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Cardiovascular magnetic resonance: Current clinical practice and future potential
Cardiovascular Magnetic Resonance: Current Clinical Practice and Future Potential Katharina Kiss, MD,*,§ Anitha Varghese, BSc, MRCP,† Michael Stiskal, MD,‡ Heinz Czembirek, MD,‡ Johannes Mlczoch, MD, FESC,* and Dudley J. Pennell, MD, FRCP, FESC, FACC† Cardiovascular magnetic resonance (CMR) is playing an increasing role in the noninvasive assessment of the cardiothoracic patient. It provides rapid, high-resolution anatomical coverage, and accurate functional cardiovascular assessment without the need for ionizing radiation. In this article, we discuss the fundamental principles of CMR and outline the established and newer indications for its use. Finally, the future potential for this technique in the cardiovascular arena is briefly outlined. Semin Thorac Cardiovasc Surg 16:235-241 © 2004 Elsevier Inc. All rights reserved. KEYWORDS cardiovascular magnetic resonance noninvasive imaging, cardiothoracic surgery
M
agnetic resonance (MR) is based on the phenomenon of the resonance of atomic nuclei to radiofrequency (RF) waves.1 Hydrogen is the most abundant element in the human body which shows this phenomenon, and it contains a single proton in its nucleus. Hydrogen nuclei align with the axis of a magnetic field to create a net longitudinal magnetization and this can be disturbed by RF energy at the resonant frequency. After a short delay, the energy is re-emitted as an RF signal which can be used to form an image. Transmission and reception of RF energy is via special aerials known as coils with subsequent conversion of this raw data into images involving ultrafast computers and Fourier transformation. The resonant frequency of hydrogen nuclei is proportional to the strength of the main magnetic field. Most clinical cardiovascular magnetic resonance (CMR) is currently performed at 1.5T (Tesla) but higher field strengths are used for research on tissue and animals. The degree of nucleus excitation is a product of both the amplitude and duration of the RF pulse, and the rate of relaxation is defined by 2 parameters known as T1 and T2. Relaxation varies according to the environment of the hydrogen in tissues. The imaging sequences can be varied to give *Department of Cardiology, Hospital of Lainz, Vienna, Austria. †Cardiovascular Magnetic Resonance Unit, Royal Brompton Hopsital, London, UK. ‡Department of Radiology, Hospital of Lainz, Vienna, Austria. §Joint first author. Address reprint requests to Katharina Kiss, MD, CMR Unit Lainz, Department of Cardiology, Hospital of Lainz, Wolkersbergenstrasse 1, 1130 Vienna, Austria. E-mail: [email protected]
1043-0679/04/$-see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1053/j.semtcvs.2004.08.009
different weighting to one of these relaxation parameters, allowing tissue characterization. The two main types of sequence used in CMR are gradient echo (GRE) and spin echo (SE). In general, when using GRE sequences, both blood and fat appear white. This technique enables the acquisition of cine images, which can identify areas of focal myocardial dysfunction and abnormal flow patterns (Fig. 1, video 1). Variations of GRE techniques include fast low-angle shot (FLASH), fast imaging with steady-state precession (FISP) and velocity mapping. In principle, velocity mapping is similar to a form of 2-dimensional Doppler.2 With SE techniques, blood generally appears black and fat appears white. This sequence is more useful for anatomical as opposed to functional imaging. Another important technique used in CMR is a prepulse to create tissue contrast. One example is the inversion recovery technique which can be used to yield high T1 contrast. CMR consists of applying these sequences and their variants to determine cardiac physiology, anatomy, tissue characterisation, and vascular angiography. Evaluation of cardiac metabolism is also possible with MR spectroscopy. Another important aspect of CMR is its excellent safety profile. The contrast agents used for MR (gadolinium chelates) are much safer than x-ray agents and are not nephrotoxic. Patients with prosthetic heart valves, sternal wires, retained epicardial pacing leads, intracoronary stents, and joint replacements can be safely scanned.3,4 CMR on patients with permanent pacemakers is being performed occasionally under strict conditions and only in specialist centres,5 and currently remains a strong relative contraindication. Implantable defibrillators are currently contraindicated. Cerebrovascular 235
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Figure 3 and Video 3a Large apical thrombus after myocardial infarction. The late enhancement image clearly shows a white area (apical) which clearly depicts the scar myocardial infarction. Video 3b Perfusion imaging of apical thrombus demonstrating the lack of contrast uptake. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
Figure 1 and Video 1 GRE technique (TrueFISP) long axis four chamber view showing normal left ventricular function. (Video loop is available online at http://www3.us.elsevierhealth.com/semtcvs/.)
aneurysm clips are problematic because of possible ferromagnetic properties and specialist advice is required.
