© 2014, Wiley Periodicals, Inc. DOI: 10.1111/echo.12399
Echocardiography
IMAGING THE RIGHT HEART
Right Ventricular Cardiomyopathies: A Multidisciplinary Approach to Diagnosis Giuseppe Limongelli, M.D., Ph.D., F.E.S.C., F.A.H.A.,* Alessandra Rea, M.D.,* Daniele Masarone, M.D.,* M. Paola Francalanci,† Aris Anastasakis, M.D., Ph.D.,‡ Raffaele Calabro’, M.D.,* Russo Maria Giovanna, M.D.,* Eduardo Bossone, M.D., Ph.D.,§ Perry Mark Elliott, M.D.,¶ and Giuseppe Pacileo, M.D.* *Division of Cardiology, Monaldi Hospital, Second University of Naples, Naples, Italy; †Department of , Rome, Italy; ‡First Cardiology Department, University of Pathology, Children’s Hospital Bambino Gesu Athens, Medical School, Athens, Greece; §Division of Cardiology, Heart Department, University of Salerno, Salerno, Italy; and ¶Department of Inherited Cardiovascular Disease, The Heart Hospital, University College London, London, United Kingdom
The physiological importance of the right ventricle (RV) has been underestimated over the past years. Finally in the early 1950s through the 1970s, cardiac surgeons recognized the importance of RV function. Since then, the importance of RV function has been recognized in many acquired cardiac heart disease. RV can be mainly or together with left ventricle (LV) affected by inherited or acquired cardiomyopathy. In fact, RV morphological and functional remodeling occurs more common during cardiomyopathies than in ischemic cardiomyopathies and more closely parallels LV dysfunction. Moreover, there are some cardiomyopathy subtypes showing a predominant or exclusive involvement of the RV, and they are probably less known by cardiologists. The clinical approach to right ventricular cardiomyopathies is often challenging. Imaging is the first step to raise the suspicion and to guide the diagnostic process. In the differential diagnosis, cardiologists should consider athlete’s heart, congenital heart diseases, multisystemic disorders, and inherited arrhythmias. However, a multiparametric and multidisciplinary approach, involving cardiologists, experts in imaging, geneticists, and pathologists with a specific expertise in these heart muscle disorders is required. (Echocardiography 2014;00:1–20) Key words: cardiomyopathy, right ventricle, arrhythmogenic RV dysplasia (ARVD) In 1616, Sir William Harvey first describes the importance of right ventricle (RV) function in his study, De Motu Cordis: “Thus the RV may be said to be made for the sake of transmitting blood through the lungs, not for nourishing them.”1 Despite this over the next 400 years, the importance of the RV have been debated, with some investigators opining well into the 20th century that the RV served no purpose other than to provide capacitance to the pulmonary circulation.2 Finally in the early 1950s through the 1970s, cardiac surgeons recognized the importance of right-sided function as they evaluated procedures to palliate right-heart hypoplasia. Since then, the importance of RV function has been recognized in pulmonary hypertension, congenital heart disease, coronary artery disease, heart failure, and valvular heart disease.3 Address for correspondence and reprint requests: Limongelli Giuseppe, M.D., Ph.D., F.E.S.C., F.A.H.A., Division of Cardiology, Monaldi Hospital, Second University of Naples, Naples, Italy. Fax: +39-081-7062815; E-mail: [email protected]
Moreover, RV can be mainly or together with left ventricle (LV) affected by inherited or acquired cardiomyopathy. RV morphological and functional remodeling occurs more common during cardiomyopathies than in ischemic cardiomyopathies and more closely parallels LV dysfunction. Also some cardiomyopathies shows a predominant or exclusive involvement of the RV, this particular type of cardiomyopathies are less know by cardiologist than the other cardiomyopathies. In this review, we explore the RV morphology and functional analysis, discussing the diagnosis of RV cardiomyopathies and the differential diagnosis with physiological and pathological conditions. Echocardiographic Evaluation of RV: The RV is anatomically subdivided into the inflow tract, the infundibulum (outflow tract), and the apex. Commonly used methods for calculating diameters, areas, and volumes of the LV are difficult to implement for the RV and are typi1
Limongelli, et al.
