Echocardiographic Assessment After Heart Transplantation

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17 Echocardiographic Assessment After Heart Transplantation

Mariska Kemna

Background

• Pediatric heart transplantation has been performed since the 1980s.
• Surgical technique involves left atrial anastomosis to avoid pulmonary vein (PV) stenosis as a consequence of PV anastomosis.
• Systemic venous connections are performed through a right atrial anastomosis in young children (Fig. 17-1) or a bicaval anastomosis in older children and adults (Fig. 17-2).
• Arterial connections are generally created in the ascending aorta (Ao) and main pulmonary artery (MPA).
image

Figure 17-1 Biatrial anastomoses at the time of cardiac transplantation. The four sites of anastomoses between the donor and recipient are the left atrium, right atrium, aorta (Ao), and pulmonary artery (PA).

(From Mavroudis C, Backer CL. Pediatric Cardiac Surgery, 3rd ed. Philadelphia: Mosby; 2003.)

image

Figure 17-2 Bicaval anastomoses at the time of cardiac transplantation. The five sites of anastomoses between the donor and recipient are the left atrium, inferior vena cava, superior vena cava, Ao, and PA.

(From Mavroudis C, Backer CL. Pediatric Cardiac Surgery, 3rd ed. Philadelphia: Mosby; 2003.)

Overview of Echocardiographic Approach

• Echocardiography (echo) serves multiple purposes after heart transplantation.1
• The focus of the echocardiographic exam shifts depending on the time since transplantation (Table 17-1).
• In the immediate post-transplantation period, all surgical connections should be carefully interrogated. In addition, acute graft dysfunction, pulmonary hypertension (PHTN), and pericardial effusions are major concerns.
• Surgical connections and graft function will need to be monitored indefinitely after transplantation.
• Some centers use echo for routine rejection monitoring after heart transplantation.
• Other centers monitor for rejection using cardiac biopsies, and echo can be used to guide the bioptome and screen for complications afterward.
• Dobutamine stress echo (DSE) can be used to monitor for graft coronary artery disease.

TABLE 17-1 USE OF ECHOCARDIOGRAPHIC MODALITIES AFTER TRANSPLANTation

Immediately After Transplantation 1 Week to 1 Year After Transplantation >1 Year After Transplantation
TEE: acute graft dysfunction (RV, LV) TTE: RV function DSE: graft coronary artery disease
TEE and TTE: RV pressure TTE: RV pressure  
TEE and TTE: surgical connections TTE: surgical connections TTE: surgical connections
TTE: acute rejection TTE: rejection TTE: rejection
TTE: pericardial effusion TTE: graft dysfunction TTE: graft dysfunction

Key Points

Postoperative concerns after heart transplantation that should be evaluated by echo include:

• Surgical connections.
• Pericardial effusion.
• Acute graft dysfunction: right ventricle and/or left ventricle (LV).
• PHTN.
• Rejection.
• Chronic graft dysfunction.
• Graft coronary artery disease.

Anatomic Imaging

• Focus on the surgical anastomoses between donor heart and recipient.
• All anastomoses should be interrogated in the appropriate views, either with transesophageal echo (TEE) or transthoracic echo (TTE) (Table 17-2).
• TEE should be done when the patient comes off cardiopulmonary bypass.

TABLE 17-2 Transesophageal and transthoracic echocardiographic views to assess the anastomoses between the donor heart and recipient

image

Venous Anastomoses

• Pulmonary side:

• Left atrial anastomosis of the donor left atrium to recipient residual left atrial cuff is performed to avoid PV anastomosis.
• This produces an echocardiographic image of gross atrial enlargement with an echodense suture line in the four-chamber (4C) view, which should not be mistaken for thrombus (Fig. 17-3).
• Pulmonary venous obstruction should be excluded in the immediate post-transplantation period with echo Doppler on intraoperative TEE and subsequent TTE.

• Systemic side:

• Right atrial anastomosis is performed in younger (smaller) children and bicaval anastomoses in older children and adults.
• Right atrial anastomosis also creates an image of an enlarged right atrium with echodense suture line.
• A bicaval connection should be interrogated for possible stenosis with Doppler imaging.
• Superior vena cava (SVC) flow velocity can be recorded from the suprasternal notch (SSN) or subcostal images. Normal SVC flow is biphasic with two distinct waves (S and D waves). A loss of this biphasic pattern or an increase in flow velocity of more than 1 m/s indicates obstruction.
• The inferior vena cava can be interrogated from the subcostal short axis (sagittal) view.
• Occasionally, abnormal congenital pulmonary and systemic connections in the native heart warrant construction of atrial baffles, which should be interrogated for obstruction.
• The presence of a left SVC in the recipient can also result in abnormal venous connections.

image

Figure 17-3 Apical four-chamber view in a heart transplant recipient showing left atrial enlargement with an echodense suture line.

