J Clin Monit Comput DOI 10.1007/s10877-014-9551-0
ORIGINAL RESEARCH
Right ventricular function in late-onset Pompe disease Abdallah Fayssoil • Olivier Nardi • Djillali Annane David Orlikowski
•
Received: 1 June 2013 / Accepted: 4 January 2014 Ó Springer Science+Business Media New York 2014
Abstract Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. The right ventricular (RV) function is a determinant parameter of clinical outcome in patients with heart failure. We sought to characterize the RV function using Doppler-echocardiography completed by Doppler tissular imaging and tricuspid annular plane systolic excursion (TAPSE) measurement. We analyzed retrospectively clinical and Doppler-echocardiographic data of patients with adult late onset Pompe disease and compared to a control group. Ten patients with late onset Pompe disease were included in our study and were compared to a control group (seven patients). Mean age was 56.7 ± 10.2 years in late onset Pompe disease versus 55 ± 21 years in control group (p = 0.65). Left ventricular ejection fraction (LVEF) was similar in the two groups (LVEF 63.7 ± 9 vs 63.7 ± 6.6 % in control group p = 0.99). LV end diastolic diameter was 40.8 ± 6 mm in Pompe disease versus 45.8 ± 6 mm in control group (p = 0.11). Mean TAPSE was similar in the two groups (25.6 ± 6.2 vs 21.5 ± 2.7 mm p = 0.23). Mean peak systolic RV velocity Sm was not significantly different in A. Fayssoil O. Nardi D. Annane D. Orlikowski Re´animation Me´dicale, Hoˆpital Raymond Poincare´ (AP-HP), Universite´ de Versailles SQY, 104 Boulevard Raymond Poincare´, 92380 Garches, France A. Fayssoil D. Annane D. Orlikowski Centre d’investigation clinique et Innovation the´rapeutique et Unite´ de recherche´ EA 4497, Garches, France A. Fayssoil (&) Critical Care Unit, Hospital Raymond Poincare (AP-HP), University of Versailles SQY, 104 Boulevard Raymond Poincare, 92380 Garches, France e-mail: [email protected]
the two groups (17.11 ± 3.4 cm/s in Pompe disease vs 16.14 ± 3.8 cm/s in control group p = 0.61). Mean peak early diastolic Ea velocity in the RV were not significantly different in the two groups (15.6 ± 5.6 vs 18.2 ± 4.9 cm/s p = 0.34). According to our data, RV systolic function seems preserved in late-onset Pompe disease. Keywords ventricle
Pompe disease Echocardiography Right
1 Introduction Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. Glycogen accumulation is caused by a deficiency of alpha 1,4 glucosidase (lysosomial enzyme). This defect leads to destruction of muscle tissue progressively. The adult form (late-onset Pompe disease) is less severe because of partial enzymatic activity. Clinical manifestations begin in the third or fourth decade with limb-girdle dystrophy. Left ventricular function has been described in the literature [1]. The right ventricular (RV) function is a determinant parameter of clinical outcome in heart failure. No data have been reported about RV function in late-onset Pompe disease. Echocardiography-Doppler is a simple and reproducible ultrasound imaging for the assessment of heart function. Moreover, Doppler tissue imaging (DTI), by studying tissular velocity is an interesting tool for analysing sub clinical ventricular dysfunction [2]. Also, the tricuspid annular plane systolic excursion (TAPSE) is an echocardiography parameter for the assessment of RV systolic function. We sought to characterize the RV function using Doppler-echocardiography completed by DTI and tricuspid annular plane systolic excursion (TAPSE) measurement.
123
J Clin Monit Comput
2 Materials and methods All adult patients with late-onset Pompe disease were included retrospectively and compared to a control group. Echocardiography was performed with a Siemens CV70. Patients were examined in the left lateral decubitus position. M-mode was performed from the parasternal long axis for the analysis of the following parameters: LV enddiastolic septal and posterior wall thickness, and LV enddiastolic dimensions. LV ejection fraction was calculated from LV volumes using Teicholtz method from parasternal long axis view or from Simpson method from the four apical chamber view. From the apical four chamber view, DTI was applied at the free wall angle of the tricuspid valve annulus. During the procedure, the angle between the Doppler beam and the longitudinal motion of the investigated structure was adjusted to a minimal level. We recorded, using DTI, the early diastolic RV peak velocity (Ea) and the RV systolic peak velocity (Sm). The TAPSE was recorded from the apical four chamber view with the M-mode cursor positioned at the free wall angle of the tricuspid valve annulus, and the excursion was measured from end-systole to end-diastole [3]. 2.1 Statistics analysis Data are expressed as mean ± SD. Data were compared using paired Student’s t test. A p value of \0.05 was considered statistically significant.
