A dvanc es i n MR I mag ing A s s e s s m e n t of A d u l t s with Congenital Heart Disease Nazima N. Kathiria, DO*, Charles B. Higgins, MD, Karen G. Ordovas, MD, MAS KEYWORDS Congenital heart disease Complex congenital cardiac disease 4D flow Ventricular strain Delayed enhancement T1 mapping 3D cardiac model Tetralogy of fallot
KEY POINTS Novel MR imaging techniques for the assessment of patients with congenital heart disease include 4-dimensional flow imaging, myocardial strain imaging, tissue characterization tools, and 3-dimensional modeling. Current clinical research publications highlight potential applications for these techniques in the near future.
Cardiac MR imaging is a well-established method for the diagnosis and follow-up of adult patients with congenital heart disease (CHD).1 One of the primary roles of MR imaging in these patients is in the postoperative assessment and guidance for the timing of reintervention. Recent advances in cardiac MR imaging have the potential to increase the scope of clinical applications in these patients, expanding its role for not only diagnosis and follow-up but also risk stratification. In this review, recent work on novel cardiac MR imaging methods in adult patients with CHD is emphasized.
NEW CLINICAL APPLICATIONS Flow Imaging Velocity-encoded cine MR imaging is a robust technique used clinically for the quantification of blood flow. In patients with CHD, the main application of this technique is to quantify regurgitant volumes and estimate the severity of cardiac shunts.
The development of 4-dimensional (4D) flow imaging has many potential applications in adult patients with CHD. The technique consists of a comprehensive evaluation of vascular hemodynamics, achieved through the combined data acquisition of 3 spatial dimensions and 3 blood flow velocity directions during the cardiac cycle. Recent work from Hope and colleagues2,3 focused on the application of 4D flow imaging in patients with coarctation of the aorta and bicuspid aortic valve. The authors showed that the quantification of collateral flow in patients with hemodynamically significant coarctation can be accurately obtained with 4D-flow imaging, using 2-dimensional (2D) flow techniques as the standard of reference.2 In addition to providing comparable collateral flow quantification to 2D flow technique, the 4D flow approach allows for a more comprehensive evaluation of the thoracic aorta flow, including assessment of aortic valve dynamics and estimation of associated aortic valve stenosis owing to bicuspid aortic valve. Finally, the 3-dimensional (3D) acquisition allows for repositioning of the flow measurement planes
The authors have nothing to disclose. Department of Radiology, Cardiac and Pulmonary Imaging, University of California, San Francisco, 505 Parnassus Avenue, San Francisco, CA 94143-0628, USA * Corresponding author. E-mail address: [email protected] Magn Reson Imaging Clin N Am 23 (2015) 35–40 http://dx.doi.org/10.1016/j.mric.2014.09.005 1064-9689/15/$ – see front matter Published by Elsevier Inc.
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INTRODUCTION
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Kathiria et al during the postprocessing analysis, unlike the standard 2D flow technique.2 Additional applications of 4D flow in patients with CHD have been investigated. A general advantage of the method is to allow for quantification of blood flow in multiple vessels with single acquisition. Therefore, patients with complex CHD can have a mapping of the venous and arterial blood flow obtained in a timely manner.4 Meadows and colleagues5 successfully used the single-acquisition 4D approach to evaluate differential pulmonary flow, pulmonary regurgitation, and pulmonary stenosis in patients with tetralogy of Fallot (TOF). Four-dimensional technique permits evaluation of multiple vessels with a single acquisition and allows for the alteration of planes of choice during the postprocessing phase, unlike with 2D flow technique. These characteristics suggest added value for 4D flow imaging in clinical evaluation of patients with CHD. The main limitations for widespread clinical applications of 4D flow include time-consuming data collection and analysis and limited spatial resolution for flow analysis in smaller vessels. The development of optimized fast sequences using sparse sampling techniques shows promise in decreasing scan time and improving spatial resolution.6