Arterial Anastomoses

• Pulmonary artery (PA):

• MPA anastomosis should be interrogated for stenosis in the parasternal short axis and long axis views on TTE.
• Occasionally, when native central PAs are abnormal, donor PAs are used, and the anastomosis with native PA tissue is made in the branch PA. These distal anastomoses will be more prone to stenosis but are sometimes poorly seen by echo, especially on TEE. When poorly seen, the presence of PA flow can be confirmed indirectly by presence of pulmonary venous flow.

• Aorta:

• Aortic anastomosis is usually performed in the ascending Ao and can be evaluated for obstruction in the suprasternal long axis view on TTE.
• If there is a native arch hypoplasia, an aortic arch reconstruction may be necessary, which should be evaluated for coarctation, analogous to methods described in Chapter 13, Myocardial Pathology.

Valve Regurgitation

• There is an increased frequency of tricuspid valve (TV) regurgitation in the transplant recipient population due to multiple factors:

• Right atrial anastomosis.
• Right ventricular dysfunction, especially early after transplantation.
• PHTN, especially early after transplantation.
• Rejection.
• Chordal rupture as a complication of cardiac biopsy (Fig. 17-4).

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Figure 17-4 Severe tricuspid regurgitation in a heart transplant recipient secondary to a flail tricuspid valve leaflet.

Pericardial Effusion

• Pericardial effusion is relatively common after heart transplantation and has a different differential diagnosis than in the nontransplant recipient (Box 17-1).
• An effusion in the immediate postoperative period is most likely due to a surgical hematoma, but rejection is the most common cause of a new pericardial effusion at any other time after heart transplantation (Fig. 17-5).
• Pericardial effusions should be evaluated for size and signs of tamponade, according to methods described in Chapter 16.

Box 17-1

Differential Diagnosis of Pericardial Effusion After Heart Transplantation

Rejection
Size discrepancy of native and donor heart
Surgical hematoma (early post-transplantation)
Perforation of ventricular free wall after cardiac biopsy
Infectious pericarditis
Inflammatory pericarditis
Malignancy (mostly metastatic disease from lymphoma)
image

Figure 17-5 Large pericardial effusion in a heart transplant recipient with moderate cellular as well as antibody-mediated rejection.

Physiologic Data

Early Post-transplantation

• Another focus of TEE and TTE in the early post-transplantation period is acute graft dysfunction.
• TEE starts with a transgastric short axis view (probe advanced into stomach in a neutral position with anteflexion) to evaluate left ventricular systolic function (fractional shortening).
• Right ventricular dilation and systolic dysfunction are relatively common in the early post-transplantation period due to graft preservation injury and/or preexisting PHTN.
• Tricuspid regurgitant jet should be measured by pulsed wave (PW) Doppler for an estimation of right ventricular pressure.

Systolic Function

• Left ventricular systolic function (ejection fraction, fractional shortening, and posterior wall thickening fraction) is an important part of the TTE exam anytime after transplantation.
• A decrease in systolic function can be caused by preservation injury, rejection, transplant coronary disease, or obstruction to outflow (usually at the anastomosis site).

Diastolic Function

• LV diastolic function is often abnormal in early post-transplantation period due to perioperative ischemia, reperfusion injury, systemic hypertension, or side effects of immunosuppressive medications.
• Normalizes in the majority of patients within the first couple of months, but can remain abnormal.2
• Abnormal diastolic function can also be one of the first signs of rejection.
• Diastolic function can remain abnormal after rejection has been treated.

Key Points

• Right ventricular dilation and decreased systolic function are relatively common in the early post-transplantation period and often normalize within days to weeks.
• Abnormal left ventricular diastolic function is often seen after transplantation.
• It will frequently recover within weeks to months but remains abnormal in a subgroup of patients.

Assessment of Diastolic Function (Table 17-3)

• Left ventricular inflow velocity:

• Measurement of E and A velocity performed at mitral leaflet tips in apical 4C view with PW Doppler.
• Normal pattern of E velocity greater than A velocity is reversed with mild diastolic dysfunction.
• More severe dysfunction can lead to a pseudonormal pattern.
• Adult heart transplant recipients often show shortening of deceleration time of early diastolic filling.3 However, deceleration time values have a very wide range in children4 and therefore are not used as much as in adults.