Current CMR Indications 1. Ischaemic Heart Disease A. Myocardial Infarction CMR is increasingly being used in the assessment of myocardial infarction in both the early and chronic phase. Its ability to assess regions of focal myocardial wall thinning and wall motion abnormalities by high-resolution cine imaging are well established. Aneurysm formation can be easily detected by both SE and GE techniques (Fig. 2, video 2a ⫹ b) and mural thrombi are clearly identified with the technique of early gadolinium enhancement (Fig. 3 video 3a ⫹ b). This involves imaging at 1 to 2 minutes after the intravenous injection of a gadolinium chelate contrast agent. Such early imaging can also be used to define the extent of microvascular obstruction (MVO) in acute infarction (Fig. 4, video 4). Areas of MVO within an acute infarct appear dark because of very slow entry of gadolinium. The presence of MVO by CMR has been shown to be an independent predictor of adverse prognosis.6 The technique of late gadolinium enhancement in-
Figure 2 and Video 2a ⴙ b GRE two-chamber view showing an extended aneurysm of the inferior wall postmyocardial infarction. The video 2b shows an additional LVOT view. (Larger version of figure and video loops are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
volves imaging of the myocardium 10 to 15 minutes after gadolinium. In the late phase, gadolinium chelates distribute in the extracellular space, which is increased in acute infarction due to cell membrane breakdown, and in chronic infarction due to fibrosis (Fig. 5a ⫹ b, video 5a ⫹ b).7 Gadolinium accumulation greatly increases the T1 relaxation and areas of abnormality show as bright signal on heavily T1 weighted scans. Typically, an inversion recovery prepulse is used to null (force to near zero) signal from normal myocardium to highlight this differential uptake. Animal experiments in acute infarction have shown that the volume of signal enhancement and infarct size are closely correlated. Late gadolinium enhancement has high resolution and can also define the transmurality of infarcts and identify whether infarction has actually occurred in borderline cases. B. Assessment of Myocardial Viability Late gadolinium enhancement has clinical application in the assessment of viability. Assessment of the percentage of transmural replacement of normal myocardium by scar is a predictor of postrevascularisation contraction recovery. In general, dysfunctional segments with less than 50% transmural replacement show improved function, whilst those with higher grades of transmural replacement fail to improve.8 Compared with resting thallium single photon emission computed tomography (SPECT), CMR has improved sensitivity, specificity, and accuracy in predicting myocardial viability early after acute myocardial infarction.9 In patients with chronic ischaemic heart disease and left ventricular dysfunc-
Figure 4 and Video 4 The dark zone embedded in the clearer zone demonstrates microvascular obstruction (MVO) after transmural posterolateral infarction (right image shows CINE short axis view after application of Gd–DTPA, left image is the corresponding viability image. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
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3. Cardiac Masses
Figure 5a ⴙ b and Video 5 a ⴙ b GRE Cine Sequence (5a) of a midventricular short axis view and corresponding late enhancement image (5b) after myocardial infarction of the posterolateral wall. In the viability image, the transmurality of the scar can be visualized. (Larger version of figure and video loops are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
tion, CMR has a high accuracy compared with 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) for the detection of myocardial viability.10 C. Dobutamine Stress Testing Compared with stress echocardiography, CMR has improved diagnostic capability related to improved results from those patients in whom echocardiographic windows are suboptimal or poor.11 CMR should be considered as a first line approach in this group of patients.
2. Valvular Heart Disease CMR can complement transthoracic and transoesophageal echocardiography (TTE and TOE) in some cases. Echocardiography is good for direct visualization of valve leaflets and their suspensory apparatus or vegetations. CMR is able to accurately quantify valvular regurgitation, peak trans-stenotic jet velocities, ventricular volumes, and myocardial mass, and can detect associated intracardiac thrombi.12 In valvular regurgitation, regurgitant flow is quantified from the reverse flow measurement in diastole with an imaging plane placed just downstream of the aortic and pulmonary valve.13 Isolated mitral regurgitation can be evaluated by subtraction of aortic flow from left ventricular stroke volume. CMR jet velocity mapping is useful for assessment of stenoses where ultrasonic access is limited as in calcified or deformed aortic valves. Jet velocity mapping is combined with cine imaging, the latter identifies the jet core and directs where subsequent imaging planes for assessment of peak velocity are placed. Imaging patients with prosthetic valves is more problematic as with echocardiography. Prosthetic valves contain no mobile hydrogen atoms and so are not visualized directly, but they do cause a localised signal void. In mitral valve surgery, CMR can depict the anatomy of the valve and surrounding structures such as papillary muscles with clarity and in any plane. (Fig. 6, video 6a ⫹ b).
CMR defines the size and anatomical relations of intra and extracardiac masses with high resolution (Fig. 7, video 7).14 The commonest intracardiac filling defect is thrombus and the imaging of this has already been discussed. CMR tissue characterization using a combination of T1 and T2 weighted images in association with gadolinium injection provides useful information. T1 and T2 weighted images differ between masses depending on their biochemical composition, and this can be used to differentiate between them. For example, pericardial cysts have a characteristic high signal on T2 weighted imaging. The fat content of tumours can be identified by acquiring images before and after fat suppression pulses. Gadolinium injection is particurly valuable in this setting. The first pass shows vascularity, the early enhancement shows associated thrombus, and the late enhancement indicates tumour fibrosis. The vascularity of malignant tumours such as angiosarcoma is usually high, but benign tumous such as haemangioma and myxoma also enhance. Generally, malignant cardiac tumours are larger, show evidence of invasion, have a broader attachment, involve more than one cardiac chamber or great vessel, and show evidence of pericardial or extracardiac extension.
4. Pericardium and Pericardial Disease Pericardial thickness is a good guide to the presence of constriction and can be readily measured using CMR. CMR estimates of pericardial thickness (usually ⬍4 mm) is greater than expected from pathological studies due to the phenomenon of chemical shift. This effect is caused by differences in the resonant frequency of protons within the thin fibrous pericardial tissue compared with the overlying layer of fat. Normal pericardium appears black with CMR since it has a low water content, but can enhance with contrast in acute inflammation, and then appears white. Pericardial effusions are black with SE sequences and bright on GE cines. Calcium also appears black on CMR and therefore, an area of pericardial calcification can simply appear as a localised area of pericardial thickening. Computed tomography (CT) is the recommended modality for confirmation or exclusion of calcification. Differentiation of constrictive pericarditis from restrictive cardiomyopathy is important since the former can be successfully treated surgically with pericardiectomy, while the latter requires medical treatment. CMR can facilitate the
Figure 6 and Video 6 Regurgitant mitral valve in short axis and long axis view. In the long axis, the free movement of the papillary muscles due to a rupture of the tendinae cordae can be seen. (Larger version of figure and video loop are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
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Figure 7a ⴙ b and Video 7 Right atrial lipoma clearly identified by applying a fat sat prepulse. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/ semtcvs/.)