3 Results Ten patients with late onset Pompe disease were included in our study (six males and four females) and compared to a control group (seven patients). Mean age was 56.7 ± 10.2 years in late onset Pompe disease versus 55 ± 21 years in control group (p = 0.65). 3/10 patients with late-onset Pompe disease disclosed a history of treated essential hypertension. Seven patients among patients with late onset Pompe disease were treated with enzyme replacement therapy (alpha glucosidase). Mean vital capacity (CV) was 34.7 ± 15.4 %. Home assisted mechanical ventilation was performed in 6/10 patients. All patients with late onset Pompe disease were in sinus rhythm. A short PR (PR duration at 80 ms) was found in one patient. One patient disclosed a right complete bundle branch block and two patients have a ratio R/V [1 in right precordial leads. LV systolic function was persevered in patients with late onset Pompe disease. Mean LV ejection fraction (LVEF) in Pompe disease was 63.7 ± 9 versus 63.7 ± 6.6 % in control group (p = 0.99). Mean LV end-diastolic diameter
123
Table 1 Echocardiographic data in Pompe disease compared to control group Pompe disease Age (years)
56.7 (10)
Control group 55 (21)
p 0.65
LVEF (%)
63.7 (9)
63.7 (6.6)
0.99
LVEDD (mm)
40.8 (6)
45.8 (6.2)
0.11
IVS (mm)
9.9 (2.4)
8.4 (1.6)
0.13
PP (mm)
10.7 (2.5)
8.8 (2.1)
0.11
91 (15.9)
0.86
LV mass (g)
89 (28)
LA diameter (mm) TAPSE (mm)
25.5 (5.3) 25.6 (6.2)
25.4 (3.7) 21.5 (2.7)
0.95 0.23
Peak Sm RV (cm/s)
17.11 (3.4)
16.14 (3.8)
0.6
Peak Ea RV (cm/s)
15.6 (5.6)
18.2 (4.9)
0.34
sPAP (mmHg)
27.5 (3.5)
28.1 (2.4)
0.66
Data are expressed as means (SD) LVEDD left ventricular end diastolic diameter, LVEF left ventricular ejection fraction, LV left ventricular, IVS inter-ventricular septal thickness in end-diastolic, PP posterior wall thickness in enddiastolic, LA left atrial, TAPSE tricuspid annular plane systolic excursion, sPAP systolic pulmonary arterial pressure
(LVEDD) was 40.8 ± 6 mm in Pompe disease versus 45.8 ± 6 mm in control group (p = 0.11). Mean LV mass was 89 ± 28 g in Pompe disease versus 91 ± 15.9 g in control group (p = 0.86). Mean left atrial diameter was similar in the two group (25.5 ± 5 mm vs 25.4 ± 3.7 p = 0.95). For the RV systolic function, mean TAPSE was not significantly different in the two groups (25.6 ± 6.2 vs 21.5 ± 2.7 mm p = 0.23). Mean peak systolic RV velocity Sm was similar in the two groups (17.11 ± 3.4 vs 16.14 ± 3.8 cm/s p = 0.61). Mean early peak RV diastolic Ea velocity were not significantly different in the two groups (15.6 ± 5.6 vs 18.2 ± 4.9 cm/s p = 0.34). Mean arterial systolic pressure calculated from the tricuspid regurgitation was similar in the two groups (27.7 ? 3.5 mmHg in Pompe disease vs 28.1 ± 2.4 mmHg in control group). The Table 1 summarises Doppler-echocardiographic data.