• Tissue Doppler imaging (TDI).

• TDI velocities of mitral annular motion (septal and lateral, obtained from the apical 4C view) are lower in transplant recipients than in normal controls.2
• Can show a reversed (E′ < A′) or restrictive (E′ and A′ both <10 cm/s) pattern, especially in the first months after transplantation.

• Isovolumic relaxation time (IVRT).

• IVRT is the interval between aortic valve closing and mitral valve (MV) opening at the onset of mitral forward flow.
• It is obtained in the apical five-chamber view with the Doppler sample volume placed midway between inflow and outflow areas so that mitral inflow (above baseline) and left ventricular outflow (below baseline) are captured simultaneously (Fig. 17-6).
• Normal values in children (30–50 ms) are lower than in adults.4
• IVRT is often prolonged in pediatric heart transplant patients (55 ± 20 ms), suggesting mild diastolic dysfunction in the transplanted heart.5
• Shortening of IVRT indicates more severe diastolic dysfunction with impaired ventricular compliance.

TABLE 17-3 ASSESSMENT OF DIASTOLIC FUNCTION

image

image

Figure 17-6 The isovolumic relaxation time (IVRT) is measured from aortic valve closure to mitral valve opening on the Doppler tracing, corresponding to the phase of the cardiac cycle where the left ventricular pressure is rapidly declining but left ventricular volume is constant.

(From Otto CM, Schwaegler RG. Echocardiography Review Guide. Philadelphia: Elsevier; 2008. Figure 7.11.)

Assessment of Systolic and Diastolic Function

• Tei index or myocardial performance index (MPI).

• A combined measure of systolic and diastolic performance.
• Equals isovolumic contraction time (IVCT) plus IVRT/aortic ejection time (Fig. 17-7).
• In the pediatric general population, abnormal when greater than 0.4.
• TDI is often increased in pediatric heart transplant recipients due to diastolic dysfunction.5

• Strain and strain rate imaging.

• TDI technique that measures strain (shortening) and strain rate (velocity of shortening) of myocardial tissue.6
• Strain is the amount of local deformation expressed as a percentage.
• Positive strain describes thickening and negative strain describes shortening of a myocardial segment, related to its original size.
• Able to differentiate between active and passive movement of myocardial segments, independent of overall cardiac motion.
• Allows for early detection of myocardial dysfunction and intraventricular dyssynchrony.
• Include myocardial viability studies and early detection of rejection and transplant coronary artery disease.
• TDI strain rate imaging measures tissue movement compared with the transducer, in one dimension at a time, and is dependent on the angle of interrogation.

• Speckle tracking.

• Measures regional tissue wall motion (myocardial deformation) by tracking speckles (natural acoustic markers) in a two-dimensional echo image and determines the velocity from the changes in speckle position (with known frame rate).
• In contrast to TDI strain rate imaging, speckle tracking can calculate strain and strain rate in multiple dimensions at a time: radial, circumferential, and longitudinal, independent of the angle of interrogation.

image

Figure 17-7 Assessment of myocardial performance index (MPI). Measurements on pulsed wave (PW) Doppler of mitral inflow and aortic outflow. MPI = (a − b)/b; aortic ejection time (ET) = b.

Rejection

Key Points

• Rejection causes multiple changes in the transplanted heart.
• No single echocardiographic parameter can reliably predict rejection.
• However, an algorithm that involves multiple echocardiographic parameters increases sensitivity and can be used for rejection surveillance instead of routine cardiac biopsies.
• Echocardiographic signs of rejection:

• Abnormal left ventricular diastolic function (early sign).
• Decreasing left ventricular systolic function (late sign).
• Rapidly increasing wall thicknesses (with decreased cavity size), especially in infants.
• New pericardial effusion.
• New-onset atrioventricular valve regurgitation (AVVR).

• Rejection causes multiple changes in the transplanted heart.
• Diastolic dysfunction occurs early in the process due to cellular infiltration and tissue edema, preceding systolic dysfunction.
• Many surveillance cardiac biopsies could be avoided with the ability to accurately diagnose subclinical rejection by echo.
• Unfortunately, no single echocardiographic parameter has sufficient negative and positive predictive power to reliably predict rejection.7
• Diastolic dysfunction is not specific enough because many transplant recipients have baseline abnormal diastolic function.
• Systolic dysfunction appears late in the process, and therefore systolic dysfunction alone is not sensitive enough.
• However, an algorithm that involves multiple echocardiographic parameters improves sensitivity and can reliably predict rejection.