analysis of diastolic septal motion during ventricular filling and the presence of this and a thickened fibrotic and/or calcified pericardium is more suggestive of a constrictive picture.15
5. Angiography CMR angiography is usually performed with the injection of gadolinium. CMR angiography of arterial and venous vessels, other than the coronaries, is rapidly becoming the clinical test of choice. Data are usually displayed as a 3D rotating cine. A. Aorta The entire length of the aorta is easily investigated by CMR. Gross morphology is rapidly obtained using multi-slice SE images in the transverse and oblique sagittal planes. The “hockey stick” view enables accurate and reproducible assessment of the diameter of the aorta in aneurysms, evaluation or exclusion of aortic dissections, and identification of coarctation. Cine imaging using true-FISP techniques are useful in all three of these conditions. High-resolution SE imaging can evaluate the extent of aortic dissections including involvement of other vessels and delineation of areas of thrombus and atheroma (Fig. 9). CMR has been shown in randomised trials to be more accurate than TOE and CT in acute dissection and also provides a safe, noninvasive and radiation free modality for follow-up.16 B. Coronary Arteries Coronary CMR can be performed using breath-hold or navigator-based, free breathing techniques with or without intravenous contrast. There have been tremendous improvements in these techniques since their first description in 1993.17 A recent multi-centre study concluded that among patients referred for their first coronary angiogram, 3D CMR allows accurate detection of coronary artery disease in the proximal and middle segments and can reliably identify or exclude left main coronary artery or three-vessel disease (Fig. 8, video 8).18 Imaging of native coronary arteries remains
challenging, but visualization of bypass grafts is more feasible due to their more superficial course, greater size, and relative lack of cardiac motion. Sequences used are primarily 3D navigator-based sequences as well as conventional SE techniques such as half-Fourier fast spin-echo, also known as HASTE. Evaluation of coronary flow reserve in bypass grafts by flow mapping pre- and postadenosine can be used to gauge significant stenosis. Congenital abnormalities of the origin and course of coronary arteries are an important cause of sudden cardiac death, especially in young adults. Their prevalence has been estimated at 0.85% in adults referred for diagnostic angiography, but up to 30% in patients with other forms of congenital heart disease.19 The most common anomaly is the left circumflex artery arising from the right sinus of Valsalva or right coronary artery, but the most clinically important variations are those which pass between the aortic root and right ventricular outflow tract (RVOT) or pulmonary artery (PA). These are associated with myocardial ischaemia or infarction as well as syncope and sudden death. Radiograph coronary angiography can identify the anomalous origin of the coronary artery but is suboptimal for defining the subsequent proximal course with relation to the aorta, RVOT and PA. This requires a tomographic technique such as CMR, which is now the gold standard. C. Carotids, Pulmonary, Renal, Mesenteric, and Peripheral Arteries Assessment of carotid disease is moving away from invasive radiograph based angiography, with its associated small but significant mortality and morbidity, to 3D CMR.20 CMR can also be used for visualisation of the pulmonary, renal, mesenteric and peripheral arteries.21 Thrombus imaging with CMR is very sensitive in the venous system,22 and comparisons with established techniques for detection of DVT and PE are under way.
6. Congenital Heart Disease A. Coarctation of the Aorta Coarctation of the aorta accounts for approximately 6% of congenital heart disease with the stenosis, usually in the region of the ligamentum arteriosum. CMR is useful in the rapid diagnosis, safe follow-up, and noninvasive assessment of severity in aortic coarctation. Initial diagnosis can be performed with SE, GE, or angiography techniques. Significant coarctation is present if the gradient at catheterization is more than 20 mm Hg in the absence of a well-developed collateral circulation. If the latter is present, there may be minimal or no gradient and there may be associated aortic atresia. A
Figure 8 Breath-hold versus non-breathhold true-FISP images of the LAD in the same patient. (Larger version of figure is available online at http://www3.us.elsevierhealth.com/semtcvs/.)
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volumes in valvular regurgitation is absent. Similar methods can be used to evaluate the significance of extracardiac shunts such as patent ductus arteriosus. C. Complex Congenital Heart Disease CMR has revolutionized the management of patients with complex congenital heart disease by providing accurate anatomical and functional intra and extracardiac assessment preand postintervention whilst obviating the need for repeated invasive cardiac catheterization. TOE is better at defining fine structures such as valves while CMR is better at showing flow, conduits and great vessel anatomy.23 Preoperative CMR is excellent for surgical planning and other uses include accurate flow quantification in the assessment of the severity of pulmonary regurgitation following repair of Fallot’s tetralogy, postoperative follow-up of patients with corrected transposition of the great arteries and evaluation of the patency of surgical conduits used in Fontan’s procedure.
7. Pharmaceutical Industry Research and Development Figure 9 MIP Reconstruction of an aortic dissection differentiating the true and false lumen.
significant gradient causes proximal pressure elevation and will lead to left ventricular hypertrophy and ultimately heart failure unless other complications supervene. CMR is used for both preoperative and postoperative evaluation in aortic coarctation. Surgical repair can be complicated by recoarctation and aneurysm formation and serial assessment of these patients is therefore essential. CMR jet velocity mapping is used to assess the gradient across the coarctation site. Additionally, accurate assessment of ventricular mass and function and the exclusion of other cardiovascular abnormalities, such as a bicuspid aortic valve, can be performed in the same examination. Routine CMR follow-up in this patient population involves continued assessment of the left ventricle as well as the coarctation site. B. ASD/VSD CMR is complementary to TTE and TOE in the evaluation of atrial septal defects and ventricular septal defects. Echocardiography is superior for the diagnosis of these defects, and CMR is used for assessment of functional significance since it can provide a noninvasive measurement of the pulmonaryto-systemic flow ratio (Qp/Qs). This involves the use of CMR velocity mapping. This uses the signal phase of each pixel which can be encoded to relate linearly with velocity and produce 2 dimensional velocity maps which correspond with the anatomy from the normal images. Because the area of a vessel can be measured and the mean velocity within the vessel calculated, absolute measurements of instantaneous flow can be derived. When run in cine mode throughout the cardiac cycle, flow curves are generated, where the area under the curve represents true flow in the vessel through the cardiac cycle. In this way, flow through the aorta and PA can be compared and used to derive a Qp/Qs. This can also be derived from comparison of right and left ventricular stroke
Ventricular function, volumes and mass is linked to prognosis in coronary artery and other cardiac disease. Radionuclide techniques and echocardiography suffer from assumptions and suboptimal image quality which makes them less reproducible than CMR.24 The improved interstudy reproducibility of CMR has been recognized by the pharmaceutical industry who are increasingly using CMR for phase 2 and 3 drug development studies to reduce costs by reducing sample sizes.