4 Discussion This is the first study that analyses the RV function in lateonset Pompe disease. Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. Glycogen accumulation in tissues is caused by a deficiency of alpha 1,4 glucosidase. The enzyme defects is estimated to be 1/40,000 live births. The severity of the disease depends of residual of enzyme activity. The adult form is less severe because of partial
J Clin Monit Comput
enzymatic activity. Heart involvement is uncommon in late-onset Pompe disease. One patient disclosed short a PR duration. A Wolff–Parkinson–White syndrome associated to glycogenosis storage has been reported in the literature [4]. In our study, the LV systolic function was preserved in patients with late onset Pompe disease and LV diameter was in normal ranges in patients (40.8 ± 6 mm in Pompe disease vs 45.8 ± 6 mm in control group p = 0.11). Stollberger and Finsterer [5] reported abnormal myocardial texture. Dilated cardiomyopathy has been described in adult’s patients [6]. Only 1 patient, in late-onset Pompe disease, disclosed LV dysfunction in the study by Soliman et al. [1]. In the study reported by Forsha et al. [7], a short PR was present in 10 % of patients and 7 % of patients disclosed LV dysfunction. The RV function is a determinant parameter of clinical outcome in heart failure. No data have been reported about RV function in late-onset Pompe disease. The tricuspid annular plane systolic displacement (TAPSE) is an echocardiography parameter for the assessment of RV systolic function. The TAPSE is obtained from the long axis four chamber view, using M-mode. This index reflects the systolic axis motion of the RV free wall in the inflow tract [8]. DTI is less preload dependent [9], compared to traditional pulsed Doppler technique. In our study, we did not find RV dysfunction using TAPSE and DTI. In conclusion, according to our data, RV systolic function seems preserved in late-onset Pompe disease.
5 Limits of our study The assessment of the RV function remains difficult because of the complex structure and asymmetrical shape of the RV. The TAPSE discloses limitations because it analyses the inflow free wall tract and not the outflow tract [10]. The TDI is limited by angle dependence. Studies have shown the superiority of magnetic resonance imaging over other techniques in studying the RV [3].
Conflict of interest
None.
References 1. Soliman OI, van der Beek NA, van Doorn PA, Vletter WB, Nemes A, Van Dalen BM, ten Cate FJ, van der Ploeg AT, Geleijnse ML. Cardiac involvement in adults with Pompe disease. J Intern Med. 2008;264(4):333–9. 2. Marwick TH. Techniques for comprehensive two dimensional echocardiographic assessment of left ventricular systolic function. Heart. 2003;89(3):2–8. 3. Lindqvist P, Henein M, Kazzam E. Right ventricular outflow tract fractional shortening: an applicable measure of right ventricular systolic function. Eur J Echocardiogr. 2003;4:29–35. 4. Bulkley BH, Hutchins GM. Pompe’s disease presenting as hypertrophic myocardiopathy with Wolff–Parkinson–White syndrome. Am Heart J. 1978;96(2):246–52. 5. Stollberger C, Finsterer J. Echocardiography in storage and neuromuscular disorders. Wien Klin Wochenschr. 2001;113 (11–12):408–15. 6. Ben-Ami R, Puglisi J, Haider T, Mehta D. The Mount Sinai Hospital clinical pathological conference: a 45-year-old man with Pompe’s disease and dilated cardiomyopathy. Mt Sinai J Med. 2001;68(3):205–12. 7. Forsha D, Li JS, Smith PB, van der Ploeg AT, Kishnani P, Pasquali SK. Late-onset treatment study investigators. Cardiovascular abnormalities in late-onset Pompe disease and response to enzyme replacement therapy. Genet Med. 2011;13(7):625–31. 8. Ghio S, Recusani F, Klersy C, Sebastiani R, Laudisa ML, Campana C, Gavazzi A, Tavazzi L. Prognostic usefulness of the tricuspid annular plane systolic excursion in patients with congestive heart failure secondary to idiopathic or ischemic dilated cardiomyopathy. Am J Cardiol. 2000;85(7):837–42. 9. De Castro S, Cavarretta E, Milan A, Caselli S, Di Angelantonio E, Vizza Carmine D, Lucchetti D, Patel A, Kuvin J, Pandian NG. Usefulness of tricuspid annular velocity in identifying global RV dysfunction in patients with primary pulmonary hypertension: a comparison with 3D echo-derived right ventricular ejection fraction. Echocardiography. 2008;25(3):289–93. 10. Lindqvist P, Calcutteea A, Henein M. Echocardiography in the assessment of right heart function. Eur J Echocardiogr. 2008;9(2):225–34.
