁰ are also consistent with this concept. A third possible explanation for circumferential arterial narrowing is loss of medial mass secondary to injury-induced SMC dropout in the media. This hypothesis is consistent with Mintz's observation that the loss of CSA in coronary arteries seemed to be independent of the device used for angioplasty. Finally, a likely cause in 20% to 25% of patients is preexisting reduction of total artery CSA before angioplasty.^{29 30}

An advantage of our study is that we measured sites proximal and distal to the restenosis, which allowed us to assess segmental variations in total CSA, VWA, and LA for each vessel. There are pitfalls in pooling lumen diameter measurements from vessels of different size. As noted by Losordo et al,³² arterial size varies according to many factors, including age, sex, body weight, height, blood pressure level, plasma lipid concentration, degree of vessel proximity, and blood flow. In our study, by comparing the proximal reference site, restenotic lesion site, and distal reference site for a given arterial segment, the potentially confounding influence of these variables was reduced. On the other hand, one limitation of our study is that we did not perform serial IVUS recordings before and 7 months after balloon angioplasty. A longitudinal study using serial IVUS examinations in symptomatic and asymptomatic patients 3 to 6 months after balloon angioplasty would provide more definitive information on the roles of constriction of the arterial circumference in association with restenosis. Finally, introduction of a catheter across a lesion may artifactually change lesion geometry by either falsely enlarging the lumen or reducing perfusion pressure, thereby causing a secondary change in vessel diameter. Such artifacts may be unresponsive to nitroglycerin.

At present, therefore, we hypothesize that restenosis includes the following components: intimal hyperplasia, recoil without fibrosis, and an as-yet-undocumented vasoconstriction or constrictive fibrosis with or without medial SMC loss. It is possible that all of these mechanisms are operative to varying degrees in different patients. Our findings indicate that regardless of mechanism, loss of CSA within the EEL appears to be a major contributor to lumen loss in restenosis, independent of the contribution of intimal hyperplasia.

	Selected Abbreviations and Acronyms

 

CSA(s) = cross-sectional area(s) ECG = electrocardiographic EEL = external elastic lamina IVUS = intravascular ultrasound LA(s) = lumen area(s) PTCA = percutaneous transluminal coronary angioplasty SMC(s) = smooth muscle cell(s) TI = thallium imaging VWA(s) = vessel wall area(s)

	Acknowledgments

 
This study was supported in part by the Lee E. Siegel, MD, Memorial Fund; the Herbert Stein, MD, Research Fund; and the Western Cardiac Fund (to Dr Luo). Dr Nishioka is a recipient of the Japanese Self-Defense Forces Central Hospital Award.

	Footnotes

 
Presented in part at the 67th Scientific Session of the American Heart Association, Dallas, Tex, November 14-17, 1994, and published in abstract form in Circulation (1994;4[pt 2]:I-61).

Received December 6, 1995; revision received March 22, 1996;

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