Echocardiographic Rejection Surveillance

• Boucek et al.8 developed an algorithm for diagnosing early rejection in pediatric heart transplant recipients that includes parameters of diastolic and systolic function (Box 17-2) as well as left ventricular mass (LVM), pericardial effusion, and AVVR.
• In the algorithm, measured patient values are compared with age-matched transplant recipients without rejection, and abnormal values provide points toward a total compiled rejection score.
• Abnormal values are dependent on patient age: younger than 6 months (Table 17-4) or older than 6 months (Table 17-5).
• A score of 5 or higher predicts significant rejection, especially if it signifies a change from the patient’s own baseline values9 (Figs. 17-8A and 17-9A).
• New-onset moderate or severe MV or TV regurgitation, newly depressed systolic function (fractional shortening <28%, with normal septal motion), or pericardial effusion predicts rejection, independent of the total rejection score.
• Echo rejection scores cannot reliably be applied until systolic and diastolic function has normalized after transplantation, although diastolic recovery is not always complete.
• In addition, there are marked variations between individuals after transplantation; hence, each patient should act as his or her own control.

Box 17-2

Components of the Pediatric Echo Rejection Score

Inflammatory parameters

Left ventricular end-diastolic volume (LVEDV)
LVM (increased wall thickness)
LVEDV/LVM
AVVR
Pericardial effusion

Systolic parameters

Left ventricular fractional shortening
IVS thickening fraction
LVPW thickening fraction

Diastolic parameters

Left ventricular filling velocity
Average-velocity LVPW thinning
Maximum velocity LVPW thinning
MV annulus E′/A′

TABLE 17-4 INFANT ECHO REJECTION SCORE (AGE < 6 MONTHS)

Parameter Threshold Score
LVEDV <30% of predicted normal for BSA 1
LVM >130% of predicted normal for BSA 1
LVEDV/LVM <0.35 1
IVS thickening <25% 1
LVPW thickening <60% 2
Filling velocity of LV <40 mm/s 1
Maximum velocity of LVPW thinning <9 mm/s 1
New MR or TR >Mild 1
E′/A′ <1.1 1

TABLE 17-5 PEDIATRIC ECHO REJECTION SCORE (AGE > 6 MONTHS)

LVEDV <60% of predicted normal for BSA 2
LVM >130% of predicted normal for BSA 1
LVEDV/LVM <0.4 1
IVS thickening <25% 1
LVPW thickening <70% 2
Filling velocity of LV <60 mm/s 1
Maximum velocity of LVPW thinning <11 mm/s 2
Average velocity of LVPW thinning <25 mm/s 1
New MR or TR >Mild 1
E′/A′ <1.1 1
image

Figure 17-8 A, Acute cellular rejection in heart transplant recipient, diagnosed by echocardiography (echo) rejection score. The rejection score was 8 when left ventricular posterior wall (LVPW) thinning was evaluated by manual digitizer, and 6 when TDI velocities were used instead of the manual digitizer. B, M-mode of the LVPW of the same patient after treatment for rejection. The LVPW thinning velocity has improved, and the rejection scores are now 2 by manual digitizer and 1 by TDI velocities.

image

Figure 17-9 A, Acute cellular rejection in heart transplant recipient diagnosed by echo rejection score. The rejection score was 6 when LVPW thinning was evaluated by manual digitizer, and 9 when LV posterior wall TDI velocities were used instead of the manual digitizer. B, M-mode of the LVPW in the same patient after treatment for rejection. The LVPW thinning velocity has improved and the rejection scores are now 2 by manual digitizer and 1 by TDI velocities.

Requirements for Data Collection

• Echo machine with strip chart recorder at 100 mm/s.
• XY plotter to digitize endocardial tracings offline.
• Endocardial tracings are obtained from high-resolution M-mode, with gains set low for optimal definition of endocardium.
• Endocardial tracings from right ventricular septal surface, left ventricular septal surface, and left ventricular posterior wall (LVPW), as well as epicardial surface tracing of the left ventricular posterior wall from parasternal short axis view (close to the MV annulus).
• Maximum and average velocities of posterior wall thinning are determined by manual digitization of least three cardiac cycles, and results are averaged.
• This offline analysis of posterior wall thinning velocities is technically demanding, and therefore TDI velocities of the posterior wall can be used as an alternative. However, values determined by TDI are dependent on heart rate (HR) and cardiac afterload.