Future CMR Uses 1. Myocardial Perfusion Approximately 6 million perfusion studies are performed annually in the USA, and all involve significant ionizing radiation. Perfusion CMR may provide the diagnostic and prognostic information obtained by this established technique without the need for ionizing radiation. Currently, perfusion CMR uses a baseline first pass rest perfusion study after intravenous gadolinium given peripherally, and a repeat study during adenosine stress. Areas of reduced perfusion appear darker than normal myocardium. Perfusion CMR also has high resolution which allows in vivo visualization of suben-
Figure 10 and Video 10 Stress perfusion imaging with septal hypokinesia and subendocardial perfusion defect. (Larger version of figure and video loop are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
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240 docardial perfusion defects for the first time (Fig. 10, video 10a ⫹ b). Quantitative analysis tools have been developed which examine the slope of signal increase during first pass or models the perfusion characteristics. Myocardial perfusion reserve can be measured and indices of rest and stress perfusion obtained. Such analysis allows the generation of parametric perfusion maps and bullseye plots, which are very similar to scintigraphy and aid immediate clinical recognition.25 Perfusion CMR scans also incorporate assessment of regional wall motion and thinning and late gadolinium enhancement.
Figure 12 High-resolution SE cross-sectional image through the right common carotid artery (RCCA) showing atheromatous plaque. (Larger version of figure is available online.)
2. Cardiac Transplantation CMR may have a future role in the assessment of acute rejection post cardiac transplantation. Acute rejection is characterized by increased cardiac mass and myocardial signal on SE sequences, indicative of myocardial oedema and/or infiltration of mononuclear cells. These changes are not specific but may provide valuable additional information in the relevant clinical setting. SE imaging of the vessel wall might also help in the detection of early graft disease often seen by intravascular ultrasound in this patient group.
3. Evaluation of Atherosclerotic plaque CMR can depict plaques (Figs. 11 and 12) and interrogate their lipid constituents and integrity of the fibrous cap, which are factors that determine the propensity for plaque rupture and thrombus formation. Plaques more prone to rupture (vulnerable plaques) have characteristic structural features including reduced vascular smooth muscle content and a thin fibrous cap overlying a large lipid core. The concept of arterial remodeling (Glagov phenomenon) is being increasingly recognized and describes how luminal cross-sectional area can be preserved in the face of advanced atherosclerosis within the arterial wall.26,27 CMR is an ideal tool for assessing remodeling and has been successfully used to show this phenomenon in relation to prolonged statin treatment on carotid and aortic atherosclerotic plaque disease.28 Detection of cor-
Figure 11 Carotid CE-MRA showing almost complete occlusion of the right internal carotid artery. (Larger version of figure is available online.)
onary atherosclerotic plaques is also possible though more diffficult.29
4. MR Spectroscopy MR spectroscopy (MRS) provides a noninvasive way of obtaining metabolic information and can be conducted on a number of important nuclei including phosphorus (31P), hydrogen (1H), and carbon (13C).30 MRS can quantify highenergy phosphate compounds such as adenosine triphosphate and creatine phosphate that fuel myocardial contraction and are necessary for myocardial viability and this technique holds future promise in the evaluation of hibernating or stunned myocardium.
Discussion High-resolution visualization of cardiac anatomy has long been a strength of CMR but more recently advances in the noninvasive evaluation of cardiac function offer exciting new applications. CMR can detect subtle changes in wall motion and ejection fraction, making it useful in the follow-up of patients postrevascularization and with heart failure. Recent work has highlighted the use of CMR with late gadolinium enhancement in the differentiation of left ventricular dysfunction related to dilated cardiomyopathy (DCM) or coronary artery disease (CAD) on the basis of myocardial patterns of enhancement.31 In CAD, a subendocardial or transmural pattern is seen while midwall changes suggest DCM. The question of myocardial viability can be accurately addressed with a combination of cine imaging and late gadolinium enhancement, with or without low dose dobutamine. CMR perfusion is in rapid development and holds particular promise in combination with cine imaging and late gadolinium enhancement. The resolution and robustness of radiograph coronary angiography for the evaluation of luminal coronary artery stenoses remains superior to CMR, but the concepts of the vulnerable plaque and arterial remodeling are calling into question the value of such luminography alone. In one decade, CMR evaluation of the coronary arterial tree has made impressive advances. These advances are sure to continue, and will importantly incorporate not only the interrogation of plaque constituents and the tomographic assessment of the vessel wall, but also the evaluation of coronary flow, flow reserve, and functional consequences to the myocardium.
Cardiovascular magnetic resonance: Current clinical practice and future potential
Conclusion CMR is poised to enter routine clinical practice in many cardiac centers worldwide. With the current pace of hardware and software developments, it will soon become an invaluable tool to both the cardiologist and cardiothoracic surgeon.
Appendix Supplementary data associated with this article can be found, in the online version, at doi: 10.1053/j.semtcvs.2004.08.009.
