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Arterioscler Thromb Vasc Biol. Author manuscript; available in PMC Jul 1, 2013.
Published in final edited form as:
PMCID: PMC3558937
NIHMSID: NIHMS385877
Potential quantitative MR imaging biomarkers of coronary remodeling in older hypertensive patients
Kai Lin, MD, MS,1 Donald M. Lloyd-Jones, MD, MS,2 Ying Liu, MD, PhD,1 Xiaoming Bi, PhD,3 Debiao Li, PhD,1* and James C. Carr, MD1
1Department of Radiology, Northwestern University, 737 N Michigan Avenue, Suite 1600, Chicago, IL 60611
2Department of Preventive Medicine, Northwestern University, 680 N Lake shore drive, Suite 1400, Chicago, IL 60611
3Cardiovascular MR R&D, Siemens Healthcare, 737 N Michigan Avenue, Suite 1600, Chicago, IL 60611
Address for correspondence: Kai Lin, kai-lin/at/northwestern.edu, Department of Radiology, Northwestern University, 737 N Michigan Avenue, Suite 1600, Chicago, IL 60611, Tel: (312)363-8469, Fax: (312)926-5991
*Current address: Cedars Sinai Medical Center, 8700 Beverly Blvd., Los Angeles, CA 90048
Objective
To detect differences in potential magnetic resonance (MR) imaging biomarkers of coronary remodeling between older hypertensive patients and healthy controls
Methods and results
Two-dimensional black-blood coronary wall MR imaging and three-dimensional whole-heart coronary MR angiography were performed on 130 participants (65–84 years), including 65 hypertensive patients and 65 healthy controls. Coronary segments derived from hypertensive participants had a higher mean coronary wall thickness, a smaller vessel area, a smaller coronary wall area, a smaller lumen area, a lower coronary distensibilit index (CDI) and a higher percent of the coronary wall occupying the vessel area (PWOV) than those from healthy controls. When the average PWOV was set as an ad hoc cutoff point, coronary segments with a high PWOV had a significantly higher mean wall thickness, a higher maximum wall thickness, a smaller vessel area, a smaller lumen area, a lower CDI and a higher coronary plaque index (CPI) compared with coronary segments with a low PWOV.
Conclusion
MR techniques are able to noninvasively detect significant differences in potential imaging biomarkers of coronary remodeling between older hypertensive patients and healthy aging controls. The PWOV is a promising remodeling feature for quantitatively evaluating the progression of coronary atherosclerosis.
Keywords: MR imaging, coronary remodeling, imaging biomarker, hypertension
Vascular remodeling is considered to be an active modification of the vessel wall in response to changes in its milieu1, 2. Such a long-term alteration of the vascular structure has been linked to the development of atherosclerotic cardiovascular diseases2. Various traditional cardiovascular risk factors, including hypertension, are able to remarkably accelerate vascular remodeling3, 4. In contrast, intensive treatments may retard or reverse this progression57. Therefore, features of vascular remodeling are expected to serve as biomarkers for quantitatively evaluating the progression of cardiovascular diseases8.
The coronary artery is one of the most important components of the cardiovascular system, and its remodeling has been recognized as a strong predictor of clinical events9. Although characterizations of coronary plaques have been described in patients with coronary artery disease (CAD)10, 11, the morphological and biomechanical changes of the remodeled coronary wall have not been comprehensively investigated in apparently healthy individuals without documented or suspected cardiovascular disease. This knowledge gap exists mainly because of the limitations of clinical methodologies. X-ray exposure and invasive examinations are major drawbacks of various clinical methods, including intravascular ultrasound (IVUS), multi-detector computed tomography (MDCT) and X-ray angiography.
In the past decade, magnetic resonance (MR) has emerged as a noninvasive method for directly observing the coronary wall12. Many indices affiliated with coronary remodeling, including coronary vessel area, lumen area, coronary wall thickening1215 and coronary wall distension16, 17, are reported to be acquired with adequate accuracy and reproducibility. Therefore, MR techniques provide a unique opportunity to assess coronary remodeling from multiple aspects in asymptomatic subjects at high risk for cardiovascular diseases, the main targets of preventive medicine. The aim of the present study was to detect differences in potential imaging biomarkers of coronary remodeling between older hypertensive patients and healthy controls using a single MR scan.