cally not performed.4 Because of the complex morphology of the RV, no single view or imaging plane will provide enough information to adequately evaluate RV structure and function. As such, cardiologist should perform thorough assessments of the RV from standard two-dimensional (2D) acoustic windows that include RV inflow tract and RV outflow tract (RVOT) views, parasternal long-axis view (PLAX), parasternal short-axis views (PSAX), and apical views. Measurements of RV chamber dimensions should include the diameters above the tricuspid valve (TV) annulus and in the mid-RV cavity, as well as the distance from the TV annulus to the RV apex5 (Fig. 1A–D). The basal diameter is generally defined as the maximal short-axis dimension in the basal one-third of the RV seen on the four-chamber view. In the normal RV, the maximal short-axis dimension is usually located in the basal one-third of the ventricular cavity. The mid-cavity diameter is measured in the middle
third of the RV at the level of the LV papillary muscles. The longitudinal dimension is drawn from the plane of the tricuspid annulus to the RV apex. The RVOT is generally considered to include the subpulmonary infundibulum, or conus, and the pulmonary valve. The subpulmonary infundibulum is a cone-shaped muscular structure that extends from the crista supraventricularis to the pulmonary valve. The RVOT is best viewed from the long-axis parasternal and subcostal windows, but it also may be evaluated from the apical window in thin individuals or adults with large rib spaces. The size of the RVOT should be measured at end-diastole on the QRS deflection. In the PLAX view, a portion of the proximal RVOT can be measured. In the PSAX view, the RVOT linear dimension can be measured from (1) the anterior aortic wall to the RV free wall above the aortic valve (RVOT-Prox) and (2) just proximal to the pulmonary valve (RVOT-Distal).
A
B
C
D
Figure 1. Evaluation of right ventricle (RV) chamber dimension. A. Measurement of RV diameter in parasternal long-axis view. B. Measurement of RV diameter in PSAX view. C. Measurement of pulmonary infundibulum/aortic valve ratio in PSAX view. D. Measurement of mid-right ventricular diameter measured in apical four-chamber view.
2
Right Ventricular Cardiomyopathies
The assessment of RV systolic function by the calculation of RV fractional area change (RVFAC) represents a “surrogate” measurement of RV ejection fraction (RVEF) and is expressed as a percentage change in the RV chamber area from end-diastole to end-systole, rather than changes in volume. The RVFAC is calculated as follows: [end-diastolic area (cmq) end-systolic area (cmq)]/end-diastolic area (cmq).6 Compared with other measures of RV systolic function, including M-mode–derived tricuspid annular motion (TAPSE) and transverse fractional shortening (Fig. 2A and B), RVFAC (Fig. 2C and D) was found to correlate best with cardiac magnetic resonance (CMR)-derived RVEF.7 Measurements of RVFAC are obtained in the apical four-chamber view. Planimetry of the RV cavity area is traced across the TV annulus along the endocardium, then around the apex at the enddiastolic and end-systolic frames. Measure of TAPSE is another method used in evaluating RV systolic function, obtained by M-Mode echocardiography. With the M-mode cursor aligned through the anterior tricuspid
annulus in the apical four-chamber view, longitudinal displacement of the annulus toward the apex during systole can be recorded. Tissue Doppler imaging (TDI) and strain imaging (SI) are newer echocardiographic methods that provide objective assessments of global and regional RV function.8 TDI and SI can complement 2D methods. Both methods are not significantly affected by volume loading conditions, and both have demonstrated acceptable reproducibility. TDI and SI are relatively easy to obtain from the tricuspid annulus and RV free wall. The peak S-waveform occurs during mechanical systole following pulmonary valve opening and represents active RV contraction. The fine three-dimensional (3D) echocardiography has emerged as a new technique capable of assessing more accurately than 2D echocardiography the size and systolic function of the RV (Fig. 3A–C). A change in RV shape and volume can be the first sign of RV dysfunction, pressure or volume overload, or arrhythmogenic RV dysplasia/cardiomyopathy.
A
B
C
D
Figure 2. Evaluation of right ventricle (RV) systolic function A. Measurement of tricuspid annular plane systolic excursion. B. Measurement of peak S-waveform at level of RV free wall. C. and D. Evaluation of fraction area change in RV.