Quantification of Ventricular Mechanics In current clinical practice, steady-state free precession (SSFP) cine images are the most useful sequences for qualitative and quantitative assessment of ventricular function. Volumetric analysis of SSFP images, usually obtained in the short-axis plane, permit quantification of ventricular volumes and ejection fractions. Furthermore, regional function can be quantified by measuring ventricular wall thickening during the cardiac cycle. Advanced techniques for quantification of regional myocardial strain have the potential to identify myocardial dysfunction before depression of global measures of ventricular contractility, such as ejection fraction. Different methods have been proposed for quantification of myocardial strain, which is usually measured in 3 components: circumferential, longitudinal, and radial strain.7 Applications of myocardial strain imaging in patients with CHD have been a recent focus of clinical research. Ordovas and colleagues8 described how MR imaging tagging (Fig. 1) can aid in the early detection of left ventricular dysfunction in patients with pulmonary regurgitation after repair of TOF and normal left ventricular ejection fraction and pulmonary regurgitation after repair of TOF. The authors showed that patients with TOF have
significantly decreased left ventricular peak circumferential strain in the base and apex levels compared with normal volunteers. Moreover, the left ventricular peak rotation at the basilar and midventricular levels was also delayed in these patients compared with volunteers. Additionally, the same investigators used SSFP cine sequences for quantification of ventricular septal excursion in patients after repair of TOF (Fig. 2). Abnormal ventricular septal excursion was associated with reduced global and septal left ventricular systolic function. It also corresponded with the presence of fibrosis at the left ventricular septum and at the right and left ventricular hinge points, suggesting the technique may be able to identify adverse interventricular interaction.9 Further applications of strain imaging in CHD include the assessment of ventricle-ventricle interaction such as in patients with a single right ventricle. Fogel and colleagues10 compared single right ventricles with systemic right ventricles and found significant differences in regional wall motion and strain in single ventricle physiology depending whether a left ventricle was present to augment function. Additionally, Young and colleagues described the directionally dependent changes in strain in postaortic coarctation repair patients. They found that subjects with an increased ejection fraction also had increased strain in the circumferential direction and decreased strain in the longitudinal direction, suggesting that the elevated ejection fraction may be related to myocardial hypertrophy.7
Scar Imaging Delayed gadolinium enhancement sequences have become a common tool in the evaluation of ischemic and nonischemic cardiomyopathies. Furthermore, it is an extremely useful prognostic tool in some CHDs, particularly in TOF. BabuNarayan and colleagues11 studied 92 adult patients after TOF repair using delayed enhancement imaging. They determined that delayed enhancement is commonly seen within the right ventricular outflow tract and ventricular septal defect patch sites but may also involve the inferior right ventricle insertion point and the left ventricle. The delayed enhancement seen within the right and left ventricles in these patients correlated with increased age, impaired exercise capacity, ventricular dysfunction, and cardiac arrhythmias.1 These findings may be helpful in guiding management, such as timing for reintervention or need for ablation to treat and prevent arrhythmias. Other forms of CHD are found to have delayed enhancement after surgery, including single
MR Imaging Assessment of Adults
Fig. 1. Tagging acquisition of a patient with TOF at end-diastole (left) and end-systole (right) at 3 separate levels from cranial (top) to caudal (bottom).
ventricle post-Norwood procedure, which is typically within the aortic homograft.12 However, additional studies on clinical relevance of abnormal delayed enhancement in CHD other than TOF remain to be determined. T1 mapping is another, more recent, novel technique for myocardial tissue characterization. Regional fibrosis can be precisely identified with delayed enhancement imaging; however, diffuse myocardial fibrosis can also be assessed through calculation of the global T1 relaxation time and extracellular volume.13,14
Broberg and colleagues13 compared the right and left ventricular volumes and the ejection fraction to evaluate for diffuse left ventricular fibrosis in 50 adult patients with CHD. Fibrosis values were significantly elevated in patients with CHD compared with normal controls. Diffuse fibrosis was highest in single right ventricle patients and cyanotic patients. Also, a relationship was found between ventricular enddiastolic volume and function. These findings could be useful for prognostic characterization of patients with CHD.