Other Echocardiographic Indicators of Rejection Described in Pediatric Heart Transplant Recipients

• Increase in the MPI; MPI of 0.64 or greater can indicate rejection.10
• Decrease in myocardial acceleration during IVC (IVA = peak IVC velocity/acceleration time), measured by TDI in basal left ventricular segments. IVA is independent of age or regional wall motion abnormalities and remains normal after heart transplantation, but decreases during rejection (baseline 1.1–1.4 m/s2, rejection 0.6–0.7 m/s2)11 (Fig. 17-10).
• In the adult heart transplant recipient population, the following diastolic parameters have been associated with rejection:

• Shortening of IVRT to less than 60 ms or decrease in IVRT of more than 20 ms.12
• More than 10% decrease in early diastolic wall motion velocity of basal posterior wall by TDI (E′ in parasternal short axis view) compared with patient’s baseline.
• Longer early diastolic time (Tem = time from onset of second heart sound to the peak of the E′).13

• Strain and strain rate imaging might also prove valuable in rejection monitoring.
• A decrease in (radial) strain and strain rate has been associated with rejection in the adult transplant recipient population.14
image

Figure 17-10 Myocardial acceleration during isovolumic contraction was determined as the slope of the upstroke of the isovolumic contraction wave.

(From Pauliks LB, Pietra BA, DeGroff CG, et al. Non-invasive detection of acute allograft detection in children by tissue Doppler imaging: myocardial velocities and myocardial acceleration during isovolumic contraction. J Heart Lung Transplant. 2005;24:S239–S248.)

Alternate Approach to Rejection Surveillance

• Although some experienced centers use echo to monitor for rejection, others use regular cardiac biopsies.
• Echo can help guide the bioptome toward the right ventricular side of the interventricular septum (IVS) for optimal tissue sampling.
• Echo is also used to monitor for complications after cardiac biopsy, including right ventricular perforation with pericardial effusion or TV regurgitation caused by rupture of TV chordae.

Dobutamine Stress Echocardiography

• Transplant coronary artery disease consists of small-vessel disease with concentric intimal proliferation and is not easily visualized on coronary angiogram.
• Dobutamine increases myocardial oxygen demand.
• DSE provides functional assessment and can unmask myocardial ischemia, evidenced by reversible regional hypokinesis or akinesis.15

Protocol

• Dobutamine infusion at initial dose of 5 µg/kg/min, followed by 10 µg/kg/min, then increase every 3 minutes in increments of 10 µg/kg/min to a maximum of 40 µg/kg/min.
• Monitor HR, blood pressure, and continuous 12-lead electrocardiography.
• Obtain TTE images in four standard views of the LV (parasternal long axis, parasternal short axis, apical 4C, apical 2C) at baseline, each stress stage (after 3 minutes of stable dose infusion), and after recovery to resting HR.
• Images are obtained in cine-loop format, with clear definition of the endocardium.
• Images are evaluated for new wall motion abnormality or worsening of baseline segmental abnormality in 16-segment model (Fig. 17-11).
• The endpoint is a target HR of 85% of the maximum HR predicted for age (220 minus age), but pediatric heart transplant recipients frequently do not reach this target, especially if general anesthesia is used during the study.
• The study is considered nondiagnostic unless the HR is at least 75% of the maximum predicted HR for age.
• DSE needs to be performed under supervision of a qualified medical professional in a procedure room with resuscitation equipment and medications readily available.
• Box 17-3 lists the criteria for early termination of DSE.
image

Figure 17-11 Echocardiographic views showing the 16-segment model of the left ventricle.

(From Di Filippi S, Semiond B, Roriz R, et al. Non-invasive detection of coronary artery disease by dobutamine-stress echocardiography in children after heart transplantation. J Heart Lung Transplant. 2001;22:876–882.)

Box 17-3

Criteria for Early Termination of DSE

Patient symptoms: chest pain, persistent headache, or discomfort
Systolic blood pressure higher than 200 mm Hg or more than two times the systolic blood pressure at rest
Diastolic blood pressure higher than 100 mm Hg
Decrease in blood pressure (>20% of resting value)
Arrhythmia
ST segment increase or decrease greater than 2 mm
Definite wall motion abnormalities in two or more adjacent segments

Troubleshooting

• If the target HR is not achieved, atropine (0.01–0.02 mg/kg/dose, minimum dose 0.1 mg, maximum dose 0.4 mg) may be added.
• The effects of dobutamine can be rapidly reversed with esmolol (0.1 mg/kg IV).
• Nitroglycerin sublingually or intravenously can be given for ischemia or hypertension.