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15. Giorgi B, Mollet NRA, Dymarkowski S, et al: Clinically suspected constrictive pericarditis: MR imaging assessment of ventricular septal motion and configuration in patients and healthy subjects. Radiology 228: 417-424, 2003 16. Nienaber CA, von Kodolitsch Y, Nicolas V, et al: The diagnosis of thoracic aortic dissection by noninvasive imaging procedures. N Engl J Med 328:1-9, 1993 17. Botnar RM, Stuber M, Danias PG, et al: Improved coronary artery definition with T2-weighted, free breathing, three-dimensional coronary MRA. Circulation 99:3139-3148, 1999 18. Kim WJ, Danias PG, Stuber M, et al: Coronary magnetic resonance angiography for the detection of coronary stenoses. N Engl J Med 345:1863-1869, 2001 19. Taylor AM, Thorne SA, Rubens MB, et al: Coronary artery imaging in grown-up congenital heart disease: Complementary role of MR and X-ray coronary angiography. Circulation 101:1670-1678, 2000 20. Ersoy H, Watts R, Sanelli P, et al: Atherosclerotic disease distribution in carotid and vertebrobasilar arteries: Clinical experience in 100 patients undergoing fluoro-triggered 3D Gd MRA. J Magn Reson Imaging 17: 545-558, 2003 21. Owen RS, Carpenter JP, Baum RA, et al: Magnetic resonance imaging of angiographically occult runoff vessels in peripheral arterial occlusive disease. N Engl J Med 326:1577-1581, 1992 22. Fraser DGW, Moody AR, Davidson IR, Martel AL, Morgan PS: Deep venous thrombosis: Diagnosis by using venous enhanced subtracted peak arterial MR venography versus conventional venography. Radiology 226:812-820, 2003 23. Hirsch R, Kilner PJ, Connelly M, et al: Diagnosis in adolescents and adults with congenital heart disease. Prospective assessment of the individual and combined roles of magnetic resonance imaging and transoesophageal echocardiography. Circulation 90:2937-2951, 1994 24. Bellenger NG, Davies LC, Francis JM, et al: Reduction in sample size for studies of remodelling in heart failure by the use of cardiovascular magnetic resonance. J Cardiovasc Magn Reson 2:271-278, 2000 25. Panting JR, Gatehouse PD, Yang GZ, et al: Echo-planar magnetic resonance myocardial perfusion imaging: Parametric map analysis and comparison with thallium SPECT. J Magn Reson Imaging 13(2):192200, 2001 26. Glagov S, Weisenberg E, Zarins CK, et al: Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316:13711375, 1987 27. Crouse III JR, Goldbourt U, Evans G, et al: Arterial enlargement in the atherosclerotic risk in communities (ARIC) Cohort. Stroke 25:13541359, 1994 28. Corti R, Fayad ZA, Fuster V, et al: Effects of lipid-lowering by simvastatin on human atherosclerotic lesions: A longitudinal study by highresolution, noninvasive magnetic resonance imaging. Circulation 104: 249-252, 2001 29. Fayad ZA, Fuster V, Fallon JT, et al: Noninvasive. In vivo human coronary artery lumen and wall imaging using black-blood magnetic resonance imaging. Circulation 102:506-510, 2000 30. Weiss RG, Kalil-Filho R, Bottomley PA: Chapter 33: Clinical Cardiac Magnetic Resonance Spectroscopy, in Manning WJ, Pennell DJ (eds): Cardiovascular Magnetic Resonance. Philadelphia, PA, Churchill Livingstone, 2002, pp 437-446 31. McCrohon JA, Moon JCC, Prasad SK, et al: Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation 108:54-59, 2003
M
agnetic resonance (MR) is based on the phenomenon of the resonance of atomic nuclei to radiofrequency (RF) waves.1 Hydrogen is the most abundant element in the human body which shows this phenomenon, and it contains a single proton in its nucleus. Hydrogen nuclei align with the axis of a magnetic field to create a net longitudinal magnetization and this can be disturbed by RF energy at the resonant frequency. After a short delay, the energy is re-emitted as an RF signal which can be used to form an image. Transmission and reception of RF energy is via special aerials known as coils with subsequent conversion of this raw data into images involving ultrafast computers and Fourier transformation. The resonant frequency of hydrogen nuclei is proportional to the strength of the main magnetic field. Most clinical cardiovascular magnetic resonance (CMR) is currently performed at 1.5T (Tesla) but higher field strengths are used for research on tissue and animals. The degree of nucleus excitation is a product of both the amplitude and duration of the RF pulse, and the rate of relaxation is defined by 2 parameters known as T1 and T2. Relaxation varies according to the environment of the hydrogen in tissues. The imaging sequences can be varied to give *Department of Cardiology, Hospital of Lainz, Vienna, Austria. †Cardiovascular Magnetic Resonance Unit, Royal Brompton Hopsital, London, UK. ‡Department of Radiology, Hospital of Lainz, Vienna, Austria. §Joint first author. Address reprint requests to Katharina Kiss, MD, CMR Unit Lainz, Department of Cardiology, Hospital of Lainz, Wolkersbergenstrasse 1, 1130 Vienna, Austria. E-mail: [email protected]
1043-0679/04/$-see front matter © 2004 Elsevier Inc. All rights reserved. doi:10.1053/j.semtcvs.2004.08.009
different weighting to one of these relaxation parameters, allowing tissue characterization. The two main types of sequence used in CMR are gradient echo (GRE) and spin echo (SE). In general, when using GRE sequences, both blood and fat appear white. This technique enables the acquisition of cine images, which can identify areas of focal myocardial dysfunction and abnormal flow patterns (Fig. 1, video 1). Variations of GRE techniques include fast low-angle shot (FLASH), fast imaging with steady-state precession (FISP) and velocity mapping. In principle, velocity mapping is similar to a form of 2-dimensional Doppler.2 With SE techniques, blood generally appears black and fat appears white. This sequence is more useful for anatomical as opposed to functional imaging. Another important technique used in CMR is a prepulse to create tissue contrast. One example is the inversion recovery technique which can be used to yield high T1 contrast. CMR consists of applying these sequences and their variants to determine cardiac physiology, anatomy, tissue characterisation, and vascular angiography. Evaluation of cardiac metabolism is also possible with MR spectroscopy. Another important aspect of CMR is its excellent safety profile. The contrast agents used for MR (gadolinium chelates) are much safer than x-ray agents and are not nephrotoxic. Patients with prosthetic heart valves, sternal wires, retained epicardial pacing leads, intracoronary stents, and joint replacements can be safely scanned.3,4 CMR on patients with permanent pacemakers is being performed occasionally under strict conditions and only in specialist centres,5 and currently remains a strong relative contraindication. Implantable defibrillators are currently contraindicated. Cerebrovascular 235
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Figure 3 and Video 3a Large apical thrombus after myocardial infarction. The late enhancement image clearly shows a white area (apical) which clearly depicts the scar myocardial infarction. Video 3b Perfusion imaging of apical thrombus demonstrating the lack of contrast uptake. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
Figure 1 and Video 1 GRE technique (TrueFISP) long axis four chamber view showing normal left ventricular function. (Video loop is available online at http://www3.us.elsevierhealth.com/semtcvs/.)
aneurysm clips are problematic because of possible ferromagnetic properties and specialist advice is required.
