Abstract
This study sought to determine the multicenter reproducibility of magnetic resonance imaging (MRI) and the compatibility of different scanner platforms in assessing carotid plaque morphology and composition. A standardized multi-contrast MRI protocol was implemented at 16 imaging sites (GE: 8; Philips: 8). Sixty-eight subjects (61 ± 8 years; 52 males) were dispersedly recruited and scanned twice within 2 weeks on the same magnet. Images were reviewed centrally using a streamlined semiautomatic approach. Quantitative volumetric measurements on plaque morphology (lumen, wall, and outer wall) and plaque tissue composition [lipid-rich necrotic core (LRNC), calcification, and fibrous tissue] were obtained. Inter-scan reproducibility was summarized using the within-subject standard deviation, coefficient of variation (CV) and intraclass correlation coefficient (ICC). Good to excellent reproducibility was observed for both morphological (ICC range 0.98–0.99) and compositional (ICC range 0.88–0.96) measurements. Measurement precision was related to the size of structures (CV range 2.5–4.9 % for morphology, 36–44 % for LRNC and calcification). Comparable measurement variability was found between the two platforms on both plaque morphology and tissue composition. In conclusion, good to excellent inter-scan reproducibility of carotid MRI can be achieved in multicenter settings with comparable measurement precision between platforms, which may facilitate future multicenter endeavors that use serial MRI to monitor atherosclerotic plaque progression.
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Corti R, Fayad ZA, Fuster V, Worthley SG, Helft G, Chesebro J, Mercuri M, Badimon JJ (2001) Effects of lipid-lowering by simvastatin on human atherosclerotic lesions: a longitudinal study by high-resolution, noninvasive magnetic resonance imaging. Circulation 104:249–252
Lima JA, Desai MY, Steen H, Warren WP, Gautam S, Lai S (2004) Statin-induced cholesterol lowering and plaque regression after 6 months of magnetic resonance imaging-monitored therapy. Circulation 110:2336–2341
Yonemura A, Momiyama Y, Fayad ZA, Ayaori M, Ohmori R, Higashi K, Kihara T, Sawada S, Iwamoto N, Ogura M, Taniguchi H, Kusuhara M, Nagata M, Nakamura H, Tamai S, Ohsuzu F (2005) Effect of lipid-lowering therapy with atorvastatin on atherosclerotic aortic plaques detected by noninvasive magnetic resonance imaging. J Am Coll Cardiol 45:733–742
Lee JM, Wiesmann F, Shirodaria C, Leeson P, Petersen SE, Francis JM, Jackson CE, Robson MD, Neubauer S, Channon KM, Choudhury RP (2008) Early changes in arterial structure and function following statin initiation: quantification by magnetic resonance imaging. Atherosclerosis 197:951–958
Underhill HR, Yuan C, Zhao XQ, Kraiss LW, Parker DL, Saam T, Chu B, Takaya N, Liu F, Polissar NL, Neradilek B, Raichlen JS, Cain VA, Waterton JC, Hamar W, Hatsukami TS (2008) Effect of rosuvastatin therapy on carotid plaque morphology and composition in moderately hypercholesterolemic patients: a high-resolution magnetic resonance imaging trial. Am Heart J 155:581–584
Boussel L, Arora S, Rapp J, Rutt B, Huston J, Parker D, Yuan C, Bassiouny H, Saloner D (2009) Atherosclerotic plaque progression in carotid arteries: monitoring with high-spatial-resolution MR imaging–multicenter trial. Radiology 252:789–796
Zhao XQ, Dong L, Hatsukami T, Phan BA, Chu B, Moore A, Lane T, Neradilek MB, Polissar N, Monick D, Lee C, Underhill H, Yuan C (2011) MR imaging of carotid plaque composition during lipid-lowering therapy: a prospective assessment of effect and time course. J Am Coll Cardiovasc Imaging 4:977–986
Sun J, Balu N, Hippe DS, Xue Y, Dong L, Zhao X, Li F, Xu D, Hatsukami TS, Yuan C (2013) Subclinical carotid atherosclerosis: short-term natural history of lipid-rich necrotic core–a multicenter study with MR imaging. Radiology 268:61–68