3
Limongelli, et al.
A
B
Figure 3. Evaluation of right ventricle (RV) function and dimension by new echocardiographic techniques. A. Evaluation of RV systolic function using two-dimensional speckle tracking. B. Evaluation of RV volumes using three-dimensional echocardiography.
The simplest and most routinely used method for assessing RV volume includes linear dimensions and areas obtained from single tomographic echocardiographic planes. The best correlations between single plane measurements and RV volumes have been obtained with the maximal short-axis dimension and the planimetered RV area (in the four-chamber view). Significant overlap has been noted, however, between normal and volume-overloaded conditions, especially for mild-to-moderate enlargement.9 In an effort to be more accurate, different approaches have been sought to directly measure RV volume. These include the area-length method and Simpson’s rule approach. However, these 2D echocardiography-derived indices have the disadvantage of being dependent of geometric assumption and have been estimated less accurate. Threedimensional echocardiography is a promising technique that could lead to more accurate assessment of RV volume. However, visualization of the anterior wall and inclusion of the infundib4
ulum in a simple model remain difficult, which explains the variable correlations with CMR and cast models.10,11 Cardiac magnetic resonance is considered the most reliable method for measuring RV volumes. An ideal index of contractility should be independent of afterload and preload, sensitive to change in inotropy, independent of heart size and mass, easy and safe to apply, and proven to be useful in the clinical setting. In clinical practice, RVEF is the most commonly used index of RV contractility. Although widely accepted, RVEF is highly dependent on loading conditions and may not adequately reflect contractility. Right ventricle fractional area change represents the ratio of systolic area change to diastolic RV area. It is measured in the four-chamber view and can be incorporated systematically into the basic echocardiographic study. In end-stage pulmonary disease, a good correlation has been reported between RVFAC and RVEF.12 In patients
Right Ventricular Cardiomyopathies
with arrhythmogenic RV dysplasia/cardiomyopathy who meet the Task Force diagnostic criteria for this condition, Yoerger and colleagues13 showed that RVFAC
Echocardiography
IMAGING THE RIGHT HEART
Right Ventricular Cardiomyopathies: A Multidisciplinary Approach to Diagnosis Giuseppe Limongelli, M.D., Ph.D., F.E.S.C., F.A.H.A.,* Alessandra Rea, M.D.,* Daniele Masarone, M.D.,* M. Paola Francalanci,† Aris Anastasakis, M.D., Ph.D.,‡ Raffaele Calabro’, M.D.,* Russo Maria Giovanna, M.D.,* Eduardo Bossone, M.D., Ph.D.,§ Perry Mark Elliott, M.D.,¶ and Giuseppe Pacileo, M.D.* *Division of Cardiology, Monaldi Hospital, Second University of Naples, Naples, Italy; †Department of , Rome, Italy; ‡First Cardiology Department, University of Pathology, Children’s Hospital Bambino Gesu Athens, Medical School, Athens, Greece; §Division of Cardiology, Heart Department, University of Salerno, Salerno, Italy; and ¶Department of Inherited Cardiovascular Disease, The Heart Hospital, University College London, London, United Kingdom
The physiological importance of the right ventricle (RV) has been underestimated over the past years. Finally in the early 1950s through the 1970s, cardiac surgeons recognized the importance of RV function. Since then, the importance of RV function has been recognized in many acquired cardiac heart disease. RV can be mainly or together with left ventricle (LV) affected by inherited or acquired cardiomyopathy. In fact, RV morphological and functional remodeling occurs more common during cardiomyopathies than in ischemic cardiomyopathies and more closely parallels LV dysfunction. Moreover, there are some cardiomyopathy subtypes showing a predominant or exclusive involvement of the RV, and they are probably less known by cardiologists. The clinical approach to right ventricular cardiomyopathies is often challenging. Imaging is the first step to raise the suspicion and to guide the diagnostic process. In the differential diagnosis, cardiologists should consider athlete’s heart, congenital heart diseases, multisystemic disorders, and inherited arrhythmias. However, a multiparametric and multidisciplinary approach, involving cardiologists, experts in imaging, geneticists, and