Current CMR Indications 1. Ischaemic Heart Disease A. Myocardial Infarction CMR is increasingly being used in the assessment of myocardial infarction in both the early and chronic phase. Its ability to assess regions of focal myocardial wall thinning and wall motion abnormalities by high-resolution cine imaging are well established. Aneurysm formation can be easily detected by both SE and GE techniques (Fig. 2, video 2a ⫹ b) and mural thrombi are clearly identified with the technique of early gadolinium enhancement (Fig. 3 video 3a ⫹ b). This involves imaging at 1 to 2 minutes after the intravenous injection of a gadolinium chelate contrast agent. Such early imaging can also be used to define the extent of microvascular obstruction (MVO) in acute infarction (Fig. 4, video 4). Areas of MVO within an acute infarct appear dark because of very slow entry of gadolinium. The presence of MVO by CMR has been shown to be an independent predictor of adverse prognosis.6 The technique of late gadolinium enhancement in-
Figure 2 and Video 2a ⴙ b GRE two-chamber view showing an extended aneurysm of the inferior wall postmyocardial infarction. The video 2b shows an additional LVOT view. (Larger version of figure and video loops are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
volves imaging of the myocardium 10 to 15 minutes after gadolinium. In the late phase, gadolinium chelates distribute in the extracellular space, which is increased in acute infarction due to cell membrane breakdown, and in chronic infarction due to fibrosis (Fig. 5a ⫹ b, video 5a ⫹ b).7 Gadolinium accumulation greatly increases the T1 relaxation and areas of abnormality show as bright signal on heavily T1 weighted scans. Typically, an inversion recovery prepulse is used to null (force to near zero) signal from normal myocardium to highlight this differential uptake. Animal experiments in acute infarction have shown that the volume of signal enhancement and infarct size are closely correlated. Late gadolinium enhancement has high resolution and can also define the transmurality of infarcts and identify whether infarction has actually occurred in borderline cases. B. Assessment of Myocardial Viability Late gadolinium enhancement has clinical application in the assessment of viability. Assessment of the percentage of transmural replacement of normal myocardium by scar is a predictor of postrevascularisation contraction recovery. In general, dysfunctional segments with less than 50% transmural replacement show improved function, whilst those with higher grades of transmural replacement fail to improve.8 Compared with resting thallium single photon emission computed tomography (SPECT), CMR has improved sensitivity, specificity, and accuracy in predicting myocardial viability early after acute myocardial infarction.9 In patients with chronic ischaemic heart disease and left ventricular dysfunc-
Figure 4 and Video 4 The dark zone embedded in the clearer zone demonstrates microvascular obstruction (MVO) after transmural posterolateral infarction (right image shows CINE short axis view after application of Gd–DTPA, left image is the corresponding viability image. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
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3. Cardiac Masses
Figure 5a ⴙ b and Video 5 a ⴙ b GRE Cine Sequence (5a) of a midventricular short axis view and corresponding late enhancement image (5b) after myocardial infarction of the posterolateral wall. In the viability image, the transmurality of the scar can be visualized. (Larger version of figure and video loops are available online at http://www3.us.elsevierhealth.com/semtcvs/.)
tion, CMR has a high accuracy compared with 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) for the detection of myocardial viability.10 C. Dobutamine Stress Testing Compared with stress echocardiography, CMR has improved diagnostic capability related to improved results from those patients in whom echocardiographic windows are suboptimal or poor.11 CMR should be considered as a first line approach in this group of patients.
2. Valvular Heart Disease CMR can complement transthoracic and transoesophageal echocardiography (TTE and TOE) in some cases. Echocardiography is good for direct visualization of valve leaflets and their suspensory apparatus or vegetations. CMR is able to accurately quantify valvular regurgitation, peak trans-stenotic jet velocities, ventricular volumes, and myocardial mass, and can detect associated intracardiac thrombi.12 In valvular regurgitation, regurgitant flow is quantified from the reverse flow measurement in diastole with an imaging plane placed just downstream of the aortic and pulmonary valve.13 Isolated mitral regurgitation can be evaluated by subtraction of aortic flow from left ventricular stroke volume. CMR jet velocity mapping is useful for assessment of stenoses where ultrasonic access is limited as in calcified or deformed aortic valves. Jet velocity mapping is combined with cine imaging, the latter identifies the jet core and directs where subsequent imaging planes for assessment of peak velocity are placed. Imaging patients with prosthetic valves is more problematic as with echocardiography. Prosthetic valves contain no mobile hydrogen atoms and so are not visualized directly, but they do cause a localised signal void. In mitral valve surgery, CMR can depict the anatomy of the valve and surrounding structures such as papillary muscles with clarity and in any plane. (Fig. 6, video 6a ⫹ b).
CMR defines the size and anatomical relations of intra and extracardiac masses with high resolution (Fig. 7, video 7).14 The commonest intracardiac filling defect is thrombus and the imaging of this has already been discussed. CMR tissue characterization using a combination of T1 and T2 weighted images in association with gadolinium injection provides useful information. T1 and T2 weighted images differ between masses depending on their biochemical composition, and this can be used to differentiate between them. For example, pericardial cysts have a characteristic high signal on T2 weighted imaging. The fat content of tumours can be identified by acquiring images before and after fat suppression pulses. Gadolinium injection is particurly valuable in this setting. The first pass shows vascularity, the early enhancement shows associated thrombus, and the late enhancement indicates tumour fibrosis. The vascularity of malignant tumours such as angiosarcoma is usually high, but benign tumous such as haemangioma and myxoma also enhance. Generally, malignant cardiac tumours are larger, show evidence of invasion, have a broader attachment, involve more than one cardiac chamber or great vessel, and show evidence of pericardial or extracardiac extension.