123
ORIGINAL RESEARCH
Right ventricular function in late-onset Pompe disease Abdallah Fayssoil • Olivier Nardi • Djillali Annane David Orlikowski
•
Received: 1 June 2013 / Accepted: 4 January 2014 Ó Springer Science+Business Media New York 2014
Abstract Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. The right ventricular (RV) function is a determinant parameter of clinical outcome in patients with heart failure. We sought to characterize the RV function using Doppler-echocardiography completed by Doppler tissular imaging and tricuspid annular plane systolic excursion (TAPSE) measurement. We analyzed retrospectively clinical and Doppler-echocardiographic data of patients with adult late onset Pompe disease and compared to a control group. Ten patients with late onset Pompe disease were included in our study and were compared to a control group (seven patients). Mean age was 56.7 ± 10.2 years in late onset Pompe disease versus 55 ± 21 years in control group (p = 0.65). Left ventricular ejection fraction (LVEF) was similar in the two groups (LVEF 63.7 ± 9 vs 63.7 ± 6.6 % in control group p = 0.99). LV end diastolic diameter was 40.8 ± 6 mm in Pompe disease versus 45.8 ± 6 mm in control group (p = 0.11). Mean TAPSE was similar in the two groups (25.6 ± 6.2 vs 21.5 ± 2.7 mm p = 0.23). Mean peak systolic RV velocity Sm was not significantly different in A. Fayssoil O. Nardi D. Annane D. Orlikowski Re´animation Me´dicale, Hoˆpital Raymond Poincare´ (AP-HP), Universite´ de Versailles SQY, 104 Boulevard Raymond Poincare´, 92380 Garches, France A. Fayssoil D. Annane D. Orlikowski Centre d’investigation clinique et Innovation the´rapeutique et Unite´ de recherche´ EA 4497, Garches, France A. Fayssoil (&) Critical Care Unit, Hospital Raymond Poincare (AP-HP), University of Versailles SQY, 104 Boulevard Raymond Poincare, 92380 Garches, France e-mail: [email protected]
the two groups (17.11 ± 3.4 cm/s in Pompe disease vs 16.14 ± 3.8 cm/s in control group p = 0.61). Mean peak early diastolic Ea velocity in the RV were not significantly different in the two groups (15.6 ± 5.6 vs 18.2 ± 4.9 cm/s p = 0.34). According to our data, RV systolic function seems preserved in late-onset Pompe disease. Keywords ventricle
Pompe disease Echocardiography Right
1 Introduction Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. Glycogen accumulation is caused by a deficiency of alpha 1,4 glucosidase (lysosomial enzyme). This defect leads to destruction of muscle tissue progressively. The adult form (late-onset Pompe disease) is less severe because of partial enzymatic activity. Clinical manifestations begin in the third or fourth decade with limb-girdle dystrophy. Left ventricular function has been described in the literature [1]. The right ventricular (RV) function is a determinant parameter of clinical outcome in heart failure. No data have been reported about RV function in late-onset Pompe disease. Echocardiography-Doppler is a simple and reproducible ultrasound imaging for the assessment of heart function. Moreover, Doppler tissue imaging (DTI), by studying tissular velocity is an interesting tool for analysing sub clinical ventricular dysfunction [2]. Also, the tricuspid annular plane systolic excursion (TAPSE) is an echocardiography parameter for the assessment of RV systolic function. We sought to characterize the RV function using Doppler-echocardiography completed by DTI and tricuspid annular plane systolic excursion (TAPSE) measurement.
123
J Clin Monit Comput
2 Materials and methods All adult patients with late-onset Pompe disease were included retrospectively and compared to a control group. Echocardiography was performed with a Siemens CV70. Patients were examined in the left lateral decubitus position. M-mode was performed from the parasternal long axis for the analysis of the following parameters: LV enddiastolic septal and posterior wall thickness, and LV enddiastolic dimensions. LV ejection fraction was calculated from LV volumes using Teicholtz method from parasternal long axis view or from Simpson method from the four apical chamber view. From the apical four chamber view, DTI was applied at the free wall angle of the tricuspid valve annulus. During the procedure, the angle between the Doppler beam and the longitudinal motion of the investigated structure was adjusted to a minimal level. We recorded, using DTI, the early diastolic RV peak velocity (Ea) and the RV systolic peak velocity (Sm). The TAPSE was recorded from the apical four chamber view with the M-mode cursor positioned at the free wall angle of the tricuspid valve annulus, and the excursion was measured from end-systole to end-diastole [3]. 2.1 Statistics analysis Data are expressed as mean ± SD. Data were compared using paired Student’s t test. A p value of \0.05 was considered statistically significant.