Interpretation

• Integration of clinical, electrocardiographic, and echocardiographic data.
• ST segment changes indicate coronary ischemia.
• Rest and stress images are compared side by side in cine-loop format.
• Wall motion of the LV is assessed in 16 segments (see Fig. 17-11), and each segment is graded as hyperkinetic, normal, hypokinetic, akinetic, or dyskinetic.
• A normal response to dobutamine constitutes an increase in wall thickening.
• New hypokinesis, akinesis, or worsening of preexisting abnormality indicates myocardial ischemia.
• Improvement of resting wall motion abnormality with low-dose dobutamine indicates myocardial viability (“hibernating” or “stunned” myocardium).

Key Points

• DSE can provide functional assessment of coronary flow and unmask myocardial ischemia.
• Myocardial ischemia is evidenced by reversible regional hypokinesis or akinesis in a 16-segment model of the LV.

References

1 Thorn EM, de Filippi CR. Echocardiography in the cardiac transplant recipient. Heart Failure Clin. 2007;3:51-67.

2 Strigl S, Hardy R, Glickstein JS, et al. Tissue Doppler-derived diastolic myocardial velocities are abnormal in pediatric cardiac transplant recipients in the absence of endomyocardial rejection. Pediatr Cardiol. 2008;29:749-754.

3 Burgess MI, Bhattacharyya A, Ray SG. Echocardiography after cardiac transplantation. J Am Soc Echocardiogr. 2002;15:917-925.

4 Cui W, Roberson DA, Zen Z, et al. Systolic and diastolic time intervals measured from Doppler tissue imaging: normal values and Z-score tables, and effects of age, heart rate and body surface area. J Am Soc Echocardiogr. 2008;21:361-370.

5 Prakash A, Printz BF, Lamour JM, Addonizio LJ, Glickstein JS. Myocardial performance index in pediatric patients after cardiac transplantation. J Am Soc Echocardiogr. 2004 May;17(5):439-442.

6 Dandel M, Lehmkuhl H, Knosalla C, et al. Strain and strain rate imaging by echocardiography—basic concepts and clinical applicability. Curr Cardiol Rev. 2009;5:133-148.

7 Mena C, Wencker D, Krumholz H, et al. Detection of heart transplant rejection in adults by echocardiographic diastolic indices: a systematic review of the literature. J Am Soc Echocardiogr. 2006;19:1295-1300.

8 Boucek MM, Mathis CM, Boucek RJJr, et al. Prospective evaluation of echocardiography for primary rejection surveillance after infant heart transplantation: comparison with endomyocardial biopsy. J Heart Lung Transplant. 1994;13:66-73.

9 Putzer GJ, Cooper D, Keehn C, et al. An improved echocardiographic rejection-surveillance strategy following pediatric heart transplantation. J Heart Lung Transplant. 2000;19:1166-1174.

10 Leonard GTJr, Fricker FJ, Pruett D. Increased myocardial performance index correlates with biopsy-proven rejection in pediatric heart transplant recipients. J Heart Lung Transplant. 2006;25:61-66.

11 Pauliks LB, Pietra BA, DeGroff CG, et al. Non-invasive detection of acute allograft detection in children by tissue Doppler imaging: myocardial velocities and myocardial acceleration during isovolumetric contraction. J Heart Lung Transplant. 2005;24:S239-S248.

12 Dandel M, Hummel M, Meyer R, et al. Left ventricular dysfunction during cardiac allograft rejection: early diagnosis, relationship to the histological severity grade, and therapeutic implications. Transplant Proc. 2002;34:2169-2173.

13 Dandel M, Hummel M, Muller J, et al. Reliability of tissue Doppler wall motion monitoring after heart transplantation for replacement of invasive routine screenings by optimally timed cardiac biopsies and catheterizations. Circulation. 2001;104:I184-I194.

14 Marciniak A, Eroglu E, Marciniak M, et al. The potential clinical role of ultrasonic strain and strain rate imaging in diagnosing acute rejection after heart transplantation. Eur J Echocardiogr. 2007;8:213-221.

15 Di Filippi S, Semiond B, Roriz R, et al. Non-invasive detection of coronary artery disease by dobutamine-stress echocardiography in children after heart transplantation. J Heart Lung Transplant. 2001;22:876-882.

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