Patient study
This study was compliant with the Health Insurance Portability and Accountability Act (HIPAA) and approved by the Institutional Review Board (IRB). One hundred and thirty participants (mean age 72.9 ± 5.1 years, range 65 – 84 years) of the Chicago Healthy Aging Low Risk MR angiography (CHARISMA) study were enrolled. Informed consent was obtained from all of the participants. The inclusion criterion was asymptomatic aging without a documented history of cardiovascular disease. The exclusion criteria were contradictions for MR scanning, heart rate > 70 beats/minute, diabetes mellitus and renal dysfunction (defined as a glomerular filtration rate < 60 mL/minute/1.73 m2). There are 65 participants with primary hypertension (73.4 ± 5.5 years) and 65 healthy controls (72.3 ± 4.6 years). Primary hypertension was defined as systolic blood pressure (SBP) > 140 mmHg, diastolic blood pressure (DBP) > 90 mmHg or blood pressure controlled with medication. For each participant, the peripheral (brachial) blood pressure was measured within 2 hours before or after the MR scans. The pulse pressure (PP) (mmHg) was defined as SBP - DBP. The information on the participants is shown in table 1.
Table 1
Table 1
Information of study population
Imaging protocol
The MR scans were performed with a 1.5-T scanner (ESPREE, SIEMENS, GERMANY). A 3-plane fast localization sequence was run for anatomical orientation for the whole scan. A black-blood half-Fourier acquisition single-shot turbo spin-echo (HASTE) sequence was run to identify the 4-chamber and short-axis views of coronary orientation. A segmented steady-state free precession (SSFP) sequence was used to acquire cardiac cine images in the 4-chamber view of the heart. The imaging parameters were as follows: TR/TE = 2.8/1.1 ms; flip angle = 65°; voxel size = 2.1 × 2.1 × 10 mm3. We acquired 22 reconstructive cardiac phases using retrospective gating. Two slices were acquired within each breath hold at the end of expiration. A motion-adapted navigator (NAV)-gated, ECG-triggered, fat-saturated, T2-prepared, segmented three-dimensional (3D) SSFP sequence was used for the non-contrast whole-heart coronary MR angiography. The 3D k-space data were collected by employing a linear order in both the phase-encoding direction and the partition-encoding direction. The in-plane resolution = 1.1 × 1.1 mm2; the slice thickness = 0.7 mm (interpolated from 1.4 mm); TR/TE = 3.7/1.7 ms; the flip angle = 90°; the lines per heartbeat = 25–33; the readout bandwidth = 870 Hz/pixel; the parallel acquisition factor = 2; the field of view (FOV) = 320 × 320 mm2. The imaging time was approximately 6–8 minutes for 88–104 slices. The whole-heart coronary MR angiography was run twice with the same parameters, aside from the different acquisition windows. The acquisition window for the first MRA scan was set at mid-diastole. For the second MRA scan, segmented imaging data were acquired in end-systole.
A multiplanar reformation (MPR) was performed on the 3D MR angiography data (acquired in mid-diastole) to localize the left main artery (LM), the left anterior descending artery (LAD) and the right coronary artery (RCA) for black-blood coronary wall imaging. Perpendicular to the long axes of the vessels and beginning at 5 mm from the ostia, we acquired 3 cross-sectional slices from the RCA (with 5 mm intervals), 1 slice from the LM and 3 slices from the LAD (with 5 mm intervals) using a NAV-gated, ECG-triggered, double inversion recovery (DIR)-prepared two-dimensional (2D) turbo spin-echo (TSE) sequence18. A spectral-selective adiabatic inversion recovery (SPAIR) pulse was applied to suppress the fat signal to improve the contrast between the coronary wall and the surrounding tissue. The imaging parameters were as follows: TR = 600–800 ms; TE = 33 ms; echo train length = 9–13; in-plane resolution = 0.9 × 0.9 mm2; slice thickness = 4.0 mm. In all cases, the duration of data acquisition was individually optimized to not exceed the coronary rest period duration and to begin after the onset of the coronary rest period in mid-diastole.