4. Pericardium and Pericardial Disease Pericardial thickness is a good guide to the presence of constriction and can be readily measured using CMR. CMR estimates of pericardial thickness (usually ⬍4 mm) is greater than expected from pathological studies due to the phenomenon of chemical shift. This effect is caused by differences in the resonant frequency of protons within the thin fibrous pericardial tissue compared with the overlying layer of fat. Normal pericardium appears black with CMR since it has a low water content, but can enhance with contrast in acute inflammation, and then appears white. Pericardial effusions are black with SE sequences and bright on GE cines. Calcium also appears black on CMR and therefore, an area of pericardial calcification can simply appear as a localised area of pericardial thickening. Computed tomography (CT) is the recommended modality for confirmation or exclusion of calcification. Differentiation of constrictive pericarditis from restrictive cardiomyopathy is important since the former can be successfully treated surgically with pericardiectomy, while the latter requires medical treatment. CMR can facilitate the
Figure 6 and Video 6 Regurgitant mitral valve in short axis and long axis view. In the long axis, the free movement of the papillary muscles due to a rupture of the tendinae cordae can be seen. (Larger version of figure and video loop are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
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Figure 7a ⴙ b and Video 7 Right atrial lipoma clearly identified by applying a fat sat prepulse. (Larger version of figure and video loop are available online at http://www3.us.elsevierhealth.com/ semtcvs/.)
analysis of diastolic septal motion during ventricular filling and the presence of this and a thickened fibrotic and/or calcified pericardium is more suggestive of a constrictive picture.15
5. Angiography CMR angiography is usually performed with the injection of gadolinium. CMR angiography of arterial and venous vessels, other than the coronaries, is rapidly becoming the clinical test of choice. Data are usually displayed as a 3D rotating cine. A. Aorta The entire length of the aorta is easily investigated by CMR. Gross morphology is rapidly obtained using multi-slice SE images in the transverse and oblique sagittal planes. The “hockey stick” view enables accurate and reproducible assessment of the diameter of the aorta in aneurysms, evaluation or exclusion of aortic dissections, and identification of coarctation. Cine imaging using true-FISP techniques are useful in all three of these conditions. High-resolution SE imaging can evaluate the extent of aortic dissections including involvement of other vessels and delineation of areas of thrombus and atheroma (Fig. 9). CMR has been shown in randomised trials to be more accurate than TOE and CT in acute dissection and also provides a safe, noninvasive and radiation free modality for follow-up.16 B. Coronary Arteries Coronary CMR can be performed using breath-hold or navigator-based, free breathing techniques with or without intravenous contrast. There have been tremendous improvements in these techniques since their first description in 1993.17 A recent multi-centre study concluded that among patients referred for their first coronary angiogram, 3D CMR allows accurate detection of coronary artery disease in the proximal and middle segments and can reliably identify or exclude left main coronary artery or three-vessel disease (Fig. 8, video 8).18 Imaging of native coronary arteries remains
challenging, but visualization of bypass grafts is more feasible due to their more superficial course, greater size, and relative lack of cardiac motion. Sequences used are primarily 3D navigator-based sequences as well as conventional SE techniques such as half-Fourier fast spin-echo, also known as HASTE. Evaluation of coronary flow reserve in bypass grafts by flow mapping pre- and postadenosine can be used to gauge significant stenosis. Congenital abnormalities of the origin and course of coronary arteries are an important cause of sudden cardiac death, especially in young adults. Their prevalence has been estimated at 0.85% in adults referred for diagnostic angiography, but up to 30% in patients with other forms of congenital heart disease.19 The most common anomaly is the left circumflex artery arising from the right sinus of Valsalva or right coronary artery, but the most clinically important variations are those which pass between the aortic root and right ventricular outflow tract (RVOT) or pulmonary artery (PA). These are associated with myocardial ischaemia or infarction as well as syncope and sudden death. Radiograph coronary angiography can identify the anomalous origin of the coronary artery but is suboptimal for defining the subsequent proximal course with relation to the aorta, RVOT and PA. This requires a tomographic technique such as CMR, which is now the gold standard. C. Carotids, Pulmonary, Renal, Mesenteric, and Peripheral Arteries Assessment of carotid disease is moving away from invasive radiograph based angiography, with its associated small but significant mortality and morbidity, to 3D CMR.20 CMR can also be used for visualisation of the pulmonary, renal, mesenteric and peripheral arteries.21 Thrombus imaging with CMR is very sensitive in the venous system,22 and comparisons with established techniques for detection of DVT and PE are under way.
6. Congenital Heart Disease A. Coarctation of the Aorta Coarctation of the aorta accounts for approximately 6% of congenital heart disease with the stenosis, usually in the region of the ligamentum arteriosum. CMR is useful in the rapid diagnosis, safe follow-up, and noninvasive assessment of severity in aortic coarctation. Initial diagnosis can be performed with SE, GE, or angiography techniques. Significant coarctation is present if the gradient at catheterization is more than 20 mm Hg in the absence of a well-developed collateral circulation. If the latter is present, there may be minimal or no gradient and there may be associated aortic atresia. A
Figure 8 Breath-hold versus non-breathhold true-FISP images of the LAD in the same patient. (Larger version of figure is available online at http://www3.us.elsevierhealth.com/semtcvs/.)
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volumes in valvular regurgitation is absent. Similar methods can be used to evaluate the significance of extracardiac shunts such as patent ductus arteriosus. C. Complex Congenital Heart Disease CMR has revolutionized the management of patients with complex congenital heart disease by providing accurate anatomical and functional intra and extracardiac assessment preand postintervention whilst obviating the need for repeated invasive cardiac catheterization. TOE is better at defining fine structures such as valves while CMR is better at showing flow, conduits and great vessel anatomy.23 Preoperative CMR is excellent for surgical planning and other uses include accurate flow quantification in the assessment of the severity of pulmonary regurgitation following repair of Fallot’s tetralogy, postoperative follow-up of patients with corrected transposition of the great arteries and evaluation of the patency of surgical conduits used in Fontan’s procedure.