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Fig. 2. Patients after repair of TOF. Delayed enhancement images in the short axis plane at the right ventricular outflow tract (RVOT) level (A) and midventricular level (B). Note the abnormal enhancement along the RVOT (arrowheads), and in the anterior and inferior ventricular junction points (arrows).
Although T1 mapping and evaluation of the extracellular volume seem promising clinically, the technique is still challenging given the variability of T1 values between scanners and different sequences used for its quantification. Moreover, larger clinical trials are necessary for confident correlations of the findings between diffuse fibrosis values and the outcomes of patients with CHD.13,14
3-Dimensional Models Challenges in surgical correction of patients with complex CHDs have led to growing interest in the cardiology community for tools to help facilitate the preoperative planning, such as with 3D plastic models of the heart. Three-dimensional cardiac specimens from computed tomography and MR imaging is a cutting-edge tool that can assist the cardiac surgeon with planning before
Fig. 3. Complex CHD patient with a double outlet right ventricle and upstairs-downstairs ventricular relationship. Virtual interactive 3D model reconstructed from a gadolinium enhancement MR angiography in an anterior (A) and posterior (B) projection.
MR Imaging Assessment of Adults the correction of complex CHD. Another potential application is to inform interventionalists on the selection of stents and catheters that would be the most effective for correction of various cardiac lesions. The cardiac models may be created as a virtual 3D structure that allows for interactive manipulation (Fig. 3). Alternatively, these 3D models can be printed to provide tangible depiction of the cardiac anatomy and potentially more precise planning of the surgical correction approach, by using stored computed tomography or MR images as a stereolithography file. Using a 3D Cartesian coordinate system, the printer creates a specimen using a mixture of fluid-binding substances and ink. Layer upon layer of plaster powder is placed to create the predetermined regions of interest in the heart.15 Dr Yoo16 has 2 years of clinical experience creating 3D plastic cardiac models for the preoperative assessment of patients with double outlet right ventricle. They suggest that this technology be expanded to produce cardiac models to permit practice procedures in patients with complex anatomy. In addition, it should encompass models of various surgical pathways such as Fontan and right ventricle to pulmonary artery conduit to further assess flow through complicated postsurgical pathways. Also, they believe a collection of teaching phantoms, including normal and pathologic cardiovascular anatomy, should be created. Finally, they suggest that the technique should eventually be enhanced to combine imaging data from multiple modalities.16 Although building 3D cardiac models of complex CHD has tremendous potential to facilitate surgical and interventional approaches for the treatment of complex CHD, the technique still has limitations. One of the primary limitations of the technique is that it is costly to generate printed heart models. In addition, it is time consuming to generate the data and then create the phantoms. Furthermore, sometimes the texture and flexibility of the material used to make the 3D model are not satisfactory to simulate the human heart and great vessels.17
SUMMARY Advanced cardiac MR techniques for myocardial tissue characterization, flow evaluation, myocardial strain analysis, and 3D modeling have been recently used for assessment of adult patients after repair of CHD. Although these methods are being used mostly in the research arena, several potential diagnostic and prognostic applications are suggested.