Image processing and measurements
Images were transferred to an imaging workstation (Dell, Studio XPS 435T, installed with Linux operation system, Ubuntu 11.0) for analysis. The image qualities of the black-blood coronary wall MR imaging and the whole-heart coronary MR angiography were graded with a modified 3-point system based on the following criteria: 1) bad image, vessel (wall) not eligible for analysis; 2) good image, vessel (wall) eligible for analysis, vessel (wall) may have some image artifacts or signal loss; and 3) excellent image, vessel (wall) observed continuously with little signal loss and with a clear border between the vessel (wall) and surrounding structures13, 18. Coronary (wall) images with a score (grade) of 2 or 3 were enrolled for quantitative analysis. The coronary wall images were then zoomed 10-fold (1000%). The outer (adventitial) and inner (luminal) boundaries of the coronary wall were manually traced by reader #1 (K.L, with 5 years of experience in cardiovascular imaging) using dedicated region-of-interest tools from Vessel MASS software (Leiden University, The Netherlands). The cross-sectional vessel area (outer contour area), luminal area, wall area (vessel area - lumen area) and wall thickness (mean and maximum) were also measured. The percent of the coronary wall occupying the vessel area (PWOV), defined as (wall area/vessel area) × 100%, was calculated for each coronary wall segment. The coronary plaque index (CPI) was defined as the ratio of maximal coronary wall thickness to minimal vessel wall thickness19.
Cross-sectional images of the coronary arteries were reconstructed using MPR, based on the eligible raw data of coronary MR angiography acquired at the end-systolic and mid-diastolic cardiac cycles. For the two sets of data/images, transverse segments of the RCA, LM and LAD (at the 7 imaging planes where the black-blood coronary wall images were acquired) were carefully identified and matched for the same anatomy based on the ostia of the coronary branches. The coronary lumen images were zoomed 10-fold (1000%) and traced manually by reader #1. The lumen areas in both systole and diastole were calculated according to their contours. The coronary distensibility index (CDI, mmHg−1) was calculated as follows: [(Lumen areasystolic − Lumen areadiastolic)/(Lumen areadiastolic × PP)] × 100017.
Repeatability and reproducibility tests
Two readers (K.L and Y.L; reader #2 had 8 years of experience in clinical radiology and was blinded to the research design) independently reviewed and measured the coronary indices using the same protocol in 10 randomly chosen hypertensive participants to test inter-observer agreement. Reader #1 repeated the coronary measurements 1 month after the first analysis to test intra-observer variation. Coronary MR imaging was repeated on 10 participants with subject repositioning to test the reproducibility of the coronary indices measured by reader #1.
Data analysis and statistical methods
The data were presented as the means ± one standard deviation (SD). On a per-patient basis, sex composition and age were compared (Chi-squared tests and t tests) between participants with and without hypertension. The coronary wall indices, including wall thickness (mean and maximum), CDI, CPI and PWOV, were compared (t tests) between coronary segments derived from the two patient groups. Correlations among coronary measurements were investigated (Pearson correlation coefficients). Coronary indices were compared (t tests) between the coronary segments using mean PWOV as a cutoff point. Bland-Altman plots were used to show the inter-observer, intra-observer and scan-rescan coronary measurement agreement based on coronary MR imaging/angiography. Statistical significance was set at a two-tailed P-value < 0.05. All of the statistical processing in this study was performed with the SPSS software (Version 13.0, SPSS Inc, Chicago, IL, USA).
The imaging data from six participants were excluded for analysis because of incomplete scanning due to uncontrollable body motion (N=3), irregular breath mode (N=1), hypertensive emergency (N=1) or scanner malfunction (N=1). In total, 124 MR scans were completed, and 525 coronary wall segments were eligible for quantitative analysis, including 259 segments (42 LM, 105 LAD and 112 RCA) from 61 hypertensive participants and 266 segments (45 LM, 116 LAD and 105 RCA) from 63 healthy controls. The acquisition windows in a single heart beat (time resolution) for the coronary MR angiography (the same in systole and diastole) and the coronary wall MRI were 85 ± 32 ms and 91 ± 8 ms, respectively. The image quality and scan efficiency were 2.39 ± 0.42, 34% ± 17% for coronary wall MR imaging and 2.55 ± 0.56, 37% ± 12% for coronary MR angiography.
No significant stenosis (> 50%) was presented in our study. Coronary segments derived from hypertensive participants have a higher mean coronary wall thickness (1.43 ± 0.26 mm vs. 1.35 ± 0.21 mm, P < 0.001), a smaller vessel area (25.06 ± 7.66 mm2 vs. 29.62 ± 10.15 mm2, P < 0.001), a smaller coronary wall area (18.49 ± 5.32 mm2 vs. 20.15 ± 5.91 mm2, P = 0.001), a smaller lumen area (6.57 ± 3.44 mm vs. 9.48 ± 5.39 mm2, P < 0.001), a lower CDI (5.30 ± 2.60 vs. 7.49 ± 3.33, P < 0.001) and a higher PWOV (74.59% ± 8.30% vs. 69.38% ± 8.99%, P < 0.001) than those from healthy aging.