pathologists with a specific expertise in these heart muscle disorders is required. (Echocardiography 2014;00:1–20) Key words: cardiomyopathy, right ventricle, arrhythmogenic RV dysplasia (ARVD) In 1616, Sir William Harvey first describes the importance of right ventricle (RV) function in his study, De Motu Cordis: “Thus the RV may be said to be made for the sake of transmitting blood through the lungs, not for nourishing them.”1 Despite this over the next 400 years, the importance of the RV have been debated, with some investigators opining well into the 20th century that the RV served no purpose other than to provide capacitance to the pulmonary circulation.2 Finally in the early 1950s through the 1970s, cardiac surgeons recognized the importance of right-sided function as they evaluated procedures to palliate right-heart hypoplasia. Since then, the importance of RV function has been recognized in pulmonary hypertension, congenital heart disease, coronary artery disease, heart failure, and valvular heart disease.3 Address for correspondence and reprint requests: Limongelli Giuseppe, M.D., Ph.D., F.E.S.C., F.A.H.A., Division of Cardiology, Monaldi Hospital, Second University of Naples, Naples, Italy. Fax: +39-081-7062815; E-mail: [email protected]
Moreover, RV can be mainly or together with left ventricle (LV) affected by inherited or acquired cardiomyopathy. RV morphological and functional remodeling occurs more common during cardiomyopathies than in ischemic cardiomyopathies and more closely parallels LV dysfunction. Also some cardiomyopathies shows a predominant or exclusive involvement of the RV, this particular type of cardiomyopathies are less know by cardiologist than the other cardiomyopathies. In this review, we explore the RV morphology and functional analysis, discussing the diagnosis of RV cardiomyopathies and the differential diagnosis with physiological and pathological conditions. Echocardiographic Evaluation of RV: The RV is anatomically subdivided into the inflow tract, the infundibulum (outflow tract), and the apex. Commonly used methods for calculating diameters, areas, and volumes of the LV are difficult to implement for the RV and are typi1
Limongelli, et al.
cally not performed.4 Because of the complex morphology of the RV, no single view or imaging plane will provide enough information to adequately evaluate RV structure and function. As such, cardiologist should perform thorough assessments of the RV from standard two-dimensional (2D) acoustic windows that include RV inflow tract and RV outflow tract (RVOT) views, parasternal long-axis view (PLAX), parasternal short-axis views (PSAX), and apical views. Measurements of RV chamber dimensions should include the diameters above the tricuspid valve (TV) annulus and in the mid-RV cavity, as well as the distance from the TV annulus to the RV apex5 (Fig. 1A–D). The basal diameter is generally defined as the maximal short-axis dimension in the basal one-third of the RV seen on the four-chamber view. In the normal RV, the maximal short-axis dimension is usually located in the basal one-third of the ventricular cavity. The mid-cavity diameter is measured in the middle
third of the RV at the level of the LV papillary muscles. The longitudinal dimension is drawn from the plane of the tricuspid annulus to the RV apex. The RVOT is generally considered to include the subpulmonary infundibulum, or conus, and the pulmonary valve. The subpulmonary infundibulum is a cone-shaped muscular structure that extends from the crista supraventricularis to the pulmonary valve. The RVOT is best viewed from the long-axis parasternal and subcostal windows, but it also may be evaluated from the apical window in thin individuals or adults with large rib spaces. The size of the RVOT should be measured at end-diastole on the QRS deflection. In the PLAX view, a portion of the proximal RVOT can be measured. In the PSAX view, the RVOT linear dimension can be measured from (1) the anterior aortic wall to the RV free wall above the aortic valve (RVOT-Prox) and (2) just proximal to the pulmonary valve (RVOT-Distal).
A
B
C
D
Figure 1. Evaluation of right ventricle (RV) chamber dimension. A. Measurement of RV diameter in parasternal long-axis view. B. Measurement of RV diameter in PSAX view. C. Measurement of pulmonary infundibulum/aortic valve ratio in PSAX view. D. Measurement of mid-right ventricular diameter measured in apical four-chamber view.