REFERENCES 1. Kilner PJ. Imaging congenital heart disease in adults. Br J Radiol 2011;84(Spec No 3):S258–68. 2. Hope MD, Meadows AK, Hope TA, et al. Clinical evaluation of aortic coarctation with 4D flow MR imaging. J Magn Reson Imaging 2010;31(3):711–8. 3. Hope MD, Hope TA, Crooke SE, et al. 4D flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging 2011;4(7): 781–7. 4. Francois CJ, Srinivasan S, Schiebler ML, et al. 4D cardiovascular magnetic resonance velocity mapping of alterations of right heart flow patterns and main pulmonary artery hemodynamics in tetralogy of Fallot. J Cardiovasc Magn Reson 2012;14:16. 5. Meadows AK, Hope MD, Saloner D, et al. 4D flow for accurate assessment of differential pulmonary arterial flow in patients with tetralogy of Fallot, in 12th Annual SCMR Scientific Session. Journal of Cardiovascular Magnetic Resonance; January 28, 2009. 6. Markl M, Frydrychowicz A, Kozerke S, et al. 4D flow MRI. J Magn Reson Imaging 2012;36(5):1015–36. 7. Augustine D, Lewandowski AJ, Lazdam M, et al. Global and regional left ventricular myocardial deformation measures by magnetic resonance feature tracking in healthy volunteers: comparison with tagging and relevance of gender. J Cardiovasc Magn Reson 2013;15:8. 8. Ordovas KG, Carlsson M, Lease KE, et al. Impaired regional left ventricular strain after repair of tetralogy of Fallot. J Magn Reson Imaging 2012; 35(1):79–85. 9. Muzzarelli S, Ordovas KG, Cannavale G, et al. Tetralogy of Fallot: impact of the excursion of the interventricular septum on left ventricular systolic function and fibrosis after surgical repair. Radiology 2011;259(2):375–83. 10. Fogel MA. A study in ventricular-ventricular interaction. Single right ventricles compared with systemic right ventricles in a dual-chamber circulation. Circulation 1995;92(2):219–30. 11. Babu-Narayan SV. Ventricular fibrosis suggested by cardiovascular magnetic resonance in adults with repaired tetralogy of fallot and its relationship to adverse markers of clinical outcome. Circulation 2006;113(3):405–13. 12. Harris MA. Delayed-enhancement cardiovascular magnetic resonance identifies fibrous tissue in children after surgery for congenital heart disease. J Thorac Cardiovasc Surg 2007;133(3):676–81. 13. Broberg CS. Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging 2010;3(6):727–34. 14. Moon JC. Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular
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Kathiria et al Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson 2013;15:92. 15. Greil GF. Stereolithographic reproduction of complex cardiac morphology based on high spatial resolution imaging. Clin Res Cardiol 2007;96(3): 176–85.
16. Thabit O, Yoo SJ. Rapid prototyping of cardiac models: current utilization and future directions. J Cardiovasc Magn Reson 2012;14:T13. 17. Abdel-Sayed S, von Segesser LK. Rapid prototyping for training purposes in cardiovascular surgery. In: Hoque M, editor. Advanced applications of rapid prototyping technology in modern engineering. Rijeka, Croatia: In Tech; 2011. p. 1–15.
KEY POINTS Novel MR imaging techniques for the assessment of patients with congenital heart disease include 4-dimensional flow imaging, myocardial strain imaging, tissue characterization tools, and 3-dimensional modeling. Current clinical research publications highlight potential applications for these techniques in the near future.
Cardiac MR imaging is a well-established method for the diagnosis and follow-up of adult patients with congenital heart disease (CHD).1 One of the primary roles of MR imaging in these patients is in the postoperative assessment and guidance for the timing of reintervention. Recent advances in cardiac MR imaging have the potential to increase the scope of clinical applications in these patients, expanding its role for not only diagnosis and follow-up but also risk stratification. In this review, recent work on novel cardiac MR imaging methods in adult patients with CHD is emphasized.
NEW CLINICAL APPLICATIONS Flow Imaging Velocity-encoded cine MR imaging is a robust technique used clinically for the quantification of blood flow. In patients with CHD, the main application of this technique is to quantify regurgitant volumes and estimate the severity of cardiac shunts.
The development of 4-dimensional (4D) flow imaging has many potential applications in adult patients with CHD. The technique consists of a comprehensive evaluation of vascular hemodynamics, achieved through the combined data acquisition of 3 spatial dimensions and 3 blood flow velocity directions during the cardiac cycle. Recent work from Hope and colleagues2,3 focused on the application of 4D flow imaging in patients with coarctation of the aorta and bicuspid aortic valve. The authors showed that the quantification of collateral flow in patients with hemodynamically significant coarctation can be accurately obtained with 4D-flow imaging, using 2-dimensional (2D) flow techniques as the standard of reference.2 In addition to providing comparable collateral flow quantification to 2D flow technique, the 4D flow approach allows for a more comprehensive evaluation of the thoracic aorta flow, including assessment of aortic valve dynamics and estimation of associated aortic valve stenosis owing to bicuspid aortic valve. Finally, the 3-dimensional (3D) acquisition allows for repositioning of the flow measurement planes
The authors have nothing to disclose. Department of Radiology, Cardiac and Pulmonary Imaging, University of California, San Francisco, 505 Parnassus Avenue, San Francisco, CA 94143-0628, USA * Corresponding author. E-mail address: [email protected] Magn Reson Imaging Clin N Am 23 (2015) 35–40 http://dx.doi.org/10.1016/j.mric.2014.09.005 1064-9689/15/$ – see front matter Published by Elsevier Inc.