For all cross-sectional segments, the PWOV (71.95% ± 9.03%) was correlated with the mean wall thickness (1.39 ± 0.24 mm, r = 0.589, P < 0.001), maximum wall thickness (1.76 ± 0.33 mm, r = 0.553, P < 0.001), vessel area (27.37 ± 9.28 mm2, r = −0.436, P < 0.001), lumen area (8.04 ± 4.76 mm2, r = −0.786, P < 0.001) and CDI (6.41 ± 3.21 mmHg−1, r = −0.452, P < 0.001). The CDI was correlated with the mean coronary wall thickness (r = −0.609, P < 0.001) and maximum wall thickness (r = −0.466, P < 0.001). Figure 1 presents the relationships among mean wall thickness, CDI and PWOV.
Figure 1
Figure 1
Figure 1
Figure 1
The relationships among mean coronary wall thickness, CDI and PWOV
When the average PWOV was set as an ad hoc cutoff point, 248 coronary segments with a high PWOV (> 71.95%) had a significantly higher mean wall thickness (1.50 ± 0.22 mm vs. 1.22 ± 0.20 mm, P < 0.001), a higher maximum wall thickness (1.90 ± 0.31 mm vs. 1.60 ± 0.28 mm, P < 0.001), a smaller vessel area (24.20 ± 7.07 mm2 vs. 30.92 ± 10.15 mm2, P < 0.001), a smaller lumen area (5.18 ± 2.18 mm2 vs. 11.23 ± 4.84 mm2, P < 0.001), a lower CDI (5.41 ± 2.78 mmHg−1 vs. 7.52 ± 3.30 mmHg−1, P <0.001) and a higher CPI (1.78 ± 0.41 vs. 1.70 ± 0.39, P = 0.035) compared with 277 coronary segments with a low PWOV (< 71.95%).
A set of images for multiple coronary segments with various remodeling patterns from a single hypertensive patient is shown in Figure 2.
Figure 2
Figure 2
The relationships among coronary wall thickness, CDI, CPI and PWOV in a single patient. A female patient with a 10-year history of hypertension was studied. Her blood pressure was 145/90 mmHg, and her body weight was 61 Kg
For the 10 randomly chosen cases, good intra-observer (r = 0.866 for CDI and r = 0.911 for wall thickness, P < 0.001) and inter-observer agreement (r = 0.812 for CDI and r = 0.898 for wall thickness, P < 0.001) were found in 43 coronary segments. The scan-rescan test showed low variation between coronary measurements in 38 coronary segments from the 10 randomly chosen cases (r = 0.751 for CDI and r = 0.816 for wall thickness, P < 0.001). See figure I in the online-only Data Supplement.
In the present study, we found that asymptomatic hypertensive elders have a thicker coronary wall, a smaller coronary vessel area, a smaller wall area, a smaller lumen area, a lower CDI and a higher PWOV than healthy controls. There are close correlations among those measurements of coronary walls. Compared with existing publications, our study is a noninvasive exploration of coronary remodeling with both morphological and functional measurements using coronary MR imaging.
Generally, the manifestations of coronary remodeling are defined jointly by changes in the vessel size and the plaque burden. Positive remodeling (a normal lumen gauge with compensatory vessel enlargement) and negative remodeling (a reduced lumen area with vessel shrinkage) are main remodeling patterns in multiple stages of atherosclerosis20. Both pathology and IVUS have been accepted as clinical standards for defining coronary remodeling. According to the classical theory of coronary remodeling developed by Glagov et al.2, the coronary wall area enlarges, but the coronary lumen may remain nearly normal until 40% of the internal elastic lamina is occupied. After the point of inflexion (40%), the coronary artery lumens begin to narrow as the plaque burden continues to grow. In another histological investigation, Varnava et al. defined percent vessel remodeling using the difference in the cross-sectional area at the plaque from the mean of the reference vessel area. Plaque sites in which vessel remodeling was ≥0% were considered to have positive remodeling and those with remodeling <0% were considered to have negative remodeling. The authors found that positive remodeling was associated with the plaque with a larger lipid core and a higher macrophage count. Such plaques were considered to be vulnerable lesions21.