Fayad ZA, Mani V, Woodward M, Kallend D, Abt M, Burgess T, Fuster V, Ballantyne CM, Stein EA, Tardif JC, Rudd JH, Farkouh ME, Tawakol A (2011) Safety and efficacy of dalcetrapib on atherosclerotic disease using novel non-invasive multimodality imaging (dal-PLAQUE): a randomised clinical trial. Lancet 378:1547–1559
Kawahara T, Nishikawa M, Kawahara C, Inazu T, Sakai K, Suzuki G (2013) Atorvastatin, etidronate, or both in patients at high risk for atherosclerotic aortic plaques: a randomized, controlled trial. Circulation 127:2327–2335
Cai JM, Hatsukami TS, Ferguson MS, Kerwin WS, Saam T, Chu BC, Takaya N, Polissar NL, Yuan C (2005) In vivo quantitative measurement of intact fibrous cap and lipid-rich necrotic core size in atherosclerotic carotid plaque: comparison of high-resolution, contrast-enhanced magnetic resonance imaging and histology. Circulation 112:3437–3444
Trivedi RA, U-King-Im JM, Graves MJ, Horsley J, Goddard M, Kirkpatrick PJ, Gillard JH (2004) MRI-derived measurements of fibrous-cap and lipid-core thickness: the potential for identifying vulnerable carotid plaques in vivo. Neuroradiology 46:738–743
Cappendijk VC, Heeneman S, Kessels AG, Cleutjens KB, Schurink GW, Welten RJ, Mess WH, van Suylen RJ, Leiner T, Daemen MJ, van Engelshoven JM, Kooi ME (2008) Comparison of single-sequence T1w TFE MRI with multisequence MRI for the quantification of lipid-rich necrotic core in atherosclerotic plaque. J Magn Reson Imaging 27:1347–1355
Alizadeh DR, Doornbos J, Tamsma JT, Stuber M, Putter H, van der Geest RJ, Lamb HJ, de Roos A (2007) Assessment of the carotid artery by MRI at 3T: a study on reproducibility. J Magn Reson Imaging 25:1035–1043
Syed MA, Oshinski JN, Kitchen C, Ali A, Charnigo RJ, Quyyumi AA (2009) Variability of carotid artery measurements on 3-Tesla MRI and its impact on sample size calculation for clinical research. Int J Cardiovasc Imaging 25:581–589
Duivenvoorden R, de Groot E, Elsen BM, Lameris JS, van der Geest RJ, Stroes ES, Kastelein JJ, Nederveen AJ (2009) In vivo quantification of carotid artery wall dimensions: 3.0-Tesla MRI versus B-mode ultrasound imaging. Circ Cardiovasc Imaging 2:235–242
Reig S, Sánchez-González J, Arango C, Castro J, González-Pinto A, Ortuño F, Crespo-Facorro B, Bargalló N, Desco M (2009) Assessment of the increase in variability when combining volumetric data from different scanners. Hum Brain Mapp 30:355–368
Saam T, Hatsukami TS, Yarnykh VL, Hayes CE, Underhill H, Chu BC, Takaya N, Cai JM, Kerwin WS, Xu DX, Polissar NL, Neradilek B, Hamar WK, Maki J, Shaw DW, Buck RJ, Wyman B, Yuan C (2007) Reader and platform reproducibility for quantitative assessment of carotid atherosclerotic plaque using 1.5T Siemens, Philips, and General Electric scanners. J Magn Reson Imaging 26:344–352
The AIM-HIGH Investigators (2011) The role of niacin in raising high-density lipoprotein cholesterol to reduce cardiovascular events in patients with atherosclerotic cardiovascular disease and optimally treated low-density lipoprotein cholesterol Rationale and study design. The Atherothrombosis Intervention in Metabolic syndrome with low HDL/high triglycerides: impact on Global Health outcomes (AIM-HIGH). Am Heart J 161:471–477
Balu N, Yarnykh VL, Scholnick J, Chu BC, Yuan C, Hayes C (2009) Improvements in carotid plaque imaging using a new eight-element phased array coil at 3T. J Magn Reson Imaging 30:1209–1214
Kerwin WS, Xu D, Liu F, Saam T, Underhill HR, Takaya N, Chu BC, Hatsukami TS, Yuan C (2007) Magnetic resonance imaging of carotid atherosclerosis: plaque analysis. Top Magn Reson Imaging 18:371–378
Liu F, Xu DX, Ferguson MS, Chu BC, Saam T, Takaya N, Hatsukami TS, Yuan C, Kerwin WS (2006) Automated in vivo segmentation of carotid plaque MRI with morphology-enhanced probability maps. Magn Reson Med 55:659–668
Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20:37–46
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York, NY