mri.theclinics.com
INTRODUCTION
36
Kathiria et al during the postprocessing analysis, unlike the standard 2D flow technique.2 Additional applications of 4D flow in patients with CHD have been investigated. A general advantage of the method is to allow for quantification of blood flow in multiple vessels with single acquisition. Therefore, patients with complex CHD can have a mapping of the venous and arterial blood flow obtained in a timely manner.4 Meadows and colleagues5 successfully used the single-acquisition 4D approach to evaluate differential pulmonary flow, pulmonary regurgitation, and pulmonary stenosis in patients with tetralogy of Fallot (TOF). Four-dimensional technique permits evaluation of multiple vessels with a single acquisition and allows for the alteration of planes of choice during the postprocessing phase, unlike with 2D flow technique. These characteristics suggest added value for 4D flow imaging in clinical evaluation of patients with CHD. The main limitations for widespread clinical applications of 4D flow include time-consuming data collection and analysis and limited spatial resolution for flow analysis in smaller vessels. The development of optimized fast sequences using sparse sampling techniques shows promise in decreasing scan time and improving spatial resolution.6
Quantification of Ventricular Mechanics In current clinical practice, steady-state free precession (SSFP) cine images are the most useful sequences for qualitative and quantitative assessment of ventricular function. Volumetric analysis of SSFP images, usually obtained in the short-axis plane, permit quantification of ventricular volumes and ejection fractions. Furthermore, regional function can be quantified by measuring ventricular wall thickening during the cardiac cycle. Advanced techniques for quantification of regional myocardial strain have the potential to identify myocardial dysfunction before depression of global measures of ventricular contractility, such as ejection fraction. Different methods have been proposed for quantification of myocardial strain, which is usually measured in 3 components: circumferential, longitudinal, and radial strain.7 Applications of myocardial strain imaging in patients with CHD have been a recent focus of clinical research. Ordovas and colleagues8 described how MR imaging tagging (Fig. 1) can aid in the early detection of left ventricular dysfunction in patients with pulmonary regurgitation after repair of TOF and normal left ventricular ejection fraction and pulmonary regurgitation after repair of TOF. The authors showed that patients with TOF have
significantly decreased left ventricular peak circumferential strain in the base and apex levels compared with normal volunteers. Moreover, the left ventricular peak rotation at the basilar and midventricular levels was also delayed in these patients compared with volunteers. Additionally, the same investigators used SSFP cine sequences for quantification of ventricular septal excursion in patients after repair of TOF (Fig. 2). Abnormal ventricular septal excursion was associated with reduced global and septal left ventricular systolic function. It also corresponded with the presence of fibrosis at the left ventricular septum and at the right and left ventricular hinge points, suggesting the technique may be able to identify adverse interventricular interaction.9 Further applications of strain imaging in CHD include the assessment of ventricle-ventricle interaction such as in patients with a single right ventricle. Fogel and colleagues10 compared single right ventricles with systemic right ventricles and found significant differences in regional wall motion and strain in single ventricle physiology depending whether a left ventricle was present to augment function. Additionally, Young and colleagues described the directionally dependent changes in strain in postaortic coarctation repair patients. They found that subjects with an increased ejection fraction also had increased strain in the circumferential direction and decreased strain in the longitudinal direction, suggesting that the elevated ejection fraction may be related to myocardial hypertrophy.7
Scar Imaging Delayed gadolinium enhancement sequences have become a common tool in the evaluation of ischemic and nonischemic cardiomyopathies. Furthermore, it is an extremely useful prognostic tool in some CHDs, particularly in TOF. BabuNarayan and colleagues11 studied 92 adult patients after TOF repair using delayed enhancement imaging. They determined that delayed enhancement is commonly seen within the right ventricular outflow tract and ventricular septal defect patch sites but may also involve the inferior right ventricle insertion point and the left ventricle. The delayed enhancement seen within the right and left ventricles in these patients correlated with increased age, impaired exercise capacity, ventricular dysfunction, and cardiac arrhythmias.1 These findings may be helpful in guiding management, such as timing for reintervention or need for ablation to treat and prevent arrhythmias. Other forms of CHD are found to have delayed enhancement after surgery, including single
MR Imaging Assessment of Adults
Fig. 1. Tagging acquisition of a patient with TOF at end-diastole (left) and end-systole (right) at 3 separate levels from cranial (top) to caudal (bottom).