7. Pharmaceutical Industry Research and Development Figure 9 MIP Reconstruction of an aortic dissection differentiating the true and false lumen.
significant gradient causes proximal pressure elevation and will lead to left ventricular hypertrophy and ultimately heart failure unless other complications supervene. CMR is used for both preoperative and postoperative evaluation in aortic coarctation. Surgical repair can be complicated by recoarctation and aneurysm formation and serial assessment of these patients is therefore essential. CMR jet velocity mapping is used to assess the gradient across the coarctation site. Additionally, accurate assessment of ventricular mass and function and the exclusion of other cardiovascular abnormalities, such as a bicuspid aortic valve, can be performed in the same examination. Routine CMR follow-up in this patient population involves continued assessment of the left ventricle as well as the coarctation site. B. ASD/VSD CMR is complementary to TTE and TOE in the evaluation of atrial septal defects and ventricular septal defects. Echocardiography is superior for the diagnosis of these defects, and CMR is used for assessment of functional significance since it can provide a noninvasive measurement of the pulmonaryto-systemic flow ratio (Qp/Qs). This involves the use of CMR velocity mapping. This uses the signal phase of each pixel which can be encoded to relate linearly with velocity and produce 2 dimensional velocity maps which correspond with the anatomy from the normal images. Because the area of a vessel can be measured and the mean velocity within the vessel calculated, absolute measurements of instantaneous flow can be derived. When run in cine mode throughout the cardiac cycle, flow curves are generated, where the area under the curve represents true flow in the vessel through the cardiac cycle. In this way, flow through the aorta and PA can be compared and used to derive a Qp/Qs. This can also be derived from comparison of right and left ventricular stroke
Ventricular function, volumes and mass is linked to prognosis in coronary artery and other cardiac disease. Radionuclide techniques and echocardiography suffer from assumptions and suboptimal image quality which makes them less reproducible than CMR.24 The improved interstudy reproducibility of CMR has been recognized by the pharmaceutical industry who are increasingly using CMR for phase 2 and 3 drug development studies to reduce costs by reducing sample sizes.
Future CMR Uses 1. Myocardial Perfusion Approximately 6 million perfusion studies are performed annually in the USA, and all involve significant ionizing radiation. Perfusion CMR may provide the diagnostic and prognostic information obtained by this established technique without the need for ionizing radiation. Currently, perfusion CMR uses a baseline first pass rest perfusion study after intravenous gadolinium given peripherally, and a repeat study during adenosine stress. Areas of reduced perfusion appear darker than normal myocardium. Perfusion CMR also has high resolution which allows in vivo visualization of suben-
Figure 10 and Video 10 Stress perfusion imaging with septal hypokinesia and subendocardial perfusion defect. (Larger version of figure and video loop are available online at http:// www3.us.elsevierhealth.com/semtcvs/.)
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Figure 12 High-resolution SE cross-sectional image through the right common carotid artery (RCCA) showing atheromatous plaque. (Larger version of figure is available online.)
2. Cardiac Transplantation CMR may have a future role in the assessment of acute rejection post cardiac transplantation. Acute rejection is characterized by increased cardiac mass and myocardial signal on SE sequences, indicative of myocardial oedema and/or infiltration of mononuclear cells. These changes are not specific but may provide valuable additional information in the relevant clinical setting. SE imaging of the vessel wall might also help in the detection of early graft disease often seen by intravascular ultrasound in this patient group.
3. Evaluation of Atherosclerotic plaque CMR can depict plaques (Figs. 11 and 12) and interrogate their lipid constituents and integrity of the fibrous cap, which are factors that determine the propensity for plaque rupture and thrombus formation. Plaques more prone to rupture (vulnerable plaques) have characteristic structural features including reduced vascular smooth muscle content and a thin fibrous cap overlying a large lipid core. The concept of arterial remodeling (Glagov phenomenon) is being increasingly recognized and describes how luminal cross-sectional area can be preserved in the face of advanced atherosclerosis within the arterial wall.26,27 CMR is an ideal tool for assessing remodeling and has been successfully used to show this phenomenon in relation to prolonged statin treatment on carotid and aortic atherosclerotic plaque disease.28 Detection of cor-
Figure 11 Carotid CE-MRA showing almost complete occlusion of the right internal carotid artery. (Larger version of figure is available online.)
onary atherosclerotic plaques is also possible though more diffficult.29
4. MR Spectroscopy MR spectroscopy (MRS) provides a noninvasive way of obtaining metabolic information and can be conducted on a number of important nuclei including phosphorus (31P), hydrogen (1H), and carbon (13C).30 MRS can quantify highenergy phosphate compounds such as adenosine triphosphate and creatine phosphate that fuel myocardial contraction and are necessary for myocardial viability and this technique holds future promise in the evaluation of hibernating or stunned myocardium.
Discussion High-resolution visualization of cardiac anatomy has long been a strength of CMR but more recently advances in the noninvasive evaluation of cardiac function offer exciting new applications. CMR can detect subtle changes in wall motion and ejection fraction, making it useful in the follow-up of patients postrevascularization and with heart failure. Recent work has highlighted the use of CMR with late gadolinium enhancement in the differentiation of left ventricular dysfunction related to dilated cardiomyopathy (DCM) or coronary artery disease (CAD) on the basis of myocardial patterns of enhancement.31 In CAD, a subendocardial or transmural pattern is seen while midwall changes suggest DCM. The question of myocardial viability can be accurately addressed with a combination of cine imaging and late gadolinium enhancement, with or without low dose dobutamine. CMR perfusion is in rapid development and holds particular promise in combination with cine imaging and late gadolinium enhancement. The resolution and robustness of radiograph coronary angiography for the evaluation of luminal coronary artery stenoses remains superior to CMR, but the concepts of the vulnerable plaque and arterial remodeling are calling into question the value of such luminography alone. In one decade, CMR evaluation of the coronary arterial tree has made impressive advances. These advances are sure to continue, and will importantly incorporate not only the interrogation of plaque constituents and the tomographic assessment of the vessel wall, but also the evaluation of coronary flow, flow reserve, and functional consequences to the myocardium.
Cardiovascular magnetic resonance: Current clinical practice and future potential
Conclusion CMR is poised to enter routine clinical practice in many cardiac centers worldwide. With the current pace of hardware and software developments, it will soon become an invaluable tool to both the cardiologist and cardiothoracic surgeon.
Appendix Supplementary data associated with this article can be found, in the online version, at doi: 10.1053/j.semtcvs.2004.08.009.
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