3 Results Ten patients with late onset Pompe disease were included in our study (six males and four females) and compared to a control group (seven patients). Mean age was 56.7 ± 10.2 years in late onset Pompe disease versus 55 ± 21 years in control group (p = 0.65). 3/10 patients with late-onset Pompe disease disclosed a history of treated essential hypertension. Seven patients among patients with late onset Pompe disease were treated with enzyme replacement therapy (alpha glucosidase). Mean vital capacity (CV) was 34.7 ± 15.4 %. Home assisted mechanical ventilation was performed in 6/10 patients. All patients with late onset Pompe disease were in sinus rhythm. A short PR (PR duration at 80 ms) was found in one patient. One patient disclosed a right complete bundle branch block and two patients have a ratio R/V [1 in right precordial leads. LV systolic function was persevered in patients with late onset Pompe disease. Mean LV ejection fraction (LVEF) in Pompe disease was 63.7 ± 9 versus 63.7 ± 6.6 % in control group (p = 0.99). Mean LV end-diastolic diameter
123
Table 1 Echocardiographic data in Pompe disease compared to control group Pompe disease Age (years)
56.7 (10)
Control group 55 (21)
p 0.65
LVEF (%)
63.7 (9)
63.7 (6.6)
0.99
LVEDD (mm)
40.8 (6)
45.8 (6.2)
0.11
IVS (mm)
9.9 (2.4)
8.4 (1.6)
0.13
PP (mm)
10.7 (2.5)
8.8 (2.1)
0.11
91 (15.9)
0.86
LV mass (g)
89 (28)
LA diameter (mm) TAPSE (mm)
25.5 (5.3) 25.6 (6.2)
25.4 (3.7) 21.5 (2.7)
0.95 0.23
Peak Sm RV (cm/s)
17.11 (3.4)
16.14 (3.8)
0.6
Peak Ea RV (cm/s)
15.6 (5.6)
18.2 (4.9)
0.34
sPAP (mmHg)
27.5 (3.5)
28.1 (2.4)
0.66
Data are expressed as means (SD) LVEDD left ventricular end diastolic diameter, LVEF left ventricular ejection fraction, LV left ventricular, IVS inter-ventricular septal thickness in end-diastolic, PP posterior wall thickness in enddiastolic, LA left atrial, TAPSE tricuspid annular plane systolic excursion, sPAP systolic pulmonary arterial pressure
(LVEDD) was 40.8 ± 6 mm in Pompe disease versus 45.8 ± 6 mm in control group (p = 0.11). Mean LV mass was 89 ± 28 g in Pompe disease versus 91 ± 15.9 g in control group (p = 0.86). Mean left atrial diameter was similar in the two group (25.5 ± 5 mm vs 25.4 ± 3.7 p = 0.95). For the RV systolic function, mean TAPSE was not significantly different in the two groups (25.6 ± 6.2 vs 21.5 ± 2.7 mm p = 0.23). Mean peak systolic RV velocity Sm was similar in the two groups (17.11 ± 3.4 vs 16.14 ± 3.8 cm/s p = 0.61). Mean early peak RV diastolic Ea velocity were not significantly different in the two groups (15.6 ± 5.6 vs 18.2 ± 4.9 cm/s p = 0.34). Mean arterial systolic pressure calculated from the tricuspid regurgitation was similar in the two groups (27.7 ? 3.5 mmHg in Pompe disease vs 28.1 ± 2.4 mmHg in control group). The Table 1 summarises Doppler-echocardiographic data.