IVUS identifies remodeled vessel walls in vivo by comparing “target” segments to adjacent sites (references); a remodeling index (lesion vessel area/reference vessel area) >1 indicates positive remodeling (enlargement), and a remodeling index <1 indicates negative remodeling. Positive remodeling was associated with acute cardiovascular events, and negative remodeling was linked with diabetes, hypertension, stenosis and ischemia2226. In a recent published clinical trial, the percent atheroma volume (PAV, defined as (Σ(external elastic membrane(EEM) area − lumen area)/Σ EEM area) × 100) was acquired with IVUS as the primary efficacy end point to evaluate the variations in the remodeling of the coronary wall under two statin regimens6.
In present study, we noninvasively described remodeled coronary wall using MR techniques. For the first time, we introduced the PWOV, an MR-specific index combing changes in both the lumen and the wall area to describe remodeled coronary wall, using both “Glagov’s method” and the PAV as prototypes. We found a significant difference in the PWOV between subjects with and without hypertension, and there were obvious disparities in major morphological and biomechanical characteristics between coronary segments with distinct PWOVs. Our results suggest that the PWOV has the potential to serve as a quantitative imaging biomarker that is affiliated with pathophysiological properties of remodeled coronary arteries. Therefore, it is promising to match the PWOV with established pathological biomarkers of coronary remodeling to estimate the progression of cardiovascular diseases and individual responses to cardiovascular regimens in clinical studies.
Nevertheless, it is worth noting the differences in describing coronary lesions between MR imaging and existing clinical methods. The vessel wall measurements described by Glagov et al.2 included only the intima. However, it is almost impossible to define the internal elastic lamina with current MR techniques. Hence, the cutoff point (40%) of the “Glagov’s model” could not be directly applied in MR imaging studies. In a study of the carotid artery, remodeling was observed with black-blood MR imaging in a population of 2,204 subjects, and a knot of remodeling patterns was found when the vessel wall occupied 64% of the whole vessel area27. Therefore, population studies are warranted to find out PWOV’s own cutoff point for discriminating coronary remodeling patterns. PAV is also an index reflecting the ratio of coronary wall to vessel size. However, PAV is a measurement for plaque volume while PWOV is for plaque area. Further studies are needed to investigate relations between PAV and PWOV in the assessment of atherosclerosis burdens.
Our study has several limitations. First, we did not use clinical examinations, such as IVUS or X-ray angiography, as references for the MR imaging/angiography because it was difficult to justify using invasive methods on asymptomatic subjects without clinical indicators. Although cardiac motion blurring may affect the accuracy of depiction for vessel wall, various existing publications proved the accuracy of MR techniques (black-blood and bright-blood) in detecting coronary lesions14, 2831. In addition, we routinely tested the reproducibility of coronary measurements to determine the reliability of our methods. Second, we were unable to discriminate certain subtle structures in the coronary plaques, such as the lipid core or calcification, due to limited spatial resolution. Therefore, the effect of those lesions on local coronary biomechanical properties could not be excluded. However, such a spatial resolution was sufficient for the quantitative evaluation of morphological changes, such as thickening of the coronary wall13, 15, 16, 19. Third, we only imaged the proximal portions (as far as 15 mm from the ostia) of the coronary branches at predefined locations since 2D black-blood coronary wall MR imaging is unable to cover the whole coronary tree. Although remodeling of the distal parts may be missed, proximal lesions on the coronary wall are generally recognized as a focus of clinical concern. Fourth, a portion of the coronary wall images (343 segments) was excluded from the quantitative analysis due to poor image quality. Using MR to observe the coronary wall is challenging. The image quality is jointly affected by various technical and physiological factors. Nevertheless, our success rate is still comparable to that of other published studies of coronary MR imaging13.
Conclusion
MR techniques are able to noninvasively detect significant differences in potential imaging biomarkers of coronary remodeling between older hypertensive patients and healthy aging controls. The PWOV is a promising remodeling feature for quantitatively evaluating the progression of coronary atherosclerosis.
Supplementary Material
Acknowledgments
Sources of Funding: This study was supported by a grant from the National Institute of Health (R01HL089695) and a grant from the American Heart Association (10CRP3050051)
Footnotes
Disclosures: One co-author, XB, is an employee of SIEMENS health care, Chicago, IL. The data and information of this study are under control by authors who are not SIEMENS employee. The other authors have no financial disclosure.
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