ventricle post-Norwood procedure, which is typically within the aortic homograft.12 However, additional studies on clinical relevance of abnormal delayed enhancement in CHD other than TOF remain to be determined. T1 mapping is another, more recent, novel technique for myocardial tissue characterization. Regional fibrosis can be precisely identified with delayed enhancement imaging; however, diffuse myocardial fibrosis can also be assessed through calculation of the global T1 relaxation time and extracellular volume.13,14
Broberg and colleagues13 compared the right and left ventricular volumes and the ejection fraction to evaluate for diffuse left ventricular fibrosis in 50 adult patients with CHD. Fibrosis values were significantly elevated in patients with CHD compared with normal controls. Diffuse fibrosis was highest in single right ventricle patients and cyanotic patients. Also, a relationship was found between ventricular enddiastolic volume and function. These findings could be useful for prognostic characterization of patients with CHD.
37
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Kathiria et al
Fig. 2. Patients after repair of TOF. Delayed enhancement images in the short axis plane at the right ventricular outflow tract (RVOT) level (A) and midventricular level (B). Note the abnormal enhancement along the RVOT (arrowheads), and in the anterior and inferior ventricular junction points (arrows).
Although T1 mapping and evaluation of the extracellular volume seem promising clinically, the technique is still challenging given the variability of T1 values between scanners and different sequences used for its quantification. Moreover, larger clinical trials are necessary for confident correlations of the findings between diffuse fibrosis values and the outcomes of patients with CHD.13,14
3-Dimensional Models Challenges in surgical correction of patients with complex CHDs have led to growing interest in the cardiology community for tools to help facilitate the preoperative planning, such as with 3D plastic models of the heart. Three-dimensional cardiac specimens from computed tomography and MR imaging is a cutting-edge tool that can assist the cardiac surgeon with planning before
Fig. 3. Complex CHD patient with a double outlet right ventricle and upstairs-downstairs ventricular relationship. Virtual interactive 3D model reconstructed from a gadolinium enhancement MR angiography in an anterior (A) and posterior (B) projection.
MR Imaging Assessment of Adults the correction of complex CHD. Another potential application is to inform interventionalists on the selection of stents and catheters that would be the most effective for correction of various cardiac lesions. The cardiac models may be created as a virtual 3D structure that allows for interactive manipulation (Fig. 3). Alternatively, these 3D models can be printed to provide tangible depiction of the cardiac anatomy and potentially more precise planning of the surgical correction approach, by using stored computed tomography or MR images as a stereolithography file. Using a 3D Cartesian coordinate system, the printer creates a specimen using a mixture of fluid-binding substances and ink. Layer upon layer of plaster powder is placed to create the predetermined regions of interest in the heart.15 Dr Yoo16 has 2 years of clinical experience creating 3D plastic cardiac models for the preoperative assessment of patients with double outlet right ventricle. They suggest that this technology be expanded to produce cardiac models to permit practice procedures in patients with complex anatomy. In addition, it should encompass models of various surgical pathways such as Fontan and right ventricle to pulmonary artery conduit to further assess flow through complicated postsurgical pathways. Also, they believe a collection of teaching phantoms, including normal and pathologic cardiovascular anatomy, should be created. Finally, they suggest that the technique should eventually be enhanced to combine imaging data from multiple modalities.16 Although building 3D cardiac models of complex CHD has tremendous potential to facilitate surgical and interventional approaches for the treatment of complex CHD, the technique still has limitations. One of the primary limitations of the technique is that it is costly to generate printed heart models. In addition, it is time consuming to generate the data and then create the phantoms. Furthermore, sometimes the texture and flexibility of the material used to make the 3D model are not satisfactory to simulate the human heart and great vessels.17
SUMMARY Advanced cardiac MR techniques for myocardial tissue characterization, flow evaluation, myocardial strain analysis, and 3D modeling have been recently used for assessment of adult patients after repair of CHD. Although these methods are being used mostly in the research arena, several potential diagnostic and prognostic applications are suggested.