4 Discussion This is the first study that analyses the RV function in lateonset Pompe disease. Pompe’s disease is a glycogen storage disease (type II) characterized by inherited autosomal recessive transmission. Glycogen accumulation in tissues is caused by a deficiency of alpha 1,4 glucosidase. The enzyme defects is estimated to be 1/40,000 live births. The severity of the disease depends of residual of enzyme activity. The adult form is less severe because of partial
J Clin Monit Comput
enzymatic activity. Heart involvement is uncommon in late-onset Pompe disease. One patient disclosed short a PR duration. A Wolff–Parkinson–White syndrome associated to glycogenosis storage has been reported in the literature [4]. In our study, the LV systolic function was preserved in patients with late onset Pompe disease and LV diameter was in normal ranges in patients (40.8 ± 6 mm in Pompe disease vs 45.8 ± 6 mm in control group p = 0.11). Stollberger and Finsterer [5] reported abnormal myocardial texture. Dilated cardiomyopathy has been described in adult’s patients [6]. Only 1 patient, in late-onset Pompe disease, disclosed LV dysfunction in the study by Soliman et al. [1]. In the study reported by Forsha et al. [7], a short PR was present in 10 % of patients and 7 % of patients disclosed LV dysfunction. The RV function is a determinant parameter of clinical outcome in heart failure. No data have been reported about RV function in late-onset Pompe disease. The tricuspid annular plane systolic displacement (TAPSE) is an echocardiography parameter for the assessment of RV systolic function. The TAPSE is obtained from the long axis four chamber view, using M-mode. This index reflects the systolic axis motion of the RV free wall in the inflow tract [8]. DTI is less preload dependent [9], compared to traditional pulsed Doppler technique. In our study, we did not find RV dysfunction using TAPSE and DTI. In conclusion, according to our data, RV systolic function seems preserved in late-onset Pompe disease.
5 Limits of our study The assessment of the RV function remains difficult because of the complex structure and asymmetrical shape of the RV. The TAPSE discloses limitations because it analyses the inflow free wall tract and not the outflow tract [10]. The TDI is limited by angle dependence. Studies have shown the superiority of magnetic resonance imaging over other techniques in studying the RV [3].
Conflict of interest
None.
References 1. Soliman OI, van der Beek NA, van Doorn PA, Vletter WB, Nemes A, Van Dalen BM, ten Cate FJ, van der Ploeg AT, Geleijnse ML. Cardiac involvement in adults with Pompe disease. J Intern Med. 2008;264(4):333–9. 2. Marwick TH. Techniques for comprehensive two dimensional echocardiographic assessment of left ventricular systolic function. Heart. 2003;89(3):2–8. 3. Lindqvist P, Henein M, Kazzam E. Right ventricular outflow tract fractional shortening: an applicable measure of right ventricular systolic function. Eur J Echocardiogr. 2003;4:29–35. 4. Bulkley BH, Hutchins GM. Pompe’s disease presenting as hypertrophic myocardiopathy with Wolff–Parkinson–White syndrome. Am Heart J. 1978;96(2):246–52. 5. Stollberger C, Finsterer J. Echocardiography in storage and neuromuscular disorders. Wien Klin Wochenschr. 2001;113 (11–12):408–15. 6. Ben-Ami R, Puglisi J, Haider T, Mehta D. The Mount Sinai Hospital clinical pathological conference: a 45-year-old man with Pompe’s disease and dilated cardiomyopathy. Mt Sinai J Med. 2001;68(3):205–12. 7. Forsha D, Li JS, Smith PB, van der Ploeg AT, Kishnani P, Pasquali SK. Late-onset treatment study investigators. Cardiovascular abnormalities in late-onset Pompe disease and response to enzyme replacement therapy. Genet Med. 2011;13(7):625–31. 8. Ghio S, Recusani F, Klersy C, Sebastiani R, Laudisa ML, Campana C, Gavazzi A, Tavazzi L. Prognostic usefulness of the tricuspid annular plane systolic excursion in patients with congestive heart failure secondary to idiopathic or ischemic dilated cardiomyopathy. Am J Cardiol. 2000;85(7):837–42. 9. De Castro S, Cavarretta E, Milan A, Caselli S, Di Angelantonio E, Vizza Carmine D, Lucchetti D, Patel A, Kuvin J, Pandian NG. Usefulness of tricuspid annular velocity in identifying global RV dysfunction in patients with primary pulmonary hypertension: a comparison with 3D echo-derived right ventricular ejection fraction. Echocardiography. 2008;25(3):289–93. 10. Lindqvist P, Calcutteea A, Henein M. Echocardiography in the assessment of right heart function. Eur J Echocardiogr. 2008;9(2):225–34.
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