2
Right Ventricular Cardiomyopathies
The assessment of RV systolic function by the calculation of RV fractional area change (RVFAC) represents a “surrogate” measurement of RV ejection fraction (RVEF) and is expressed as a percentage change in the RV chamber area from end-diastole to end-systole, rather than changes in volume. The RVFAC is calculated as follows: [end-diastolic area (cmq) end-systolic area (cmq)]/end-diastolic area (cmq).6 Compared with other measures of RV systolic function, including M-mode–derived tricuspid annular motion (TAPSE) and transverse fractional shortening (Fig. 2A and B), RVFAC (Fig. 2C and D) was found to correlate best with cardiac magnetic resonance (CMR)-derived RVEF.7 Measurements of RVFAC are obtained in the apical four-chamber view. Planimetry of the RV cavity area is traced across the TV annulus along the endocardium, then around the apex at the enddiastolic and end-systolic frames. Measure of TAPSE is another method used in evaluating RV systolic function, obtained by M-Mode echocardiography. With the M-mode cursor aligned through the anterior tricuspid
annulus in the apical four-chamber view, longitudinal displacement of the annulus toward the apex during systole can be recorded. Tissue Doppler imaging (TDI) and strain imaging (SI) are newer echocardiographic methods that provide objective assessments of global and regional RV function.8 TDI and SI can complement 2D methods. Both methods are not significantly affected by volume loading conditions, and both have demonstrated acceptable reproducibility. TDI and SI are relatively easy to obtain from the tricuspid annulus and RV free wall. The peak S-waveform occurs during mechanical systole following pulmonary valve opening and represents active RV contraction. The fine three-dimensional (3D) echocardiography has emerged as a new technique capable of assessing more accurately than 2D echocardiography the size and systolic function of the RV (Fig. 3A–C). A change in RV shape and volume can be the first sign of RV dysfunction, pressure or volume overload, or arrhythmogenic RV dysplasia/cardiomyopathy.
A
B
C
D
Figure 2. Evaluation of right ventricle (RV) systolic function A. Measurement of tricuspid annular plane systolic excursion. B. Measurement of peak S-waveform at level of RV free wall. C. and D. Evaluation of fraction area change in RV.
3
Limongelli, et al.
A
B
Figure 3. Evaluation of right ventricle (RV) function and dimension by new echocardiographic techniques. A. Evaluation of RV systolic function using two-dimensional speckle tracking. B. Evaluation of RV volumes using three-dimensional echocardiography.
The simplest and most routinely used method for assessing RV volume includes linear dimensions and areas obtained from single tomographic echocardiographic planes. The best correlations between single plane measurements and RV volumes have been obtained with the maximal short-axis dimension and the planimetered RV area (in the four-chamber view). Significant overlap has been noted, however, between normal and volume-overloaded conditions, especially for mild-to-moderate enlargement.9 In an effort to be more accurate, different approaches have been sought to directly measure RV volume. These include the area-length method and Simpson’s rule approach. However, these 2D echocardiography-derived indices have the disadvantage of being dependent of geometric assumption and have been estimated less accurate. Threedimensional echocardiography is a promising technique that could lead to more accurate assessment of RV volume. However, visualization of the anterior wall and inclusion of the infundib4
ulum in a simple model remain difficult, which explains the variable correlations with CMR and cast models.10,11 Cardiac magnetic resonance is considered the most reliable method for measuring RV volumes. An ideal index of contractility should be independent of afterload and preload, sensitive to change in inotropy, independent of heart size and mass, easy and safe to apply, and proven to be useful in the clinical setting. In clinical practice, RVEF is the most commonly used index of RV contractility. Although widely accepted, RVEF is highly dependent on loading conditions and may not adequately reflect contractility. Right ventricle fractional area change represents the ratio of systolic area change to diastolic RV area. It is measured in the four-chamber view and can be incorporated systematically into the basic echocardiographic study. In end-stage pulmonary disease, a good correlation has been reported between RVFAC and RVEF.12 In patients
Right Ventricular Cardiomyopathies
with arrhythmogenic RV dysplasia/cardiomyopathy who meet the Task Force diagnostic criteria for this condition, Yoerger and colleagues13 showed that RVFAC