REFERENCES 1. Kilner PJ. Imaging congenital heart disease in adults. Br J Radiol 2011;84(Spec No 3):S258–68. 2. Hope MD, Meadows AK, Hope TA, et al. Clinical evaluation of aortic coarctation with 4D flow MR imaging. J Magn Reson Imaging 2010;31(3):711–8. 3. Hope MD, Hope TA, Crooke SE, et al. 4D flow CMR in assessment of valve-related ascending aortic disease. JACC Cardiovasc Imaging 2011;4(7): 781–7. 4. Francois CJ, Srinivasan S, Schiebler ML, et al. 4D cardiovascular magnetic resonance velocity mapping of alterations of right heart flow patterns and main pulmonary artery hemodynamics in tetralogy of Fallot. J Cardiovasc Magn Reson 2012;14:16. 5. Meadows AK, Hope MD, Saloner D, et al. 4D flow for accurate assessment of differential pulmonary arterial flow in patients with tetralogy of Fallot, in 12th Annual SCMR Scientific Session. Journal of Cardiovascular Magnetic Resonance; January 28, 2009. 6. Markl M, Frydrychowicz A, Kozerke S, et al. 4D flow MRI. J Magn Reson Imaging 2012;36(5):1015–36. 7. Augustine D, Lewandowski AJ, Lazdam M, et al. Global and regional left ventricular myocardial deformation measures by magnetic resonance feature tracking in healthy volunteers: comparison with tagging and relevance of gender. J Cardiovasc Magn Reson 2013;15:8. 8. Ordovas KG, Carlsson M, Lease KE, et al. Impaired regional left ventricular strain after repair of tetralogy of Fallot. J Magn Reson Imaging 2012; 35(1):79–85. 9. Muzzarelli S, Ordovas KG, Cannavale G, et al. Tetralogy of Fallot: impact of the excursion of the interventricular septum on left ventricular systolic function and fibrosis after surgical repair. Radiology 2011;259(2):375–83. 10. Fogel MA. A study in ventricular-ventricular interaction. Single right ventricles compared with systemic right ventricles in a dual-chamber circulation. Circulation 1995;92(2):219–30. 11. Babu-Narayan SV. Ventricular fibrosis suggested by cardiovascular magnetic resonance in adults with repaired tetralogy of fallot and its relationship to adverse markers of clinical outcome. Circulation 2006;113(3):405–13. 12. Harris MA. Delayed-enhancement cardiovascular magnetic resonance identifies fibrous tissue in children after surgery for congenital heart disease. J Thorac Cardiovasc Surg 2007;133(3):676–81. 13. Broberg CS. Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging 2010;3(6):727–34. 14. Moon JC. Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular
39
40
Kathiria et al Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson 2013;15:92. 15. Greil GF. Stereolithographic reproduction of complex cardiac morphology based on high spatial resolution imaging. Clin Res Cardiol 2007;96(3): 176–85.
16. Thabit O, Yoo SJ. Rapid prototyping of cardiac models: current utilization and future directions. J Cardiovasc Magn Reson 2012;14:T13. 17. Abdel-Sayed S, von Segesser LK. Rapid prototyping for training purposes in cardiovascular surgery. In: Hoque M, editor. Advanced applications of rapid prototyping technology in modern engineering. Rijeka, Croatia: In Tech; 2011. p. 1–15.