Friedman L, Glover GH (2006) Report on a multicenter fMRI quality assurance protocol. J Magn Reson Imaging 23:827–839
Vidal A, Bureau Y, Wade T, Spence JD, Rutt BK, Fenster A, Parraga G (2008) Scan-rescan and intra-observer variability of magnetic resonance imaging of carotid atherosclerosis at 1.5 T and 3.0 T. Phys Med Biol 53:6821–6835
Saam T, Kerwin WS, Chu BC, Cai JM, Kampschulte A, Hatsukami TS, Zhao XQ, Polissar NL, Neradilek B, Yarnykh VL, Flemming K, Huston J, Insull W, Morrisett JD, Rand SD, Demarco KJ, Yuan C (2005) Sample size calculation for clinical trials using magnetic resonance imaging for the quantitative assessment of carotid atherosclerosis. J Cardiovasc Magn Reson 7:799–808
Li F, Yarnykh VL, Hatsukami TS, Chu B, Balu N, Wang J, Underhill HR, Zhao X, Smith R, Yuan C (2010) Scan-rescan reproducibility of carotid atherosclerotic plaque morphology and tissue composition measurements using multicontrast MRI at 3T. J Magn Reson Imaging 31:168–176
Wasserman BA, Astor BC, Sharrett AR, Swingen C, Catellier D (2010) MRI measurements of carotid plaque in the atherosclerosis risk in communities (ARIC) study: methods, reliability and descriptive statistics. J Magn Reson Imaging 31:406–415
Takaya N, Cai JM, Ferguson MS, Yarnykh VL, Chu BC, Saam T, Polissar NL, Sherwood J, Cury RC, Anders RJ, Broschat KO, Hinton D, Furie KL, Hatsukami TS, Yuan C (2006) Intra- and interreader reproducibility of magnetic resonance imaging for quantifying the lipid-rich necrotic core is improved with gadolinium contrast enhancement. J Magn Reson Imaging 24:203–210
Touze E, Toussaint JF, Coste J, Schmitt E, Bonneville F, Vandermarcq P, Gauvrit JY, Douvrin F, Meder JF, Mas JL, Oppenheim C (2007) Reproducibility of high-resolution MRI for the identification and the quantification of carotid atherosclerotic plaque components: consequences for prognosis studies and therapeutic trials. Stroke 38:1812–1819
Kerwin WS, Liu F, Yarnykh V, Underhill H, Oikawa M, Yu W, Hatsukami TS, Yuan C (2008) Signal features of the atherosclerotic plaque at 3.0 Tesla versus 1.5 Tesla: Impact on automatic classification. J Magn Reson Imaging 28:987–995
Liu W, Balu N, Sun J, Zhao X, Chen H, Yuan C, Zhao H, Xu J, Wang G, Kerwin WS (2012) Segmentation of carotid plaque using multicontrast 3D gradient echo MRI. J Magn Reson Imaging 35:812–819
Acknowledgments
This study was supported by a Grant from the Foundation for the National Institutes of Health Biomarkers Consortium made possible by funds from Merck, Pfizer, and Abbott, and by R01HL088214. Carotid coils were provided by GE Healthcare and Philips Healthcare. This manuscript represents the views of the authors and not necessarily those of the National Institutes of Health or the United States government.
Conflict of interest
Xue-Qiao Zhao reported research grants from Abbvie, Kowa, Merck, and Pfizer. Daniel S. Hippe reported grant support for analysis of unrelated data from GE Healthcare, Philips Healthcare, Society of Interventional Radiology, and RSNA Research and Education Foundation. Thomas S. Hatsukami reported research grants from Philips Healthcare. Michael T. Klimas is an employee of Merck. Robert J. Padley is an employee of Abbvie and reported stocks of Abbvie. Bradley T. Wyman was a former employee of Pfizer and reported stocks of Pfizer. Chun Yuan reported research grants from NIH, VP Diagnostics, Philips Healthcare, and consulting fees from Bristol Myers Squibb Medical Imaging and Philips Healthcare. The remaining authors reported no conflicts of interest.
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Sun, J., Zhao, XQ., Balu, N. et al. Carotid magnetic resonance imaging for monitoring atherosclerotic plaque progression: a multicenter reproducibility study. Int J Cardiovasc Imaging 31, 95–103 (2015). https://doi.org/10.1007/s10554-014-0532-7
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DOI: https://doi.org/10.1007/s10554-014-0532-7